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applied sciences Review Hormonal Interactions Underlying Rootstock-Induced Vigor Control in Horticultural Crops 1 , † 1 , 2 , † 3 4 1 1 Faisal Hayat , Juan Li *, Shahid Iqbal , Ummara Khan , Nadia Ahmed Ali , Yang Peng , Leming Hong , 5 6 1 , 1 1 7 Sumeera Asghar , Hafiz Umer Javed , Caiqin Li *, Wenpei Song , Panfeng Tu , Jiezhong Chen and Muhammad Adnan Shahid College of Horticulture, Zhongkai University of Agriculture and Engineering, Guangzhou 510408, China Horticultural Science Department, North Florida Research and Education Center, University of Florida/IFAS, Quincy, FL 32351, USA College of Food Science and Technology, Nanjing Agricultural University, Nanjing 210095, China College of Agriculture and Biotechnology, Zhejiang University, Hangzhou 310058, China Institute of Agro-Bioengineering, College of Life Sciences, Guizhou University, Guiyang 550025, China College of Chemistry and Chemical Engineering, Zhongkai University of Agriculture and Engineering, Guangzhou 510225, China College of Horticulture, South China Agricultural University, Guangzhou 510642, China * Correspondence: 13751774213@139.com (J.L.); licaiqin@zhku.edu.cn (C.L.); Tel.: +86-137-5177-4213 (J.L.) † These authors contributed equally to this work. Abstract: Grafting has been utilized to develop horticultural crops to increase plant vigor, yield potential, and tolerance to various environmental stresses. Grafting employs selected rootstocks of the same species or near relatives. Moreover, dwarfing is a desirable feature for intensive cultiva- tion and efficient orchard management. However, information on the regulatory mechanisms of rootstock-induced vigor control remains unclear. Numerous studies comprehend the physiological and molecular mechanism of rootstock control scion vigor, which has significantly improved our understanding regarding vigor control processes in apple, litchi, pear, citrus, etc. This review summa- rizes the current knowledge on the impact of rootstocks on scion vigor and hormonal mechanisms involved in dwarfing, such as auxin (IAA), cytokinins (CK), abscisic acid (ABA), gibberellic acids (GAs), and brassinosteroids (BR). This study will provide fascinating information for future studies Citation: Hayat, F.; Li, J.; Iqbal, S.; Khan, U.; Ali, N.A.; Peng, Y.; Hong, on rootstock-induced dwarfing effects and accelerate the breeding of dwarfing rootstocks. L.; Asghar, S.; Javed, H.U.; Li, C.; et al. Hormonal Interactions Underlying Keywords: fruit tree; vigor control; dwarfing mechanism; hormonal signaling Rootstock-Induced Vigor Control in Horticultural Crops. Appl. Sci. 2023, 13, 1237. https://doi.org/10.3390/ app13031237 1. Introduction Academic Editor: Yurii K. Gun'ko Grafting has been widely used for the asexual propagation of horticultural crops to manage plant-specific traits, including stress tolerance and vigor control [1,2]. Modern fruit Received: 17 December 2022 orchards rely on scion varieties grafted onto rootstocks, which makes them complicated Revised: 3 January 2023 objects for investigating shoot–root communications [3,4]. Rootstocks are utilized in vari- Accepted: 10 January 2023 ous fruit trees to enhance nutrient uptake and transport by improving yield, quality, and Published: 17 January 2023 tolerance to numerous stresses, such as drought, salinity, heavy metals, and extreme tem- peratures [2,5,6]. Choosing the best rootstock is one of the critical decisions in establishing a fruit orchard and achieving better tree performance. Copyright: © 2023 by the authors. Dwarfing rootstock under high-density plantations is important to ensure maximum Licensee MDPI, Basel, Switzerland. output and facilitate mechanized harvesting [7,8]. Size-controlling rootstocks have become This article is an open access article prominent due to their short stature and easier harvesting and spraying [9]. Additionally, distributed under the terms and various factors affect the vigor of rootstock-induced growth, including hormones, phenolic conditions of the Creative Commons compounds, carbohydrates, and mineral nutrients [10,11]. The dwarfing mechanism has Attribution (CC BY) license (https:// gained more attention from researchers and scientists during the past 50 years (Table 1). creativecommons.org/licenses/by/ 4.0/). Appl. Sci. 2023, 13, 