Far-red light promotes Botrytis cinerea disease development in tomato leaves via jasmonate-dependent modulation of soluble sugars.

Plants experience a decrease in the red:far-red light ratio (R:FR) when grown at high planting density. In addition to eliciting the shade avoidance response, low R:FR also enhances plant susceptibility to pathogens via modulation of defense hormone-mediated responses. However, other mechanisms, also affected by low R:FR, have not been considered as potential components in FR-induced susceptibility. Here, we identify FR-induced accumulation of leaf soluble sugars as a novel component of FR-induced susceptibility. We observed that phytochrome inactivation by FR or phytochrome B mutation was associated with elevated leaf glucose and fructose levels and enhanced disease severity caused by Botrytis cinerea. By experimentally manipulating internal leaf sugar levels, we found that the FR-induced susceptibility in tomato was partly sugar-dependent. Further analysis revealed that the observed sugar accumulation in supplemental FR occurred in a jasmonic acid (JA)-dependent manner, and the JA biosynthesis mutant def1 also displayed elevated soluble sugar levels, which was rescued by exogenous methyl jasmonate (MeJA) application. We propose that the reduced JA responsiveness under low R:FR promotes disease symptoms not only via dampened induction of defense responses, but also via increased levels of soluble sugars that supports pathogen growth in tomato leaves.

Courbier S ，Grevink S ，Sluijs E ，Bonhomme PO ，Kajala K ，Van Wees SCM ，Pierik R ... -  《-》

Mechanisms of far-red light-mediated dampening of defense against Botrytis cinerea in tomato leaves.

Plants detect neighboring competitors through a decrease in the ratio between red and far-red light (R:FR). This decreased R:FR is perceived by phytochrome photoreceptors and triggers shade avoidance responses such as shoot elongation and upward leaf movement (hyponasty). In addition to promoting elongation growth, low R:FR perception enhances plant susceptibility to pathogens: the growth-defense tradeoff. Although increased susceptibility in low R:FR has been studied for over a decade, the associated timing of molecular events is still unknown. Here, we studied the chronology of FR-induced susceptibility events in tomato (Solanum lycopersicum) plants pre-exposed to either white light (WL) or WL supplemented with FR light (WL+FR) prior to inoculation with the necrotrophic fungus Botrytis cinerea (B.c.). We monitored the leaf transcriptional changes over a 30-h time course upon infection and followed up with functional studies to identify mechanisms. We found that FR-induced susceptibility in tomato is linked to a general dampening of B.c.-responsive gene expression, and a delay in both pathogen recognition and jasmonic acid-mediated defense gene expression. In addition, we found that the supplemental FR-induced ethylene emissions affected plant immune responses under the WL+FR condition. This study improves our understanding of the growth-immunity tradeoff, while simultaneously providing leads to improve tomato resistance against pathogens in dense cropping systems.

Courbier S ，Snoek BL ，Kajala K ，Li L ，van Wees SCM ，Pierik R ... -  《-》

The jasmonate signaling pathway in tomato regulates susceptibility to a toxin-dependent necrotrophic pathogen.

Egusa M ，Ozawa R ，Takabayashi J ，Otani H ，Kodama M ... -  《-》

Linking phytochrome to plant immunity: low red : far-red ratios increase Arabidopsis susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin.

Shade-intolerant plants respond to low red : far-red (R : FR) ratios, which signal the proximity of potential competitors, by down-regulating immune responses. Here we investigated the mechanisms underlying this immune suppression in Arabidopsis. We used genetic, transcriptomic and metabolomic approaches to examine the functional connections between R : FR ratio and Arabidopsis resistance to the fungus Botrytis cinerea. Low R : FR ratios reduced the concentration of indol-3-ylmethyl glucosinolate (I3M) (an indolic glucosinolate, iGS) and camalexin in plants inoculated with B. cinerea, and attenuated the I3M response triggered by jasmonate elicitation. These effects on metabolite abundance correlated with reduced expression of iGS and camalexin biosynthetic genes. Furthermore, the effect of low R : FR increasing Arabidopsis susceptibility to B. cinerea was not present in mutants deficient in the biosynthesis of camalexin (pad3) or metabolism of iGS (pen2). Finally, in a mutant deficient in the JASMONATE ZIM DOMAIN-10 (JAZ10) protein, which does not respond to low R : FR with increased susceptibility to B. cinerea, supplemental FR failed to down-regulate iGS production. These results indicate that suppression of Arabidopsis immunity against B. cinerea by low R : FR ratios is mediated by reduced levels of Trp-derived defenses, and provide further evidence for a functional role of JAZ10 in the link between phytochrome and jasmonate signaling.

Cargnel MD ，Demkura PV ，Ballaré CL 《-》

Reduced susceptibility of tomato stem to the necrotrophic fungus Botrytis cinerea is associated with a specific adjustment of fructose content in the host sugar pool.

Plant soluble sugars, as main components of primary metabolism, are thought to be implicated in defence against pathogenic fungi. However, the function of sucrose and hexoses remains unclear. This study aimed to identify robust patterns in the dynamics of soluble sugars in sink tissues of tomato plants during the course of infection by the necrotrophic fungus Botrytis cinerea . Distinct roles for glucose and fructose in defence against B. cinerea were hypothesized. We examined sugar contents and defence hormonal markers in tomato stem tissues before and after infection by B. cinerea , in a range of abiotic environments created by various nitrogen and water supplies. Limited nitrogen or water supplies increased tomato stem susceptibility to B. cinerea . Glucose and fructose contents of tissues surrounding infection sites evolved differently after inoculation. The fructose content never decreased after inoculation with B. cinerea , while that of glucose showed either positive or negative variation, depending on the abiotic environment. An increase in the relative fructose content (defined as the proportion of fructose in the soluble sugar pool) was observed in the absence of glucose accumulation and was associated with lower susceptibility. A lower expression of the salicylic acid marker PR1a , and a lower repression of a jasmonate marker COI1 were associated with reduced susceptibility. Accordingly, COI1 expression was positively correlated with the relative fructose contents 7 d after infection. Small variations of fructose content among the sugar pool are unlikely to affect intrinsic pathogen growth. Our results highlight distinct use of host glucose and fructose after infection by B. cinerea and suggest strongly that adjustment of the relative fructose content is required for enhanced plant defence.

Lecompte F ，Nicot PC ，Ripoll J ，Abro MA ，Raimbault AK ，Lopez-Lauri F ，Bertin N ... -  《-》