Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

Alexandru M. F. Tomescu; Gar W. Rothwell

doi:10.1186/s13227-022-00192-7

Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

Tomescu, Alexandru M. F.; Rothwell, Gar W. 2022-03-02 00:00:00 Fossils constitute the principal repository of data that allow for independent tests of hypotheses of biological evolu- tion derived from observations of the extant biota. Traditionally, transformational series of structure, consisting of sequences of fossils of the same lineage through time, have been employed to reconstruct and interpret morpho- logical evolution. More recently, a move toward an updated paradigm was fueled by the deliberate integration of developmental thinking in the inclusion of fossils in reconstruction of morphological evolution. The vehicle for this is provided by structural fingerprints—recognizable morphological and anatomical structures generated by (and reflective of ) the deployment of specific genes and regulatory pathways during development. Furthermore, because the regulation of plant development is both modular and hierarchical in nature, combining structural fingerprints recognized in the fossil record with our understanding of the developmental regulation of those structures pro- duces a powerful tool for understanding plant evolution. This is particularly true when the systematic distribution of specific developmental regulatory mechanisms and modules is viewed within an evolutionary (paleo-evo-devo) framework. Here, we discuss several advances in understanding the processes and patterns of evolution, achieved by tracking structural fingerprints with their underlying regulatory modules across lineages, living and fossil: the role of polar auxin regulation in the cellular patterning of secondary xylem and the parallel evolution of arborescence in lycophytes and seed plants; the morphology and life history of early polysporangiophytes and tracheophytes; the role of modularity in the parallel evolution of leaves in euphyllophytes; leaf meristematic activity and the parallel evolu- tion of venation patterns among euphyllophytes; mosaic deployment of regulatory modules and the diverse modes of secondary growth of euphyllophytes; modularity and hierarchy in developmental regulation and the evolution of equisetalean reproductive morphology. More generally, inclusion of plant fossils in the evo-devo paradigm has informed discussions on the evolution of growth patterns and growth responses, sporophyte body plans and their homology, sequences of character evolution, and the evolution of reproductive systems. Keywords: Developmental regulation, Evo-devo, Fossil, Leaf, Modularity, Morphology, Rooting organ, Secondary growth, Strobilus, Structural fingerprint *Correspondence: mihai@humboldt.edu Department of Biological Sciences, California Polytechnic State University Humboldt, Arcata, CA 95521, USA Full list of author information is available at the end of the article © The Author(s) 2022. 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The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Tomescu and Rothwell EvoDevo (2022) 13:8 Page 2 of 19 Fossils provide invaluable evidence of evolution At macroevolutionary scales, ecological crisis Since their earliest occurrences in the fossil record more is the driver of evolution than 400 million years ago, vascular plants have diversi- Of equal importance for documenting structural change fied tremendously. While living species are characterized through time, the fossil record provides convincing evi- by a sporophyte that is differentiated into a wide array of dence for the fundamental processes that underlie plant organs and parts, including stems, leaves, roots, sporan- evolution [3]. While evolution traditionally has been gia, seeds, cones, flowers, and fruits, the most ancient explained within the context of classical and population vascular plant sporophytes consisted of simple branch- genetics, as early as the 1970s tests of those traditional ing axes with terminal sporangia, a morphology that cur- evolutionary hypotheses using paleontological data rently seems to have preceded the evolution of typical began to reveal patterns of change over broader tempo- xylem and phloem [1]. Deeper in evolutionary time and ral scales additional to those predicted by genetics-based plant phylogeny, bryophyte-grade embryophytes pos- evolutionary theory at the population level [7]. Popula- sessed sporophytes consisting of little more than a single tion genetics theory predicts that natural selection is the sporangium [2]. The origin of the ancestral tracheophyte driving force for evolutionary change and that such selec- body plan and its transition from this simple organiza- tive forces are most impactful within well-established tion to the complex sporophytes present in most modern ecosystems. At macroevolutionary scales, the paleonto- tracheophyte lineages were accompanied by numerous logical record reveals that the most rapid evolutionary dramatic changes in plant structure [3, 4]. Understand- diversifications occur immediately after biological catas - ing these changes within a developmental framework is trophes, at moments when extinction has dramatically key to reconstructing plant evolution and phylogeny, reduced biotic selective pressures and has opened up and necessarily requires integration of data on develop- vast swaths of ecological space for colonization by new mental regulation, obtained from living plants, with data species [8, 9]. Both macroevolutionary theory (e.g., [10]) from the fossil record. To answer questions on the evo- and paleontologically established patterns of evolution- lution of development, studies of living plants focus on ary change indicate that the reestablishment of complex careful studies of gene expression and function with the plant communities leads to long periods of evolution- aim to gradually document regulatory pathways respon- ary stasis that witness only small-scale selection-driven sible for specific developmental processes. These studies evolutionary modification [11, 12]. Therefore, the fos - have made significant strides toward understanding the sil record reveals that evolutionary diversification is the principles of plant developmental regulation and have least rapid when genetically based evolutionary theory revealed the complexity of regulatory interactions which, predicts it should reach its highest rates. This apparent even in model species, are often still largely unknown. contradiction is mostly a matter of scale—natural selec- Additionally, sequencing of algal streptophyte and plant tion acts primarily as a filter removing maladapted phe - genomes and transcriptomes over the last decade has notypes at microevolutionary scales, and less as a driving opened opportunities for predicting the makeup of gene force at macroevolutionary scales [13–17]—and this is regulatory networks in different lineages, thus informing especially apparent within a paleontologically sanctioned hypotheses about the evolution of these networks (e.g., context. [5, 6]). Understanding morphological evolution—i.e., evolu- The evo‑devo paradigm and the role tionary changes in plant structure—within a develop- of morphology mental framework also necessitates in-depth knowledge A growing appreciation for the role of development in of both the intermediate stages that populate the differ - evolution, whose understanding has been dramatically ent trajectories of evolutionary change, and of the order elevated by the advent of developmental molecular biol- in which they occurred within each lineage. Most of ogy, has fostered an improved perception of evolutionary these intermediate stages of evolutionary changes that process [18, 19]. Within this context, we now recognize have transformed plants over time are not present among that the genome encodes the program that determines species of the modern flora, and are preserved only in ontogeny, and it is that program which evolves through the fossil record. Therefore, fossils provide vital evidence, time [3]. For each organism, the genetic program is unavailable otherwise, for understanding the origins of implemented through the processes of development. modern plant structure and for reconstructing the pat- As a result, the phenotype of an organism at any point terns of structural changes through time that have pro- during its ontogeny represents the cumulative structural duced the morphological diversity that characterizes evidence for the developmental processes that generated modern vegetation. it. In turn, these reflect the deployment of the genetic program, i.e., the activity of regulatory mechanisms that T omescu and Rothwell EvoDevo (2022) 13:8 Page 3 of 19 direct those developmental processes. Therefore, changes turn, allowed for branching. Evidence in support of this in the genetic program produce predictable changes in hypothesis is provided by apogamous sporophytes of the the phenotype of the resulting organisms, which we refer living moss Physcomitrium patens, wherein the combina- to as morphological evolution [20]. tion of gene silencing and auxin transport inhibition pro- For example, the origin of branching in the sporophyte duces a comparable heterochronic change that results in phase of the embryophyte life cycle was, alongside the an elongated and branched axial sporophyte body [22]. evolution of xylem and phloem, a seminal event leading Indeed, the oldest known branched sporophytes, which to the evolution of vascular plants [21]. That change may characterize the polysporangiophyte clade (Fig. 1), show be hypothesized to have resulted from the prolongation bryophyte-grade features, such as bryophyte-type pho- of the time during which the sporophyte underwent api- tosynthate-conducting cells in the absence of true trac- cal growth before going through a transition to reproduc- heids [1] and nutritional dependence on the gametophyte tive growth and the production of terminal sporangia [3, phase [23, 24]. 4]. According to this hypothesis, a change in develop- Because phenotypes are the direct result of develop- mental regulation in the early sporophyte stage of bry- ment under the control of genetic regulation, the wed- ophyte-grade plants resulted in the origin of potentially ding of paleontology (i.e., phenotypes through time) indeterminate growth from an apical meristem which, in with regulatory genetics (i.e., genomic changes leading Fig. 1 A phylogenetic framework for the groups discussed throughout the paper; a polygon denotes uncertainty in the relationships among different lineages of that group (mostly due to conflict between the results of different analyses); Trim = Trimerophytes Tomescu and Rothwell EvoDevo (2022) 13:8 Page 4 of 19 off without affecting the activity of other modules) [26]. Additionally, interactions among regulatory modules can be hierarchical. In an experimental study of vascular cambial growth in the angiosperm Ficus, Lev-Yadun [27] demonstrated that girdling induces transient production of wood in which rays develop normally but the axial system exhibits dra- matically altered anatomy, differentiating into isodia - metric parenchyma. Although the study did not address Fig. 2 Anatomical and morphological features seen in organisms directly the specific genetic and molecular factors that bear witness to the activity of specific regulatory modules. Studies control these developmental processes, this example of living organisms can identify the regulatory entities of specific developmental processes, which produce well-defined phenotypic illustrates both modularity and hierarchy of modules in traits. Such phenotypic traits, thus, represent structural fingerprints developmental regulation. The different effects that the of the deployment of those developmental regulators. In turn, girdling treatment had on the anatomy of the two systems identification of structural fingerprints in fossils provides evidence of secondary xylem—radial (rays) and axial (tracheary for the activity of their corresponding regulatory entities in extinct elements, xylem parenchyma, fibers)—indicates that the lineages, informing the evolutionary history of those regulators two aspects of development can proceed independently of each other. In turn, this implies that their regulation is uncoupled and, thus, distinct regulatory modules, at least to phenotypic changes) provides a framework for under- in terms of patterns of cell division and differentiation. standing the evolution of development (Fig. 2). Within Girdling, on the other hand, did not directly affect the this context, the developmental underpinnings of mor- three-dimensional organization of secondary xylem (into phology take on a much more central role in understand- two distinct systems), which suggests that this organiza- ing both the patterns and processes of plant evolution, tion is controlled at a different hierarchical level of devel - and the fossil record provides access to direct evidence opmental regulation. of that evolution. Building on data and ideas published Evidence for modularity in developmental regula- by ourselves and others, here we focus on the modular tion abounds in all biological systems and discussions of nature of developmental regulation emphasizing the developmental modularity provide a meeting place for role of fossils in supporting or generating hypotheses on developmental and evolutionary biologists [28]. The evi - modularity and its role in morphological diversity and dence is often provided by regulatory mechanisms whose evolution. These have never been considered together in activation—or lack thereof—is independent of their a comprehensive discussion of the role of fossils in docu- broader regulatory context, ontogenetic timing, or posi- menting the modular nature of development and its reg- tion of deployment, thus indicating that they represent ulation, which have otherwise been widely discussed in distinct regulatory modules. Such are the several regula- “neontological” evo-devo. tors that induce different histological differentiation or morphogenetic effects which, in different combinations, Developmental regulation is modular are responsible for distinct morphologies that bridge the and hierarchic reptilian scale to avian feather spectrum of tetrapod skin Throughout the ontogeny of an organism, developmental appendages [29]. In plants, we see examples of modular- regulation is a complex, dynamic system of physical inter- ity when different aspects of the development of the same actions between proteins, hormones, small RNAs, etc. tissue, tissue system or organ are controlled indepen- An important feature of this system is that the strength dently: the control of vascular proliferation and vascular and duration of interactions between its different com - organization that are genetically separable [30]; xylem ponents change during ontogeny; the changes separate and phloem cell differentiation from procambium con - subsets of strongly interdependent interactions that can trolled independently of the neat separation of the two be regarded as distinct regulatory modules (e.g., the vari- tissues within vascular bundles [31]; differentiation of ational modules of Pavlicev and Wagner [25]). Thus, the secondary phloem and secondary xylem controlled inde- modules are subsets of the broader system of interac- pendently of each other [32]; blade expansion and leaflet tions; they