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To grow or not to grow : specific lipoxygenases control wound-induced growth restriction

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To Grow or Not to Grow: Speci fi c Lipoxygenases Control Wound-Induced Growth Restriction

As most vegetable growers know, plants have a lot of predators. Repetitive wounding events caused by her- bivorous insects and necrotrophic pathogens often lead to tissue damage and growth restriction. When Arabi- dopsis (Arabidopsis thaliana) is subjected to recurrent wounding, leaf growth is dramatically reduced. In na- ture, similar stunted phenotypes can be observed in ornamental bonsai plants cultivated by skilled gar- deners or when plants are attacked by herbivorous mammals or insects. In these contexts, plants over- produce jasmonates, of which the best known is jas- monic acid (JA; Browse, 2009). Inhibition of vegetative growth, as part of the wound response, occurs in wild- type plants but not in JA mutants (Zhang and Turner, 2008). Jasmonates are also required for reproductive growth, as impairment in JA synthesis or perception results in male sterility (Stintzi and Browse, 2000; Park et al., 2002).

JA synthesis is initiated in plastids where 13- lipoxygenases (LOX) add oxygen to the polyunsaturated fatty acids linolenic acid (18:3) and hexadecatrienoic acid (16:3) to form the corresponding 13-hydroperoxides, which are then cyclized to 12-oxo-phytodienoic acid, the JA precursor. In Arabidopsis leaves, JA biosynthesis depends on four specific 13-LOXs (LOX2, LOX3, LOX4 and LOX6). Their roles in reproductive devel- opment have been characterized; however, the function of each of these enzymes in controlling vegetative growth remains elusive.

In this issue of Plant Physiology, Yang et al. (2020) used a genetic approach to elucidate the contribution of each LOX to Arabidopsis rosette growth restriction in response to wounding. Analysis of plants with loss-of- functionloxalleles subjected to serial wounding assays showed that LOX3 and to a lesser extent LOX4 pro- duce the majority of JA precursors necessary for wound-induced rosette growth restriction. The authors exploited the fatty acid oxygenation upregulated2 (fou2) genetic background that overaccumulates JA, which in turn triggers a transcriptomic signature similar to that produced by chewing insects (Bonaventure et al., 2007a, 2007b). Thefou2mutant harbors a mutation in the putative voltage sensor of theTWO PORE CHAN- NEL1gene, which encodes a Ca21-permeant nonselec- tive cation channel. Yang et al. (2020) found that the severe JA-induced growth inhibition infou2is largely suppressed by mutations inLOX3 andLOX4. Collec- tively, these data reveal the roles of LOX3 and LOX4 in rosette growth and suggest, strikingly, that the stunted

and bonsai-like wound phenotypes could be recapitu- lated through genetic activation of 13-LOXs in the ab- sence of wounding (Fig. 1).

Furthermore, to test if the bonsai-like phenotype could be genetically phenocopied in unwounded tis- sues, Yang et al. (2020) investigated the relevance of LOX3 activation in phloem tissue, since LOX3 promoter activity spans the xylem and phloem and both these tissues are known to play major roles in leaf-to-leaf signaling (Chauvin et al., 2016; Nguyen et al., 2018). To accomplish this, Yang et al. (2020) designed a novel and elegant system where they expressed different variants of the TCP1 protein, under a phloem-specific promoter, and introduced it in theloxquadruple and triple mutant backgrounds with and without a functionalLOX3. Phe- notypic and biochemical analyses revealed that express- ing a hyperactive version of TCP1 genetically activates LOX3-dependent JA production and strongly constrains rosette growth in the absence of wounding (Fig. 1).

Therefore, this new study by Yang et al. (2020) reveals how plants suffer the slings and arrows of herbivory and decide to grow or, more often, not to grow, defining specific functions forLOX3-and phloem-derived signals and providing an exciting genetic tool that will be valuable to further mechanistically elucidate the wound response and cell signaling during specific stresses.

Amna Mhamdi1,2 ORCID ID: 0000-0001-9959-1362 Department of Plant Biotechnology and Bioinformatics, and VIB Center for Plant Systems Biology, Ghent University, 9052 Ghent, Belgium

Figure 1. Schematic representation of distinct functions of 13-LOXs in Arabidopsis. The leaf-specific LOX2, LOX3, LOX4, and LOX6 contrib- ute to the synthesis of jasmonate precursors and play specific roles in growth restriction in response to wounding or in defense. Overall, the specificity of LOXs seems to be dictated by their spatial and cell-specific expression. Reprinted from Yang, Lenglet-Hilfiker, et al. (2020), figure 5.

1Author for contact: amna.mhamdi@psb.ugent.be.

2Senior author.

www.plantphysiol.org/cgi/doi/10.1104/pp.20.01207

1210 Plant PhysiologyÒ,November 2020, Vol. 184, pp. 1210–1211, www.plantphysiol.orgÓ2020 American Society of Plant Biologists. All Rights Reserved.

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LITERATURE CITED

Bonaventure G, Gfeller A, Proebsting WM, Hörtensteiner S, Chételat A, Martinoia E, Farmer EE(2007a) A gain-of-function allele of TPC1 acti- vates oxylipin biogenesis after leaf wounding in Arabidopsis. Plant J49:

889–898

Bonaventure G, Gfeller A, Rodríguez VM, Armand F, Farmer EE(2007b) The fou2 gain-of-function allele and the wild-type allele of Two Pore Channel 1 contribute to different extents or by different mechanisms to defense gene expression in Arabidopsis. Plant Cell Physiol 48:

1775–1789

Browse J(2009) Jasmonate passes muster: A receptor and targets for the defense hormone. Annu Rev Plant Biol60:183–205

Chauvin A, Lenglet A, Wolfender JL, Farmer EE(2016) Paired hierarchical organization of 13-lipoxygenases in Arabidopsis. Plants (Basel)5:16

Nguyen CT, Kurenda A, Stolz S, Chételat A, Farmer EE(2018) Identifi- cation of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc Natl Acad Sci USA115:10178–10183

Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J31:1–12

Stintzi A, Browse J(2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis.

Proc Natl Acad Sci USA97:10625–10630

Yang TH, Lenglet-Hilker A, Stolz S, Glauser G, Farmer EE (2020) Jasmonate precursor biosynthetic enzymes LOX3 and LOX4 control wound-response growth restriction. Plant Physiol 184: 1172–1180 Zhang Y, Turner JG(2008) Wound-induced endogenous jasmonates stunt

plant growth by inhibiting mitosis. PLoS ONE3:e3699

Plant Physiol. Vol. 184, 2020 1211

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