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‘Genome’ doesn’t cover it: Introducing Gene Systems Hypothesis and Functional Gene Systems

‘Genome’ doesn’t cover it: Introducing Gene Systems Hypothesis and Functional Gene Systems BioscienceHorizons Volume 10 2017 10.1093/biohorizons/hzx005 ............................................................................................ ..................................................................... Review article ‘Genome’ doesn’t cover it: introducing gene systems hypothesis and functional gene systems James O. Fredrickson Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU, UK *Corresponding author: Institut des Sciences de l’Evolution de Montpellier, UMR 5554, Universite Montpellier 2, Montpellier, France. Email: j.fredrickson.10@aberdeen.ac.uk Supervisor: David E. Salt, Room A02 Plant Sciences, Sutton Bonington, Campus, Sutton Bonington, Leicestershire LE12 5RD, UK. ............................................................................................ ..................................................................... Traditionally, the genes which contribute to the phenotype of a eukaryotic organism were considered to be housed within its nuclear genome, but today thisisoften understood to notbethe case.In order to better understand how high- level complex phenotypic expressions arise I propose a conceptual framework composed of core systems biology ideas integrated with current understanding of genetic systems: gene systems hypothesis (GSH). The implications of this GSH framework allow for an organism level functional gene system (O-FGS) definition which incorporates the integration of macro- and micro-symbiont gene systems. In support of the proposed O-FGS definition a brief review of current literature is presented which demonstrates the influence of micro- and macro-symbionts in plant and animal development, growth and persistence. Key words: symbiosis, systems biology, mutualism, emergent, phenotype Submitted on 24 May 2014; editorial decision on 22 May 2017 ............................................................................................ ..................................................................... Introduction to not be appropriate when considering higher level complex phenotypes. The word ‘genome’ was created and defined by Hans Winkler who merged the word ‘gene’ with the suffix -ome, which A substantial body of current work which investigates means body (Winkler, 1920). This initial definition provides multicellular organismal function does not consider genetic the conceptual definition of the genome—the genes in the material which resides outside of the somatic cells of the body. During the time when the human genome was being organism in question (Bose, 2013; Bolger et al., 2014). A sequenced Matt Ridley wrote a book describing the human prime example of this is found in recent work on rice growth genome which began by saying that all of the genetically and function where most studies focus on ‘germplasm encoded information needed to make a human was contained improvement’ and attempt to attribute various complex phe- in the DNA of the human genome (Ridley, 2006). The notypes, such as drought tolerance, to just a few key genetic conclusion within his book is that these genes are the controllers markers (Xue et al., 2008; Cairns et al., 2011; Pray et al., of organismal development and function. The idea that the 2011; Serraj et al., 2011; Jagadish et al., 2012). Systems biol- information required for function and development is derived ogy should be important when considering genes involved in from the genes in an organism’s somatic cells still prevails organismal function, and indeed there are calls for integrating today. This assumption has yielded a lot of adequate results molecular systems through to ecosystems for plant breeding when low level cellular and basic structural phenomena are (Keurentjes et al., 2011), and there are also advancements considered. However, strict adherence to this assumption seems being made in regards to systems biology of plants and ............................................................................................... .................................................................. © The Author 2017. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. microbes, but mainly involving infection dynamics and disease in this case is the genetic code (including coding regions and cis (Pritchard and Birch, 2011; Garbutt et al., 2014). In these cases, regulatory elements), where the emergent property is the func- systems dynamics and pathogenic microbes are taken into tional gene product which results from the interactions between account, but inclusion of beneficial symbionts are still lacking. nuclear and cytoplasmic proteins, RNAs, and the surrounding In this review I will explain why any attempt to understand the DNA in response to environmental stimuli. All levels of bio- basis of an organism’s higher level functions or phenotypes can- logical functionality, from this basic system level up to the not just consider an organism’s ‘germplasm’ alone, but must organism, are complex systems which can be considered. also include the genes its macro- and micro-symbionts. In order However, due to the abundance of them, only a select few will to integrate the host organism with all of its symbionts I will pro- be used to make the argument for GSH, though all are possible pose a systems theory based framework which should be utilized effective candidates. Also, GSH applies to biological systems when trying to conceptualize how an individual organism with which exist at levels higher than the organism, such as commu- all of its symbionts, or functional gene system (FGS), works. nities and ecosystems; these will not be discussed because they extend beyond the context of this review. In all cases, biological systems do not exist independently and their functions are not Gene systems hypothesis static; they exist in and respond to changes in external condi- tions. Consideration of environment is essential to understand Gene systems hypothesis (GSH) is the intuitive result of the the functionality of complex biological systems at any level. integration of many concepts and thought processes which are currently not often combined in modern biological Defining environment research methodologies. In order to present GSH more clearly I will first briefly explain the most pertinent aspects of the Everything is environment foundational concepts. Biological systems adapt to a constantly changing environ- ment. The fundamental unit of most biological systems is Systems biology DNA. DNA, as a macromolecule, is quite inert. DNA must first interact with its immediate environment to be biologic- GSH is formed from a body of current scientific understanding ally active: transcription factors must bind to it in order to integrated within the concept of systems biology. Systems biology make mRNA, which will interact with a ribosome, which will is the biological application of von Bertalanffy’s general systems help it to interact with tRNAs in the cellular environment, theory (GST) (von Bertalanffy, 1950). GST and systems biology which will ultimately result in formation of a peptide. Of are abstract ideas and mathematical models which attempt to course, all of these cellular systems are composed of molecules explain complex biological systems. Functional biological entities which are themselves, the results of complex systems. In this are the result of multi-component complex systems. The com- way of thinking, all biological systems and their emergent plexity of biological phenomena is the reason for instances of functions constitute the environment of all other biological reductionist inadequacy and the importance of a systems biology systems. These systems are constantly interacting with each conceptual context. The most relevant qualities of complex sys- other and the abiotic environment. The varying interactions tems and their resultant phenomena are outlined below. between components of the complex system influence the sys- System complexity arises from non-linear interactions tem output (Trewavas, 2006; Bose, 2013). Equally important between the components of systems and their emergent proper- to recognizing that these systems are interacting with their ties. System components which behave in a way that is influ- environments is that the way they influence, and are influ- enced by multiple properties of some of the other components enced by, their environment is directly related to the organiza- of the system are described as interacting in a non-linear man- tion of the system components in space and time. ner. These non-linear interactions result in unpredictable or, emergent properties. An emergent property is unexpected System/environment interaction within space and time because its existence cannot be derived from total knowledge of This concept is well documented throughout biology. This the lower components of the system; this is due to the non- relationship is obvious at the molecular level. A gene’s protein linear relationship of the interactions of the lower components. product interacts with other proteins to produce some prod- Hence, an emergent property of a system is greater than the uct (quaternary protein structure, signal transduction path- sum of the properties of the system components (Bedau, 1997; way, etc.). This product has emergent functions associated Bose, 2013). These emergent properties of biological systems with it and these functions affect the immediate cellular envir- are what biologists recognize as organismal phenotypes. These onment at the moment in time when they act (quaternary emergent system properties integrate at many levels to create protein binds substrate and produces product; signal trans- higher level complex phenotypes at the level of the organism. duction pathway is activated by an environmental signal and Complex biological systems exist across multiple levels of causes a local response). Interacting systems have immediate organization. In this discourse I will often refer to lower level and local effects on their environments. As the distance in systems. Lower level systems, in this sense, are the various com- space and time between the interacting systems increases, plex systems which integrate to produce the biological entity the resultant function, or change in the environment, also commonly recognized as an organism. The lowest level system decreases, in general (von Bertalanffy, 1950). This decrease is ............................................................................................... .................................................................. 