are tightly integrated internally, on one hand initiation uncoupled during compound leaf morphogen- (i.e., within-module interactions are strictly dependent esis [33]; floral organ length and corolla limb dimensions on each other), and on the other hand are independent varying independently in two closely related species of from, or more loosely integrated with, other such sub- the same genus [34]. sets of interactions (i.e., modules can be turned on and T omescu and Rothwell EvoDevo (2022) 13:8 Page 5 of 19 Another example is the reiteration of structural mod- about the evolution of morphological complexity as a ules consisting of four nuclei (whose makeup is likely mosaic of features combined in different ways and assem - determined by the same regulatory mechanism) among bled in different sequences in different major lineages the diverse types of angiosperm megagametophyte devel- [44, 45]. opment [35]. Along similar lines, the same set of regula- tory interactions may be deployed in different locations Structural fingerprints provide evidence within the plant, like in the case of a module that regu- for the deployment of regulatory modules lates cell wall remodeling, expressed in both lateral root across phylogeny and time emergence and petal abscission [36]; and, more gener- The anatomical and morphological features seen in ally, in the development of ectopic structures of many organisms bear witness to the activity and, sometimes, kinds. Conversely, different developmental fates can be interactions of specific regulatory mechanisms. When determined in cells that share the same identity by the a specific developmental process can be matched with action of distinct regulatory modules, such as pericycle specific anatomical or morphological features, those fea - cells induced into either lateral root primordium found- tures represent structural n fi gerprints of the activity of ers or cork cambium initials by the integration of differ - regulatory mechanisms that control that process (Fig. 2). ent developmental cues into distinct regulatory modules In other words, in such cases studying morphology can [37]. At a broader biological scale, there is evidence for teach us about developmental regulation. In plants, spe- regulatory mechanisms transferred between the gameto- cifically, identification of such fingerprints is facilitated phyte and sporophyte generations [38–42]. by the fact that the position of cells is largely fixed; cells In an evolutionary perspective, the modularity of are attached to each other by their walls, in the posi- developmental regulation allows for broad variation in tion in which they arise by cell division. As a result, the the organization of ontogenetic trajectories over evolu- relative arrangement of cells records sequences of cell tionary time, with different phenotypic outcomes in dif - division, allowing for more detailed reconstruction of ferent organisms. The roots of variability reside in the developmental processes. Such is, for instance, the easily degree of integration of the modules, which can be more distinguishable patterning of merophytes that form from or less tightly integrated—i.e., interacting with, influ - immediate derivatives of the apical cell and show corre- enced by or dependent on, each other—in ways that can sponding arrangements around and behind the latter in be hierarchical or not. Variability also arises from the bryophyte or equisetalean apical meristems (Fig. 3a–d); combinatorial nature of the activation (or lack thereof ) of or the arrangement of cells in cross sections of second- different modules—i.e., different modules being turned ary tissues, which records the sequence of past periclinal on or off separately or in concert—at different stages in and anticlinal divisions in the cambial initials (Fig. 3e–h). ontogeny. Together, these sources of variation underpin Similarly, at a larger scale, the patterns of sporangiophore a vast amount of potential diversity in ontogenetic trajec- (i.e., fertile appendage) numbers and sizes along equise- tories, able to generate an equally vast amount of poten- talean fertile internodes (Fig. 3i) record the polarity of tial phenotypic diversity. Such potential provides the raw meristematic activity in intercalary meristems (Fig. 3j). material for morphological evolution. Thus, for example, Although genetic regulation, which results in structural analyses of plant comparative morphology across evolu- features of plants, is a transitory process not available for tionary time and phylogenetic space have assembled data direct examination from fossils, these features—struc- that indicate different pathways of accretion of complex - tural fingerprints—do accurately reflect the regulatory ity in different lineages [43, 44], and support hypotheses genetics by which they were produced. Therefore, when (See figure on next page.) Fig. 3 In plants, cells are attached to each other by their walls, in the position in which they arise by cell division. As a result, the relative arrangement of cells records sequences of cell division, allowing for reconstruction of developmental processes. The arrangement of cells at the tip of Physcomitrium moss embryos (a, b) reveals growth from an apical cell (images courtesy of C. Jill Harrison); embryo outlined in blue inside the archegonium in a, orange lines emphasize the cells arrangement. The patterning of merophytes formed from derivatives of the apical cell is easily distinguishable in longitudinal sections of Equisetum root (c) and shoot (d) apical meristems and reflects the sequence of divisions of the apical cell; root and stem merophytes traced in orange; root cap merophytes traced in brown in c. Anticlinal (multiplicative) divisions (between arrowheads in e) of vascular cambium initials produce additional files of cells observed in cross sections of secondary tissues (in a Pinus stem). “Doubled” tracheid files (arrowheads in f) are fingerprints that reveal the exact location and timing (measured in wood thickness or growth rings) of symmetric divisions of the cambial initials. Asymmetric divisions of cambial initials initiate rays (arrowhead in g), whose inner ends (arrowhead in h) mark the position and timing of the asymmetric division. Patterns of sporangiophore numbers and sizes along fertile internodes of the Permian equisetalean Cruciaetheca (i) record the basipetal direction of tissue and organ maturation within internodes (j), generated by growth from intercalary meristems; sporangiophores in red, in the image tracing in i and in the diagram in j; internodes gray in i; nodes gray in j; j modified from [47]. Scale bars 20 µm in (a, b); 50 µm in (c, d); 20 µm in (e–h); 1 cm in (i) Tomescu and Rothwell EvoDevo (2022) 13:8 Page 6 of 19 Fig. 3 (See legend on previous page.) T omescu and Rothwell EvoDevo (2022) 13:8 Page 7 of 19 structural fingerprints are identified in fossils, they can upstream of locations where polar auxin flow in the cam - be employed to infer the specific regulatory mechanisms bium has been impeded by obstructions, such as axillary by which they developed [46] (Fig. 2). Because in living buds and lateral branches [48, 55, 56]. Such “auxin swirls” plants we can tie these fingerprints to specific, detailed therefore represent anatomical fingerprints for polar regulatory mechanisms, we can circumscribe the exact auxin regulation of secondary xylem patterning and were nature of regulatory modules and of interactions within the first structural fingerprint to be recognized in fossil and between modules that generate the structural finger - plants [3, 46]. prints. If compared between extant plant lineages, this Because xylem has excellent fossilization potential, type of information can reveal the degree of variation wood anatomy is among the most common sources of in the structure and interactions of regulatory modules data in the plant fossil record. Herein, swirls of tracheary that characterize different lineages. Studies that integrate elements provide powerful evidence (1) for polar auxin structural fingerprints and molecular-genetic regulation transport as a regulatory mechanism of tissue pattern- in living plants allow us to infer the same relationships ing during vascular cambial growth shared among sev- between gene regulation and structure in extinct plants. eral major plant clades [57], and (2) for the antiquity of This opens up a whole new window onto the evolution of polar auxin regulation in secondary tissue patterning. development, by allowing us to trace the presence of reg- This demonstrated shared mechanism suggests that at ulatory processes and the activity of specific regulatory least some of the basic regulatory elements in the con- modules in phylogenetic space and evolutionary time. In trol of secondary growth may have been part of a devel- other words, this methodology allows us to connect the opmental toolkit shared among all euphyllophytes, or regulatory genetics of living forms to their long-extinct even all tracheophytes [45, 58]. The same structural ancestors and precursors (or, at least, to form hypothe- fingerprint identified in the rooting structures (rhizo - ses about such connections) within an empirically based morphs) of Pennsylvanian (c. 310 million-years) arbo- framework (e.g., [47]). rescent lepidodendralean lycophytes demonstrated that For example, if a particular regulatory pathway is these positively gravitropic axes have acropetal auxin shared by sister clades, then we can hypothesize that transport, unlike the shoots to which they are homolo- they share a common developmental tool kit which has gous [59], and similar, instead, to other rooting structures been inherited from a common ancestor that possessed with different homologies [60, 61]. In turn, this shared that tool kit [3]. Those hypotheses can then be tested by directionality of polar auxin transport implies that acro- searching for the structural fingerprint of those tool kits petal auxin flow transcends organ identity and is more in specimens of the common ancestor (or extinct sis- tightly linked to positively gravitropic axes, independ- ter group) of the two clades. An example of that sort of ent of their homology [62]—whether they be roots (as hypothesis test is presented below for the role of polar in most extant tracheophytes), modified shoots (in isoe - auxin regulation in the development of vascular tissue. talean and lepidodendrid lycophyte rhizomorphs, and in drepanophycalean lycophyte rooting axes), rhizophores A quintessential structural fingerprint and its (in Selaginella), or simple undifferentiated axes (in zos - implications terophylls) (Fig. 4). Regulation of both primary and secondary vascular tis- sue production (specification, differentiation) by the Combining structural fingerprints directional transport of auxin (polar auxin transport) is By the beginning of the Silurian (444 million-years ago), probably a common denominator of development in vas- the first members of the clade characterized by branched cular plants, wherein it evolved increasing sophistication sporophytes and including all vascular plants (i.e., poly- at successively more derived levels of their phylogeny [3, sporangiophytes), had emerged [63] out of a plexus of 48, 49]. Studies in angiosperms have demonstrated that early embryophytes whose earliest bryophyte-grade rep- polar auxin transport and the auxin gradients it gener- resentatives go at least as far back as the Middle Ordo- ates, established early in embryogenesis, are responsible vician (468 million-years ago; [64]). If trilete spores are, for primary vascular architecture (procambium specifi - indeed, exclusively characteristic of vascular plants and cation, vascular tissue differentiation), as well as cambial not of all the embryophytes, as has been proposed by identity and functioning in secondary growth (e.g., [50– Steemans et al. [65], then vascular plants and, by exten- 54]). During secondary growth from a vascular cambium, sion, polysporangiophytes may have evolved as early as polar auxin regulation of cell positioning and growth 455 million-years ago, around the beginning of the Late direction produces characteristic circular patterns in Ordovician [66, 67]. Direct information on these plants is specific positions in the secondary xylem. These pat - available exclusively from fossils, which provide multiple terns consist of swirls of tracheary elements positioned structural fingerprints that when combined, allow us to Tomescu and Rothwell EvoDevo (2022) 13:8 Page 8 of 19 Fig. 4 In contrast to the shoots (green), polar auxin transport (PAT; depicted by blue arrows) is acropetal in the roots of seed plants and the rhizophores of selaginellalean lycopsids, whose homologies are equivocal. Additionally, fingerprints for the directionality of PAT demonstrate that the rhizomorphs of lepidodendralean lycopsids, which are shoot homologs with rooting function, also had acropetal PAT [60]. This shared directionality of PAT implies that acropetal auxin flow transcends organ identity and is more tightly linked to the positively gravitropic response or rooting function of axes (gray), independent of their homology. In turn, this suggests that the positively gravitropic axes with rooting functions produced by K-branching in zosterophylls with simple body plan may also have had acropetal PAT (dashed blue arrows) reconstruct the morphology and life history of these tra- Devonian (c. 410 million-years old) polysporangiophytes cheophyte ancestors. such as Aglaophyton, Rhynia, Horneophyton or Nothia Early polysporangiophytes had diminutive sporophytes [70]. This inference is based on the thalloid form of fos - that were only little more than branched versions of bry- sils found associated with (but not attached to) branched ophyte-grade sporophytes [4]. The small size of the spo - sporophytes in Silurian and Early Devonian layers at rophytes is immediately apparent in the fossils [23, 63]. multiple locations [71, 72]—some of which bear transfer The branching of these sporophytes indicates that they cells typical of the gametophyte–sporophyte connection grew from apical meristems, but their diminutive size, in bryophytes [24]—and on structural and chemical evi- scant branching, and presence of sporangia terminating dence that some of these fossils are plants [73–75]. all branches (e.g., [1, 4, 63]) indicate that their meris- tematic growth was determinate. The small size of these Echoes of modularity sporophytes also supports the hypothesis that they were The leaves of ferns and seed plants nutritionally dependent on the gametophytes [23], like The Euphyllophytina is the largest and most diverse of the sporophytes of bryophytes. The dependence of spo - the two major clades of living vascular plants, and is rep- rophytes on the gametophytes is also consistent with the resented in the modern flora by seed plants (flowering inference that their growth was determinate. Recently it plants, gymnosperms) and several lineages of seed-free has become apparent that these early sporophytes had plants (marattialean, ophioglossalean, and leptospo- specialized photosynthate-conducting cells similar to rangiate ferns, equisetaleans, and psilotaleans—i.e., those of bryophytes [1], but it is less clear whether the Psilotum and Tmesipteris). The overwhelming major - earliest polysporangiophyte sporophytes possessed tra- ity of the extant euphyllophytes show stem–leaf–root cheid-based