1237. https://doi.org/10.3390/app13031237 https://www.mdpi.com/journal/applsci Appl. Sci. 2023, 13, 1237 2 of 14 Table 1. Hormonal evidence underlying dwarfing mechanism among various tree species. Crop Treatments Combinations Reported Effect References Dwarfing was caused by decreased MdPIN8 Different graft combinations with or expression in the M9 interstem or inadequate root [12] without interstock. zeatin synthesis. Dwarfing may be triggered by low IPT5b expression Different apple rootstocks and high levels of methylation in the promoter [13] region in the M9 rootstock. The DELLA protein RGA-like (RGL) gene represses the gibberellin signaling pathway. Further research M.9 and SH40 interstocks [14] revealed that MdWRKY24 might influence plant dwarfing via the synergistic effect of MdRGL1/2/3. Apple The complex process of growth reduction is Dwarfing self-rootstock, dwarfing mediated by several transcription factors, genes [15] interstock, and vigorous rootstock involved in sugar metabolism, and IAA, CK, ABA, and GA pathways. GID1c gene expression in the ‘SH6’ rootstock decreased with GA content compared with other Malus domestica, tested rootstocks. Moreover, the upregulation of Malus honanensis, GID1c gene triggered the significant genes involved [16] M. honanensis cv. S19, and ‘SH6’ in hormone biosynthesis and metabolism, improving the coregulation of several hormones involved in plant growth and inhibiting dwarfing characteristics. Breadfruit plants grafted on marang rootstocks may exhibit a dwarf phenotype due to the Breadfruit plants grafted onto downregulation of AaGA20ox3 gene. GA deficiency [17] Marang rootstocks may contribute to rootstock-induced breadfruit dwarfing. Breadfruit 1. Breadfruit scions grafted onto marang In breadfruit scions, disruption of pathways (Artocarpus odoratissimus) rootstock. regulating nutrient transport, cell wall biosynthesis, 2. Breadfruit scions grafted onto sucrose utilization, and networks of hormone [18] breadfruit rootstocks, self-graft (control) transduction may inhibit cell proliferation and stem 3. Breadfruit seedlings (non-graft) elongation, resulting in a dwarf phenotype. GA2ox gene was only found to be upregulated in Vigorous cultivar (FZX) and dwarf ZNX samples, implying that GA might play an Litchi [19] cultivar (ZNX). essential role in regulating huge variation between vigorous and dwarf litchi cultivars. Mutant lines with high levels of endogenous ABA Mutant and wild type and ABA pathway gene transcripts showed that the [20] PbPAT14 function is related to the ABA pathway. When dwarf pears were compared to arborescent, their heights were reduced by 62.8%, and their Dwarf phenotype and internode lengths were noticeably shorter. Changes [21] arborescent phenotype in genes expression in GA and BR degradation and signal transmission may explain the reduced number of cells in dwarf plants. Pear Morphological traits showed that ‘601D’ had shorter internodal length, lower stomata density, greater Dwarfing ‘601D’ and vigorous ‘601T’ stomata size, and increased photosynthetic capacity. [22] In addition, an excessive accumulation of ABA is responsible for the dwarfing mechanism of ‘601D’. Differences in expression in shoot tips and stems ‘Xueqing’/‘QN101’/‘Douli’, between ‘QN101’ and ‘OHF51’ reveal a connection [23] ‘Xueqing’/‘OHF51’/‘Douli’ between IAA polar transport and dwarfing potential. Appl. Sci. 2023, 13, 1237 3 of 14 Table 1. Cont. Crop Treatments Combinations Reported Effect References When interstock lengths were between 20 and 25 cm, dwarfism was more prominent. Persimmon Three different grafting combinations. [24] DKGA2ox1 and MIR171f_3 influence persimmon dwarfism via regulating scion GA content. IAA and GA levels were lower in ‘Kanshu’ grafted Sweet Two different graft combinations onto the ‘Nantong-xiaofangshi’ interstock compared [25] Persimmon with no interstock. Plant hormones are essential for controlling plant growth and development. These hormones are important signaling molecules throughout the lifecycle of a plant and function as genetically programmed hormones. Every cell in a plant can produce hormones and transport them to suitable organs and tissues [26–29]. Even at lower concentrations, these hormones regulate numerous aspects of plant growth and development, such as IAA, GA, CKs, ABA, BR, ethylene, and jasmonic acid (JA) [30]. On the other