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ARS Home » Pacific West Area » Albany, California » Western Regional Research Center » Crop Improvement and Genetics Research » Research » Publications at this Location » Publication #312439
Title: Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species

Author
item GOU, JIN-YING - Fudan University
item LI, KUN - Shandong University
item WU, KATI - University Of California
item WANG, XIAODONG - University Of California
item LIN, HUIQIONG - University Of California
item CANTU, DARIO - University Of California
item UAUY, CRISTOBAL - John Innes Center
item DOBOM-ALONSO, ALBOR - John Innes Center
item MIDORIKAWA, TAKAMUFI - University Of California
item INOUE, KENTARO - University Of California
item SANCHEZ, JUAN - University Of California
item FU, DAOLIN - Shandong University
item Blechl, Ann
item WALLINGTON, EMMA - National Institute Of Agricultural Botany (NIAB)
item FAHIMA, TZION - University Of Haifa
item MEETA, MADHU - Punjab Agricultural University
item EPSTEIN, LYNN - University Of California
item DUBCOVSKY, JORGE - University Of California

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/21/2015
Publication Date: 6/15/2015
Citation: Gou, J., Li, K., Wu, K., Wang, X., Lin, H., Cantu, D., Uauy, C., Dobom-Alonso, A., Midorikawa, T., Inoue, K., Sanchez, J., Fu, D., Blechl, A.E., Wallington, E., Fahima, T., Meeta, M., Epstein, L., Dubcovsky, J. 2015. Wheat stripe rust resistance protein WKS1 reduces the ability of the thylakoid-associated ascorbate peroxidase to detoxify reactive oxygen species. The Plant Cell. 27:1755-1770.

Interpretive Summary: Stripe rust is a fungal disease of wheat that causes large production losses in many parts of the world. Host plant resistance is a cost-effective and environmentally friendly way to control the disease. “Slow rusting” partial resistance genes that retard growth of most of the races of the pathogen are known and have proven to be more durable over time in production agriculture than race-specific resistances. This paper reports progress in characterizing the mode of action of a “slow rusting” gene from emmer wheat called Yr36, also known as WKS1. The WKS1 protein encoded by this gene is imported into plant cell chloroplasts, where it adds a phosphorus molecule to the enzyme ascorbate peroxidase. The phosphorus addition decreases the activity of the enzyme and its ability to detoxify the reactive oxygen molecules produced in chloroplasts. The levels of reactive oxygen build up over time, killing the leaf cell and thus limiting the cell-to-cell spread of fungi that have invaded those leaf cells. This response takes several days longer than cell death responses mediated by typical race-specific resistance genes, thus accounting for the partial resistance characteristic of the Yr36 gene. Because it has a different mode of action, the Yr36 gene is most effective when combined with other types of stripe rust resistance genes to provide durable protection against many races of the pathogen.

Technical Abstract: Stripe rust is a devastating fungal disease of wheat caused by Puccinia striiformis f. sp. tritici(Pst). The WKS1 resistance gene has an unusual combination of serine/threonine kinase and START lipid-binding domains and confers partial resistance to Pst. Here we show that wheat plants transformed with the complete WKS1 variant WKS1.1) are resistant to Pst whereas those transformed with an alternative splice variant with a truncated START domain WKS1.2) are susceptible. WKS1.1 and WKS1.2 preferentially bind to the same lipids (phosphatidic acid and phosphatidylinositol phosphates) but differ in their protein-protein interactions. WKS1.1 is targeted to the chloroplast where it phosphorylates the thylakoid-associated ascorbate peroxidase(tAPX) and reduces its ability to detoxify peroxides. Increased expression of WKS1.1 in transgenic wheat accelerates leaf senescence in the absence of Pst. Based on these results, we propose that the phosphorylation of tAPX by WKS1.1 reduces the ability of the cells to detoxify reactive oxygen species and contributes to cell death. This response takes several days longer than typical hypersensitive cell death responses, thus allowing the limited pathogen growth and restricted sporulation that is characteristic of the WKS1 partial resistance response to Pst.