Growth responses to competition1 and defence responses to the attack of consumer organisms2 are two classic examples of adaptive phenotypic plasticity in plants. However, the mechanistic and functional links between these responses are not well understood. Jasmonates, a family of lipid-derived signals, are potent growth inhibitors and central regulators of plant immunity to herbivores and pathogens3,4, with both roles being evolutionarily conserved from bryophytes5 to angiosperms6. When shade-intolerant plants perceive the proximity of competitors using the photoreceptor phytochrome B, they activate the shade-avoidance syndrome and downregulate jasmonate responses7. Despite the central implications of this light-mediated change in the growth/defence balance for plant adaptation and crop yield8,9, the mechanisms by which photoreceptors relay light cues to the jasmonate signalling pathway remain poorly understood10. Here, we identify a sulfotransferase (ST2a) that is strongly upregulated by plant proximity perceived by phytochrome B via the phytochrome B–phytochrome interacting factor signalling module. By catalysing the formation of a sulfated jasmonate derivative, ST2a acts to reduce the pool of precursors of active forms of jasmonates and represents a direct molecular link between photoreceptors and hormone signalling in plants. The metabolic step defined by this enzyme provides a molecular mechanism for prioritizing shade avoidance over defence under intense plant competition.
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The data that support the findings of this study are available from the corresponding author upon request.
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We thank I. Cerrudo, P. Karssemeijer and B. F. Alliani for help with the initial characterization of st2a lines and P. V. Demkura, E. Goschala, B. Rothe, D. Veit and A. Weber for excellent technical assistance. This work was supported by the Agencia Nacional de Promoción Científica y Tecnológica, Universidad de Buenos Aires and The New Phytologist Trust (C.L.B. and A.T.A.), the Max Planck Society (J.G.), National Science Foundation (grant no. IOS-1557439, A.J.K.), University of Lausanne and Swiss National Science Foundation (C.F.), a Georg Forster Research Award from the Alexander von Humboldt Foundation (C.L.B.) and a Deutscher Akademischer Austauschdienst Fellowship (G.L.F.-M.).
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended Data Fig. 1 AT5G07010 (ST2a) belongs to a small cluster of MeJA-upregulated genes that are also upregulated under conditions of phyB inactivation.
Heat map (upper part) showing a cluster of genes (approximately 25 % of the genes upregulated by 200 µM MeJA) that are expressed more strongly in the phyB-9 mutant than in Col-0 plants, and mean expression values + /− 1 SD (lower part) of this set of genes. This cluster contains AT5G07010 (ST2a) (for a full list of genes in this cluster, see Supplementary Data File 3). b, Examination of publicly available microarray data shows that among the genes included in categories with GO terms that contain the word “jasmonic”, AT5G07010 stands out for being the most strongly upregulated gene in plants exposed to low R:FR ratios (see arrow). For each gene, dots indicate the average of seven independent microarray experiments (see Methods for details); bars indicate 95 % confidence intervals. c, qPCR analysis demonstrated strong upregulation of ST2a in response to supplemental FR radiation and downregulation by supplemental UVB radiation under our experimental conditions (5-week-old Col-0 plants; relative expression data were normalized to the mean of the Ambient control). Bars indicate treatment means; thin bars = 1 SE; n = 4 biological replicates (small open circles); differences between light treatments tested by one-way ANOVA.
Extended Data Fig. 2 Upregulation of ST2a expression is mediated by PIFs and MYCs in response to low R:FR ratio and wounding, respectively.
a, In a pif4pif5pif7 triple mutant, which does not activate morphological responses to low R:FR ratios, the transcription of ST2a was normally upregulated by mechanical wounding, but not at all by supplemental FR radiation. GxL indicates the significance of the genotype x light interaction term in wounded plants (two-way ANOVA), and different letters indicate significant differences between means (Tukey). b, Effect of FR supplementation on ST2a expression in multiple pif mutants. Different letters indicate significant differences between genotype means in plants exposed to FR. c, Effect of mechanical wounding on ST2a expression in multiple myc mutants. In the wounding treatments, rosettes were harvested 4 h after being mechanically damaged (see Methods). Genotype effects in b and c were tested using one-way ANOVA; different letters indicate significant differences between genotype means (Tukey test). Bars indicate means; thin bars = 1 SE; n = 4 (a) or 3 (b, c) biological replicates (small open circles).
Extended Data Fig. 3 FR regulates the transcription of several genes involved in jasmonate metabolism.
Expression of genes encoding for the following enzymes were measured by qPCR in Col-0 Arabidopsis rosettes exposed to two light conditions (Amb or FR) at different times (0, 0.5, 1, 3 and 6 h) after MeJA (200 μM) treatment: ILL6 and IAR3; JOX/JAO; CYP94B3 and CYP94C1; ST2a; and JAR1. The bar charts show the relative expression data, only for those genes and time points in which FR had a significant (P < 0.05) effect (one-way ANOVA). Bars indicate means; thin bars = 1 SE; at each time point, n = 3 independent biological replicates (small open circles).
Extended Data Fig. 4 FR radiation reduced the concentrations of OH-JA and the sum of JA-Ile conjugates in wounded plants and the concentration of these compounds was higher in st2a-1 than in Col-0.
Bars indicate means; thin bars = 1 SE; at each time point, the interactive effects of genotype and light were tested using two-way ANOVA; n = 5 independent biological replicates (small open circles). Significant (P < 0.05) terms in the factorial analysis are indicated for each panel.
FR fails to upregulate the pool of HSO4-JA in a pif4 pif5 pif7 triple knock-out mutant, where FR fails to upregulate ST2a expression. Samples for metabolite analysis were taken 4 h after wounding. The dotted/dashed lines parallel to the abscissa indicate the basal levels of HSO4-JA in plant of both genotypes harvested before the wounding treatment. Bars indicate means for wounded plants; thin bars = 1 SE; n = 6 independent pools of 3 rosettes each (small open circles). The interactive effect of genotype and light were tested using two-way ANOVA; different letters indicate significant differences between means. b, In Col-0 plants, there is a tight, significant positive correlation between ST2a mRNA and HSO4-JA concentration in rosette tissues (two-tailed Spearman test). Different levels of ST2a gene expression were obtained by varying the amount of mechanical damage (see Methods for details). Samples were taken 4 h after wounding (each datum point represents an independent pool of 3 rosettes).
Supplementary Figs. 1–10, Tables 1 and 2, and methods.
Over-represented GO categories in RNA-seq data reported in Fig. 3b.
Identification codes for sulfotransferase sequences.
List of genes included in the heat map of Extended Data Fig. 1a.
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Fernández-Milmanda, G.L., Crocco, C.D., Reichelt, M. et al. A light-dependent molecular link between competition cues and defence responses in plants. Nat. Plants 6, 223–230 (2020). https://doi.org/10.1038/s41477-020-0604-8