hand, it is insufficient to comprehend how plant hormones and their complex communication networks are involved in vigor-controlling processes. Besides plant hormones, minerals, phenolic chemicals, and carbohydrates are also essential in rootstock-induced vigor effects. However, the detailed effects of these factors involved in dwarfing mechanisms are poorly understood. This review provides an understanding of the hormonal regulation of the rootstock-induced Appl. Sci. 2023, 13, x FOR PEER REVIEW 4 of 14 dwarfing mechanism. An illustration of different plant hormone and their role in plant growth is given in Figure 1. Figure 1. An illustration of various plant hormones and their role in dwarfing mechanisms. Figure 1. An illustration of various plant hormones and their role in dwarfing mechanism. 2. Rootstocks Control Scion Morphology 2. Rootstocks Control Scion Morphology Rootstocks have a noticeable effect on the morphological characteristics of the scion Rootstocks have a noticeable effect on the morphological characteristics of the scion part. Dwarfing rootstocks have varying effects on the vegetative growth of grafted part. Dwarfing rootstocks have varying effects on the vegetative growth of grafted plants, plants, including includi plant ng pla height, nt heig primary ht, prima shoot ry sholength, ot length number , number of ofnodes, nodes, in internodal ternodal leng length, th, branch branch composition, composit tr io unk n, trunk cross-sectional cross-sectiona ar l a ere a a (TCSA), (TCSA), and and yi yield eld (K [a 6rlida ,10,22 ğ et ,31 a]. l., Likewise, 2014 [31]; Hayat et al., 2020 [10]; Khan et al., 2020 [6]; Liu et al., 2022 [22]). Basile et al. (2003) found that 1- Marini et al. [32] showed that ‘Golden Delicious’ apple trees grafted onto vigorous P.22 year-old peach trees grafted onto dwarfing K146-44 rootstock had lower TCSA than those rootstock had greater tree vigor and canopy volume than those grafted onto dwarfing grafted on Nemaguard rootstocks. Likewise, Marini et al. (2009) [32] showed that ‘Golden ‘M-9’ rootstock. Santos et al. [33] examined the growth characteristics of sweet cherry Delicious’ apple trees grafted onto vigorous P.22 rootstock had greater tree vigor and can- grafted onto several rootstocks. In addition, they noticed that rootstocks had a considerable opy volume than those grafted onto dwarfing ‘M-9’ rootstock. Santos et al. (2002) [33] examined the growth characteristics of sweet cherry grafted onto several rootstocks and noticed that rootstocks had a considerable influence on the shoot length, internode length, and trunk cross-sectional area (TCSA). Moreover, ‘Shatangju’ mandarin grafted onto ‘Rough lemon’ and ‘Canton lemon’ rootstocks had greater shoot length, trunk diameter, and internodal length; however, trees grafted with ‘Fragrant orange’ and ‘Red tangerine’ rootstock had the lowest values of morphological traits and weakest growth vigor (Liu et al., 2017) [34]. Likevise, Hayat et al. (2020) [10] reported that ‘Red Fuji’ apple scion cultivar grafted onto dwarfing ‘M-9′ rootstock produced dwarf size trees, whereas taller root- stocks, such as ‘Baleng’ and ‘Chistock-1′, increased primary shoot length and other vege- tative traits. In addition, the root system of the ‘Baleng’ ‘Red Fuji’ apple rootstock was more vigorous, with greater root volume, root length, surface area, number of forks, and number of tips. The root is the primary organ that transports water and nutrients from the soil medium to the aerial portion, thus the root morphology has a significant impact on growth vigor and yield (Gregory et al., 2013) [35]. Dwarfing, or vigor reduction phenomena, are typically linked with short internodes (Weibel et al. 2003) [36]. Additionally, plant growth regulators promote shorter internodes than untreated trees (Webster 2002) [37]. Furthermore, Sitarek and Bartosiewicz (2011) [38] research revealed that the trunk cross-sectional areas of trees grafted onto M46 and P. divaricata rootstock were much more significant than other rootstocks. On the other hand, trees grafted with ‘Wangenheim Prune’ rootstock displayed lower morphological values Appl. Sci. 2023, 13, 1237 4 of 14 influence on the shoot length, internode length, and trunk cross-sectional area (TCSA). Moreover, ‘Shatangju’ mandarin grafted onto ‘Rough lemon’ and ‘Canton lemon’ rootstocks