2 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. dependent on the degree of bifurcation effect the lower level or influenced by lower level gene systems which come from system change has on higher level systems. Bifurcation is the symbionts. phenomenon in complex systems where a small change in a The conclusion that symbiont genes can be as important for parameter of a lower level system can have a large change in a organismal function as those found in the organismal germ- higher level system output (Bose, 2013). A clear example of plasm suggests that a new functional demarcation should be this in ecological studies is the ‘keystone species’ where the made in the characterization of organismal entities. GST tells population dynamics of a single species has an unexpected us that a complex system maintains homoeostasis within a and disproportionate effect on community structure (Press, changing environment over time, or throughout various phases 1998). The previously mentioned molecular examples were of its functional existence, through its intrinsic stability (von instances of interaction over space and time. Organization in Bertalanffy, 1950). Phases of functional existence, in the case space and time also has influence over system output. of a eukaryotic organism, could be loosely defined as early From the molecular and cellular levels, spatial and tem- development, growth and persistence, and reproduction. These poral system organizational relationships are also easy to con- are certainly not necessarily distinct phases and this list is not ceptualize, and their potential for or organismal change is exhaustive, but this is a basic functional framework of a eukar- clear. Auxin’s involvement in coleoptile phototropism is a yote’s life, and will serve as a structure for the following exam- good example. After light is sensed by the tip of the coleoptile, ples. The definition of the organismal FGS (O-FGS) should be auxin is sent down the side of the tissue opposite to that inclusive of all of the specific genes/gene systems (hereafter: which the light was sensed on which causes local cell elong- genes) which contribute to the maintenance of homoeostasis ation and subsequent bending toward the light source within an organism during the phases of its life. I suggest that (Hasegawa and Sakoda, 1988). Spatial organization is inte- an O-FGS includes the DNA of all associated beneficial sym- grated with temporal organization as well. For example, bionts and its own nuclear and organellar DNA. plants must change the amount of water that gets pulled up The proposed FGS, and subsequent O-FGS definition through their roots depending on its water needs which should enhance biologists’ understanding of gene × pheno- change throughout the day. This diurnal flux of water is type interactions in a way that a traditional genomic defin- mediated by local changes in active aquaporins in root mem- ition cannot. The hologenome concept has been proposed to branes. In times of greater water demand more aquaporins address organisms and their microbiomes (Rosenberg et al., are produced/activated. Also, in areas of greater water 2007; Zilber-Rosenberg and Rosenberg, 2008). While the demand, such as deeper places in the soil profile where water hologenome falls nicely into the GSH framework outlined is more difficult to access, more active aquaporins are present above, it differs from the O-FGS in not including contribu- (McElrone et al., 2007 and references therein). Overall trends tions of macro-symbionts, and by potentially including tem- of system organization in space and time at the organismal porally non-significant commensal interactions (Bordenstein level are more complicated. Gene expression profiles change and Theis, 2015). In the following sections, I will discuss how in relation to stages of development, spatial location in the micro- and macro-symbionts are able to positively influence body (different organs, tissues, cell types, etc.) (Swynghedauw, the functioning of an organismal genetic system. In some 2006), and in response external environmental factors, both cases, however, symbiont influence may not be positive, such biotic and abiotic (Mopper et al.,2004). This is a subject for as in the case of parasites and agents of disease. Such organ- other reviews and, while it is certainly relevant, it will not be isms (and viruses) would not be included in an O-FGS as dis- discussed here for the sake of brevity and clarity. The ability of ease is an example of system disturbance and dysfunction; it all of these lower level components to change their behaviour to should be mentioned, however, that including a disease agent maintain homoeostasis and consistent higher level system out- in an O-FGS and studying the resulting phenotype could be put is the system’s ‘stability’ (von Bertalanffy, 1950; Bose, useful in disease research. A further clarification is needed in 2013). System stability is important for the functioning of lower the case of parasites and disease agents; their host is part of and higher level systems due to constraint effects of inter-level their own O-FGS as their host is required for their phases of interactions (Trewavas, 2006; Bose, 2013). In this case different functional existence. Groupings of O-FGSs are not obligator- levels of systems which border each other have top-down and ily inclusive; whether or not a gene should be included in an bottom-up interactions with each other and these interac- O-FGS should be determined on a case-by-case basis based on tions are vital for the functioning of higher level systems. the known contribution of said gene to organismal function. It is critical to recognize that due to the contextual nature Defining the functional gene system of an O-FGS, it is highly unlikely that two organisms will of an organism have the same O-FGS; O-FGSs should be identified for indi- vidual organisms, though at a certain point it would certainly The spatial/temporal organization of complex biological sys- be useful to generalize the O-FGS of organisms of one species tems previously described pertain to traditionally understood living in a certain context. The list of genes within an O-FGS gene systems; the genes that regulate the body come from the is dynamic over time; therefore, describing the complete host’s body cells’ genetic components. I will later argue that O-FGS of any given organism would only be able to be done higher level organismal system functions are often controlled ............................................................................................... .................................................................. 3 Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. retrospectively, after the death of the organism. This is due to While endophytes interact with the plant exclusively when the fact that genes may be constantly undergoing transcrip- they are inside, or entering (Hardoim, van Overbeek, van tional regulation, or even may be entering and leaving the Elsas, 2008), these horizontally acquired PGPRs interact with organismal system entirely (symbiont shuffling/swapping the plant in an epi- and endophytic way. This interaction is (reviewed Gilbert et al., 2010), or horizontal gene transfer). typically related to nutrient acquisition or growth promotion. This complete O-FGS would be nearly impossible to actually Animal systems contain similar classifications of primary describe, and even if it was, it would be massive and difficult or, obligate, microbes and secondary, or, facultative microbes. to work with. However, it could be useful to describe the O- Primary endosymbionts are obligate symbionts in that they are FGS of an organism during a time period of interest, such as required for host survival throughout many life stages. They during a functional life stage or during the onset of an envir- share a long evolutionary history and usually reside within spe- onmental change; researchers have moved in this direction in cialized tissues, such as bacteriomes in insects. These symbionts modern genomic studies with microarrays and other high- usually are associated with aiding in digestion and nutrient throughput technologies (Liu et al., 2007, for example). acquisition (Feldhaar, 2011), and are essential to the host’s development, growth, and homoeostasis. While interactions with obligate microbial symbionts provide grounded support Essential microbial symbiosis for GSH, they are well understood, obvious, and will not be discussed further. Secondary endosymbionts are usually con- The O-FGS definition I have proposed above requires an sidered facultative and do not have long evolutionary histories understanding of the relationship between a host and its vari- with their hosts. They reside largely in the haemocoel in insects ous beneficial microbial symbionts. For the purposes of this and in the intestinal tracts of other animals and can be acquired discourse I will define microbial symbionts as Friesen et al. vertically and horizontally. (2011) outlined originally for plants, though the word plant is interchangeable with any host title: microbial symbionts are Symbiotic microbes influence development, growth and ‘…microbes [which] interact with their plant hosts intimately; homoeostasis [that] can influence plant metabolism and hormonal pathways In simplified terms, the basis of the microbe–host mutualism in addition to providing novel nutritional or biosynthetic cap- is as follows: the host provides a growth environment rich in acities.’ These authors further explain the implications of the carbohydrate and nutrients and the microbes provide protec- above definition by suggesting that these microbial communi- tion from the effects of biotic and abiotic stresses and aid in ties change the phenotype of the plant (host) and have implica- growth and nutritional processes via the creation or modifica- tions for the plant’s interaction at ecosystem and evolutionary tion of biochemical pathways (reviewed Friesen et al., 2011). levels. In this section, I will focus on the host/microbe symbiotic This environment is either within the host, notably the gut in interactions and the importance of microbial symbionts for animals and various tissues in plants, or in the rhizosphere in successful organismal function. the case of epiphytic PGPRs. Within plants, endophytic bac- teria have direct access to photosynthate within the localized Within plant and animal systems area of the plant they inhabit (Gaiero et al., 2013), while Different classifications of microbes PGPRs mostly depend on root secretions for their carbon There are different types of microbes which live in and around source. In the case of fungal microbes, mainly mycorrhiza in plants which have an effect on their physiology and growth. this case, the organism is large and exists both inside the host Some of these microbes are endophytic, which means they organism and in the environment. The carbohydrate is live within the plant. There are two groups of endophytes obtained where the fungus is closely associated with the root. which affect plants differently: the obligate endophytes and In animals the majority of bacteria reside in or near the gut the facultative endophytes (reviewed in Friesen et al., 2011). and obtain their carbohydrate from the ingested food of the Obligate endophytes cannot exist in nature without their host. The cost to the host of providing nutrient and habitat host. Facultative endophytes do exist independently in nature, for the microbes is, at the least, balanced by the symbionts’ but will colonize a plant when they get a chance (Hardoim, positive effects on organismal function in most cases. van Overbeek, van Elsas, 2008). The specification of these groups is important because of the implications for the evolu- Development tionary history of each organism. Obligate endophytes are It has been shown experimentally that bacterial endophyte usually acquired vertically in the seed; these microbes are community composition changes in relation to plant physio- developmentally inseparable from their hosts in nature. logical and hormonal alterations which occur with age Facultative endophytes, while also influential, are not as (Gaiero et al., 2013 and sources within). The most well under- intimately associated with their hosts and as such do not exert stood developmental influence of microbes through phytohor- such a consistent (Gilbert et al., 2010) and large effect on mone action is the mechanisms by which microbes increase or plant traits (Pillay and Nowak, 1997). decrease plant ethylene levels. The inhibition of ethylene pro- Another important group of microbes to consider is duction is caused by microbes which produce ACC deami- known as plant-growth-promoting-rhizobacteria (PGPR). nase which degrades ACC, an essential ethylene precursor ............................................................................................... .................................................................. 4 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. (Hardoim, van Overbeek, van Elsas, 2008). Changes in which fixes N and produces active phytohormones such as microbial community during development regulate the bal- auxins and gibberellins (Lugtenberg, Chin-A-Woeng, Bloemberg, ance of ethylene related functions. High ethylene levels are 2002), which increase rooting and further increase nutrient needed for seeds to exit their dormant state, but if there is uptake (Steenhoudt and Vanderleyden, 2000). The Azospirillum too much ethylene after dormancy is broken there are nega- example is not an obscure case; plant associated microbes as a tive effects on other aspects of development. Dormant seeds whole are capable of producing every phytohormone known contain ethylene producing endophytes and not ACC (Friesen et al.,2011). degrading endophytes, but once dormancy is broken the Growth is influenced in animal systems largely via the sup- plant recruits facultative ACC degrading endophytes which, plementation of nutrients from beneficial microbes. The pri- in turn, regulates ethylene levels. Because endophytes and mary symbiont Buchnera in aphids supplements the host’s epiphytic PGPRs have the ability to influence phytohormone poor quality sap diet with essential amino acids and vitamins levels and nutrient availability they have the ability to (Zientz, Dandekar, Gross, 2004; Gündüz and Douglass, 2009). greatly influence not only plant growth, but also plant func- This type of interaction is very common in insects with nutrient tions at higher levels (reviewed in Hardoim, van Overbeek, poor diets such as cellulose and blood feeding insects as well van Elsas, 2008). as other sap feeders (reviewed Feldhaar, 2011). A less direct Although the field is still at quite a young stage, there is example is where a Streptmomyces symbiont makes antifungal considerable evidence for the importance of symbionts in products which aid in protection of fungus-farming-ants’ fun- various stages of development of animals, particularly in gus crops from loss due to parasitic Escovopsis fungal infection post-embryonic stages (reviewed in McFall-Ngai et al., 2013). (Seipke et al.,2011). In this way the bacterium exists within the The removal of symbionts from the egg masses the stink bug O-FGS of the ants in that they would likely suffer severe losses Halyomorpha halys results in dramatic decrease in fecundity to their essential food source without the genetic material con- and survivorship in first and, especially, second generation tained within the bacteria, even though these genes do not act individuals, demonstrating the importance of vertically trans- on them directly. Another well investigated system is of the mitted microbes in development (Taylor et al., 2014). broiler chicken where the spatial and temporal analyses of gut Submarine bathymodiolin bivalves are known to harbour microbe presence indicate characteristic community differences chemosynthetic bacteria epi- and endo-symbiotically on their which correspond to functions involving gut development, gills which may supply some or all of the animal’s energy improving carbohydrate and nitrogen acquisition, as well as requirements during adult life stages. While no symbionts are immunity (Pan and Yu, 2014). Similarly, changes in community known to associate with the bathymodiolin during larval composition also occur in the gut of the mosquito Anopheles stages, it is clear that young bivalves horizontally acquire gambiae during stages of development and after a blood meal. microbes from a very young age after settling in sulphide/sul- In this case the microbes are implicated in coping with reactive phate rich environments, suggesting their importance in estab- oxygen species during the digestion of the blood meal (Wang lishment and development (Laming et al.,2015). McFall-Ngai et al., 2011). (2014) extensively reviews current understanding of the Euprymna scolopes–Vibrio fischeri symbiosis in relation to not Homoeostasis only the acquisition of the V. fischeri endosymbionts, but also Throughout the life of the plant, symbiotic microbes aid in the mechanisms by which host tissue development is orche- the maintenance of homoeostasis of the organism by aiding in strated by the symbiont. Furthermore, there is evidence to sug- adaptation to dynamic environment. Liu et al. (2007) found gest that symbiotic bacteria in mice have evolved a contingent that AM colonization aids Medicago truncatula in resisting a dependency relationship where they supply essential develop- common bacterial pathogen. The cause of this increased mental signals important for immune system and perhaps also resistance was found to be related to changes in gene expres- brain development (reviewed in Selosse, Bessis, Pozo, 2014). sion locally and systemically in response to or caused by the AM colonization. The systemic gene expression change indi- Growth cates that there is a long distance signal present which allows Symbionts come at various energetic costs to the host. the AM to have an influence on the