Remodeling of the polysaccharide-rich cell wall surrounding all plant cells may accompany increased susceptibility to Botrytis cinerea, a pathogenic fungus that rots most fruit. Tomato fruit ripening is an example of plant cell wall disassembly that coincides with increased pathogen susceptibility. While ripening tomato fruit and Botrytis express similar plant cell wall degrading enzymes, previous work demonstrated that the enzymes produced by ripening fruit are crucial for the ripening-associated increase in susceptibility. Observations that not all non-ripening tomato mutants are resistant to Botrytis, suggested that some, but not all, ripening events are responsible for fruit susceptibility to decomposition. The mechanism(s) that make ripe fruit susceptible include cell wall disassembly which provides B. cinerea with accessible nutrients in circumstances where anti-pathogen responses are limited. This project identifies 1) polysaccharide targets of fruit cell wall remodeling proteins, 2) B. cinerea and fruit gene expression changes and 3) proteins produced by both interactors, to link specific components of the wall architecture to pathogen perception and the consequent susceptibility. The researchers' expertise in polysaccharide characterization and simultaneous plant and pathogen transcriptome and proteome analyses allows evaluation of wall architecture, infection, and ripening, thereby expanding knowledge about the diversity of fungal decomposing strategies and the plasticity of plant responses. This project uses an economically significant pathogen and fruit; the results may be applied to other crop plants and plant parts whose wall architecture is altered. The researchers have strong ties to US and international agricultural sectors enhancing the education of high school and undergraduate students, including individuals from agricultural communities in Costa Rica and Mexico and from small underserved undergraduate and technical institutions.
The goal of the research in our group is to improve the quality of acceptably ripened fruit. Loss of fruit to decay by fungal pathogens has imposed significant costs on producers and consumers. Up to 90% of ripe fruit crops are destroyed by spoilage due to infections by rot-causing pathogens. An aim of the program is to identify why ripe tomato fruit are more easily infected and decomposed by the generalist necrotrophic fungus, Botrytis cinerea, than unripe fruit. The scientific question addressed is whether increased susceptibility is an inevitable and inherent part of ripening or whether susceptibility and ripening are separable processes. If the ripening and susceptibility can be distinguished and separated, then it should be possible to develop or select for varieties whose fruit ripen acceptably but do not become susceptible to aggressive rot-causing infections as they mature. The project identified processes that occur in tomato fruit hosts and in the infecting fungus that enable the pathogen to grow on ripe fruit. The project utilized tomato fruit because of the extensive physiological, genomic and mutant resources that have been developed to investigate the regulation and events that occur as the fruit ripen. The work focused primarily on events and processes involving the extracellular polysaccharide matrix of the fruit cell wall. The composition and architecture of cell wall had been identified as key factors that determined whether Botrytis is able to infect fruit. The production of enzymes that disassemble host cell walls is also one of the first virulence functions expressed by the infecting fungus. Beyond the applications for improving fruit quality, the research addressed questions about terminal development (in the case of fruit, ripening) in tissues and how external agents, such as pathogens, can impact development and metabolism in senescing tissues. The intellectual merits of this project are that (1) we have shown that not all ripening processes are necessary for fruit to be susceptible to infections by Botrytis, (2) we have identified that processes that target the fruit host cell wall are key for determining whether infections advance, (3) we have defined which cell wall targeting enzymes of the pathogen and the host are needed for infections, (4) we have demonstrated that infections of unripe with Botrytis accelerate ripening. The broader impact of this work is that we have defined which ripening processes should be targeted to improve the resistance of ripe fruit to decomposing diseases. Ripe fruit are important for healthy human diets and improving the resistance of fruit will reduce wastage due to spoilage and decrease the potential of damaged fruit to contain human disease causing pathogens. The research program trained a Latina PhD graduate student and supported undergraduate research by university and high school students and postdoctoral work by visiting scientists. The work resulted in 7 peer-reviewed accepted publications, 3 manuscripts submitted for peer review, 2 book chapters, and 2 publications in the final stages of preparation in addition to oral presentations at international symposia.
