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Title: Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants

Author
item ANDERSON, RYAN - Virginia Polytechnic Institution & State University
item CASADY, MEGAN - Virginia Polytechnic Institution & State University
item FEE, RACHEL - Virginia Polytechnic Institution & State University
item Vaughan, Martha
item DEB, DEVDUTTA - Virginia Polytechnic Institution & State University
item FEDKENHEUER, KEVIN - Virginia Polytechnic Institution & State University
item Huffaker, Alisa
item Schmelz, Eric
item TYLER, BRETT - Virginia Bioinformatics Institute
item MCDOWELL, J - Virginia Polytechnic Institution & State University

Submitted to: Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/27/2012
Publication Date: 8/1/2012
Citation: Anderson, R.G., Casady, M.S., Fee, R.A., Vaughan, M.M., Deb, D., Fedkenheuer, K., Huffaker, A., Schmelz, E.A., Tyler, B.M., Mcdowell, J.M. 2012. Homologous RXLR effectors from Hyaloperonospora arabidopsidis and Phytophthora sojae suppress immunity in distantly related plants. Plant Journal. DOI: 10.1111/j.1365-313X.2012.05079.x.

Interpretive Summary: The success or failure of crop plant pathogens is dependent on their ability to escape or suppress host immunity. Many pathogens, such and downy mildew, manipulate plant immunity by secreting effector proteins into plants cells. Downy mildew, Hyaloperonospora arabidopsidis contains many effector proteins with a conserved RXLR motif, a few of which are shared by the soybean pathogen Phytophthora sojae. The rather widespread occurrence of a small related group of pathogen effectors suggests action upon conserved host plant targets. In collaboration with researchers from Virginia Tech, scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, have discovered that the conserved homologous effector proteins from Hyaloperonospora and Phytophthora, namely HaRxLR96 PsAvh163, both suppress the immune responses of soybean. In contrast HaRxLR96 suppresses the immune response in tobacco while PsAvh163 causes cell death. Transgenic Arabidopsis plants expressing either of these effectors are more susceptible to pathogens. Both of the effector proteins interfere with the induction of salicylic acid-responsive defense genes. However, salicylic acid biosynthesis was not affected. This work demonstrates that related effectors from diverse plant pathogens can manipulate the immunity of diverse plant species strongly supporting the hypothesis of conserved plant targets. The discovery of mechanisms by which pathogens manipulate plant immunity can be leveraged to ultimately improve crop plant resistance.

Technical Abstract: Diverse pathogens secrete effector proteins into plant cells to manipulate host cellular processes. Oomycete pathogens contain very large complements of predicted effector genes defined by an RXLR host cell entry motif. The genome of Hyaloperonospora arabidopsidis (Hpa, downy mildew of Arabidopsis) contains at least 134 candidate RXLR effector genes. Only a small subset of these genes is conserved in related oomycetes from the Phytophthora genus. Here, we describe a comparative functional characterization of the Hpa RXLR effector HaRxL96 and a homologous gene, PsAvh163, from the soybean pathogen Phytophthora sojae. HaRxL96 and PsAvh163 are induced during early stages of infection and carry a functional RXLR motif that is sufficient for protein uptake into plant cells. Both effectors can suppress immune responses in soybean. HaRxL96 suppresses immunity in Nicotiana, while PsAvh163 induces an HR-like cell death response that is dependent on RAR1 and Hsp90.1. Transgenic Arabidopsis expressing HaRxL96 or PsAvh163 exhibit elevated susceptibility to virulent and avirulent Hpa as well as decreased callose deposition in response to non-pathogenic P. syringae. Both effectors interfere with induction of salicylic acid-responsive defense gene induction, but do not affect salicylic acid biosynthesis. Together, these experiments demonstrate that evolutionarily conserved effectors from different oomycete species can suppress immunity in plant species that are divergent from the source pathogen’s host.