whole plant gene expres- Mycorrhizal interactions are known to receive as much as sion profile. Without these local and systematic gene expres- 20% of the total produced photosynthate (reviewed in sion profile changes induced by the AM relationship the plant Augé, 2001), yet the net result of mycorrhizal colonization is shows severe disease phenotype. AM fungi are known to still normally positive. Mycorrhizal growth benefits to their influence abiotic stress interactions as well. AM fungal colon- host include, but are not limited to, increased resistance to ization has been reported to increase stomatal conductance many abitotic stress factors (Singh, Singh Gill, Tuteja, 2011) and growth during drought conditions (Augé, 2004). Augé and increased nutrient uptake. Facultative endophytes and (2001) exhaustively reviewed AM effects on plant water rela- PGPRs can aid in capture of nutrient sources already in the tions during drought and found that there are many general soil which promotes rapid growth and successful invasion of mechanisms by which AM confer resistance such as: P and C plants in a new environment (Rout et al., 2013). Another nutritional balances and an interaction with host gene expres- example of a beneficial microbe is the PGPR Azospirillum sion timing. One such gene expression change caused by AM ............................................................................................... .................................................................. 5 Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. which could change water relations during drought would be pea aphid from red to green, which helps to avoid being eaten that of an aquaporin-producing gene, which was among those by ladybirds. However, while this change makes it more genes affected by AM colonization (Liu et al., 2007). favourable to endoparasitic wasp attacks it has been observed that Rickettsiella commonly occurs with other bacteria that Bacterial symbionts are also known to enhance host resist- confer resistance to endoparasitc wasps (Oliver, Smith, ance to biotic and abiotic stresses. Various endophytic Russell, 2014). microbes contribute to host plant systemic acquired resistance (SAR) which helps the plant to respond and effectively stop the spread of disease. Once again, this is possible because the Including macro-symbionts into the bacteria are able to produce phytohormones, in this case sali- O-FGS with ant–plant examples cylic acid which is active in plant SAR responses (reviewed in Friesen et al., 2011; for example Maurhofer et al., 1998). Ant–plant mutualisms should also be considered in a O-FGS Lanna-Filho et al. (2013) report that endophytic bacteria in context in regards to relations of all partners in functional life the genus Bacillus secrete antibiotics and gaseous organic sig- stages. Myrmecochorous plants require ants to disperse their nalling molecules which aid in long distance defense responses seeds into safe, nutrient rich refuse chambers which may be in tomato (Solanum lycopersicum). They also report that, crit- themselves considered the extended phenotype of the ant ically, Bacillus also secretes proteins which aid in disease (Lengyel et al., 2010). In many myrmecophytous systems ants resistance via direct interaction in induced systematic resist- obligatorily live within the plant, and are fed directly by the ance (ISR) pathways. There are also many examples of bac- plant while defending the plant from herbivores. Refuse teria conferring abiotic stress relief. The common endophytic stored in domatia, and saprotrophic fungi living within, are bacteria Pseudomonas and Gigaspora confer heavy metal known to be important factors in N uptake for the plant resistance via moderation of plant systemic ethylene levels via (Mayer et al.,2014). Also, endophytic fungi in Acacia leaves an ACC degrading pathway. Endophytic bacteria can also (González-Teuber, Jiménez-Alemán, Boland, 2014) and bac- have an influence over stomatal aperture and confer resistance teria which live in the feet of associated ants (González-Teuber, to drought (reviewed in Friesen et al., 2011; for example Kaltenpoth, Boland, 2014) produce antifungal compounds Arnold and Engelbrecht, 2007). Facultative bacterial endo- which protect plant leaves from parasite infection. In the case phytes can mitigate low nutrient stress as seen in the well- of myrmecophyte systems the plant is usually considered the known Fabaceae–rhizobia interaction with N supplementa- host, and here many symbionts, including ants, come together tion. This stress mitigation function is essential to the successful to contribute to its O-FGS. While only ant–plant systems were functioning of the plant host in low nutrient environments. presented here it is clear how macro-symbionts may be included A final important idea to consider is that microbe commu- into the O-FGS of other organisms. nities and their products vary over time and within different structures of the plant (Gilbert et al., 2010). The realizable effect on plant phenotype and the mechanisms behind these Conclusion variables is still largely unknown (Gaiero et al., 2013), Thinking of organisms as functioning strictly in terms of their although there is evidence to suggest that microbes which genomic material may work for low level processes, but often influence ethylene levels can aid recently germinated plants is insufficient for considering higher level phenotypic expres- cope with environmental stresses (Hardoim, van Overbeek, sions. After synthesizing some fundamental ideas from gen- van Elsas, 2008). It is evident, however, that spatial/temporal eral systems theory and systems biology it is possible to patterns of symbiotic microbial activities have an important generally describe scales of genetic interaction over space and function in the life of the host. Functions in growth, develop- time. The resulting GSH serves as a conceptual framework to ment and homoeostasis happen over time, and as such they think about issues involving poorly understood complex phe- adapt to changing environmental conditions. Changing notypes and an illustration of the type of dynamics which microbial presence is essential to the maintenance of these might be at play. From GSH arise Functional Gene Systems organismal functions within an ever changing environment. which are sublevels of genetic interaction within time and Secondary endosymbionts are understood to aid in reduc- space. Finally the case is made that to define the Organismal- tion of heat and viral stress, such as in the Drosophila– FGS it should be necessary in many cases to take microbial Wolbachia interactions, and a consortium of bacteria is and macro-symbionts into the consideration, especially if try- understood to aid in protecting pea aphids against endopara- ing to understand complex organism-scale phenomena. sitic wasps (reviewed in Feldhaar, 2011). In the latter case the resistance seems to be at least partially conferred by a bac- teriophage within one member of the bacterial consortia that Acknowledgements creates toxins that target the cells of the endoparasitic larvae (Oliver, Leather, Cook, 2009). Body coloration is also Thank you to David Salt for engaging in talks with me about important for insects to avoid predators and parasites. GSH. Thank you to James Robert Downie, Kester Ratcliff, Infection with Rickettsiella bacteria changes the colour of the David Salt, and two anonymous editors for helpful revisions. ............................................................................................... .................................................................. 6 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. Gilbert, S. F., McDonald, E., Boyle, N. et al. (2010) Symbiosis as a source Author biography of selectable epigenetic variation: taking the heat for the big guy, Philosophical Transactions of the Royal Society of London. Series B, James graduated from the University of Aberdeen with an Biological Sciences, 365, 671–678. honours degree in plant science, and is currently pursuing a master’s degree in the Erasmus Mundus + Evolutionary González-Teuber, M., Jiménez-Alemán, G. H. and Boland, W. (2014) Foliar Biology (MEME) programme. His interests include studying endophytic fungi as potential protectors from pathogens in myrme- the nature and consequences of symbiosis in the scope organ- cophytic Acacia plants, Communicative & Integrative Biology,7, ismal functioning and evolutionary trajectories, particularly e970500. in cases involving plants and insects. He is also concerned González-Teuber, M., Kaltenpoth, M. and Boland, W. (2014) Mutualistic with topics of cultural evolution and the impact of culture on ants as an indirect defence against leaf pathogens, The New society and the planet, and the interface where these merge Phytologist, 202, 640–650. with biology. Gündüz, E. A. and Douglas, A. E. 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Fischer, Jena. hemiparasites in nutrient poor ecosystems, Oikos, 82, 609–611. Xue, C., Yang, X., Bouman, B. A. M. et al. (2008) Optimizing yield, water Pritchard, L. and Birch, P. (2011) A systems biology perspective on requirements, and water productivity of aerobic rice for the North plant–microbe interactions: biochemical and structural targets of China Plain, Irrigation Science, 26, 459–474. pathogen effectors, Plant Science, 180, 584–603. Zientz, E., Dandekar, T. and Gross, R. (2004) Metabolic interdependence Ridley, M. (2006) Genome: The Autobiography of a Species in 23 of obligate intracellular bacteria and their insect hosts, Microbiology Chapters, HarperCollins, New York. and Molecular Biology Reviews: MMBR, 68, 745–770. Rosenberg, E., Koren, O., Reshef, L. et al. (2007) The role of microorgan- Zilber-Rosenberg, I. and Rosenberg, E. 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‘Genome’ doesn’t cover it: Introducing Gene Systems Hypothesis and Functional Gene Systems

