ARS | Publication request: Competitive Interaction Between Phytophthora Infestans Effectors Leads to Increased Aggressiveness on Plants Containing Broad-Spectrum Late Blight Resistance

Submitted to: PLoS One
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: April 13, 2010
Publication Date: May 7, 2010
Citation: Halterman, D.A., Chen, Y., Sopee, J., Berduo, J., Sanchez, A. 2010. Competitive Interaction Between Phytophthora Infestans Effectors Leads to Increased Aggressiveness on Plants Containing Broad-Spectrum Late Blight Resistance. PLoS One. PLoS ONE 5(5): e10536. Available: http://www.plosone.org/article/info:doi%2F10.1371%2Fjournal.pone.0010536.

Interpretive Summary: The potato late blight resistance (R) gene RB is distinct from most plant R genes in that it confers resistance to a broad spectrum of pathogen isolates. RB recognizes the presence of members of the Phytophthora infestans effector family IPI-O to elicit resistance. In this manuscript we have studied IpiO diversity from 40 different P. infestans cultures (isolates) collected from Guatemala, Thailand, and the United States. We have found that all of the isolates contain IPI-O variants that can be recognized by RB. However, some of these isolates contain an extraordinarily large number of variants. Some isolates also contain an IPI-O variant (IPI-O4) that is not recognized by RB. Isolates containing IPI-O4 are able to overcome RB resistance to cause significantly more disease than isolates that do not contain IPI-O4. We show that the presence of IPI-O4 blocks the ability of RB to recognize the presence of other IPI-O variants and turn on resistance responses.

Technical Abstract: Potato late blight is a particularly destructive plant disease caused by the oomycete pathogen Phytophthora infestans (Mont.) de Bary. Late blight has remained particularly problematic despite intensive breeding efforts to integrate resistance into cultivated potato. This is due to the pathogen’s ability to quickly evolve to overcome major resistance genes. The RB gene, identified in the wild potato species S. bulbocastanum, encodes a protein that confers broad-spectrum resistance to most P. infestans isolates through its recognition of highly conserved members of the corresponding pathogen effector family IPI-O. IpiO is a multigene family of effectors and while the majority of IPI-O proteins are recognized by RB to elicit host resistance, some variants exist that are able to elude detection (e.g. IPI-O4). Analysis of ipiO variants among 40 different P. infestans isolates collected from Guatemala, Thailand, and the United States revealed a high degree of complexity within this gene family. Isolate aggressiveness was found to be associated with increased ipiO diversity and the presence of the ipiO4 variant. Furthermore, isolates expressing IPI-O4 are capable of overcoming RB-mediated resistance in transgenic potato plants even when resistance-eliciting IPI-O variants are present. We have found that expression of IPI-O4 via Agrobacterium is capable of blocking recognition of another IPI-O variant leading to inactivation of RB-mediated programmed cell death in Nicotiana benthamiana.