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Title: Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins

Author
item HELLIWELL, EMILY - Pennsylvania State University
item VEGA, ARREGUIN - Virginia Polytechnic Institution & State University
item SHI, ZI - Pennsylvania State University
item Bailey, Bryan
item XIO, SHUNYUAN - University Of Maryland
item MAXIMOVA, SIELA - Pennsylvania State University
item TYLER, BRETT - Oregon State University
item GUILTINAN, MARK - Pennsylvania State University

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/16/2015
Publication Date: 7/27/2015
Citation: Helliwell, E.E., Vega, A.J., Shi, Z., Bailey, B.A., Xio, S., Maximova, S.N., Tyler, B.M., Guiltinan, M. 2015. Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins. Plant Biotechnology Journal. 14:875–886.

Interpretive Summary: Pathogens reduce the yield of the tropical tree Theobroma cacao, the source of chocolate, where ever it is grown. Several pathogens of cacao have the potential to cause complete yield loss. Farmers who grow cacao often depend on cacao as a cash crop. Crop losses due to disease can be devastating to farmer’s finances, in addition to the major limitations placed on global cacao supplies and the resulting cost to producers and consumers. In many interactions with, the pathogen secretes proteins know as effectors that hijack the plant’s defenses making the plant highly susceptible to diseases. Transgenic cacao seedlings were produced in the laboratory that produce proteins that block the action of the pathogen secreted proteins and protect cacao from disease. The techniques and tools developed through this research suggest potential approaches for reducing losses in cacao and other crops due to disease. By reducing losses to disease the lives of farmers producing cacao can be improved and the global supplies of cacao stabilized to the benefit of the cocoa industry and the consumer of cocoa products.

Technical Abstract: The internalization of oomycete and fungal pathogen effectors into host plant cells has been reported to be blocked by proteins that bind to the effectors’ cell entry receptor, phosphatidylinositol-3-phosphate (PI3P). This finding suggested a novel strategy for disease control by engineering plants to secrete PI3P-binding proteins. In this study we have tested this strategy using the chocolate tree Theobroma cacao, as a proof of concept crop model system. Transient expression and secretion of four different PI3P-binding proteins in detached leaves of T. cacao greatly reduced infection by two oomycetes, Phytophthora capsici and Phytophthora palmivora, that cause black pod disease. Lesion size and pathogen growth were reduced by up to 85%. Resistance was not conferred by proteins lacking a secretory leader, by proteins with mutations in their PI3P-binding site, or by a secreted PI4P-binding protein. Stably transformed, transgenic T. cacao plants expressing two different PI3P-binding proteins showed substantially enhanced resistance to both P. capsici and P. palmivora, as well as to the fungal pathogen Colletotrichum theobromicola, as measured by detached leaf pathogenicity assays. These results demonstrate that secretion of PI3P-binding proteins is an effective way to increase disease resistance in T. cacao against oomycete and fungal pathogens, and potentially in other plants against a broad spectrum of pathogens.