Exploring growth-defence trade-offs in Arabidopsis: phytochrome B inactivation requires JAZ10 to suppress plant immunity but not to trigger shade-avoidance responses.

Under conditions that involve a high risk of competition for light among neighbouring plants, shade-intolerant species often display increased shoot elongation and greater susceptibility to pathogens and herbivores. The functional links between morphological and defence responses to crowding are not well understood. In Arabidopsis, the protein JAZ10 is thought to play a key role connecting the inactivation of the photoreceptor phytochrome B (phyB), which takes place under competition for light, with the repression of jasmonate-mediated plant defences. Here, we show that a null mutation of the JAZ10 gene in Arabidopsis did not affect plant growth nor did it suppress the shade-avoidance responses elicited by phyB inactivation. However, the jaz10 mutation restored many of the defence traits that are missing in the phyB mutant, including the ability to express robust responses to jasmonate and to accumulate indolic glucosinolates. Furthermore, the jaz10phyB double mutant showed a significantly increased resistance to the pathogenic fungus Botrytis cinerea compared with the phyB parental line. Our results demonstrate that, by inactivating JAZ10, it is possible to partially uncouple shade avoidance from defence suppression in Arabidopsis. These findings may provide clues to improve plant resistance to pathogens in crops that are planted at high density.

To grow or defend? Low red : far-red ratios reduce jasmonate sensitivity in Arabidopsis seedlings by promoting DELLA degradation and increasing JAZ10 stability.

How plants balance resource allocation between growth and defense under conditions of competitive stress is a key question in plant biology. Low red : far-red (R : FR) ratios, which signal a high risk of competition in plant canopies, repress jasmonate-induced defense responses. The mechanism of this repression is not well understood. We addressed this problem in Arabidopsis by investigating the role of DELLA and JASMONATE ZIM domain (JAZ) proteins. We showed that a quintuple della mutant and a phyB mutant were insensitive to jasmonate for several physiological readouts. Inactivation of the photoreceptor phyB by low R : FR ratios rapidly reduced DELLA protein abundance, and the inhibitory effect of FR on jasmonate signaling was missing in the gai-1 mutant, which encodes a stable version of the GAI DELLA protein. We also demonstrated that low R : FR ratios and the phyB mutation stabilized the protein JAZ10. Furthermore, we demonstrated that JAZ10 was required for the inhibitory effect of low R : FR on jasmonate responses, and that the jaz10 mutation restored jasmonate sensitivity to the phyB mutant. We conclude that, under conditions of competition for light, plants redirect resource allocation from defense to rapid elongation by promoting DELLA degradation and enhancing JAZ10 stability.

Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism.

Light is an important modulator of plant immune responses. Here, we show that inactivation of the photoreceptor phytochrome B (phyB) by a low red/far-red ratio (R:FR), which is a signal of competition in plant canopies, down-regulates the expression of defense markers induced by the necrotrophic fungus Botrytis cinerea, including the genes that encode the transcription factor ETHYLENE RESPONSE FACTOR1 (ERF1) and the plant defensin PLANT DEFENSIN1.2 (PDF1.2). This effect of low R:FR correlated with a reduced sensitivity to jasmonate (JA), thus resembling the antagonistic effects of salicylic acid (SA) on JA responses. Low R:FR failed to depress PDF1.2 mRNA levels in a transgenic line in which PDF1.2 transcription was up-regulated by constitutive expression of ERF1 in a coronatine insensitive1 (coi1) mutant background (35S::ERF1/coi1). These results suggest that the low R:FR effect, in contrast to the SA effect, requires a functional SCFCOI1-JASMONATE ZIM-DOMAIN (JAZ) JA receptor module. Furthermore, the effect of low R:FR depressing the JA response was conserved in mutants impaired in SA signaling (sid2-1 and npr1-1). Plant exposure to low R:FR ratios and the phyB mutation markedly increased plant susceptibility to B. cinerea; the effect of low R:FR was (1) independent of the activation of the shade-avoidance syndrome, (2) conserved in the sid2-1 and npr1-1 mutants, and (3) absent in two RNA interference lines disrupted for the expression of the JAZ10 gene. Collectively, our results suggest that low R:FR ratios depress Arabidopsis (Arabidopsis thaliana) immune responses against necrotrophic microorganisms via a SA-independent mechanism that requires the JAZ10 transcriptional repressor and that this effect may increase plant susceptibility to fungal infection in dense canopies.

Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades.

Plants respond to a reduction in the red/far-red ratio (R:FR) of light, caused by the proximity of other plants, by initiating morphological changes that improve light capture. In Arabidopsis, this response (shade avoidance syndrome, SAS) is controlled by phytochromes (particularly phyB), and is dependent on the TAA1 pathway of auxin biosynthesis. However, when grown in real canopies, we found that phyB mutants and mutants deficient in TAAI (sav3) still display robust SAS responses to increased planting density and leaf shading. The SAS morphology (leaf hyponasty and reduced lamina/petiole ratio) could be phenocopied by exposing plants to blue light attenuation. These responses to blue light attenuation required the UV-A/blue light photoreceptor cry1. Moreover, they were mediated through mechanisms that showed only limited overlap with the pathways recruited by phyB inactivation. In particular, pathways for polar auxin transport, auxin biosynthesis and gibberellin signaling that are involved in SAS responses to low R:FR were not required for the SAS responses to blue light depletion. By contrast, the brassinosteroid response appeared to be required for the full expression of the SAS phenotype under low blue light. The phyB and cry1 inactivation pathways appeared to converge in their requirement for the basic/helix-loop-helix (bHLH) transcription factors PHYTOCHROME INTERACTING FACTORs 4 and 5 (PIF4 and PIF5) to elicit the SAS phenotype. Our results suggest that blue light is an important control of SAS responses, and that PIF4 and PIF5 are critical hubs for a diverse array of signaling routes that control plant architecture in canopies.

Blue light regulated shade avoidance.

Most plants grow in dense vegetation with the risk of being out-competed by neighboring plants. These neighbors can be detected not only through the depletion in light quantity that they cause, but also through the change in light quality, which plants perceive using specific photoreceptors. Both the reduction of the red:far-red ratio and the depletion of blue light are signals that induce a set of phenotypic traits, such as shoot elongation and leaf hyponasty, which increase the likelihood of light capture in dense plant stands. This set of phenotypic responses are part of the so called shade avoidance syndrome (SAS). This addendum discusses recent findings on the regulation of the SAS of Arabidopsis thaliana upon blue light depletion. Keller et al. and Keuskamp et al. show that the low blue light attenuation induced shade avoidance response of seedling and rosette-stage A. thaliana plants differ in their hormonal regulation. These studies also show there is a regulatory overlap with the R:FR-regulated SAS.