Fredrickson, James O.
Bioscience Horizons , Volume 10 – Jun 13, 2017
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BioscienceHorizons Volume 10 2017 10.1093/biohorizons/hzx005 ............................................................................................ ..................................................................... Review article ‘Genome’ doesn’t cover it: introducing gene systems hypothesis and functional gene systems James O. Fredrickson Institute of Biological and Environmental Sciences, University of Aberdeen, Cruickshank Building, St. Machar Drive, Aberdeen AB24 3UU, UK *Corresponding author: Institut des Sciences de l’Evolution de Montpellier, UMR 5554, Universite Montpellier 2, Montpellier, France. Email: j.fredrickson.10@aberdeen.ac.uk Supervisor: David E. Salt, Room A02 Plant Sciences, Sutton Bonington, Campus, Sutton Bonington, Leicestershire LE12 5RD, UK. ............................................................................................ ..................................................................... Traditionally, the genes which contribute to the phenotype of a eukaryotic organism were considered to be housed within its nuclear genome, but today thisisoften understood to notbethe case.In order to better understand how high- level complex phenotypic expressions arise I propose a conceptual framework composed of core systems biology ideas integrated with current understanding of genetic systems: gene systems hypothesis (GSH). The implications of this GSH framework allow for an organism level functional gene system (O-FGS) definition which incorporates the integration of macro- and micro-symbiont gene systems. In support of the proposed O-FGS definition a brief review of current literature is presented which demonstrates the influence of micro- and macro-symbionts in plant and animal development, growth and persistence. Key words: symbiosis, systems biology, mutualism, emergent, phenotype Submitted on 24 May 2014; editorial decision on 22 May 2017 ............................................................................................ ..................................................................... Introduction to not be appropriate when considering higher level complex phenotypes. The word ‘genome’ was created and defined by Hans Winkler who merged the word ‘gene’ with the suffix -ome, which A substantial body of current work which investigates means body (Winkler, 1920). This initial definition provides multicellular organismal function does not consider genetic the conceptual definition of the genome—the genes in the material which resides outside of the somatic cells of the body. During the time when the human genome was being organism in question (Bose, 2013; Bolger et al., 2014). A sequenced Matt Ridley wrote a book describing the human prime example of this is found in recent work on rice growth genome which began by saying that all of the genetically and function where most studies focus on ‘germplasm encoded information needed to make a human was contained improvement’ and attempt to attribute various complex phe- in the DNA of the human genome (Ridley, 2006). The notypes, such as drought tolerance, to just a few key genetic conclusion within his book is that these genes are the controllers markers (Xue et al., 2008; Cairns et al., 2011; Pray et al., of organismal development and function. The idea that the 2011; Serraj et al., 2011; Jagadish et al., 2012). Systems biol- information required for function and development is derived ogy should be important when considering genes involved in from the genes in an organism’s somatic cells still prevails organismal function, and indeed there are calls for integrating today. This assumption has yielded a lot of adequate results molecular systems through to ecosystems for plant breeding when low level cellular and basic structural phenomena are (Keurentjes et al., 2011), and there are also advancements considered. However, strict adherence to this assumption seems being made in regards to systems biology of plants and ............................................................................................... .................................................................. © The Author 2017. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/ licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. microbes, but mainly involving infection dynamics and disease in this case is the genetic code (including coding regions and cis (Pritchard and Birch, 2011; Garbutt et al., 2014). In these cases, regulatory elements), where the emergent property is the func- systems dynamics and pathogenic microbes are taken into tional gene product which results from the interactions between account, but inclusion of beneficial symbionts are still lacking. nuclear and cytoplasmic proteins, RNAs, and the surrounding In this review I will explain why any attempt to understand the DNA in response to environmental stimuli. All levels of bio- basis of an organism’s higher level functions or phenotypes can- logical functionality, from this basic system level up to the not just consider an organism’s ‘germplasm’ alone, but must organism, are complex systems which can be considered. also include the genes its macro- and micro-symbionts. In order However, due to the abundance of them, only a select few will to integrate the host organism with all of its symbionts I will pro- be used to make the argument for GSH, though all are possible pose a systems theory based framework which should be utilized effective candidates. Also, GSH applies to biological systems when trying to conceptualize how an individual organism with which exist at levels higher than the organism, such as commu- all of its symbionts, or functional gene system (FGS), works. nities and ecosystems; these will not be discussed because they extend beyond the context of this review. In all cases, biological systems do not exist independently and their functions are not Gene systems hypothesis static; they exist in and respond to changes in external condi- tions. Consideration of environment is essential to understand Gene systems hypothesis (GSH) is the intuitive result of the the functionality of complex biological systems at any level. integration of many concepts and thought processes which are currently not often combined in modern biological Defining environment research methodologies. In order to present GSH more clearly I will first briefly explain the most pertinent aspects of the Everything is environment foundational concepts. Biological systems adapt to a constantly changing environ- ment. The fundamental unit of most biological systems is Systems biology DNA. DNA, as a macromolecule, is quite inert. DNA must first interact with its immediate environment to be biologic- GSH is formed from a body of current scientific understanding ally active: transcription factors must bind to it in order to integrated within the concept of systems biology. Systems biology make mRNA, which will interact with a ribosome, which will is the biological application of von Bertalanffy’s general systems help it to interact with tRNAs in the cellular environment, theory (GST) (von Bertalanffy, 1950). GST and systems biology which will ultimately result in formation of a peptide. Of are abstract ideas and mathematical models which attempt to course, all of these cellular systems are composed of molecules explain complex biological systems. Functional biological entities which are themselves, the results of complex systems. In this are the result of multi-component complex systems. The com- way of thinking, all biological systems and their emergent plexity of biological phenomena is the reason for instances of functions constitute the environment of all other biological reductionist inadequacy and the importance of a systems biology systems. These systems are constantly interacting with each conceptual context. The most relevant qualities of complex sys- other and the abiotic environment. The varying interactions tems and their resultant phenomena are outlined below. between components of the complex system influence the sys- System complexity arises from non-linear interactions tem output (Trewavas, 2006; Bose, 2013). Equally important between the components of systems and their emergent proper- to recognizing that these systems are interacting with their ties. System components which behave in a way that is influ- environments is that the way they influence, and are influ- enced by multiple properties of some of the other components enced by, their environment is directly related to the organiza- of the system are described as interacting in a non-linear man- tion of the system components in space and time. ner. These non-linear interactions result in unpredictable or, emergent properties. An emergent property is unexpected System/environment interaction within space and time because its existence cannot be derived from total knowledge of This concept is well documented throughout biology. This the lower components of the system; this is due to the non- relationship is obvious at the molecular level. A gene’s protein linear relationship of the interactions of the lower components. product interacts with other proteins to produce some