water-conducting tissues, as the oldest tra- organography in their vegetative sporophyte; excep- cheids discovered to date are significantly younger—424 tions include a few highly derived angiosperms with million-years old [68]. This is close to the (slightly older, reduced or incompletely differentiated sporophytes (e.g., ca. 432 million-years) age of the oldest known sporo- Podostemaceae, Lemnaceae), ferns (e.g., Salvinia lack- phytes that reached sizes consistent with physiological ing roots) and psilotaleans (which lack roots entirely and independence [69]. whose lateral appendages may or may not be reduced The gametophytes that supported these diminu - leaves; [76]). Because of this, early phylogenetic analy- tive sporophytes were probably thalloid, like those of ses of living species have inferred that the derived stem– hornworts and liverworts and unlike those of younger, leaf–root organography has evolved only once among T omescu and Rothwell EvoDevo (2022) 13:8 Page 9 of 19 euphyllophytes [77]. However, all members of the basal Adaxial–abaxial polarity is reflected in the flattened grade of fossil euphyllophytes, referred to as trimero- morphology of leaves and, even in the absence of this phytes, have plesiomorphic sporophyte morphology morphology, can be ascertained based on the bilateral consisting of simple branching axes that were vascular- patterning of the vascular tissues that supply these lat- ized and bore sporangia, but were not differentiated into eral appendages (i.e., phloem positioned abaxially and roots, stems and leaves. The absence of leaves in the tri - xylem adaxially). Using structural fingerprints for the two merophytes, coupled with their phylogenetic position leaf-defining features—leaf morphology for determinate among euphyllophytes [21, 78], and with fossil evidence growth and polarity of leaf vascular tissues for adaxial– for the evolution of euphyllophyte leaves [79, 80], pro- abaxial polarity—and querying the fossil record of early vide compelling evidence that leaves evolved indepen- ferns and seed plants, Sanders et al. [79] demonstrated dently and in parallel, from such leafless trimerophytes, that whereas seed plants evolved determinate growth in several different euphyllophyte lineages [81]. Thus, the before adaxial–abaxial polarity in the leaves, in filicalean leaves of different euphyllophyte clades that appear to be fern leaves evolution of adaxial–abaxial polarity preceded homologous to neontologists, actually resulted from par- determinacy (Fig. 5). Aside from supporting hypoth- allel evolution [78–82]. This is one of the most compel - eses of independent evolution of leaves in ferns and ling examples of fossils and morphology allowing for the seed plants, reflecting different trajectories in terms of recognition of analogy (or homoplasy; similar characters sequence of character evolution, this is consistent with a in two groups that evolved independently by parallel or modular nature of the regulators of leaf determinacy and convergent evolution) and its distinction from homology adaxial–abaxial polarity, which allows for independence (i.e., characters in two groups that are inherited from a in the deployment of these two features. Thus, structural common ancestor that had those characters). fingerprints for developmental mechanisms preserved in Two main structural changes that have led to the evolu- fossils provide evidence for the modular nature of spe- tion of leaves from leafless trimerophyte axes are (1) the cific aspects of leaf developmental regulation. change from indeterminate to determinate growth, and Venation is an additional facet of leaf (or pinnule) (2) the origin of abaxial–adaxial patterning in the transi- organization that reveals structural fingerprints of the tion from radial to bilateral growth [83]. Leaves of living meristematic activities which generated it. Tracking the euphyllophytes typically have both determinate growth deployment of these activities across plant phylogeny and and bilateral (abaxial–adaxial) polarity, and available evi- the fossil record reveals further evidence for the parallel dence suggests that each of these properties is controlled evolution of leaves within Euphyllophytina. The paleon - by distinct regulatory modules. Because data available tological record documents leaf evolution within several currently on gene expression patterns offer only a spotty clades of Paleozoic euphyllophytes and provides direct coverage of the taxonomic breadth of living euphyllo- evidence for parallel changes in pinnule structure and phytes, and because those data are not matched in terms leaf venation in each [80]. Specifically, the fossil record of taxonomic coverage by data on gene function, infer- demonstrates that in each of at least four clades (i.e., seed ences on gene functions in different lineages can only plants, ferns, equisetaleans, and progymnosperms) the be tentative at this point. Nevertheless, recurrent pat- most ancient representatives produced ultimate lateral terns of expression, some of which are complemented units (e.g., pinnules) that had linear laminar segments by functional data, provide indications on putative gene with marginal vein endings, and that successively more functions. For instance, meristematic activity at the shoot recent representatives progressed through parallel modi- apex is probably maintained by class I KNOX genes and fications to (1) divergent venation with marginal vein LFY in both ferns and angiosperms (at least insofar as endings; (2) convergent venation with marginal vein end- this can be predicted based on studies in model species). ings; (3) reticulate venation with marginal vein endings; These genes are probably also responsible for prolifera - and (4) reticulate venation with internal vein endings tive growth in the leaves of both ferns and angiosperms (summarized by Rothwell et al. [3]). Although the com- (e.g., compound leaves) [81, 84–87]. Thus, determinacy plete series of structural/meristematic modifications was of growth in leaves may well reflect the evolution of achieved in only ferns and seed plants, these parallel evo- regulatory mechanisms that repress these genes, such as lutionary trajectories of leaf venation represent structural the ARP group genes that repress KNOX I gene activity. fingerprints for a succession of parallel changes in the Similarly, adaxial–abaxial polarity (sometimes referred to meristems that contributed to the evolution of euphyl- as dorsiventral polarity) seems to result from the expres- lophyte leaves (or their ultimate segments in the case of sion of, and interactions between, class III HD-ZIP genes compound leaves) in all four clades. (promoters of adaxial identity) and KANADI genes (pro- moters of abaxial identity), in all euphyllophytes [88–90]. Tomescu and Rothwell EvoDevo (2022) 13:8 Page 10 of 19 Fig. 5 Euphyllophyte leaves are thought to have evolved from lateral branching systems like those seen in early representatives of the clade (e.g., Psilophyton). Structural fingerprints for adaxial–abaxial polarity (dorsiventral polarity) observed in fossils indicate that whereas seed plants evolved determinate growth before adaxial–abaxial polarity in the leaves, in filicalean fern leaves evolution of adaxial–abaxial polarity preceded determinacy. The early fern Psalixochlaena exhibits adaxial–abaxial polarity in its leaves (i.e., protoxylem on the adaxial side and phloem on the abaxial side of the leaf vascular bundle cross-sectioned in the figure), which had indeterminate growth; in contrast, the leaves of the early seed plant Elkinsia had determinate growth but their vascularization had radial symmetry (protoxylem surrounded by metaxylem in the vascular bundle cross-sectioned in the figure), at least in their terminal segments. This observation provides one of the lines of evidence supporting independent evolution of leaves in ferns and seed plants Secondary growth that vascular cambial growth originated independently in The modularity of developmental regulation takes on the different lineages. This perspective has its roots in the a much broader scope if we consider the evolution of perceptions that (1) the first occurrences of secondary vascular cambial growth (secondary growth) and the growth in the different lineages are much younger than diversity of modes of secondary growth that have arisen the origin of tracheophytes; and (2) that the anatomy of among tracheophytes. One of the major unanswered secondary tissues shows significant differences between questions regarding the evolution of secondary growth is major lineages [92]. whether vascular cambial growth evolved independently The traditional view on the evolution of vascular cam - in different tracheophyte lineages or only once, at the bial growth is currently reshaped by evidence coming base of the clade. The fossil record demonstrates that vas - from two directions. First, anatomical evidence suggests cular cambial growth was present, outside of seed plants, that some mechanisms regulating cambial growth, such in multiple currently extinct tracheophyte lineages that as control by polar auxin transport of cambial identity go back to the Middle Devonian (c. 390 million-years and activity, are shared among major tracheophyte lin- ago) [91]. Based on these, the traditional view has been eages that span the lycopsids and the euphyllophytes: T omescu and Rothwell EvoDevo (2022) 13:8 Page 11 of 19 lepidodendrales, equisetaleans, progymnosperms, and comparative studies. Irrespective of the latter, this possi- spermatophytes [57, 60, 93]. Second, accumulating dis- bility prompts the question: could regulation of vascular coveries [58, 94–96] point to much earlier origins of vas- cambial growth have originated in the common ances- cular cambial growth than previously thought, at least in tor of euphyllophytes, or even the common ancestor of the euphyllophyte clade. Together, these lines of evidence euphyllophytes and lycopsids? suggest that regulators of secondary growth may have To begin answering this question, Tomescu and become part of the euphyllophyte developmental toolkit Groover [45] have proposed an updated perspective that very early in the evolution of the clade. Unfortunately, approaches vascular cambial growth as a complex devel- comparative genomic approaches cannot be applied to opmental process that is highly modular (Fig. 6). In this address this because, aside from seed plants, all other perspective, the diverse anatomies of secondary tissues euphyllophyte lineages with cambial vascular growth seen in different extinct lineages (and which represent are extinct, thus allowing recourse only to anatomy for diverse modes of secondary growth) reflect a mosaic Fig. 6 A perspective proposed by Tomescu and Groover [45] (top panel) regards vascular cambial growth as a complex modular developmental feature that is the sum of multiple component processes, each controlled by an independent regulatory module. In this perspective, component processes are deployed in a mosaic pattern among plant lineages, and their different combinations result in as many distinct modes of secondary growth. If each component process leaves a structural fingerprint in the anatomy of secondary tissues, the combinations of component processes can be inferred for the modes of secondary growth observed in the fossil record. This perspective allows for a basic set of component processes that could have defined a hypothetical single common origin of secondary growth across tracheophytes (or across euphyllophytes), underpinned by a basic toolkit of corresponding regulatory modules representing a deep homology (sensu Shubin et al. [99]) in the clade. In the traditional perspective on secondary growth (bottom panel), the implicit assumption was that of vascular cambial growth as a unitary developmental feature that was assembled de novo in each taxonomic group that evolved secondary growth independently and in parallel with other groups Tomescu and Rothwell EvoDevo (2022) 13:8 Page 12 of 19 pattern of expression of distinct, more-or-less independ- understanding of structural fingerprints characteristic for ent developmental regulatory modules. Although they specific developmental processes, combined in the con - are as yet poorly circumscribed or simply unidentified text of an evolutionary-developmental perspective that is [45], these hypothesized regulatory modules are thought rooted in modularity of developmental regulatory mech- to be individually responsible for different component anisms, can contribute to the construction of testable processes that comprise secondary growth (Fig. 7)—e.g., hypotheses about the evolutionary origins of secondary symmetrical or asymmetrical anticlinal divisions of cam- growth. bial cells, bidirectional production of new tissues. The distinctiveness and independence of the hypothesized Modularity and hierarchy regulatory modules are supported by anatomical obser- Within the paradigm of modularity in developmental reg- vations and developmental experiments and could be ulation, information preserved in fossils and recognized as tested, in principle, by altering the activity of different structural fingerprints for specific developmental regula - modules, when the regulatory interactions that control tors can also lead to inferences of hierarchy in the deploy- vascular cambial growth are better circumscribed. ment of regulatory modules. An example is the case of Importantly, the activity of the different regulatory the regulatory mechanisms that underlie the reproductive modules proposed by Tomescu and Groover [45] can morphologies of living and extinct equisetaleans of the be recognized based on specific anatomical fingerprints family Equisetaceae. The strobilus of Equisetum has been that are preserved in the wood (secondary xylem) and for a long time a puzzle in terms of homology and mor- adjacent tissues of plants, including fossil plants. The phological evolution. The different types of reproductive presence or absence of these fingerprints in the wood morphologies found in fossil relatives of Equisetum that of different lineages (Fig. 7) suggests that the regulatory go back to the Permian (c. 290 million-years ago) had cre- modules are deployed differently among different line - ated a stalemate in the interpretation of the homology of ages, living and extinct—some are shared among mul- the strobilus (reviewed by Ref. [47, 97]). The contradictory tiple lineages, while others are apomorphic for distinct homology implications of the different types of reproduc - lineages. Thus, information preserved in fossils and an tive morphologies stemmed from rigid application of the Fig. 7 Structural (anatomical) fingerprints (in black, at left) preserved in the secondary tissues of plants living and extinct provide evidence for specific component processes of vascular cambial growth (in purple, at left) and the activity of their corresponding regulatory modules. Different combinations of such fingerprints define the distinct modes of secondary growth that differentiate seed plants from extinct sphenophyllalean sphenopsids and zygopterid ferns T omescu and Rothwell EvoDevo (2022) 13:8 Page 13 of 19 morphological model of the shoot as an alternation of lead to determinate apical growth, and (3) repress node- nodes and internodes. In brief, the frustrating question internode differentiation and intercalary meristematic was: Are