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 ... -  《-》

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 ... -  《-》

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 《-》

Role of dioxygenase α-DOX2 and SA in basal response and in hexanoic acid-induced resistance of tomato (Solanum lycopersicum) plants against Botrytis cinerea.

Resistance of tomato (Solanum Lycopersicum) to the fungal pathogen Botrytis cinerea requires complex interplay between hormonal signalling. In this study, we explored the involvement of new oxylipins in the tomato basal and induced response to this necrotroph through the functional analysis of the tomato α-dioxygenase2 (α-DOX2)-deficient mutant divaricata. We also investigated the role of SA in the defence response against this necrotrophic fungus using SA-deficient tomato nahG plants. The plants lacking dioxigenase α-DOX2, which catalyses oxylipins production from fatty acids, were more susceptible to Botrytis, and hexanoic acid-induced resistance (Hx-IR) was impaired; hence α-DOX2 is required for both tomato defence and the enhanced protection conferred by natural inducer hexanoic acid (Hx) against B. cinerea. The divaricata plants accumulated less pathogen-induced callose and presented lower levels of jasmonic acid (JA) and 12-oxo-phytodienoic acid (OPDA) upon infection if compared to the wild type. Glutathion-S-transferase (GST) gene expression decreased and ROS production significantly increased in Botrytis-infected divaricata plants. These results indicate that absence of α-DOX2 influences the hormonal changes, oxidative burst and callose deposition that occur upon Botrytis infection in tomato. The study of SA-deficient nahG tomato plants showed that the plants with low SA levels displayed increased resistance to Botrytis, but were unable to display Hx-IR. This supports the involvement of SA in Hx-IR. NaghG plants displayed reduced callose and ROS accumulation upon infection and an increased GST expression. This reflects a positive relationship between SA and these defensive mechanisms in tomato. Finally, Hx boosted the pathogen-induced callose in nahG plants, suggesting that this priming mechanism is SA-independent. Our results support the involvement of the oxylipins pathway and SA in tomato response to Botrytis, probably through complex crosstalk of the hormonal balance with callose and ROS accumulation, and reinforce the role of the oxidative stress in the outcome of the plant-Botrytis interaction.

Angulo C ，de la O Leyva M ，Finiti I ，López-Cruz J ，Fernández-Crespo E ，García-Agustín P ，González-Bosch C ... -  《-》

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

Cerrudo I ，Keller MM ，Cargnel MD ，Demkura PV ，de Wit M ，Patitucci MS ，Pierik R ，Pieterse CM ，Ballaré CL ... -  《-》