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Timing is everything: Stomatal manipulation facilitates Puccinia graminis entry in dark, resulting in counter evolution of barley Rpg5 immune receptor

Shyam Solanki: Plant Pathology Department, North Dakota State University

<div>The integrated decoy hypothesis explains the evolution of dual plant NLR resistance gene loci, where one NLR partner contains an <u>I</u>ntegrated <u>S</u>ensory <u>D</u>omain (ISD) that represent virulence effector targets translocated to NLRs to function as pathogen baits. The barley NLRs, <em>Rpg5</em> and <em>HvRga1,</em> are both required for resistance to <em>Puccinia graminis (Pg)</em>, the stem rust pathogen. Functional <em>Rpg5</em> alleles have a protein kinase (PK) ISD, and the putative progenitor of the ISD was identified and designated guard cell associated kinase 1 (<em>Gak1)</em>. Comparative analysis shows that <em>Gak1</em> is a paralog of the <em>Arabidopsis </em>stomatal protein kinase required for light responsive stomatal opening. Confocal laser microscopy determined <em>Pg</em> entry through stomata in the dark and qPCR on cDNA from laser microdissected stomata showed high levels of <em>Gak1</em> compared to whole leaf samples, supporting the hypothesis that <em>Pg</em> may manipulate stomata localized Gak1, allowing for stomata opening and pathogen entry at night, a new paradigm in <em>Pg</em>-barley interaction. Y2H identified HvVOZ1 as an Rpg5 ISD interactor and in <em>Arabidopsis</em> it has been shown that<em> Atvoz1/Atvoz2</em> mutants have reduced stomatal opening. AtVoz1 also interacts with the PhyB far red light receptor, thus we hypothesize interplay between Gak1/HvVoz1 and a <em>Pg </em>effector that manipulates the stomates to open allowing entry during the night. However, barley counter evolved a Rpg5-Gak1 ISD to recognize Gak1 manipulation resulting in resistance responses.</div>

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