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Regulation of Tissue Repair in Plants

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Regulation of Tissue Repair in Plants COMMENTARY Regulation of tissue repair in plants James B. Reid1 and John J. Ross School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia recent report in PNAS by Asa- gene, one of a family of amino- hina et al. (1) addresses the fas- cyclopropane carboxylic acid synthase A cinating question of tissue repair genes that regulates the rate-limiting in plants. According to recent step in ethylene biosynthesis. suggestions, plants and animals might Jasmonic acid (JA), another plant hor- share cellular mechanisms that allow re- mone, may also play a role (1). JA is generation of tissues after damage (2). a known regulator of plant responses to However, plants and animals differ greatly both biotic and abiotic stresses (10), in their mode of development and their and genes involved in its biosynthesis are ability to respond to damage-inducing en- up-regulated after incision, which is vironmental factors (3). Terrestrial plants shown by microarray and quantitative RT- cannot move their whole body in response PCR analyses (1). One such gene, the to environmental cues, and, because of lipoxygenase gene LOX2, is up-regulated their cell walls, they also lack cellular mo- below the incision in a similar pattern bility within the plant. This means that to RAP2.6L, and application of methyl plants must regenerate damaged tissue jasmonate up-regulates RAP2.6L expres- through cellular regeneration at the point sion. Although studies using the expres- of damage. Traditionally, this regeneration sion of biosynthesis genes to infer was considered to occur by dedifferen- hormone levels need to be treated with tiation of existing mature cells followed by extreme caution (11), it seems that cell division to form callus and differenti- Fig. 1. Model of tissue repair in the Arabidopsis wounding up-regulates this gene inde- ation to form the cellular constituents of inflorescence stem based on the work by Asahina pendently of auxin (1). the new tissue, although details of this et al. (1). The differential control of the TFs ANA- Overall, these results provide a testable process have been questioned recently (4). CO71 and RAP2.6L in the upper and lower sides, model of some of the early molecular respectively, of an incision and their suggested Plants experience many types of tissue regulation by the plant hormones auxin, ethylene, steps involved in tissue repair. Un- damage, including that caused by herbiv- and jasmonic acid (JA) are shown along with as- derstanding the molecular targets of the ory and other forms of physical wounding sociated synthesis genes. TFs and moving beyond correlations to (e.g., breakage because of wind or ice or show the direct regulation of the TFs trampling by animals). They have de- by the hormones implicated will go a long repair of the wound is inhibited, indi- veloped elaborate responses to this dam- way to elucidating the control of this cating the importance of the TFs for the age. For example, herbivory results in essential plant response. Thus far, the repair process. a suite of responses; some are fast-acting effects of directly applying hormones on Importantly, the work by Asahina et al. and local, whereas others may be quite the expression of the TF genes are less (1) provides evidence that the TFs are long-lived and systemic in nature, allowing impressive than the effects of stem incision regulated by plant hormones, with a focus the plant to develop a response at the (cutting) or decapitation (removal of ma- on auxin. This hormone also regulates whole-plant level to attack by particular terial at the top of the stem, including animal species (5). TFs involved in root tissue repair after flowers) (1). For example, in cut stems, One of the simplest forms of damage to damage by laser ablation (9). In the pres- decapitation dramatically reduces plants is the splitting or laceration of tis- ent case (1), the possible involvement of ANAC071 expression, but applying auxin sue. This type of wounding is frequent auxin implies communication between to the decapitation site does not signifi- under both natural and agronomic con- other parts of the plant and the repair site. cantly reverse that effect (figure 3 in ref. ditions. It is also common with some of Auxin is a mobile hormone, moving 1). Possibly, the dose used (1 mM auxin in our well-established horticultural and re- down the stem in a polar transport stream, lanolin paste) is inadequate to restore search techniques (e.g., grafting). Indeed, and molecular evidence is presented that the auxin content of stems. In previous grafting and the subsequent tissue repair auxin accumulates on the upper (acrope- research, a similar dose did not fully re- have been vital for the identification of tal) side of the incision and depletes on the store the auxin level to