had greater shoot length, trunk diameter, and internodal length; however, trees grafted with ‘Fragrant orange’ and ‘Red tangerine’ rootstock had the lowest values of morphological traits and weakest growth vigor [34]. Likewise, Hayat et al. [10] reported that scion cultivar grafted onto dwarfing ‘M-9’ rootstock produced dwarf size trees, whereas taller rootstocks, such as ‘Baleng’ and ‘Chistock-1’, increased primary shoot length and other vegetative traits. In addition, the root system of the ‘Baleng’ rootstock was more vigorous, with greater root volume, root length, surface area, number of forks, and number of tips. The root is the primary organ that transports water and nutrients from the soil medium to the aerial portion, thus the root morphology has a significant impact on growth vigor and yield [35]. Dwarfing, or vigor reduction phenomena, are typically linked with short intern- odes [36]. Additionally, plant growth regulators promote shorter internodes than untreated trees [37]. Furthermore, Sitarek and Bartosiewicz [38] reported that the trunk cross-sectional areas of trees grafted onto M46 and P. divaricata rootstock were much more significant than other rootstocks. On the other hand, trees grafted with the ‘Wangenheim Prune’ rootstock displayed lower morphological values and dwarfing characteristics. Salustiana scion culti- var grafted on ‘Rough lemon’ rootstock produced the most extended primary shoot length, largest trunk diameter, and vigorous root system [6]. In a recent study, Hayat et al. [39] found that ‘Shatangju’ mandarin scion grafted onto ‘Flying Dragon’ rootstock produces dwarf plants. Moreover, vigor reduction in the ‘Flying Dragon’ rootstock is attributed to a lower node number, shorter internodal length, and a smaller trunk diameter of the scion. The relationship between a genotype’s dwarfing potential and a genetic, physio- logical feature would benefit the early selection of dwarf rootstocks [40]. Therefore, it can be concluded from the literature that size-controlling rootstocks significantly affect scion morphological traits, including plant height, primary shoot length, internodal length, leaf size, number of nodes, number of branches, TCSA, and weight of the overground part. 3. Role of Plant Growth Retardants (PGRs) in Plant Development Controlling tree height and canopy size in high-density fruit cultivations increase orchard efficiency and productivity without damaging plants [41]. The exogenous ap- plication of plant growth retardants is an efficient technique to achieve dwarfing in fruit trees. Numerous plant growth regulators that affect cell division and elongation, including paclobutrazol, CK, and daminozide (B9), have demonstrated their role in dwarfing [42–45]. Among these, paclobutrazol and B9 are called ‘plant growth retardants’ (PGRs) because they suppress plant growth and development by reducing the production of GA and IAA [46]. Furthermore, exogenous mannitol treatment has been reported to inhibit plant development by inducing drought stress [47]. However, the mechanisms behind PGR-mediated growth reduction in fruit species are still unknown, which limits their agricultural application. 4. Effect of Multiple Plant Hormones in Rootstock-Induced Dwarfing 4.1. Auxin (IAA) Auxins are a class of phytohormones that control various processes of plant growth and development [48]. Auxins are primarily recognized for their potential to promote embryogenesis, tissue patterning, differential growth, and cell elongation [49,50]. Indole-3- acetic acid (IAA) is predominantly produced in meristematic tissues of young leaves and transported to the root sections by phloem and cambium [51]. Additionally, IAA application can stimulate plant height and shoot length [52]. IAA content in the scion portion improved after bridging and replacing interstock bark with vigorous interstock, and the scion part became a standard-level tree [53,54]. The polar IAA inhibitor N-1-naphthylphthalamic acid restricted IAA transport in the stem of vigorous rootstocks, contributing to a substantial reduction in shoot growth and root zeatin levels [12]. Similarly, Song et al. [55] found that ‘Fuji’ apple trees grown onto taller ‘MM111’ rootstock had greater IAA levels than those grafted onto size-controlling ‘M.9’ rootstock. In another study, it was reported that Appl. Sci. 2023, 13, 1237 5 of 