the sporangium-bearing appendages (sporan- activity in the fertile phytomers, respectively. Whether giophores) attached at the nodes or along the internodes? these hypotheses on the existence and functions of regu- This was important for understanding whether the stro - latory modules could be tested experimentally by alter- bilus of Equisetum is homologous to multiple nodes, each ing developmental regulatory pathways (e.g., repressing bearing a single whorl of sporangiophores, or to a single growth determinacy in the strobilus meristem by overex- internode with multiple sporangiophore whorls attached pressing KNOX I family genes) will depend on our ability along it. This is a fundamental question with implications to genetically manipulate living Equisetum, a capability for morphological evolution in one of the major tracheo- that has yet to be achieved. phyte lineages—represented today solely by the genus From an epistemic standpoint, this case study demon- Equisetum, the equisetalean clade in an excellent example strates how a hypothesis generated by data from living of a long phylogenetic branch wherein homology issues plants is tested and confirmed using data from the fos - can only be resolved by querying the rich fossil record of sil record [61]. In turn, this provides a framework for the group [98]. subsequent hypotheses that included data from living Studies of development in living Equisetum show that Equisetum and fossil plants, to offer a novel explanation, shoots grow as a result of the combined activity of the api- involving a hierarchy of regulatory modules, of the ori- cal meristem, which generates phytomers, and intercalary gin of the Equisetum strobilus and other reproductive meristems, which are responsible for elongation of the morphologies of fossil equisetaleans. This updated per - internode in each phytomer. This suggested that an empha - spective on the Equisetum strobilus generates further sis on the phytomeric structure of the shoot, rather than the hypotheses about evolution and the deep fossil record, node-internode alternation, may provide a more appropri- explaining the origin and evolution of the equisetalean ate paradigm within which to understand homology in the sporangiophore, all of which are possible only because Equisetum strobilus and, more broadly, in equisetacean developmental and evolutionary data have been pre- reproductive morphology [47]. At the same time, current served in the fossil record. understanding of plant developmental regulation indicates (1) that meristems of all types are equivalent in their fun- Conclusions damental capacities, including the capacity to transition to The paleontological record provides the best evidence reproductive growth (except for root apical meristems); and for evolutionary pattern. Using structural fingerprints (2) that at least some of the regulatory mechanisms effect - for plant development, we can also address fundamental ing this transition are shared broadly among tracheophytes questions about evolutionary process. Studies applying [47]. Together, these observations led to the hypothesis that the epistemic framework of this paleo-evo-devo perspec- in equisetaceans the switch to a reproductive developmental tive and methodology illuminate our understanding of program happens in the intercalary meristems responsible how evolution proceeds by successive modifications of for internode elongation and, as a result, sporangiophore plant development, which are controlled, in turn, by the whorls are produced along the internodes of fertile phytom- activities of regulatory genes and growth regulators. This ers and follow a basipetal sequence of maturation (Fig. 3j). approach further clarifies that developmental regulation The hypothesis of reproductive growth in internode of plant growth is both modular and hierarchical. When intercalary meristems generates predictions (i.e., hypoth- coupled with another base of knowledge informed by the eses) about morphological patterns produced by such a fossil record—our understanding of the overall pattern mode of development. These morphological patterns of plant phylogeny—characterization of such develop- can be used as structural fingerprints (i.e., hypothesis mental modules, of the lineages in which they have been tests), which can be recognized in the equisetacean fossil deployed, and of the order in which they have accumu- record, confirming the presence of intercalary reproduc - lated in divergent lineages, provide a backbone for iden- tive growth (Fig. 3i, j), the only instance of its kind known tifying both the specific processes and the patterns by in tracheophytes [47]. This confirmation provides an which evolution has proceeded. Continued exploration updated framework for understanding the origin of the of three directions—(1) the composition, structure, and Equisetum strobilus and of other reproductive morpholo- functioning of gene regulatory networks that underpin gies present among equisetacean equisetaleans. These all aspects of the morphological variety seen across the different morphologies are best explained as resulting diverse extant plant lineages; (2) the distinct morpho- from deployment of independent regulatory modules in logical and anatomical signatures (i.e., structural fin - a hierarchic sequence (Fig. 8): the regulatory modules gerprints) of regulatory modules that are shared among (1) turn on reproductive growth in the phytomer, (2) multiple extant lineages; and (3) the occurrence of such Tomescu and Rothwell EvoDevo (2022) 13:8 Page 14 of 19 Fig. 8 The realization that a reproductive program can be activated in the intercalary meristem of individual equisetacean internodes, leading to development of sporangiophores along them, opened up a new avenue for interpreting the reproductive structures of extinct (Cruciaetheca, Peltotheca) and living (Equisetum) equisetaceans as illustrating a cumulative sequence of deployment (gray arrow at top) of independent regulatory modules for three developmental processes (in purple, at bottom) responsible for the different features (in black, at bottom) that characterize specific reproductive morphologies; cross bars separate phytomers in the shoot diagrams and phytomers bearing sporangiophores are red; modified from [47] Funding fingerprints in the fossil record, across geologic time and Open Access funding provided by Ohio University. phylogenetic space—will lead to deeper and more mean- ingful integration of data from the fossil record in the Availability of data and materials Not applicable. overall tapestry of the evolution of development through- out the history of plant life. Declarations Acknowledgements We thank Jill Harrison for the invitation to contribute to this issue and support Ethics approval and consent to participate throughout the editorial process, as well as for sharing Physcomitrium embryo Not applicable. images. We are also indebted to Dennis K. Walker for producing the Equisetum root tip slide. Insightful comments from two anonymous reviewers improved Consent for publication the manuscript significantly. Not applicable. Authors’ contributions Competing interests AMFT and GWR developed the project, wrote the paper and approved the The authors declare that they have no competing interests. final manuscript. Both authors read and approved the final manuscript. T omescu and Rothwell EvoDevo (2022) 13:8 Page 15 of 19 Glossary embryo within the arche- Acropetal (1) movement (e.g., of a gonium, with living repre- hormone) from the base sentatives that are assign- toward the apex of an able to vascular plants and organ. (2) Pattern of tissue bryophytes (i.e., mosses, maturation along a struc- liverworts and hornworts). ture or organ, in which the The term embryophytes is basal region is the earliest synonymous to land plants to mature and tissue matu- and Kingdom Plantae. ration progresses toward Equisetaleans Major clade of vascular the tip (distal region) of the plants that includes living structure or organ. Anto- Equisetum and fossil repre- nym: basipetal. sentatives that extend back Anticlinal division Orientation of the plane of through time to at least the cell division perpendicular Late Devonian. to the outer surface of an Euphyllophytes One of the two major organ. clades of vascular plants Axis (pl.: axes) Ancestral vegetative organ that includes as living of polysporangiophytes representatives the flow - and tracheophytes that ering plants, gymno- branches to produce more sperms, ferns (maratti- than one terminal sporan- aleans, ophioglossaleans, gium, and that has, via evo- and leptosporangiates), lution, given rise to stems, equisetaleans (i.e., Equi- leaves, and roots that char- setum), and psilotaleans acterize the sporophytes of (i.e., Psilotum and Tmesip- living vascular plants. teris); informal name for Basipetal (1) movement (e.g., of a Sub-division Euphyllophy- hormone) from the apex tina of Kenrick and Crane toward the base of an [21]. Euphyllophytes are organ. (2) Pattern of tissue the sister group of lyco- maturation along a struc- phytes (Sub-division Lyco- ture or organ, in which the phytina). Several extinct apical region is the earliest pteridophyte-grade groups to mature and tissue matu- (including the earliest rep- ration progresses toward resentatives of the clade, the base (proximal region) named trimerophytes) are of the structure or organ. also euphyllophytes. Antonym: acropetal.Gametophyte Haploid multicellular Derivative of an apical phase of the embryophyte cell (apical cell derivative) Cell produced directly by life cycle that develops by the division of an apical mitosis from a spore, and cell. that consists of a vegeta- Determinate growth tive body and one or more (n., determinacy) Gr owth pattern in which gametangia that produce growth ceases once a set gametes. developmental checkpoint Indeterminate growth Growth pattern in which is reached. Antonym: inde- growth continues indefi- terminate growth. nitely throughout the life Embryophytes Major group of strepto- span of the organism. phytes that produce an Antonym: determinate Tomescu and Rothwell EvoDevo (2022) 13:8 Page 16 of 19 growth. that is tightly integrated Intercalary meristem The mer istematic region internally (by interactions at the base of each inter- among a subset of the com- node, found in some plant ponent parts of the system) groups, such as the equi- but relatively independent setaleans and grasses from other such units. (Poaceae). Node Position along a stem Internode Length of stem between where one or more leaves two successive positions are attached. where leaves are attached Phytomer Modular unit of a shoot (i.e., nodes). consisting of one node Lycophytes One of the two major (with the attached leaf) clades of vascular plants and the subtending that includes as living rep- internode. resentatives the lycopsids Polysporangiophytes The clade of embryophytes Lycopodium s.l., Phyllo- (land plants) that share the glossum, Selaginella, and branched sporophyte as a Isoetes; informal name for synapomorphy (informal Sub-division Lycophy- name for Super-division tina of Kenrick and Crane Polysporangiomorpha of [21]. Lycophytes are the Kenrick and Crane [21]). sister group of euphyl- Psilotaleans (Psilotales) The clade of homosporous lophytes (Sub-division vascular plants consisting Euphyllophytina). Several of the two living genera extinct groups, includ- Psilotum and Tmesipteris. ing lepidodendrid and No fossils of this clade have pleuromeialean lycopsids, been discovered to date. drepanophycaleans, and Regulatory module Subset of regulatory inter- the earliest representa- actions (i.e., module; see tives of the clade, named definition of modular - zosterophylls, are also ity above) that are tightly lycophytes. integrated internally, but Merophyte Group of clonally related can act largely independ- cells resulting from ent of other such subsets sequential cell divisions (or modules) of a broader that originate in a sin- system of regulatory inter- gle derivative of the api- actions and is responsible cal cell of a meristem. The for a well-circumscribed arrangement of mero- developmental or morpho- phytes with respect to each logical outcome. other may reflect the order Rhizomorph Rooting organ of isoe- and pattern of cell divi- talean lycophytes, includ- sions by which they have ing the living Isoetes and been produced. lepidodendralean trees, Modularity, module Property of complex sys- that is derived from (i.e., tems that refers to the rela- homologous to) a shoot or tive degrees of connectiv- shoot system. ity or integration between Shoot Vegetative organ system component parts of the of vascular plants that system. Within a modular consists of a stem and the system, a module is a unit leaves that it produces. T omescu and Rothwell EvoDevo (2022) 13:8 Page 17 of 19 Sporangiophore Reproductive organ of gene interactions/regula- equisetaleans consisting tory module), and whose of an appendage bear- presence in an organism ing sporangia. Sporan- is used as evidence for the giophores are thought to activity of that regulator. have evolved from fertile Thalloid Type of plant body with- lateral branching systems out complex organization, of trimerophyte-grade especially lacking distinct euphyllophytes (see defi- stems, leaves or roots. nition of euphyllophytes Many bryophytes have above). In the only living thalloid sporophytes, and equisetalean, Equisetum, many homosoprous vas- sporangiophores are pel- cular plants have thalloid tate in shape, with a nar- gametophytes. row stalk and a broad head Tracheophyte Another name for vascu- that bears sporangia on its lar plants, a group char- underside (i.e., the side that acterized by sporophytes faces toward the subtend- possessing specialized ing stem). water- and photosynthate- Sporophyte Diploid phase of the conducting tissues, which embryophyte life cycle that include specialized water- develops by mitosis from a conducting cells (i.e., trac- zygote, passes through an heids, vessel elements). embryo stage, and consists Transformational series A s equence of different of a vegetative body that species that depict the bears one or more sporan- transformation of one spe- gia, which produce haploid cific type of structure to spores by meiosis. another. Transformational Stem Evolutionarily derived series of fossils through organ of vascular plants time constitute the tra- that consists of an alterna- ditional paleontological tion of nodes and inter- evidence for organismal nodes, as well as a succes- (morphological) evolution. sion of phytomers, bears Author details leaves at the nodes, has Department of Biological Sciences, California Polytechnic State University Humboldt, Arcata, CA 95521, USA. Department of Environmental and Plant complex internal struc- Biology, Ohio University, Athens, OH 45701, USA. Department of Botany ture, and may have inde- and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA. terminate growth (see Received: 28 September 2021 Accepted: 29 January 2022 definitions of axis, inter - node, node, and phytomer above). Strobilus (pl.: strobili) Agg regation of sporan- References gium-bearing appendages 1. Edwards D, Morris JL, Axe L, Duckett JG, Pressel S, Kenrick P. 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Publisher: Springer Journals
Copyright: Copyright © The Author(s) 2022
eISSN: 2041-9139
DOI: 10.1186/s13227-022-00192-7
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Abstract

