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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:BackgroundBotrytis 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.ResultsThe 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).ConclusionResults 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:BackgroundBcGs1, 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.ResultsWe 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.ConclusionsThe 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

Constitutive Defense Mechanisms Have a Major Role in the Resistance of Woodland Strawberry Leaves Against <i>Botrytis cinerea</i>.

Project description:The necrotrophic fungus Botrytis cinerea is a major threat to strawberry cultivation worldwide. By screening different Fragaria vesca genotypes for susceptibility to B. cinerea, we identified two genotypes with different resistance levels, a susceptible genotype F. vesca ssp. vesca Tenno 3 (T3) and a moderately resistant genotype F. vesca ssp. vesca Kreuzkogel 1 (K1). These two genotypes were used to identify the molecular basis for the increased resistance of K1 compared to T3. Fungal DNA quantification and microscopic observation of fungal growth in woodland strawberry leaves confirmed that the growth of B. cinerea was restricted during early stages of infection in K1 compared to T3. Gene expression analysis in both genotypes upon B. cinerea inoculation suggested that the restricted growth of B. cinerea was rather due to the constitutive resistance mechanisms of K1 instead of the induction of defense responses. Furthermore, we observed that the amount of total phenolics, total flavonoids, glucose, galactose, citric acid and ascorbic acid correlated positively with higher resistance, while H2O2 and sucrose correlated negatively. Therefore, we propose that K1 leaves are more resistant against B. cinerea compared to T3 leaves, prior to B. cinerea inoculation, due to a lower amount of innate H2O2, which is attributed to a higher level of antioxidants and antioxidant enzymes in K1. To conclude, this study provides important insights into the resistance mechanisms against B. cinerea, which highly depend on the innate antioxidative profile and specialized metabolites of woodland strawberry leaves.

| S-EPMC9298464 | biostudies-literature

Transcriptome Mechanisms of Tomato Seedlings Induced by Low-Red to Far-Red Light Ratio under Calcium Nitrate Stress.

Project description:In recent times, the excessive accumulation of nitrate has been one of the main reasons for the secondary salinization of greenhouse soils. Light plays a key role in a plant's growth, development, and response to stress. A low-red to far-red (R:FR) light ratio could enhance plant salinity tolerance, but the mechanism at a molecular level is unclear. Thus, we analyzed the transcriptome responses of tomato seedlings to calcium nitrate stress under either a low R:FR ratio (0.7) or normal light conditions. Under calcium nitrate stress, a low R:FR ratio enhanced both the antioxidant defense system and the rapid physiological accumulation of proline in tomato leaves, which promoted plant adaptability. Using weighted gene co-expression network analysis (WGCNA), three modules including 368 differentially expressed genes (DEGs) were determined to be significantly associated with these plant traits. Functional annotations showed that the responses of these DEGs to a low R:FR ratio under excessive nitrate stress were enriched in the areas of hormone signal transduction, amino acid biosynthesis, sulfide metabolism, and oxidoreductase activity. Furthermore, we identified important novel hub genes encoding certain proteins, including FBNs, SULTRs, and GATA-like transcription factor, which may play a vital role in low R:FR light-induced salt responses. These findings offer a new perspective on the mechanisms and environmental implications behind low R:FR ratio light-modulated tomato saline tolerance.

| S-EPMC9963801 | 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

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

Tomato SlWRKY3 Negatively Regulates Botrytis cinerea Resistance via TPK1b

Project description: Not available

| S-EPMC11207927 | biostudies-literature

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

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