prod- Hence, an emergent property of a system is greater than the uct (quaternary protein structure, signal transduction path- sum of the properties of the system components (Bedau, 1997; way, etc.). This product has emergent functions associated Bose, 2013). These emergent properties of biological systems with it and these functions affect the immediate cellular envir- are what biologists recognize as organismal phenotypes. These onment at the moment in time when they act (quaternary emergent system properties integrate at many levels to create protein binds substrate and produces product; signal trans- higher level complex phenotypes at the level of the organism. duction pathway is activated by an environmental signal and Complex biological systems exist across multiple levels of causes a local response). Interacting systems have immediate organization. In this discourse I will often refer to lower level and local effects on their environments. As the distance in systems. Lower level systems, in this sense, are the various com- space and time between the interacting systems increases, plex systems which integrate to produce the biological entity the resultant function, or change in the environment, also commonly recognized as an organism. The lowest level system decreases, in general (von Bertalanffy, 1950). This decrease is ............................................................................................... .................................................................. 2 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. dependent on the degree of bifurcation effect the lower level or influenced by lower level gene systems which come from system change has on higher level systems. Bifurcation is the symbionts. phenomenon in complex systems where a small change in a The conclusion that symbiont genes can be as important for parameter of a lower level system can have a large change in a organismal function as those found in the organismal germ- higher level system output (Bose, 2013). A clear example of plasm suggests that a new functional demarcation should be this in ecological studies is the ‘keystone species’ where the made in the characterization of organismal entities. GST tells population dynamics of a single species has an unexpected us that a complex system maintains homoeostasis within a and disproportionate effect on community structure (Press, changing environment over time, or throughout various phases 1998). The previously mentioned molecular examples were of its functional existence, through its intrinsic stability (von instances of interaction over space and time. Organization in Bertalanffy, 1950). Phases of functional existence, in the case space and time also has influence over system output. of a eukaryotic organism, could be loosely defined as early From the molecular and cellular levels, spatial and tem- development, growth and persistence, and reproduction. These poral system organizational relationships are also easy to con- are certainly not necessarily distinct phases and this list is not ceptualize, and their potential for or organismal change is exhaustive, but this is a basic functional framework of a eukar- clear. Auxin’s involvement in coleoptile phototropism is a yote’s life, and will serve as a structure for the following exam- good example. After light is sensed by the tip of the coleoptile, ples. The definition of the organismal FGS (O-FGS) should be auxin is sent down the side of the tissue opposite to that inclusive of all of the specific genes/gene systems (hereafter: which the light was sensed on which causes local cell elong- genes) which contribute to the maintenance of homoeostasis ation and subsequent bending toward the light source within an organism during the phases of its life. I suggest that (Hasegawa and Sakoda, 1988). Spatial organization is inte- an O-FGS includes the DNA of all associated beneficial sym- grated with temporal organization as well. For example, bionts and its own nuclear and organellar DNA. plants must change the amount of water that gets pulled up The proposed FGS, and subsequent O-FGS definition through their roots depending on its water needs which should enhance biologists’ understanding of gene × pheno- change throughout the day. This diurnal flux of water is type interactions in a way that a traditional genomic defin- mediated by local changes in active aquaporins in root mem- ition cannot. The hologenome concept has been proposed to branes. In times of greater water demand more aquaporins address organisms and their microbiomes (Rosenberg et al., are produced/activated. Also, in areas of greater water 2007; Zilber-Rosenberg and Rosenberg, 2008). While the demand, such as deeper places in the soil profile where water hologenome falls nicely into the GSH framework outlined is more difficult to access, more active aquaporins are present above, it differs from the O-FGS in not including contribu- (McElrone et al., 2007 and references therein). Overall trends tions of macro-symbionts, and by potentially including tem- of system organization in space and time at the organismal porally non-significant commensal interactions (Bordenstein level are more complicated. Gene expression profiles change and Theis, 2015). In the following sections, I will discuss how in relation to stages of development, spatial location in the micro- and macro-symbionts are able to positively influence body (different organs, tissues, cell types, etc.) (Swynghedauw, the functioning of an organismal genetic system. In some 2006), and in response external environmental factors, both cases, however, symbiont influence may not be positive, such biotic and abiotic (Mopper et al.,2004). This is a subject for as in the case of parasites and agents of disease. Such organ- other reviews and, while it is certainly relevant, it will not be isms (and viruses) would not be included in an O-FGS as dis- discussed here for the sake of brevity and clarity. The ability of ease is an example of system disturbance and dysfunction; it all of these lower level components to change their behaviour to should be mentioned, however, that including a disease agent maintain homoeostasis and consistent higher level system out- in an O-FGS and studying the resulting phenotype could be put is the system’s ‘stability’ (von Bertalanffy, 1950; Bose, useful in disease research. A further clarification is needed in 2013). System stability is important for the functioning of lower the case of parasites and disease agents; their host is part of and higher level systems due to constraint effects of inter-level their own O-FGS as their host is required for their phases of interactions (Trewavas, 2006; Bose, 2013). In this case different functional existence. Groupings of O-FGSs are not obligator- levels of systems which border each other have top-down and ily inclusive; whether or not a gene should be included in an bottom-up interactions with each other and these interac- O-FGS should be determined on a case-by-case basis based on tions are vital for the functioning of higher level systems. the known contribution of said gene to organismal function. It is critical to recognize that due to the contextual nature Defining the functional gene system of an O-FGS, it is highly unlikely that two organisms will of an organism have the same O-FGS; O-FGSs should be identified for indi- vidual organisms, though at a certain point it would certainly The spatial/temporal organization of complex biological sys- be useful to generalize the O-FGS of organisms of one species tems previously described pertain to traditionally understood living in a certain context. The list of genes within an O-FGS gene systems; the genes that regulate the body come from the is dynamic over time; therefore, describing the complete host’s body cells’ genetic components. I will later argue that O-FGS of any given organism would only be able to be done higher level organismal system functions are often controlled ............................................................................................... .................................................................. 3 Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. retrospectively, after the death of the organism. This is due to While endophytes interact with the plant exclusively when the fact that genes may be constantly undergoing transcrip- they are inside, or entering (Hardoim, van Overbeek, van tional regulation, or even may be entering and leaving the Elsas, 2008), these horizontally acquired PGPRs interact with organismal system entirely (symbiont shuffling/swapping the plant in an epi- and endophytic way. This interaction is (reviewed Gilbert et al., 2010), or horizontal gene transfer). typically related to nutrient acquisition or growth promotion. This complete O-FGS would be nearly impossible to actually Animal systems contain similar classifications of primary describe, and even if it was, it would be massive and difficult or, obligate, microbes and secondary, or, facultative microbes. to work with. However, it could be useful to describe the O- Primary endosymbionts are obligate symbionts in that they are FGS of an organism during a time period of interest, such as required for host survival throughout many life stages. They during a functional life stage or during the onset of an envir- share a long evolutionary history and usually reside within spe- onmental change; researchers have moved in this direction in cialized tissues, such as bacteriomes in insects. These symbionts modern genomic studies with microarrays and other high- usually are associated with aiding in digestion and nutrient throughput technologies (Liu et al., 2007, for example). acquisition (Feldhaar, 2011), and are essential to the host’s development, growth, and homoeostasis. While interactions with obligate microbial symbionts provide grounded support Essential microbial symbiosis for GSH, they are well understood, obvious, and will not be discussed further. Secondary endosymbionts are usually con- The O-FGS definition I have proposed above requires an sidered facultative and do not have long evolutionary histories understanding of the relationship between a host and its vari- with their hosts. They reside largely in the haemocoel in insects ous beneficial microbial symbionts. For the purposes of this and in the intestinal tracts of other animals and can be acquired discourse I will define microbial symbionts as Friesen et al. vertically and horizontally. (2011) outlined originally for plants, though the word plant is interchangeable with any host title: microbial symbionts are Symbiotic microbes influence development, growth and ‘…microbes [which] interact with their plant hosts intimately; homoeostasis [that] can influence plant metabolism and hormonal pathways In simplified terms, the basis of the microbe–host mutualism in addition to providing novel nutritional or biosynthetic cap- is as follows: the host provides a growth environment rich in acities.’ These authors further explain the implications of the carbohydrate and nutrients and the microbes provide protec- above definition by suggesting that these microbial communi- tion from the effects of biotic and abiotic stresses and aid in ties change the phenotype of the plant (host) and have implica- growth and nutritional processes via the creation or modifica- tions for the plant’s interaction at ecosystem and evolutionary tion of biochemical pathways (reviewed Friesen et al., 2011). levels. In this section, I will focus on the host/microbe symbiotic This environment is either within the host, notably the gut in interactions and the importance of microbial symbionts for animals and various tissues in plants, or in the rhizosphere in successful organismal function. the case of epiphytic PGPRs. Within plants, endophytic bac- teria have direct access to photosynthate within the localized Within plant and animal systems area of the plant they inhabit (Gaiero et al., 2013), while Different classifications of microbes PGPRs mostly depend on root secretions for their carbon There are different types of microbes which live in and around source. In the case of fungal microbes, mainly mycorrhiza in plants which have an effect on their physiology and growth. this case, the organism is large and exists both inside the host Some of these microbes are endophytic, which means they organism and in the environment. The carbohydrate is live within the plant. There are two groups of endophytes obtained where the fungus is closely associated with the root. which affect plants differently: the obligate endophytes and In animals the majority of bacteria reside in or near the gut the facultative endophytes (reviewed in Friesen et al., 2011). and obtain their carbohydrate from the ingested food of the Obligate endophytes cannot exist in nature without their host. The cost to the host of providing nutrient and habitat host. Facultative endophytes do exist independently in nature, for the microbes is, at the least, balanced by the symbionts’ but will colonize a plant when they get a chance (Hardoim, positive effects on organismal function in most cases. van Overbeek, van Elsas, 2008). The specification of these groups is important because of the implications for the evolu- Development tionary history of each organism. Obligate endophytes are It has been shown experimentally that bacterial endophyte usually acquired vertically in the seed; these microbes are community composition changes in relation to plant physio- developmentally inseparable from their hosts in nature. logical and hormonal alterations which occur with age Facultative endophytes, while also influential, are not as (Gaiero et al., 2013 and sources within). The most well under- intimately associated with their hosts and as such do not exert stood developmental influence of microbes through phytohor- such a consistent (Gilbert et al., 2010) and large effect on mone action is the mechanisms by which microbes increase or plant traits (Pillay and Nowak, 1997). decrease plant ethylene levels. The inhibition of ethylene pro- Another important group of microbes to consider is duction is caused by microbes which produce ACC deami- known as plant-growth-promoting-rhizobacteria (PGPR). nase which degrades ACC, an essential ethylene precursor ............................................................................................... .................................................................. 4 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. (Hardoim, van Overbeek, van Elsas, 2008). Changes in which fixes N and produces active phytohormones such as microbial community during development regulate the bal- auxins and gibberellins (Lugtenberg, Chin-A-Woeng, Bloemberg, ance of ethylene related functions. High ethylene levels are 2002), which increase rooting and further increase nutrient needed for seeds to exit their dormant state, but if there is uptake (Steenhoudt and Vanderleyden, 2000). The Azospirillum too much ethylene after dormancy is broken there are nega- example is not an obscure case; plant associated microbes as a tive effects on other aspects of development. Dormant seeds whole are capable of producing every phytohormone known contain ethylene producing endophytes and not ACC (Friesen et al.,2011). degrading endophytes, but once dormancy is broken the Growth is influenced in animal systems largely via the sup- plant recruits facultative ACC degrading endophytes which, plementation of nutrients from beneficial microbes. The pri- in turn, regulates ethylene levels. Because endophytes and mary symbiont Buchnera in aphids supplements the host’s epiphytic PGPRs have the ability to influence phytohormone poor quality sap diet with essential amino acids and vitamins levels and nutrient availability they have the ability to (Zientz, Dandekar, Gross, 2004; Gündüz and Douglass, 2009). greatly influence not only plant growth, but also plant func- This type of interaction is very common in insects with nutrient tions at higher levels (reviewed in Hardoim, van Overbeek, poor diets such as cellulose and blood feeding insects as well van Elsas, 2008). as other sap feeders (reviewed Feldhaar, 2011). A less direct Although the field is still at quite a young stage, there is example is where a Streptmomyces symbiont makes antifungal considerable evidence for the importance of symbionts in products which aid in protection of fungus-farming-ants’ fun- various stages of development of animals, particularly in gus crops from loss due to parasitic Escovopsis fungal infection post-embryonic stages (reviewed in McFall-Ngai et al., 2013). (Seipke et al.,2011). In this way the bacterium exists within the The removal of symbionts from the egg masses the stink bug O-FGS of the ants in that they would likely suffer severe losses Halyomorpha halys results in dramatic decrease in fecundity to their essential food source without the genetic material con- and survivorship in first and, especially, second generation tained within the bacteria, even though these genes do not act individuals, demonstrating the importance of vertically trans- on them directly. Another well investigated system is of the mitted microbes in development (Taylor et al., 2014). broiler chicken where the spatial and temporal analyses of gut Submarine bathymodiolin bivalves are known to harbour microbe presence indicate characteristic community differences chemosynthetic bacteria epi- and endo-symbiotically on their which correspond to functions involving gut development, gills which may supply some or all of the animal’s energy improving carbohydrate and nitrogen acquisition, as well as requirements during adult life stages. While no symbionts are immunity (Pan and Yu, 2014). Similarly, changes in community known to associate with the bathymodiolin during larval composition also occur in the gut of the mosquito Anopheles stages, it is clear that young bivalves horizontally acquire gambiae during stages of development and after a blood meal. microbes from a very young age after settling in sulphide/sul- In this case the microbes are implicated in coping with reactive phate rich environments, suggesting their importance in estab- oxygen species during the digestion of the blood meal (Wang lishment and development (Laming et al.,2015). McFall-Ngai et al., 2011). (2014) extensively reviews current understanding of the Euprymna scolopes–Vibrio fischeri symbiosis in relation to not Homoeostasis only the acquisition of the V. fischeri endosymbionts, but also Throughout the life of the plant, symbiotic microbes aid in the mechanisms by which host tissue development is orche- the maintenance of homoeostasis of the organism by aiding in strated by the symbiont. Furthermore, there is evidence to sug- adaptation to dynamic environment. Liu et al. (2007) found gest that symbiotic bacteria in mice have evolved a contingent that AM colonization aids Medicago truncatula in resisting a dependency relationship where they supply essential develop- common bacterial pathogen. The cause of this increased mental signals important for immune system and perhaps also resistance was found to be related to changes in gene