Fossils constitute the principal repository of data that allow for independent tests of hypotheses of biological evolu- tion derived from observations of the extant biota. Traditionally, transformational series of structure, consisting of sequences of fossils of the same lineage through time, have been employed to reconstruct and interpret morpho- logical evolution. More recently, a move toward an updated paradigm was fueled by the deliberate integration of developmental thinking in the inclusion of fossils in reconstruction of morphological evolution. The vehicle for this is provided by structural fingerprints—recognizable morphological and anatomical structures generated by (and reflective of ) the deployment of specific genes and regulatory pathways during development. Furthermore, because the regulation of plant development is both modular and hierarchical in nature, combining structural fingerprints recognized in the fossil record with our understanding of the developmental regulation of those structures pro- duces a powerful tool for understanding plant evolution. This is particularly true when the systematic distribution of specific developmental regulatory mechanisms and modules is viewed within an evolutionary (paleo-evo-devo) framework. Here, we discuss several advances in understanding the processes and patterns of evolution, achieved by tracking structural fingerprints with their underlying regulatory modules across lineages, living and fossil: the role of polar auxin regulation in the cellular patterning of secondary xylem and the parallel evolution of arborescence in lycophytes and seed plants; the morphology and life history of early polysporangiophytes and tracheophytes; the role of modularity in the parallel evolution of leaves in euphyllophytes; leaf meristematic activity and the parallel evolu- tion of venation patterns among euphyllophytes; mosaic deployment of regulatory modules and the diverse modes of secondary growth of euphyllophytes; modularity and hierarchy in developmental regulation and the evolution of equisetalean reproductive morphology. More generally, inclusion of plant fossils in the evo-devo paradigm has informed discussions on the evolution of growth patterns and growth responses, sporophyte body plans and their homology, sequences of character evolution, and the evolution of reproductive systems. Keywords: Developmental regulation, Evo-devo, Fossil, Leaf, Modularity, Morphology, Rooting organ, Secondary growth, Strobilus, Structural fingerprint *Correspondence: mihai@humboldt.edu Department of Biological Sciences, California Polytechnic State University Humboldt, Arcata, CA 95521, USA Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Tomescu and Rothwell EvoDevo (2022) 13:8 Page 2 of 19 Fossils provide invaluable evidence of evolution At macroevolutionary scales, ecological crisis Since their earliest occurrences in the fossil record more is the driver of evolution than 400 million years ago, vascular plants have diversi- Of equal importance for documenting structural change fied tremendously. While living species are characterized through time, the fossil record provides convincing evi- by a sporophyte that is differentiated into a wide array of dence for the fundamental processes that underlie plant organs and parts, including stems, leaves, roots, sporan- evolution [3]. While evolution traditionally has been gia, seeds, cones, flowers, and fruits, the most ancient explained within the context of classical and population vascular plant sporophytes consisted of simple branch- genetics, as early as the 1970s tests of those traditional ing axes with terminal sporangia, a morphology that cur- evolutionary hypotheses using paleontological data rently seems to have preceded the evolution of typical began to reveal patterns of change over broader tempo- xylem and phloem [1]. Deeper in evolutionary time and ral scales additional to those predicted by genetics-based plant phylogeny, bryophyte-grade embryophytes pos- evolutionary theory at the population level [7]. Popula- sessed sporophytes consisting of little more than a single tion genetics theory predicts that natural selection is the sporangium [2]. The origin of the ancestral tracheophyte driving force for evolutionary change and that such selec- body plan and its transition from this simple organiza- tive forces are most impactful within well-established tion to the complex sporophytes present in most modern ecosystems. At macroevolutionary scales, the paleonto- tracheophyte lineages were accompanied by numerous logical record reveals that the most rapid evolutionary dramatic changes in plant structure [3, 4]. Understand- diversifications occur immediately after biological catas - ing these changes within a developmental framework is trophes, at moments when extinction has dramatically key to reconstructing plant evolution and phylogeny, reduced biotic selective pressures and has opened up and necessarily requires integration of data on develop- vast swaths of ecological space for colonization by new mental regulation, obtained from living plants, with data species [8, 9]. Both macroevolutionary theory (e.g., [10]) from the fossil record. To answer questions on the evo- and paleontologically established patterns of evolution- lution of development, studies of living plants focus on ary change indicate that the reestablishment of complex careful studies of gene expression and function with the plant communities leads to long periods of evolution- aim to gradually document regulatory pathways respon- ary stasis that witness only small-scale selection-driven sible for specific developmental processes. These studies evolutionary modification [11, 12]. Therefore, the fos - have made significant strides toward understanding the sil record reveals that evolutionary diversification is the principles of plant developmental regulation and have least rapid when genetically based evolutionary theory revealed the complexity of regulatory interactions which, predicts it should reach its highest rates. This apparent even in model species, are often still largely unknown. contradiction is mostly a matter of scale—natural selec- Additionally, sequencing of algal streptophyte and plant tion acts primarily as a filter removing maladapted phe - genomes and transcriptomes over the last decade has notypes at microevolutionary scales, and less as a driving opened opportunities for predicting the makeup of gene force at macroevolutionary scales [13–17]—and this is regulatory networks in different lineages, thus informing especially apparent within a paleontologically sanctioned hypotheses about the evolution of these networks (e.g., context. [5, 6]). Understanding morphological evolution—i.e., evolu- The evo‑devo paradigm and the role tionary changes in plant structure—within a develop- of morphology mental framework also necessitates in-depth knowledge A growing appreciation for the role of development in of both the intermediate stages that populate the differ - evolution, whose understanding has been dramatically ent trajectories of evolutionary change, and of the order elevated by the advent of developmental molecular biol- in which they occurred within each lineage. Most of ogy, has fostered an improved perception of evolutionary these intermediate stages of evolutionary changes that process [18, 19]. Within this context, we now recognize have transformed plants over time are not present among that the genome encodes the program that determines species of the modern flora, and are preserved only in ontogeny, and it is that program which evolves through the fossil record. Therefore, fossils provide vital evidence, time [3]. For each organism, the genetic program is unavailable otherwise, for understanding the origins of implemented through the processes of development. modern plant structure and for reconstructing the pat- As a result, the phenotype of an organism at any point terns of structural changes through time that have pro- during its ontogeny represents the cumulative structural duced the morphological diversity that characterizes evidence for the developmental processes that generated modern vegetation. it. In turn, these reflect the deployment of the genetic program, i.e., the activity of regulatory mechanisms that T omescu and Rothwell EvoDevo (2022) 13:8 Page 3 of 19 direct those developmental processes. Therefore, changes turn, allowed for branching. Evidence in support of this in the genetic program produce predictable changes in hypothesis is provided by apogamous sporophytes of the the phenotype of the resulting organisms, which we refer living moss Physcomitrium patens, wherein the combina- to as morphological evolution [20]. tion of gene silencing and auxin transport inhibition pro- For example, the origin of branching in the sporophyte duces a comparable heterochronic change that results in phase of the embryophyte life cycle was, alongside the an elongated and branched axial sporophyte body [22]. evolution of xylem and phloem, a seminal event leading Indeed, the oldest known branched sporophytes, which to the evolution of vascular plants [21]. That change may characterize the polysporangiophyte clade (Fig. 1), show be hypothesized to have resulted from the prolongation bryophyte-grade features, such as bryophyte-type pho- of the time during which the sporophyte underwent api- tosynthate-conducting cells in the absence of true trac- cal growth before going through a transition to reproduc- heids [1] and nutritional dependence on the gametophyte tive growth and the production of terminal sporangia [3, phase [23, 24]. 4]. According to this hypothesis, a change in develop- Because phenotypes are the direct result of develop- mental regulation in the early sporophyte stage of bry- ment under the control of genetic regulation, the wed- ophyte-grade plants resulted in the origin of potentially ding of paleontology (i.e., phenotypes through time) indeterminate growth from an apical meristem which, in with regulatory genetics (i.e., genomic changes leading Fig. 1 A phylogenetic framework for the groups discussed throughout the paper; a polygon denotes uncertainty in the relationships among different lineages of that group (mostly due to conflict between the results of different analyses); Trim = Trimerophytes Tomescu and Rothwell EvoDevo (2022) 13:8 Page 4 of 19 off without affecting the activity of other modules) [26]. Additionally, interactions among regulatory modules can be hierarchical. In an experimental study of vascular cambial growth in the angiosperm Ficus, Lev-Yadun [27] demonstrated that girdling induces transient production of wood in which rays develop normally but the axial system exhibits dra- matically altered anatomy, differentiating into isodia - metric parenchyma. Although the study did not address Fig. 2 Anatomical and morphological features seen in organisms directly the specific genetic and molecular factors that bear witness to the activity of specific regulatory modules. Studies control these developmental processes, this example of living organisms can identify the regulatory entities of specific developmental processes, which produce well-defined phenotypic illustrates both modularity and hierarchy of modules in traits. Such phenotypic traits, thus, represent structural fingerprints developmental regulation. The different effects that the of the deployment of those developmental regulators. In turn, girdling treatment had on the anatomy of the two systems identification of structural fingerprints in fossils provides evidence of secondary xylem—radial (rays) and axial (tracheary for the activity of their corresponding regulatory entities in extinct elements, xylem parenchyma, fibers)—indicates that the lineages, informing the evolutionary history of those regulators two aspects of development can proceed independently of each other. In turn, this implies that their regulation is uncoupled and, thus, distinct regulatory modules, at least to phenotypic changes) provides a framework for under- in terms of patterns of cell division and differentiation. standing the evolution of development (Fig. 2). Within Girdling, on the other hand, did not directly affect the this context, the developmental underpinnings of mor- three-dimensional organization of secondary xylem (into phology take on a much more central role in understand- two distinct systems), which suggests that this organiza- ing both the patterns and processes of plant evolution, tion is controlled at a different hierarchical level of devel - and the fossil record provides access to direct evidence opmental regulation. of that evolution. Building on data and ideas published Evidence for modularity in developmental regula- by ourselves and others, here we focus on the modular tion abounds in all biological systems and discussions of nature of developmental regulation emphasizing the developmental modularity provide a meeting place for role of fossils in supporting or generating hypotheses on developmental and evolutionary biologists [28]. The evi - modularity and its role in morphological diversity and dence is often provided by regulatory mechanisms whose evolution. These have never been considered together in activation—or lack thereof—is independent of their a comprehensive discussion of the role of fossils in docu- broader regulatory context, ontogenetic timing, or posi- menting the modular nature of development and its reg- tion of deployment, thus indicating that they represent ulation, which have otherwise been widely discussed in distinct regulatory modules. Such are the several regula- “neontological” evo-devo. tors that induce different histological differentiation or morphogenetic effects which, in different combinations, Developmental regulation is modular are responsible for distinct morphologies that bridge the and hierarchic reptilian scale to avian feather spectrum of tetrapod skin Throughout the ontogeny of an organism, developmental appendages [29]. In plants, we see examples of modular- regulation is a complex, dynamic system of physical inter- ity when different aspects of the development of the same actions between proteins, hormones, small RNAs, etc. tissue, tissue system or organ are controlled indepen- An important feature of this system is that the strength dently: the control of vascular proliferation and vascular and duration of interactions between its different com - organization that are genetically separable [30]; xylem ponents change during ontogeny; the changes separate and phloem cell differentiation from procambium con - subsets of strongly interdependent interactions that can trolled independently of the neat separation of the two be regarded as distinct regulatory modules (e.g., the vari- tissues within vascular bundles [31]; differentiation of ational modules of Pavlicev and Wagner [25]). Thus, the secondary phloem and secondary xylem controlled inde- modules are subsets of the broader system of interac- pendently of each other [32]; blade expansion and leaflet tions; they are tightly integrated internally, on one hand initiation uncoupled during compound leaf morphogen- (i.e., within-module interactions are strictly dependent esis [33]; floral organ length and corolla limb dimensions on each other), and on the other hand are independent varying independently in two closely related species of from, or more loosely integrated with, other such sub- the