14 dwarfism is caused by a decline in indole-acetic acid (IAA) content and by the associated changes in the IAA:ABA (abscisic acid) content ratio in the crabapple plants in both growing conditions [1,56]. Additionally, dwarfing rootstocks had noticeably lower expression levels of the MdYUCCA10a gene in their roots and leaves than invigorating rootstocks. Therefore, the best-supported argument is that dwarfing rootstocks acquire less IAA from the scion part, consequently, limit root growth and root-synthesized cytokinin transported to the aerial part again, which in turn reduces plant growth [57,58]. In this way, the dwarfing ‘M.9’ rootstock had lower amounts of labeled IAA in cambial sap than the more vigorous ‘M.26’ and ‘MM.106’ rootstocks [59]. Moreover, the ‘M.9’ dwarfing rootstock transported the labeled IAA downward at a slower rate than the ‘MM.11’ vigorous rootstock [60]. In another study, Liu et al. [34] found that the vigorous ‘Canton lemon’ (Citrus limonia Os- beck) rootstock had a maximum level of IAA in roots. However, the roots of the dwarfing ‘Fragrant orange’ rootstock had the lowest levels. Previous research also suggests that the lowered transport ability of IAA in dwarfing rootstock is linked with the imbalanced distribution of IAA efflux carrier proteins [61–63]. It has been demonstrated that different PIN gene expression levels may affect IAA levels [64]. Furthermore, IAA is transported from the scion part to the root portion through polar auxin transport (PAT), regulated by the PIN auxin efflux carriers [65–67]. On the other hand, Gan et al. [68] revealed that tobacco plants overexpressing apple MdPIN1b enhanced polar IAA transport and reduced MdPIN1b expression in the M9 interstem, which may cause apple dwarfism. The inflorescence axis of the mutant (pinl-1) exhibits a distinctive structure and lowered IAA polar transport activity [69,70]. Modifications in the Arabidopsis gene PIN3 significantly influence stem and lateral root development [71]. A CT repeat deletion in the promoter of the PcPIN-L gene is associated with decreased promoter activity in dwarf-type pears, which may impair polar IAA transport and result in a dwarf phenotype [43]. 4.2. Gibberellins (GAs) Gibberellins are crucial for plant development and dwarfing traits [72–74]. Addition- ally, GAs are essential hormones that regulate apical meristem differentiation by lowering their levels during dormancy and upregulating at dormancy release or bud burst [75]. Previous studies have shown that GAs can affect grafted plants even when transported nonpolar over long distances [76]. Moreover, GA metabolism is linked with the dwarfing ability of plants [45]. Dwarfing induced by GA can be categorized into two groups: a responsive mutant related to GA signaling and a synthetic dwarf mutant linked with the GA anabolic pathway. Further, synthetic dwarf mutants have a GA deficit because of defective GA synthetase or other enzymes. The treatment of GA can potentially re- store synthetic dwarf mutants to their standard size. In addition, Bulley et al. [77] found that the expression of GA20oxidase gene was downregulated in the apple scion cultivar, when grafted onto vigorous rootstocks. GAs and their precursors are produced in the root portion and transported to the shoot by the xylem, where they can be metabolized to produce bioactive GAs [78,79]. Both monocot and dicot plants exhibit dwarf phenotypes due to mutations defective in GA biosynthesis; in contrast, GA treatments enhance plant growth [80]. GA20ox is a multifunctional enzyme that converts GA12 or GA53 into GA9 or GA20 through three oxidation stages [81]. Suppression of GA20ox gene decreases GA levels and induces dwarfism in numerous crops [82,83]. Additionally, size-controlling apple rootstocks restrict root-produced GA to aerial parts [84,85]. However, the application of GA restored the node numbers on the primary axis and secondary shoots of vigor reduction or dwarfing rootstock [86]. Gibberellin- insensitive Dwarf1 (GID1), the GA receptor in the signal pathway, can interact with GA to degrade DELLA repressor proteins after forming a GA-dependent complex and then regu- late various physiological and biochemical activities in plants [87–90]. Recent studies have shown that breadfruit scion grafted onto marang rootstocks had significantly greater ex- pression of the GA catabolic gene (AaGA2ox1), and lower expression of the GA biosynthetic Appl. Sci. 2023, 13, 1237 6 of 14 (AaGA20ox3) gene at various time points. Additionally, it was shown that scions grafted onto marang rootstocks accumulated more DELLA proteins (GA-signaling repressors), suggesting increased repression of GA response in scions grafted on marang rootstocks. This may result from the downregulation of GA biosynthesis or the upregulation of the GA deactivation pathway [17]. Plants with an abundance of DELLA often exhibit a dwarf phenotype [91]. There is strong evidence that rootstock-induced dwarfing is caused by a disruption in GA metabolism. 