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

ABSTRACT: 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.

SUBMITTER: Courbier S

PROVIDER: S-EPMC8566310 | biostudies-literature |

REPOSITORIES: biostudies-literature

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

Project description: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.

| S-EPMC7693051 | biostudies-literature

Far-red enriched light delays tomato transcriptome modulations in response to Botrytis cinerea infection

Project description:We performed a transcriptome analysis of a 30 -hour infection time course aiming to unravel hormonal and metabolic pathways affected by FR which would in turn modulate disease resistance. Our data show that supplemental FR, received before pathogen inoculation, triggers the FR-induced susceptibility, which is associated with a delay in pathogen recognition and defense activation via JA and possibly ethylene signaling. The transcriptome analysis highlighted a set of six PROTEINASE INHIBITOR genes (PI) that are induced only in WL-treated samples. As PI genes are described to be JA-responsive genes, the FR-induced susceptibility in tomato is possibly due to a dampening of JA-mediated gene induction and expression affecting defense responses resulting in more susceptible plants.

2020-09-30 | GSE157831 | GEO

Characterization of miRNAs associated with Botrytis cinerea infection of tomato leaves.

Project description:Botrytis cinerea Pers. Fr. is an important pathogen causing stem rot in tomatoes grown indoors for extended periods. MicroRNAs (miRNAs) have been reported as gene expression regulators related to several stress responses and B. cinerea infection in tomato. However, the function of miRNAs in the resistance to B. cinerea remains unclear.The miRNA expression patterns in tomato in response to B. cinerea stress were investigated by high-throughput sequencing. In total, 143 known miRNAs and seven novel miRNAs were identified and their corresponding expression was detected in mock- and B. cinerea-inoculated leaves. Among those, one novel and 57 known miRNAs were differentially expressed in B. cinerea-infected leaves, and 8 of these were further confirmed by quantitative reverse-transcription PCR (qRT-PCR). Moreover, five of these eight differentially expressed miRNAs could hit 10 coding sequences (CDSs) via CleaveLand pipeline and psRNAtarget program. In addition, qRT-PCR revealed that four targets were negatively correlated with their corresponding miRNAs (miR319, miR394, and miRn1).Results of sRNA high-throughput sequencing revealed that the upregulation of miRNAs may be implicated in the mechanism by which tomato respond to B. cinerea stress. Analysis of the expression profiles of B. cinerea-responsive miRNAs and their targets strongly suggested that miR319, miR394, and miRn1 may be involved in the tomato leaves' response to B. cinerea infection.

| S-EPMC4311480 | biostudies-literature

Lignin metabolism involves Botrytis cinerea BcGs1- induced defense response in tomato.

Project description:BACKGROUND:BcGs1, a cell wall-degrading enzyme (CWDE), was originally derived from Botrytis cinerea. Our previous study revealed that BcGs1 could trigger defense responses and protect plants against various pathogens. We researched the defense response mechanism underlying this BcGs1 elicitation in tomato. RESULTS:We revealed that the two domains were required for BcGs1's full necrosis activity. According to analysis and quantitative real-time PCR of the up-regulated proteins and genes filtered by iTRAQ-based quantitative proteome approach, oxidative metabolism and phenylpropanoid metabolism were speculated to be involved in BcGs1-triggered defense response in tomato. Furthermore, experimental evidence showed that BcGs1 triggered reactive oxygen species (ROS) burst and increased the level of phenylalanine-ammonia lyase (PAL) and peroxidase (POD) enzyme activity, as well as lignin accumulation. Moreover, histochemical analysis revealed that infiltration of BcGs1 in tomato leaves exhibited cell wall thickening compared with untreated plants. CONCLUSIONS:The results suggested that BcGs1 activated the basal defense response included lignin metabolism contributed to BcGs1-induced resistance to Botrytis. cinerea infection in tomato.

| S-EPMC5987389 | biostudies-literature

Botrytis cinerea induces local hypoxia in Arabidopsis leaves.

Project description:Low oxygen availability often is associated with soil waterlogging or submergence, but may occur also as hypoxic niches in otherwise aerobic tissues. Experimental evidence assigns a role in Botrytis cinerea resistance to a group of oxygen-unstable Ethylene Response Factors (ERF-VII). Given that infection by B. cinerea often occurs in aerobic organs such as leaves, where ERF-VII stability should be compromised, we explored the possibility of local leaf hypoxia at the site of infection. We analyzed the expression of hypoxia-responsive genes in infected leaves. Confocal microscopy was utilized to verify the localization of the ERF-VII protein RAP2.12. Oxygen concentration was measured to evaluate the availability of oxygen (O2 ). We discovered that infection by B. cinerea induces increased respiration, leading to a drastic drop in the O2 concentration in an otherwise fully aerobic leaf. The establishment of a local hypoxic area results in stabilization and nuclear relocalization of RAP2.12. The possible roles of defence elicitors, ABA and ethylene were evaluated. Local hypoxia at the site of B. cinerea infection allows the stabilization of ERF-VII proteins. Hypoxia at the site of pathogen infection generates a nearly O2 -free environment that may affect the stability of other N-degron-regulated proteins as well as the metabolism of elicitors.

| S-EPMC7754360 | biostudies-literature

Far-red enriched light delays tomato transcriptome modulations in response to Botrytis cinerea infection

Project description:Far-red enriched light delays tomato transcriptome modulations in response to Botrytis cinerea infection

| PRJNA662936 | ENA

Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea.