same genus [34]. sets of interactions (i.e., modules can be turned on and T omescu and Rothwell EvoDevo (2022) 13:8 Page 5 of 19 Another example is the reiteration of structural mod- about the evolution of morphological complexity as a ules consisting of four nuclei (whose makeup is likely mosaic of features combined in different ways and assem - determined by the same regulatory mechanism) among bled in different sequences in different major lineages the diverse types of angiosperm megagametophyte devel- [44, 45]. opment [35]. Along similar lines, the same set of regula- tory interactions may be deployed in different locations Structural fingerprints provide evidence within the plant, like in the case of a module that regu- for the deployment of regulatory modules lates cell wall remodeling, expressed in both lateral root across phylogeny and time emergence and petal abscission [36]; and, more gener- The anatomical and morphological features seen in ally, in the development of ectopic structures of many organisms bear witness to the activity and, sometimes, kinds. Conversely, different developmental fates can be interactions of specific regulatory mechanisms. When determined in cells that share the same identity by the a specific developmental process can be matched with action of distinct regulatory modules, such as pericycle specific anatomical or morphological features, those fea - cells induced into either lateral root primordium found- tures represent structural n fi gerprints of the activity of ers or cork cambium initials by the integration of differ - regulatory mechanisms that control that process (Fig. 2). ent developmental cues into distinct regulatory modules In other words, in such cases studying morphology can [37]. At a broader biological scale, there is evidence for teach us about developmental regulation. In plants, spe- regulatory mechanisms transferred between the gameto- cifically, identification of such fingerprints is facilitated phyte and sporophyte generations [38–42]. by the fact that the position of cells is largely fixed; cells In an evolutionary perspective, the modularity of are attached to each other by their walls, in the posi- developmental regulation allows for broad variation in tion in which they arise by cell division. As a result, the the organization of ontogenetic trajectories over evolu- relative arrangement of cells records sequences of cell tionary time, with different phenotypic outcomes in dif - division, allowing for more detailed reconstruction of ferent organisms. The roots of variability reside in the developmental processes. Such is, for instance, the easily degree of integration of the modules, which can be more distinguishable patterning of merophytes that form from or less tightly integrated—i.e., interacting with, influ - immediate derivatives of the apical cell and show corre- enced by or dependent on, each other—in ways that can sponding arrangements around and behind the latter in be hierarchical or not. Variability also arises from the bryophyte or equisetalean apical meristems (Fig. 3a–d); combinatorial nature of the activation (or lack thereof ) of or the arrangement of cells in cross sections of second- different modules—i.e., different modules being turned ary tissues, which records the sequence of past periclinal on or off separately or in concert—at different stages in and anticlinal divisions in the cambial initials (Fig. 3e–h). ontogeny. Together, these sources of variation underpin Similarly, at a larger scale, the patterns of sporangiophore a vast amount of potential diversity in ontogenetic trajec- (i.e., fertile appendage) numbers and sizes along equise- tories, able to generate an equally vast amount of poten- talean fertile internodes (Fig. 3i) record the polarity of tial phenotypic diversity. Such potential provides the raw meristematic activity in intercalary meristems (Fig. 3j). material for morphological evolution. Thus, for example, Although genetic regulation, which results in structural analyses of plant comparative morphology across evolu- features of plants, is a transitory process not available for tionary time and phylogenetic space have assembled data direct examination from fossils, these features—struc- that indicate different pathways of accretion of complex - tural fingerprints—do accurately reflect the regulatory ity in different lineages [43, 44], and support hypotheses genetics by which they were produced. Therefore, when (See figure on next page.) Fig. 3 In plants, cells are attached to each other by their walls, in the position in which they arise by cell division. As a result, the relative arrangement of cells records sequences of cell division, allowing for reconstruction of developmental processes. The arrangement of cells at the tip of Physcomitrium moss embryos (a, b) reveals growth from an apical cell (images courtesy of C. Jill Harrison); embryo outlined in blue inside the archegonium in a, orange lines emphasize the cells arrangement. The patterning of merophytes formed from derivatives of the apical cell is easily distinguishable in longitudinal sections of Equisetum root (c) and shoot (d) apical meristems and reflects the sequence of divisions of the apical cell; root and stem merophytes traced in orange; root cap merophytes traced in brown in c. Anticlinal (multiplicative) divisions (between arrowheads in e) of vascular cambium initials produce additional files of cells observed in cross sections of secondary tissues (in a Pinus stem). “Doubled” tracheid files (arrowheads in f) are fingerprints that reveal the exact location and timing (measured in wood thickness or growth rings) of symmetric divisions of the cambial initials. Asymmetric divisions of cambial initials initiate rays (arrowhead in g), whose inner ends (arrowhead in h) mark the position and timing of the asymmetric division. Patterns of sporangiophore numbers and sizes along fertile internodes of the Permian equisetalean Cruciaetheca (i) record the basipetal direction of tissue and organ maturation within internodes (j), generated by growth from intercalary meristems; sporangiophores in red, in the image tracing in i and in the diagram in j; internodes gray in i; nodes gray in j; j modified from [47]. Scale bars 20 µm in (a, b); 50 µm in (c, d); 20 µm in (e–h); 1 cm in (i) Tomescu and Rothwell EvoDevo (2022) 13:8 Page 6 of 19 Fig. 3 (See legend on previous page.) T omescu and Rothwell EvoDevo (2022) 13:8 Page 7 of 19 structural fingerprints are identified in fossils, they can upstream of locations where polar auxin flow in the cam - be employed to infer the specific regulatory mechanisms bium has been impeded by obstructions, such as axillary by which they developed [46] (Fig. 2). Because in living buds and lateral branches [48, 55, 56]. Such “auxin swirls” plants we can tie these fingerprints to specific, detailed therefore represent anatomical fingerprints for polar regulatory mechanisms, we can circumscribe the exact auxin regulation of secondary xylem patterning and were nature of regulatory modules and of interactions within the first structural fingerprint to be recognized in fossil and between modules that generate the structural finger - plants [3, 46]. prints. If compared between extant plant lineages, this Because xylem has excellent fossilization potential, type of information can reveal the degree of variation wood anatomy is among the most common sources of in the structure and interactions of regulatory modules data in the plant fossil record. Herein, swirls of tracheary that characterize different lineages. Studies that integrate elements provide powerful evidence (1) for polar auxin structural fingerprints and molecular-genetic regulation transport as a regulatory mechanism of tissue pattern- in living plants allow us to infer the same relationships ing during vascular cambial growth shared among sev- between gene regulation and structure in extinct plants. eral major plant clades [57], and (2) for the antiquity of This opens up a whole new window onto the evolution of polar auxin regulation in secondary tissue patterning. development, by allowing us to trace the presence of reg- This demonstrated shared mechanism suggests that at ulatory processes and the activity of specific regulatory least some of the basic regulatory elements in the con- modules in phylogenetic space and evolutionary time. In trol of secondary growth may have been part of a devel- other words, this methodology allows us to connect the opmental toolkit shared among all euphyllophytes, or regulatory genetics of living forms to their long-extinct even all tracheophytes [45, 58]. The same structural ancestors and precursors (or, at least, to form hypothe- fingerprint identified in the rooting structures (rhizo - ses about such connections) within an empirically based morphs) of Pennsylvanian (c. 310 million-years) arbo- framework (e.g., [47]). rescent lepidodendralean lycophytes demonstrated that For example, if a particular regulatory pathway is these positively gravitropic axes have acropetal auxin shared by sister clades, then we can hypothesize that transport, unlike the shoots to which they are homolo- they share a common developmental tool kit which has gous [59], and similar, instead, to other rooting structures been inherited from a common ancestor that possessed with different homologies [60, 61]. In turn, this shared that tool kit [3]. Those hypotheses can then be tested by directionality of polar auxin transport implies that acro- searching for the structural fingerprint of those tool kits petal auxin flow transcends organ identity and is more in specimens of the common ancestor (or extinct sis- tightly linked to positively gravitropic axes, independ- ter group) of the two clades. An example of that sort of ent of their homology [62]—whether they be roots (as hypothesis test is presented below for the role of polar in most extant tracheophytes), modified shoots (in isoe - auxin regulation in the development of vascular tissue. talean and lepidodendrid lycophyte rhizomorphs, and in drepanophycalean lycophyte rooting axes), rhizophores A quintessential structural fingerprint and its (in Selaginella), or simple undifferentiated axes (in zos - implications terophylls) (Fig. 4). Regulation of both primary and secondary vascular tis- sue production (specification, differentiation) by the Combining structural fingerprints directional transport of auxin (polar auxin transport) is By the beginning of the Silurian (444 million-years ago), probably a common denominator of development in vas- the first members of the clade characterized by branched cular plants, wherein it evolved increasing sophistication sporophytes and including all vascular plants (i.e., poly- at successively more derived levels of their phylogeny [3, sporangiophytes), had emerged [63] out of a plexus of 48, 49]. Studies in angiosperms have demonstrated that early embryophytes whose earliest bryophyte-grade rep- polar auxin transport and the auxin gradients it gener- resentatives go at least as far back as the Middle Ordo- ates, established early in embryogenesis, are responsible vician (468 million-years ago; [64]). If trilete spores are, for primary vascular architecture (procambium specifi - indeed, exclusively characteristic of vascular plants and cation, vascular tissue differentiation), as well as cambial not of all the embryophytes, as has been proposed by identity and functioning in secondary growth (e.g., [50– Steemans et al. [65], then vascular plants and, by exten- 54]). During secondary growth from a vascular cambium, sion, polysporangiophytes may have evolved as early as polar auxin regulation of cell positioning and growth 455 million-years ago, around the beginning of the Late direction produces characteristic circular patterns in Ordovician [66, 67]. Direct information on these plants is specific positions in the secondary xylem. These pat - available exclusively from fossils, which provide multiple terns consist of swirls of tracheary elements positioned structural fingerprints that when combined, allow us to Tomescu and Rothwell EvoDevo (2022) 13:8 Page 8 of 19 Fig. 4 In contrast to the shoots (green), polar auxin transport (PAT; depicted by blue arrows) is acropetal in the roots of seed plants and the rhizophores of selaginellalean lycopsids, whose homologies are equivocal. Additionally, fingerprints for the directionality of PAT demonstrate that the rhizomorphs of lepidodendralean lycopsids, which are shoot homologs with rooting function, also had acropetal PAT [60]. This shared directionality of PAT implies that acropetal auxin flow transcends organ identity and is more tightly linked to the positively gravitropic response or rooting function of axes (gray), independent of their homology. In turn, this suggests that the positively gravitropic axes with rooting functions produced by K-branching in zosterophylls with simple body plan may also have had acropetal PAT (dashed blue arrows) reconstruct the morphology and life history of these tra- Devonian (c. 410 million-years old) polysporangiophytes cheophyte ancestors. such as Aglaophyton, Rhynia, Horneophyton or Nothia Early polysporangiophytes had diminutive sporophytes [70]. This inference is based on the thalloid form of fos - that were only little more than branched versions of bry- sils found associated with (but not attached to) branched ophyte-grade sporophytes [4]. The small size of the spo - sporophytes in Silurian and Early Devonian layers at rophytes is immediately apparent in the fossils [23, 63]. multiple locations [71, 72]—some of which bear transfer The branching of these sporophytes indicates that they cells typical of the gametophyte–sporophyte connection grew from apical meristems, but their diminutive size, in bryophytes [24]—and on structural and chemical evi- scant branching, and presence of sporangia terminating dence that some of these fossils are plants [73–75]. all branches (e.g., [1, 4, 63]) indicate that their meris- tematic growth was determinate. The small size of these Echoes of modularity sporophytes also supports the hypothesis that they were The leaves of ferns and seed plants nutritionally dependent on the gametophytes [23], like The Euphyllophytina is the largest and most diverse of the sporophytes of bryophytes. The dependence of spo - the two major clades of living vascular plants, and is rep- rophytes on the gametophytes is also consistent with the resented in the modern flora by seed plants (flowering inference that their growth was determinate. Recently it plants, gymnosperms) and several lineages of seed-free has become apparent that these early sporophytes had plants (marattialean, ophioglossalean, and leptospo- specialized photosynthate-conducting cells similar to rangiate ferns, equisetaleans, and psilotaleans—i.e., those of bryophytes [1], but it is less clear whether the Psilotum and Tmesipteris). The overwhelming major - earliest polysporangiophyte sporophytes possessed tra- ity of the extant euphyllophytes show stem–leaf–root cheid-based water-conducting tissues, as the oldest tra- organography in their vegetative sporophyte; excep- cheids discovered to date are significantly younger—424 tions include a few highly derived angiosperms with million-years old [68]. This is close to the (slightly older, reduced or incompletely differentiated sporophytes (e.g., ca. 432 million-years) age of the oldest known