4.3. Abscisic Acid (ABA) Abscisic acid (ABA) is a crucial phytohormone that controls plant growth, develop- ment, and stress responses [92]. ABA is usually produced in the roots and supplied to the leaves through the xylem or quickly synthesized in the leaves [93,94]. It is crucial for nu- merous physiological functions in plants, including stomatal closure, leaf senescence, seed germination, cuticular wax accumulation, osmotic regulation, bud dormancy, and growth inhibition [95]. ABA can also cause dwarfism in higher plants by controlling plant growth and tolerance responses to various stresses [96,97]. It is commonly believed that elevated ABA levels cause dwarfism because ABA acts as a growth inhibitor [98,99]. Compared to vigorous rootstocks, dwarfing apple rootstocks have higher levels of ABA and lower ABA:IAA ratios [58]. The greater levels of ABA in the branch bark of size-controlling apple rootstocks can be used as a marker for selecting dwarfing rootstock. Additionally, MdNAC1 gene overexpression causes dwarfism in transgenic apples by regulating endogenous ABA and BR production [100]. In pear, the ultrastructural study reported that thinner or shorter stems cause size reduction because of a decrease in cell numbers. Mutant lines with high levels of endogenous ABA and ABA pathway gene transcripts showed that the PbPAT14 function is related to the ABA pathway [20]. Similarly, in Arabidopsis, elevated endogenous ABA concentrations inhibit shoot growth [101]. This implies that a rootstock with high amounts of ABA will decrease stomatal conductance and gas exchange, resulting in low yield and reduced growth vigor in grafted plants. Recently, Qureshi et al. [102] reported a negative correlation between the ABA content of scion and rootstock with tree vigor, leaf gas exchange, photosynthetic pigments, and yield. Furthermore, Rough lemon, Poncirus trifoliata, and Fraser hybrid rootstocks had low concentrations of ABA, while Cox mandarin, Troyer citrange, and Benton rootstocks had significantly higher concentrations of ABA. These higher or lower ABA levels explain their attributes as vigorous or dwarfing rootstocks and greatly influence scion growth characteristics. Similar results were described by Kamboj et al. [103], indicating a negative correlation between ABA levels and trees. According to Noda et al. [104], citrus trees grafted on dwarfing rootstocks had greater ABA levels in their shoots compared with citrus trees grafted on taller rootstocks. The reduced plant growth was believed to be caused by the higher ABA levels. Similarly, Tworkoski and Fazio [96] found that increased levels of ABA cause lower hydraulic con- ductivity in dwarfing rootstocks, impacting tree development and yield. In addition, root growth inhibition is associated with high ABA levels in ‘Jonathan’ apple micro-cuttings. Further, high levels of abscisic acid (ABA) are believed to play a critical role in inhibiting the formation of adventitious roots (ARs) in apples [105]. In sweet cherry (Prunus mahaleb L.), Moghadam and Shabani [106] observed that vigorous rootstocks had the lowest ABA/IAA ratio compared with dwarfing rootstocks. They also found a strong correlation between growth vigor and ABA concentrations in shoot bark. Recently, root development was considerably suppressed in Qingzhen 1 apple plants after the exogenous application of ABA compared with control plants [44]. Conclusively, ABA levels were found to be higher (act as growth inhibitor) and impede growth features by reducing the accumulation of other hormones. Appl. Sci. 2023, 13, 1237 7 of 14 4.4. Cytokinin (CK) Cytokinins (CKs) are synthesized in the root tips and transported to the shoot part, where they control