the level of intact two new plant hormones over the last 5 lower (basipetal) side. This information stems, although the hormone was years: the strigolactones for branching (6) is used to develop a model in which auxin applied repeatedly (12). Similarly, apply- and the floral stimulus or florigen for regulates TFs, which then initiate cell di- ing 2 mM methyl jasmonate has only flowering (7). However, the molecular vision in the pith and ultimately repair the a moderate effect on RAP2.6L expression basis of tissue repair has remained largely wound (Fig. 1). compared with cutting (figure 5 in ref. 1). unknown. The paper by Asahina et al. (1) Roles for other plant hormones are also The possible roles of other hormones in provides some welcome insights into the suggested (1). The ethylene-insensitive tissue repair also require examination. ein2 repair process, since it shows that two mutant does not undergo the same In an earlier paper, Asahina et al. (13) plant-specific transcription factors (TFs), repair as WT plants because of a lack of ANAC071 and RAP2.6L, are strongly up- cell division in the pith. The expression of regulated on the upper (ANAC071) and ANAC071 is reduced in ein2 plants sug- Author contributions: J.B.R. and J.J.R. wrote the paper. lower (RAP2.6L) sides of an incision in the gesting that wound-induced ethylene may The authors declare no conflict of interest. infloresence stem. When the expression of enhance the auxin response. Ethylene See companion article 10.1073/pnas.1110443108. these TFs is down-regulated using chime- levels are not directly measured but are 1To whom correspondence should be addressed. E-mail: ric repressor silencing technology (8), inferred from the expression of the ACS2 [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1114432108 PNAS Early Edition | 1of2 Downloaded by guest on September 26, 2021 noted the importance of another growth- dedifferentiation during wound repair not directly prevent the growth of other promoting hormone, gibberellin (GA), (18). Like RAP2.6L, WIND1 belongs organs, and, therefore, repair is not es- in the repair process. In that case, hypo- sential, although protection from addi- cotyls of tomato and cucumber were Overall, these results tional damage/invasion is advantageous to studied. In considering the issue of auxin the plant. However, the stem is essential vs. GA, it should be borne in mind that provide a testable model for subsequent organ development (e.g., high auxin content can lead to high GA leaves, roots, flowers, and seeds) because content, because auxin promotes GA syn- of some of the early of its critical role in connectivity, sup- thesis and inhibits its deactivation (14, 15). port, and nutrient transport. Although However, in the tomato hypocotyl, the molecular steps involved new shoots may arise from axillary buds pattern of gene expression after cotyledon if the upper stem is damaged, the con- removal is not consistent with an auxin- in tissue repair. sequences for the plant may be much mediated effect on GA levels (16), in- greater than if an individual determinate organ is damaged. dicating the importance of GA per se. It to the apetela2/ethylene response factor is suggested that, in hypocotyls, GA is WIND1 The involvement of cell division in the TF family. Interestingly, is not repair process has been known or assumed a key factor in the reunion of cortical cells included in a list of genes up-regulated by whereas, in the pith cells of inflorescence Arabidopsis for a long time, and implicating plant the wounding of stems (1). hormones in the reformation of tissues, stems, auxin is a major player (1). In Consistent with evidence that auxin may this context, it is worth noting that GA- particularly vascular tissues, is likewise not not be the key factor in hypocotyl repair, new (19). The contribution by Asahina deficient pea mutants can be easily grafted WIND1 RAP2.6L (unlike ) is apparently et al. (1) is the characterization of specific epicotyl to epicotyl and epicotyl to stem not responsive to auxin (18). The work by TFs, which, according to their model, form (17), indicating that GA is not essential Iwase et al. (18) implicated another hor- a molecular link between plant hormones for tissue reunion in that system. mone, cytokinin, in TF-mediated repair, and the cell division response in the pith. It is also possible that different TFs but this time the hormone seemed to act Their work (1) provides a foundation for regulate the repair response in hypocotyls downstream and not upstream of WIND1. fl determining whether tissue repair is con- and in orescence stems because, earlier Different plant organs are affected in trolled by similar TFs and plant hor- this year, Iwase et al. (18) reported that different ways by both physical damage mones in different tissues and different another recently discovered TF gene, and predation, and these differences may plant taxa.
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