sporo- Podostemaceae, Lemnaceae), ferns (e.g., Salvinia lack- phytes that reached sizes consistent with physiological ing roots) and psilotaleans (which lack roots entirely and independence [69]. whose lateral appendages may or may not be reduced The gametophytes that supported these diminu - leaves; [76]). Because of this, early phylogenetic analy- tive sporophytes were probably thalloid, like those of ses of living species have inferred that the derived stem– hornworts and liverworts and unlike those of younger, leaf–root organography has evolved only once among T omescu and Rothwell EvoDevo (2022) 13:8 Page 9 of 19 euphyllophytes [77]. However, all members of the basal Adaxial–abaxial polarity is reflected in the flattened grade of fossil euphyllophytes, referred to as trimero- morphology of leaves and, even in the absence of this phytes, have plesiomorphic sporophyte morphology morphology, can be ascertained based on the bilateral consisting of simple branching axes that were vascular- patterning of the vascular tissues that supply these lat- ized and bore sporangia, but were not differentiated into eral appendages (i.e., phloem positioned abaxially and roots, stems and leaves. The absence of leaves in the tri - xylem adaxially). Using structural fingerprints for the two merophytes, coupled with their phylogenetic position leaf-defining features—leaf morphology for determinate among euphyllophytes [21, 78], and with fossil evidence growth and polarity of leaf vascular tissues for adaxial– for the evolution of euphyllophyte leaves [79, 80], pro- abaxial polarity—and querying the fossil record of early vide compelling evidence that leaves evolved indepen- ferns and seed plants, Sanders et al. [79] demonstrated dently and in parallel, from such leafless trimerophytes, that whereas seed plants evolved determinate growth in several different euphyllophyte lineages [81]. Thus, the before adaxial–abaxial polarity in the leaves, in filicalean leaves of different euphyllophyte clades that appear to be fern leaves evolution of adaxial–abaxial polarity preceded homologous to neontologists, actually resulted from par- determinacy (Fig. 5). Aside from supporting hypoth- allel evolution [78–82]. This is one of the most compel - eses of independent evolution of leaves in ferns and ling examples of fossils and morphology allowing for the seed plants, reflecting different trajectories in terms of recognition of analogy (or homoplasy; similar characters sequence of character evolution, this is consistent with a in two groups that evolved independently by parallel or modular nature of the regulators of leaf determinacy and convergent evolution) and its distinction from homology adaxial–abaxial polarity, which allows for independence (i.e., characters in two groups that are inherited from a in the deployment of these two features. Thus, structural common ancestor that had those characters). fingerprints for developmental mechanisms preserved in Two main structural changes that have led to the evolu- fossils provide evidence for the modular nature of spe- tion of leaves from leafless trimerophyte axes are (1) the cific aspects of leaf developmental regulation. change from indeterminate to determinate growth, and Venation is an additional facet of leaf (or pinnule) (2) the origin of abaxial–adaxial patterning in the transi- organization that reveals structural fingerprints of the tion from radial to bilateral growth [83]. Leaves of living meristematic activities which generated it. Tracking the euphyllophytes typically have both determinate growth deployment of these activities across plant phylogeny and and bilateral (abaxial–adaxial) polarity, and available evi- the fossil record reveals further evidence for the parallel dence suggests that each of these properties is controlled evolution of leaves within Euphyllophytina. The paleon - by distinct regulatory modules. Because data available tological record documents leaf evolution within several currently on gene expression patterns offer only a spotty clades of Paleozoic euphyllophytes and provides direct coverage of the taxonomic breadth of living euphyllo- evidence for parallel changes in pinnule structure and phytes, and because those data are not matched in terms leaf venation in each [80]. Specifically, the fossil record of taxonomic coverage by data on gene function, infer- demonstrates that in each of at least four clades (i.e., seed ences on gene functions in different lineages can only plants, ferns, equisetaleans, and progymnosperms) the be tentative at this point. Nevertheless, recurrent pat- most ancient representatives produced ultimate lateral terns of expression, some of which are complemented units (e.g., pinnules) that had linear laminar segments by functional data, provide indications on putative gene with marginal vein endings, and that successively more functions. For instance, meristematic activity at the shoot recent representatives progressed through parallel modi- apex is probably maintained by class I KNOX genes and fications to (1) divergent venation with marginal vein LFY in both ferns and angiosperms (at least insofar as endings; (2) convergent venation with marginal vein end- this can be predicted based on studies in model species). ings; (3) reticulate venation with marginal vein endings; These genes are probably also responsible for prolifera - and (4) reticulate venation with internal vein endings tive growth in the leaves of both ferns and angiosperms (summarized by Rothwell et al. [3]). Although the com- (e.g., compound leaves) [81, 84–87]. Thus, determinacy plete series of structural/meristematic modifications was of growth in leaves may well reflect the evolution of achieved in only ferns and seed plants, these parallel evo- regulatory mechanisms that repress these genes, such as lutionary trajectories of leaf venation represent structural the ARP group genes that repress KNOX I gene activity. fingerprints for a succession of parallel changes in the Similarly, adaxial–abaxial polarity (sometimes referred to meristems that contributed to the evolution of euphyl- as dorsiventral polarity) seems to result from the expres- lophyte leaves (or their ultimate segments in the case of sion of, and interactions between, class III HD-ZIP genes compound leaves) in all four clades. (promoters of adaxial identity) and KANADI genes (pro- moters of abaxial identity), in all euphyllophytes [88–90]. Tomescu and Rothwell EvoDevo (2022) 13:8 Page 10 of 19 Fig. 5 Euphyllophyte leaves are thought to have evolved from lateral branching systems like those seen in early representatives of the clade (e.g., Psilophyton). Structural fingerprints for adaxial–abaxial polarity (dorsiventral polarity) observed in fossils indicate that whereas seed plants evolved determinate growth before adaxial–abaxial polarity in the leaves, in filicalean fern leaves evolution of adaxial–abaxial polarity preceded determinacy. The early fern Psalixochlaena exhibits adaxial–abaxial polarity in its leaves (i.e., protoxylem on the adaxial side and phloem on the abaxial side of the leaf vascular bundle cross-sectioned in the figure), which had indeterminate growth; in contrast, the leaves of the early seed plant Elkinsia had determinate growth but their vascularization had radial symmetry (protoxylem surrounded by metaxylem in the vascular bundle cross-sectioned in the figure), at least in their terminal segments. This observation provides one of the lines of evidence supporting independent evolution of leaves in ferns and seed plants Secondary growth that vascular cambial growth originated independently in The modularity of developmental regulation takes on the different lineages. This perspective has its roots in the a much broader scope if we consider the evolution of perceptions that (1) the first occurrences of secondary vascular cambial growth (secondary growth) and the growth in the different lineages are much younger than diversity of modes of secondary growth that have arisen the origin of tracheophytes; and (2) that the anatomy of among tracheophytes. One of the major unanswered secondary tissues shows significant differences between questions regarding the evolution of secondary growth is major lineages [92]. whether vascular cambial growth evolved independently The traditional view on the evolution of vascular cam - in different tracheophyte lineages or only once, at the bial growth is currently reshaped by evidence coming base of the clade. The fossil record demonstrates that vas - from two directions. First, anatomical evidence suggests cular cambial growth was present, outside of seed plants, that some mechanisms regulating cambial growth, such in multiple currently extinct tracheophyte lineages that as control by polar auxin transport of cambial identity go back to the Middle Devonian (c. 390 million-years and activity, are shared among major tracheophyte lin- ago) [91]. Based on these, the traditional view has been eages that span the lycopsids and the euphyllophytes: T omescu and Rothwell EvoDevo (2022) 13:8 Page 11 of 19 lepidodendrales, equisetaleans, progymnosperms, and comparative studies. Irrespective of the latter, this possi- spermatophytes [57, 60, 93]. Second, accumulating dis- bility prompts the question: could regulation of vascular coveries [58, 94–96] point to much earlier origins of vas- cambial growth have originated in the common ances- cular cambial growth than previously thought, at least in tor of euphyllophytes, or even the common ancestor of the euphyllophyte clade. Together, these lines of evidence euphyllophytes and lycopsids? suggest that regulators of secondary growth may have To begin answering this question, Tomescu and become part of the euphyllophyte developmental toolkit Groover [45] have proposed an updated perspective that very early in the evolution of the clade. Unfortunately, approaches vascular cambial growth as a complex devel- comparative genomic approaches cannot be applied to opmental process that is highly modular (Fig. 6). In this address this because, aside from seed plants, all other perspective, the diverse anatomies of secondary tissues euphyllophyte lineages with cambial vascular growth seen in different extinct lineages (and which represent are extinct, thus allowing recourse only to anatomy for diverse modes of secondary growth) reflect a mosaic Fig. 6 A perspective proposed by Tomescu and Groover [45] (top panel) regards vascular cambial growth as a complex modular developmental feature that is the sum of multiple component processes, each controlled by an independent regulatory module. In this perspective, component processes are deployed in a mosaic pattern among plant lineages, and their different combinations result in as many distinct modes of secondary growth. If each component process leaves a structural fingerprint in the anatomy of secondary tissues, the combinations of component processes can be inferred for the modes of secondary growth observed in the fossil record. This perspective allows for a basic set of component processes that could have defined a hypothetical single common origin of secondary growth across tracheophytes (or across euphyllophytes), underpinned by a basic toolkit of corresponding regulatory modules representing a deep homology (sensu Shubin et al. [99]) in the clade. In the traditional perspective on secondary growth (bottom panel), the implicit assumption was that of vascular cambial growth as a unitary developmental feature that was assembled de novo in each taxonomic group that evolved secondary growth independently and in parallel with other groups Tomescu and Rothwell EvoDevo (2022) 13:8 Page 12 of 19 pattern of expression of distinct, more-or-less independ- understanding of structural fingerprints characteristic for ent developmental regulatory modules. Although they specific developmental processes, combined in the con - are as yet poorly circumscribed or simply unidentified text of an evolutionary-developmental perspective that is [45], these hypothesized regulatory modules are thought rooted in modularity of developmental regulatory mech- to be individually responsible for different component anisms, can contribute to the construction of testable processes that comprise secondary growth (Fig. 7)—e.g., hypotheses about the evolutionary origins of secondary symmetrical or asymmetrical anticlinal divisions of cam- growth. bial cells, bidirectional production of new tissues. The distinctiveness and independence of the hypothesized Modularity and hierarchy regulatory modules are supported by anatomical obser- Within the paradigm of modularity in developmental reg- vations and developmental experiments and could be ulation, information preserved in fossils and recognized as tested, in principle, by altering the activity of different structural fingerprints for specific developmental regula - modules, when the regulatory interactions that control tors can also lead to inferences of hierarchy in the deploy- vascular cambial growth are better circumscribed. ment of regulatory modules. An example is the case of Importantly, the activity of the different regulatory the regulatory mechanisms that underlie the reproductive modules proposed by Tomescu and Groover [45] can morphologies of living and extinct equisetaleans of the be recognized based on specific anatomical fingerprints family Equisetaceae. The strobilus of Equisetum has been that are preserved in the wood (secondary xylem) and for a long time a puzzle in terms of homology and mor- adjacent tissues of plants, including fossil plants. The phological evolution. The different types of reproductive presence or absence of these fingerprints in the wood morphologies found in fossil relatives of Equisetum that of different lineages (Fig. 7) suggests that the regulatory go back to the Permian (c. 290 million-years ago) had cre- modules are deployed differently among different line - ated a stalemate in the interpretation of the homology of ages, living and extinct—some are shared among mul- the strobilus (reviewed by Ref. [47, 97]). The contradictory tiple lineages, while others are apomorphic for distinct homology implications of the different types of reproduc - lineages. Thus, information preserved in fossils and an tive morphologies stemmed from rigid application of the Fig. 7 Structural (anatomical) fingerprints (in black, at left) preserved in the secondary tissues of plants living and extinct provide evidence for specific component processes of vascular cambial growth (in purple, at left) and the activity of their corresponding regulatory modules. Different combinations of such fingerprints define the distinct modes of secondary growth that differentiate seed plants from extinct sphenophyllalean sphenopsids and zygopterid ferns T omescu and Rothwell EvoDevo (2022) 13:8 Page 13 of 19 morphological model of the shoot as an alternation of lead to determinate apical growth, and (3) repress node- nodes and internodes. In brief, the frustrating question internode differentiation and intercalary meristematic was: Are the sporangium-bearing appendages (sporan- activity in the fertile phytomers, respectively. Whether giophores) attached at the nodes or along the internodes? these hypotheses on the existence and functions of regu- This was important for understanding whether the stro - latory modules could be tested experimentally by alter- bilus of Equisetum is homologous to multiple nodes, each ing