the cell cycle and various developmental processes [74,107]. Further- more, CKs also play a critical role in modulating plant vigor when dwarfing rootstocks are employed. According to Avery [108], the more vigorous rootstock MM106 had more Cks than dwarfing rootstocks (M.9 and M27). Depletion of solutes (e.g., CKs) in xylem sap due to graft union may also reduce vigor [60,109]. Skene and Antcliff [110] found similar findings that grapevine scions grafted on the vigor-controlling rootstock had minimum levels of CKs passing from roots to shoots compared to those grafted onto the rootstock of more vigorous ones. Moreover, CK-like activity in branch sap is greater in vigorous ‘Volkamer lemon’ rootstock compared with trees grafted onto the least vigorous ‘Troyer ’ (Poncirus trifoliata Citrus sinensis) rootstock [111]. Kamboj et al. [103] reported that the amount of CKs in shoot sap varies depending on the source of the rootstock; the more vigorous (MM106) rootstock has more CKs than dwarfing (M9 and M27) rootstocks. Similarly, Sorce et al. [112] reported a positive correlation between tree vigor and the transport rate of CK in grafted and un-grafted peach trees. Furthermore, Isopentenyl transferases are essential enzymes for cytokinin synthesis [113]. Gene expression of IPT genes directly affects endogenous CK levels [114–116]. IPT fusion gene expression has been shown to improve cytokinin levels in transgenic plants [117]. The zeatin-riboside (ZR) synthetase IPT5b gene mutants in Arabidopsis have low endogenous active forms and severe dwarfism [118]. In apples, reduced IPT3 expression led to decreased cytokinin pro- duction in the roots of dwarfing rootstocks. As a result, the scion part received insufficient amounts of cytokinin, which lowered their IAA concentration and permanently reduced tree vigor and vegetative growth [64]. Moreover, lower expression of IPT5b gene in apples resulted in poor zeatin biosynthesis and dwarfing [13]. They hypothesized that the dwarf- ing effect in ‘Fuji’/M.9 (scion/rootstock combination) was due to the weak production ability of CK in the roots of M.9 rootstock. However, dwarfing in ‘Fuji’/M.9/Baleng Crab (scion/interstem/rootstock) graft combination was mediated by decreased expression of MdPIN8 gene in the bark of M.9 interstem, which lowered basipetal transport of IAA and root IAA supply, thereby inhibiting root zeatin biosynthesis. In addition, inadequate zeatin synthesis in the roots also caused a mild zeatin shortage in the shoots, restricting the shoots’ vegetative growth. In a recent study, Yan et al. [90] reported that greater expression levels of MdIPT5 gene in vigorous rootstock boost zeatin amounts to encourage cell division and internode length. On the other hand, lower expression levels of MdIPT5 gene in dwarfing rootstock deliver defective zeatin, which in turn causes a reduction in internode length. This could be explained by the inadequate cytokinin synthesis capacity triggered by poorly developed roots [119,120]. As a result, one of the underlying mechanisms that contribute to the dwarf tree phenotype may be a reduced capacity for cytokinin synthesis and transport. 4.5. Brassinosteroid (BR) BRs are steroid hormones that control various physiological functions, and distur- bance of BR signaling is usually associated with significant vegetative abnormalities such as dwarfism [121,122]. Previous research has shown that exogenously applied BR treatment significantly improved apple tree growth, and the endogenous BR contents enhanced in the shoot tips of BR-treated plants [123,124]. Similarly, the Arabidopsis dwarf mutant dwarf7-1, which lacks BR biosynthetic genes, exhibits decreased BR synthesis and slower cell division and shoot growth rates. In addition, dwarfing was also mediated by lower expression of BR biosynthesis genes (MdDWF4 and MdBSK) in conjunction with enhanced expression of MdBKI1 and MdBIN2 genes [125]. The exogenous treatment of BR enhanced endogenous levels of GA and IAA [126]. The expression of genes involved in IAA syn- thesis (MdYUCCA10 and MdTAA1) and transport (MdPIN1, MdPIN7- 8, MdABCB1, and MdABCB19) was dramatically increased after BR treatment. The mechanisms underlying the interaction between BR and IAA have numerous effects, including hormone synthesis, transport, and signal transduction [127,128]. These findings suggest that BR may enhance Appl. Sci. 2023, 13, 1237 8 of 14 IAA levels by stimulating the expression of IAA synthesis genes and promoting polar transport [129]. Genes involved in BR biosynthesis, including the CYP90A1 gene and three brassinosteroid-6-oxidase genes, were downregulated in the vigor reduction rootstock stem tissues [18]. The BR signal transduction system, which is regulated by receptor kinases, regulates plant growth and development. Moreover, several components of the BR signal transduction pathway are encoded by the genes BAK1, BRI1, BSK1, BRI1, BKI1, CDG1, BIN2, BSU1, and BZR1/2 [130]. 