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

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 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, an ELISA-based glycomics technique to assess 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 pectic 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{Delta} bcpg1{Delta}bcpg2 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. One-Sentence SummaryPhysiological, transcriptional, and glycomic evidence indicates Botrytis cinerea hastens tomato fruit ripening to facilitate infection by a mechanism dependent on the fungal enzymes Bcpg1 and Bcpg2.