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Botrytis cinerea infection accelerates ripening and cell wall disassembly in tomato fruit to promote disease

ABSTRACT: Postharvest fungal pathogens benefit from the increased host susceptibility that occurs during fruit ripening. In unripe fruit, pathogens often remain quiescent and unable to cause disease until ripening begins, emerging at this point into destructive necrotrophic lifestyles that quickly result in fruit decay. Here, we demonstrate that one such pathogen, Botrytis cinerea, actively induces ripening processes in order to facilitate infections and promote disease. Assessments of ripening progression revealed that B. cinerea accelerated external coloration, ethylene production, and softening in unripe fruit, while mRNA sequencing of inoculated unripe fruit confirmed the corresponding upregulation of host genes involved in ripening processes, such as ethylene biosynthesis and cell wall degradation. Furthermore, ELISA-based glycomics profiling of fruit cell wall polysaccharides revealed remarkable similarities in the cell wall polysaccharide changes caused by both infections of unripe fruit and ripening of healthy fruit, particularly in the increased accessibility of pectin polysaccharides. Virulence and additional ripening assessment experiments with B. cinerea knockout mutants showed that induction of ripening is dependent on the ability to infect the host and break down pectin. The B. cinerea double knockout Δbcpg1Δbcpg2 lacking two critical pectin degrading enzymes was found to be incapable of emerging from quiescence even long after the fruit had ripened at its own pace, suggesting that the failure to accelerate ripening severely inhibits fungal survival on unripe fruit. These findings demonstrate that active induction of ripening in unripe tomato fruit is an important infection strategy for B. cinerea.

ORGANISM(S): Botrytis cinerea Solanum lycopersicum

PROVIDER: GSE183836 | GEO | 2022/01/01

REPOSITORIES: GEO

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Project description:Worldwide, 20-25% of all harvested fruit and vegetables are lost annually in the field and throughout the postharvest supply handling chain due to spoilage by fungal pathogens. Most impactful postharvest pathogens exhibit necrotrophic lifestyles, resulting in rotting of the host tissues and complete loss of marketable commodities. Necrotrophic fungi can readily infect ripe fruit leading to the rapid establishment of disease symptoms. However, these pathogens generally fail to infect unripe fruit, or remain quiescent until host and environmental conditions stimulate a successful infection. Current research on necrotrophic infections of fruit was mainly focused on the host by characterizing genetic and physicochemical factors that inhibit or promote the disease. However, the pathogenicity and virulence strategies employed by necrotrophic pathogens in ripe and unripe fruit are mostly understudied. Here, we provide a first comparative transcriptomics study of fungal postharvest pathogens: Botrytis cinerea, Rhizopus stolonifer and Fusarium acuminatum, all of which display necrotrophic behavior when infecting fruit. We de novo assembled and annotated the transcriptomes of R. stolonifer, and F. acuminatum and performed a differential gene expression analysis comparing the three fungal transcriptomes during fruit infection with that of fungal in-vitro growth. Analysis of the differentially expressed genes for enrichment of functional annotations revealed shared strategies of the three fungi during infection of compatible (ripe fruit) and incompatible (unripe fruit) hosts. We furthermore selected candidate genes that are involved in these strategies to characterize their expression during infection of unripe and ripe-like fruit of the non-ripening (nor) tomato mutant, both of which are physiologically and biochemically similar to unripe wildtype fruit. By enabling a better understanding of fungal necrotrophic infection strategies, we move closer to generating accurate models of fruit diseases and development of early detection tools and effective management strategies.

Project description:Tomato fruit ripening is under the control of ethylene as well as a group of ethylene-independent transcription factors, including NON-RIPENING (NOR) and RIPENING INHIBITOR (RIN). During ripening, the linear carotene lycopene accumulates at the expense of cyclic carotenoids. Fruit-specific overexpression of LYCOPENE β-CYCLASE (LCYb) under the control of the PHYTOENE DESATURASE (PDS) promoter resulted in increased levels of β-carotene and ABA and in decreased ethylene levels. Genes regulated by ABA, or involved in its synthesis and signaling, were overexpressed, while those associated with ethylene and cell wall remodeling were repressed. In agreement with the transcriptional data, LCYb-overexpressing fruits exhibited increased density of cell wall material containing linear, under-methylated pectins and displayed an array of additional ripening phenotypes, including delayed softening, increased turgor, enhanced shelf life and a thicker cuticle with a higher content of cutin monomers and triterpenoids. The levels of several primary metabolites and phenylpropanoids also changed in the transgenics, which could be attributed to delayed fruit ripening and to ABA respectively. Network correlation analysis suggests that ABA, acting through NOR and RIN, is responsible for many of the above phenotypes. These data reinforce suggestions that ABA plays an important role in tomato fruit ripening and provide clues that fruit b-carotene, acting as a precursor for ABA, actively participates in controlling the ripening process rather than merely being an output thereof. Overexpression of a LCYb gene from Arabidopsis under the control of the ripening-associated PDS promoter leads to ripe tomato fruits accumulating high β-carotene levels. Using several independent transgenic lines, we conducted a system-wide study of the effect of increased β-carotene levels on tomato fruit ripening and shelf life. Our data suggest that β-carotene, acting through ABA, is involved in a regulatory loop within the network controlling tomato fruit ripening.