4.6. Phenols Phenols have been suggested as potential growth-regulating substances in tree size mediated by dwarfing rootstocks. No causal link has been established between growth and phenol accumulation; however, phenol accumulation in the graft lowers tissue viability, slowing IAA breakdown and the subsequent root cytokinins response [131,132]. The rootstock’s bark plays a crucial part in dwarfing mechanism. The presence of phenols in the bark may be responsible for the bark’s growth-inhibiting characteristics [133]. According to Moghadam and Khalighi [134], dwarf mahaleb (Prunus mahaleb L.) genotypes had leaves and stem bark with higher phenolic contents than high vigor genotypes. Furthermore, the total phenolic content and mineral nutrition of Mahaleb genotypes differed according to vigor capacity, suggesting they can be utilized to predict growth vigor. According to Mendel and Cohen [135], phenols may serve as important inhibitors in citrus rootstocks. In addition, apple peel samples contained the highest number of phenolic compounds, whereas the lowest number of phenolic compounds were found in the peel samples of semi- vigorous rootstock EM 01 [136]. Mainla et al. [137] reported that the dwarfing effects of B.396 and M.26 rootstocks may have had a favorable impact on polyphenol concentrations because canopies with lower vegetative growth provided better lighting conditions for fruits. This may be linked to greater levels of metabolic stress caused by the genetic adjustment of metabolism between rootstock and scion cultivars. Compared with M.9 and M.26, the semi-vigorous MM106 rootstock obtained a maximum phenolic content. Similarly, Nachit and Feucht [138] found that apple rootstocks overgrowing had more p-coumaric and p-hydroxybenzoic acids than those growing slowly. 5. Conclusions Grafting is a traditional method for improving horticultural traits. Commercial fruit production relies on grafting with rootstocks to control plant-specific features, including vigor reduction or dwarfing of the scion. The promising outcome of dwarfing trees has attracted the attention of farmers worldwide because of their potential for greater planting densities per unit area, increased yield potential, easy harvest, spraying, and pruning. Dwarfing of scion due to rootstock is a complicated process influenced by numerous factors. Among them, hormonal changes have been suggested as a possible mechanism by which rootstocks affect scion vigor by modifying root–shoot chemical signaling. Genes in hormone biosynthesis or signaling pathways have been linked with dwarfing traits. Additionally, hormones are delivered as signaling molecules, encouraging tissue differentiation above and below the graft union. IAA, CK, GA, and BR are essential hormones controlling plant growth in different fruit trees, and a complex network of more than one plant hormone is involved in the rootstock-induced dwarfing effect. In contrast, increased ABA levels (acts as a growth inhibitor) are associated with dwarfing. Overall, hormones play an essential role in rootstock-mediated dwarfing effects. Author Contributions: J.L. and F.H. Conceptualization, F.H., S.I., U.K. and L.H. contributed to writing and original draft preparation; J.L., N.A.A., Y.P., M.A.S., S.A., H.U.J., W.S. and C.L. edited the manuscript; J.L., P.T. and J.C. contributed to supervision, project administration, funding acquisition. All authors have read and agreed to the published version of the manuscript. Appl. 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Applied Sciences – Multidisciplinary Digital Publishing Institute
Published: Jan 17, 2023
Keywords: fruit tree; vigor control; dwarfing mechanism; hormonal signaling
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