developmental regulatory pathways (e.g., repressing bearing a single whorl of sporangiophores, or to a single growth determinacy in the strobilus meristem by overex- internode with multiple sporangiophore whorls attached pressing KNOX I family genes) will depend on our ability along it. This is a fundamental question with implications to genetically manipulate living Equisetum, a capability for morphological evolution in one of the major tracheo- that has yet to be achieved. phyte lineages—represented today solely by the genus From an epistemic standpoint, this case study demon- Equisetum, the equisetalean clade in an excellent example strates how a hypothesis generated by data from living of a long phylogenetic branch wherein homology issues plants is tested and confirmed using data from the fos - can only be resolved by querying the rich fossil record of sil record [61]. In turn, this provides a framework for the group [98]. subsequent hypotheses that included data from living Studies of development in living Equisetum show that Equisetum and fossil plants, to offer a novel explanation, shoots grow as a result of the combined activity of the api- involving a hierarchy of regulatory modules, of the ori- cal meristem, which generates phytomers, and intercalary gin of the Equisetum strobilus and other reproductive meristems, which are responsible for elongation of the morphologies of fossil equisetaleans. This updated per - internode in each phytomer. This suggested that an empha - spective on the Equisetum strobilus generates further sis on the phytomeric structure of the shoot, rather than the hypotheses about evolution and the deep fossil record, node-internode alternation, may provide a more appropri- explaining the origin and evolution of the equisetalean ate paradigm within which to understand homology in the sporangiophore, all of which are possible only because Equisetum strobilus and, more broadly, in equisetacean developmental and evolutionary data have been pre- reproductive morphology [47]. At the same time, current served in the fossil record. understanding of plant developmental regulation indicates (1) that meristems of all types are equivalent in their fun- Conclusions damental capacities, including the capacity to transition to The paleontological record provides the best evidence reproductive growth (except for root apical meristems); and for evolutionary pattern. Using structural fingerprints (2) that at least some of the regulatory mechanisms effect - for plant development, we can also address fundamental ing this transition are shared broadly among tracheophytes questions about evolutionary process. Studies applying [47]. Together, these observations led to the hypothesis that the epistemic framework of this paleo-evo-devo perspec- in equisetaceans the switch to a reproductive developmental tive and methodology illuminate our understanding of program happens in the intercalary meristems responsible how evolution proceeds by successive modifications of for internode elongation and, as a result, sporangiophore plant development, which are controlled, in turn, by the whorls are produced along the internodes of fertile phytom- activities of regulatory genes and growth regulators. This ers and follow a basipetal sequence of maturation (Fig. 3j). approach further clarifies that developmental regulation The hypothesis of reproductive growth in internode of plant growth is both modular and hierarchical. When intercalary meristems generates predictions (i.e., hypoth- coupled with another base of knowledge informed by the eses) about morphological patterns produced by such a fossil record—our understanding of the overall pattern mode of development. These morphological patterns of plant phylogeny—characterization of such develop- can be used as structural fingerprints (i.e., hypothesis mental modules, of the lineages in which they have been tests), which can be recognized in the equisetacean fossil deployed, and of the order in which they have accumu- record, confirming the presence of intercalary reproduc - lated in divergent lineages, provide a backbone for iden- tive growth (Fig. 3i, j), the only instance of its kind known tifying both the specific processes and the patterns by in tracheophytes [47]. This confirmation provides an which evolution has proceeded. Continued exploration updated framework for understanding the origin of the of three directions—(1) the composition, structure, and Equisetum strobilus and of other reproductive morpholo- functioning of gene regulatory networks that underpin gies present among equisetacean equisetaleans. These all aspects of the morphological variety seen across the different morphologies are best explained as resulting diverse extant plant lineages; (2) the distinct morpho- from deployment of independent regulatory modules in logical and anatomical signatures (i.e., structural fin - a hierarchic sequence (Fig. 8): the regulatory modules gerprints) of regulatory modules that are shared among (1) turn on reproductive growth in the phytomer, (2) multiple extant lineages; and (3) the occurrence of such Tomescu and Rothwell EvoDevo (2022) 13:8 Page 14 of 19 Fig. 8 The realization that a reproductive program can be activated in the intercalary meristem of individual equisetacean internodes, leading to development of sporangiophores along them, opened up a new avenue for interpreting the reproductive structures of extinct (Cruciaetheca, Peltotheca) and living (Equisetum) equisetaceans as illustrating a cumulative sequence of deployment (gray arrow at top) of independent regulatory modules for three developmental processes (in purple, at bottom) responsible for the different features (in black, at bottom) that characterize specific reproductive morphologies; cross bars separate phytomers in the shoot diagrams and phytomers bearing sporangiophores are red; modified from [47] Funding fingerprints in the fossil record, across geologic time and Open Access funding provided by Ohio University. phylogenetic space—will lead to deeper and more mean- ingful integration of data from the fossil record in the Availability of data and materials Not applicable. overall tapestry of the evolution of development through- out the history of plant life. Declarations Acknowledgements We thank Jill Harrison for the invitation to contribute to this issue and support Ethics approval and consent to participate throughout the editorial process, as well as for sharing Physcomitrium embryo Not applicable. images. We are also indebted to Dennis K. Walker for producing the Equisetum root tip slide. Insightful comments from two anonymous reviewers improved Consent for publication the manuscript significantly. Not applicable. Authors’ contributions Competing interests AMFT and GWR developed the project, wrote the paper and approved the The authors declare that they have no competing interests. final manuscript. Both authors read and approved the final manuscript. T omescu and Rothwell EvoDevo (2022) 13:8 Page 15 of 19 Glossary embryo within the arche- Acropetal (1) movement (e.g., of a gonium, with living repre- hormone) from the base sentatives that are assign- toward the apex of an able to vascular plants and organ. (2) Pattern of tissue bryophytes (i.e., mosses, maturation along a struc- liverworts and hornworts). ture or organ, in which the The term embryophytes is basal region is the earliest synonymous to land plants to mature and tissue matu- and Kingdom Plantae. ration progresses toward Equisetaleans Major clade of vascular the tip (distal region) of the plants that includes living structure or organ. Anto- Equisetum and fossil repre- nym: basipetal. sentatives that extend back Anticlinal division Orientation of the plane of through time to at least the cell division perpendicular Late Devonian. to the outer surface of an Euphyllophytes One of the two major organ. clades of vascular plants Axis (pl.: axes) Ancestral vegetative organ that includes as living of polysporangiophytes representatives the flow - and tracheophytes that ering plants, gymno- branches to produce more sperms, ferns (maratti- than one terminal sporan- aleans, ophioglossaleans, gium, and that has, via evo- and leptosporangiates), lution, given rise to stems, equisetaleans (i.e., Equi- leaves, and roots that char- setum), and psilotaleans acterize the sporophytes of (i.e., Psilotum and Tmesip- living vascular plants. teris); informal name for Basipetal (1) movement (e.g., of a Sub-division Euphyllophy- hormone) from the apex tina of Kenrick and Crane toward the base of an [21]. Euphyllophytes are organ. (2) Pattern of tissue the sister group of lyco- maturation along a struc- phytes (Sub-division Lyco- ture or organ, in which the phytina). Several extinct apical region is the earliest pteridophyte-grade groups to mature and tissue matu- (including the earliest rep- ration progresses toward resentatives of the clade, the base (proximal region) named trimerophytes) are of the structure or organ. also euphyllophytes. Antonym: acropetal.Gametophyte Haploid multicellular Derivative of an apical phase of the embryophyte cell (apical cell derivative) Cell produced directly by life cycle that develops by the division of an apical mitosis from a spore, and cell. that consists of a vegeta- Determinate growth tive body and one or more (n., determinacy) Gr owth pattern in which gametangia that produce growth ceases once a set gametes. developmental checkpoint Indeterminate growth Growth pattern in which is reached. Antonym: inde- growth continues indefi- terminate growth. nitely throughout the life Embryophytes Major group of strepto- span of the organism. phytes that produce an Antonym: determinate Tomescu and Rothwell EvoDevo (2022) 13:8 Page 16 of 19 growth. that is tightly integrated Intercalary meristem The mer istematic region internally (by interactions at the base of each inter- among a subset of the com- node, found in some plant ponent parts of the system) groups, such as the equi- but relatively independent setaleans and grasses from other such units. (Poaceae). Node Position along a stem Internode Length of stem between where one or more leaves two successive positions are attached. where leaves are attached Phytomer Modular unit of a shoot (i.e., nodes). consisting of one node Lycophytes One of the two major (with the attached leaf) clades of vascular plants and the subtending that includes as living rep- internode. resentatives the lycopsids Polysporangiophytes The clade of embryophytes Lycopodium s.l., Phyllo- (land plants) that share the glossum, Selaginella, and branched sporophyte as a Isoetes; informal name for synapomorphy (informal Sub-division Lycophy- name for Super-division tina of Kenrick and Crane Polysporangiomorpha of [21]. Lycophytes are the Kenrick and Crane [21]). sister group of euphyl- Psilotaleans (Psilotales) The clade of homosporous lophytes (Sub-division vascular plants consisting Euphyllophytina). Several of the two living genera extinct groups, includ- Psilotum and Tmesipteris. ing lepidodendrid and No fossils of this clade have pleuromeialean lycopsids, been discovered to date. drepanophycaleans, and Regulatory module Subset of regulatory inter- the earliest representa- actions (i.e., module; see tives of the clade, named definition of modular - zosterophylls, are also ity above) that are tightly lycophytes. integrated internally, but Merophyte Group of clonally related can act largely independ- cells resulting from ent of other such subsets sequential cell divisions (or modules) of a broader that originate in a sin- system of regulatory inter- gle derivative of the api- actions and is responsible cal cell of a meristem. The for a well-circumscribed arrangement of mero- developmental or morpho- phytes with respect to each logical outcome. other may reflect the order Rhizomorph Rooting organ of isoe- and pattern of cell divi- talean lycophytes, includ- sions by which they have ing the living Isoetes and been produced. lepidodendralean trees, Modularity, module Property of complex sys- that is derived from (i.e., tems that refers to the rela- homologous to) a shoot or tive degrees of connectiv- shoot system. ity or integration between Shoot Vegetative organ system component parts of the of vascular plants that system. Within a modular consists of a stem and the system, a module is a unit leaves that it produces. T omescu and Rothwell EvoDevo (2022) 13:8 Page 17 of 19 Sporangiophore Reproductive organ of gene interactions/regula- equisetaleans consisting tory module), and whose of an appendage bear- presence in an organism ing sporangia. Sporan- is used as evidence for the giophores are thought to activity of that regulator. have evolved from fertile Thalloid Type of plant body with- lateral branching systems out complex organization, of trimerophyte-grade especially lacking distinct euphyllophytes (see defi- stems, leaves or roots. nition of euphyllophytes Many bryophytes have above). In the only living thalloid sporophytes, and equisetalean, Equisetum, many homosoprous vas- sporangiophores are pel- cular plants have thalloid tate in shape, with a nar- gametophytes. row stalk and a broad head Tracheophyte Another name for vascu- that bears sporangia on its lar plants, a group char- underside (i.e., the side that acterized by sporophytes faces toward the subtend- possessing specialized ing stem). water- and photosynthate- Sporophyte Diploid phase of the conducting tissues, which embryophyte life cycle that include specialized water- develops by mitosis from a conducting cells (i.e., trac- zygote, passes through an heids, vessel elements). embryo stage, and consists Transformational series A s equence of different of a vegetative body that species that depict the bears one or more sporan- transformation of one spe- gia, which produce haploid cific type of structure to spores by meiosis. another. Transformational Stem Evolutionarily derived series of fossils through organ of vascular plants time constitute the tra- that consists of an alterna- ditional paleontological tion of nodes and inter- evidence for organismal nodes, as well as a succes- (morphological) evolution. sion of phytomers, bears Author details leaves at the nodes, has Department of Biological Sciences, California Polytechnic State University Humboldt, Arcata, CA 95521, USA. Department of Environmental and Plant complex internal struc- Biology, Ohio University, Athens, OH 45701, USA. Department of Botany ture, and may have inde- and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA. terminate growth (see Received: 28 September 2021 Accepted: 29 January 2022 definitions of axis, inter - node, node, and phytomer above). Strobilus (pl.: strobili) Agg regation of sporan- References gium-bearing appendages 1. Edwards D, Morris JL, Axe L, Duckett JG, Pressel S, Kenrick P. 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EvoDevo – Springer Journals

Published: Mar 2, 2022

Keywords: Developmental regulation; Evo-devo; Fossil; Leaf; Modularity; Morphology; Rooting organ; Secondary growth; Strobilus; Structural fingerprint

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Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

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Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

Fossils and plant evolution: structural fingerprints and modularity in the evo-devo paradigm

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