Project description:Botrytis cinerea, a model necrotrophic fungal pathogen that causes gray mold as it infects different organs on more than 200 plant species, is a significant contributor to postharvest rot in fresh fruit and vegetables, including tomatoes. By describing host and pathogen proteomes simultaneously in infected tissues, the plant proteins that provide resistance and allow susceptibility and the pathogen proteins that promote colonization and facilitate quiescence can be identified. This study characterizes fruit and fungal proteins solubilized in the B. cinerea-tomato interaction using shotgun proteomics. Mature green, red ripe wild type and ripening inhibited (rin) mutant tomato fruit were infected with B. cinerea B05.10, and the fruit and fungal proteomes were identified concurrently 3 days postinfection. One hundred eighty-six tomato proteins were identified in common among red ripe and red ripe-equivalent ripening inhibited (rin) mutant tomato fruit infected by B. cinerea. However, the limited infections by B. cinerea of mature green wild type fruit resulted in 25 and 33% fewer defense-related tomato proteins than in red and rin fruit, respectively. In contrast, the ripening stage of genotype of the fruit infected did not affect the secreted proteomes of B. cinerea. The composition of the collected proteins populations and the putative functions of the identified proteins argue for their role in plant-pathogen interactions.

| S-EPMC4874510 | biostudies-literature

Molecular mechanism of BjCHI1-mediated plant defense against Botrytis cinerea infection.

Project description:Plant chitinases are a group of proteins associated with defense against pathogen attack. BjCHI1 is the first characterized chitinase containing two chitin binding domains (CBDs). Investigations have shown that BjCHI1 inhibits growth of fungal phytopathogens and agglutinates Gram-negative bacteria. Our recent studies revealed that expression of BjCHI1 mRNA is largely induced upon infection of Botrytis cinerea via a R2R3-MYB transcription factor BjMYB1 interacting with a W box-like element (Wbl-4) in the BjCHI1 promoter. The enhanced expression pattern of BjMYB1 was similar to that of BjCHI1 and associated with resistant phenotype against B. cinerea. These findings suggest that BjCHI1 is involved in host defense against fungal attack through interaction with BjMYB1. Here, we review the recent studies on BjCHI1 and propose a model of BjCHI1-mediated plant defense against fungal attack.

| S-EPMC5289518 | biostudies-literature

Tomato SlMKK2 and SlMKK4 contribute to disease resistance against Botrytis cinerea.

Project description:BACKGROUND: Mitogen-activated protein kinase (MAPK) cascades are highly conserved signaling modules that mediate the transduction of extracellular stimuli via receptors/sensors into intracellular responses and play key roles in plant immunity against pathogen attack. However, the function of tomato MAPK kinases, SlMKKs, in resistance against Botrytis cinerea remains unclear yet. RESULTS: A total of five SlMKK genes with one new member, SlMKK5, were identified in tomato. qRT-PCR analyses revealed that expression of SlMKK2 and SlMKK4 was strongly induced by B. cinerea and by jasmonic acid and ethylene precursor 1-amino cyclopropane-1-carboxylic acid. Virus-induced gene silencing (VIGS)-based knockdown of individual SlMKKs and disease assays identified that SlMKK2 and SlMKK4 but not other three SlMKKs (SlMKK1, SlMKK3 and SlMKK5) are involved in resistance against B. cinerea. Silencing of SlMKK2 or SlMKK4 resulted in reduced resistance to B. cinerea, increased accumulation of reactive oxygen species and attenuated expression of defense genes after infection of B. cinerea in tomato plants. Furthermore, transient expression of constitutively active phosphomimicking forms SlMKK2DD and SlMKK4DD in leaves of Nicotiana benthamiana plants led to enhanced resistance to B. cinerea and elevated expression of defense genes. CONCLUSIONS: VIGS-based knockdown of SlMKK2 and SlMKK4 expression in tomato and gain-of-function transient expression of constitutively active phosphomimicking forms SlMKK2DD and SlMKK2DD in N. benthamiana demonstrate that both SlMKK2 and SlMKK4 function as positive regulators of defense response against B. cinerea.

| S-EPMC4094914 | biostudies-literature

Expression data from Col-0 and pil5 imbibed seeds after far-red or far-red/red light irradiation.

Project description:PIL5 is a key negative regulator of phytochrome mediated seed germination and PIL5 protein is degraded by red light irradiation through phytochrome. The microarray aimed to find various red light-regulated genes and PIL5-regulated genes in the imbibed seeds. Keywords: genetic modification

2010-01-12 | GSE14374 | GEO

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