expres- brain development (reviewed in Selosse, Bessis, Pozo, 2014). sion locally and systemically in response to or caused by the AM colonization. The systemic gene expression change indi- Growth cates that there is a long distance signal present which allows Symbionts come at various energetic costs to the host. the AM to have an influence on the whole plant gene expres- Mycorrhizal interactions are known to receive as much as sion profile. Without these local and systematic gene expres- 20% of the total produced photosynthate (reviewed in sion profile changes induced by the AM relationship the plant Augé, 2001), yet the net result of mycorrhizal colonization is shows severe disease phenotype. AM fungi are known to still normally positive. Mycorrhizal growth benefits to their influence abiotic stress interactions as well. AM fungal colon- host include, but are not limited to, increased resistance to ization has been reported to increase stomatal conductance many abitotic stress factors (Singh, Singh Gill, Tuteja, 2011) and growth during drought conditions (Augé, 2004). Augé and increased nutrient uptake. Facultative endophytes and (2001) exhaustively reviewed AM effects on plant water rela- PGPRs can aid in capture of nutrient sources already in the tions during drought and found that there are many general soil which promotes rapid growth and successful invasion of mechanisms by which AM confer resistance such as: P and C plants in a new environment (Rout et al., 2013). Another nutritional balances and an interaction with host gene expres- example of a beneficial microbe is the PGPR Azospirillum sion timing. One such gene expression change caused by AM ............................................................................................... .................................................................. 5 Review article Bioscience Horizons � Volume 10 2017 ............................................................................................... .................................................................. which could change water relations during drought would be pea aphid from red to green, which helps to avoid being eaten that of an aquaporin-producing gene, which was among those by ladybirds. However, while this change makes it more genes affected by AM colonization (Liu et al., 2007). favourable to endoparasitic wasp attacks it has been observed that Rickettsiella commonly occurs with other bacteria that Bacterial symbionts are also known to enhance host resist- confer resistance to endoparasitc wasps (Oliver, Smith, ance to biotic and abiotic stresses. Various endophytic Russell, 2014). microbes contribute to host plant systemic acquired resistance (SAR) which helps the plant to respond and effectively stop the spread of disease. Once again, this is possible because the Including macro-symbionts into the bacteria are able to produce phytohormones, in this case sali- O-FGS with ant–plant examples cylic acid which is active in plant SAR responses (reviewed in Friesen et al., 2011; for example Maurhofer et al., 1998). Ant–plant mutualisms should also be considered in a O-FGS Lanna-Filho et al. (2013) report that endophytic bacteria in context in regards to relations of all partners in functional life the genus Bacillus secrete antibiotics and gaseous organic sig- stages. Myrmecochorous plants require ants to disperse their nalling molecules which aid in long distance defense responses seeds into safe, nutrient rich refuse chambers which may be in tomato (Solanum lycopersicum). They also report that, crit- themselves considered the extended phenotype of the ant ically, Bacillus also secretes proteins which aid in disease (Lengyel et al., 2010). In many myrmecophytous systems ants resistance via direct interaction in induced systematic resist- obligatorily live within the plant, and are fed directly by the ance (ISR) pathways. There are also many examples of bac- plant while defending the plant from herbivores. Refuse teria conferring abiotic stress relief. The common endophytic stored in domatia, and saprotrophic fungi living within, are bacteria Pseudomonas and Gigaspora confer heavy metal known to be important factors in N uptake for the plant resistance via moderation of plant systemic ethylene levels via (Mayer et al.,2014). Also, endophytic fungi in Acacia leaves an ACC degrading pathway. Endophytic bacteria can also (González-Teuber, Jiménez-Alemán, Boland, 2014) and bac- have an influence over stomatal aperture and confer resistance teria which live in the feet of associated ants (González-Teuber, to drought (reviewed in Friesen et al., 2011; for example Kaltenpoth, Boland, 2014) produce antifungal compounds Arnold and Engelbrecht, 2007). Facultative bacterial endo- which protect plant leaves from parasite infection. In the case phytes can mitigate low nutrient stress as seen in the well- of myrmecophyte systems the plant is usually considered the known Fabaceae–rhizobia interaction with N supplementa- host, and here many symbionts, including ants, come together tion. This stress mitigation function is essential to the successful to contribute to its O-FGS. While only ant–plant systems were functioning of the plant host in low nutrient environments. presented here it is clear how macro-symbionts may be included A final important idea to consider is that microbe commu- into the O-FGS of other organisms. nities and their products vary over time and within different structures of the plant (Gilbert et al., 2010). The realizable effect on plant phenotype and the mechanisms behind these Conclusion variables is still largely unknown (Gaiero et al., 2013), Thinking of organisms as functioning strictly in terms of their although there is evidence to suggest that microbes which genomic material may work for low level processes, but often influence ethylene levels can aid recently germinated plants is insufficient for considering higher level phenotypic expres- cope with environmental stresses (Hardoim, van Overbeek, sions. After synthesizing some fundamental ideas from gen- van Elsas, 2008). It is evident, however, that spatial/temporal eral systems theory and systems biology it is possible to patterns of symbiotic microbial activities have an important generally describe scales of genetic interaction over space and function in the life of the host. Functions in growth, develop- time. The resulting GSH serves as a conceptual framework to ment and homoeostasis happen over time, and as such they think about issues involving poorly understood complex phe- adapt to changing environmental conditions. Changing notypes and an illustration of the type of dynamics which microbial presence is essential to the maintenance of these might be at play. From GSH arise Functional Gene Systems organismal functions within an ever changing environment. which are sublevels of genetic interaction within time and Secondary endosymbionts are understood to aid in reduc- space. Finally the case is made that to define the Organismal- tion of heat and viral stress, such as in the Drosophila– FGS it should be necessary in many cases to take microbial Wolbachia interactions, and a consortium of bacteria is and macro-symbionts into the consideration, especially if try- understood to aid in protecting pea aphids against endopara- ing to understand complex organism-scale phenomena. sitic wasps (reviewed in Feldhaar, 2011). In the latter case the resistance seems to be at least partially conferred by a bac- teriophage within one member of the bacterial consortia that Acknowledgements creates toxins that target the cells of the endoparasitic larvae (Oliver, Leather, Cook, 2009). Body coloration is also Thank you to David Salt for engaging in talks with me about important for insects to avoid predators and parasites. GSH. Thank you to James Robert Downie, Kester Ratcliff, Infection with Rickettsiella bacteria changes the colour of the David Salt, and two anonymous editors for helpful revisions. ............................................................................................... .................................................................. 6 Bioscience Horizons � Volume 10 2017 Review article ............................................................................................... .................................................................. Gilbert, S. F., McDonald, E., Boyle, N. et al. (2010) Symbiosis as a source Author biography of selectable epigenetic variation: taking the heat for the big guy, Philosophical Transactions of the Royal Society of London. Series B, James graduated from the University of Aberdeen with an Biological Sciences, 365, 671–678. honours degree in plant science, and is currently pursuing a master’s degree in the Erasmus Mundus + Evolutionary González-Teuber, M., Jiménez-Alemán, G. H. and Boland, W. (2014) Foliar Biology (MEME) programme. His interests include studying endophytic fungi as potential protectors from pathogens in myrme- the nature and consequences of symbiosis in the scope organ- cophytic Acacia plants, Communicative & Integrative Biology,7, ismal functioning and evolutionary trajectories, particularly e970500. in cases involving plants and insects. He is also concerned González-Teuber, M., Kaltenpoth, M. and Boland, W. (2014) Mutualistic with topics of cultural evolution and the impact of culture on ants as an indirect defence against leaf pathogens, The New society and the planet, and the interface where these merge Phytologist, 202, 640–650. with biology. Gündüz, E. A. and Douglas, A. E. 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