AUTHOR=Battache Mélissa , Lebrun Marc-Henri , Sakai Kaori , Soudière Olivier , Cambon Florence , Langin Thierry , Saintenac Cyrille 

TITLE=Blocked at the Stomatal Gate, a Key Step of Wheat Stb16q-Mediated Resistance to Zymoseptoria tritici

JOURNAL=Frontiers in Plant Science

VOLUME=13

YEAR=2022

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.921074

DOI=10.3389/fpls.2022.921074

ISSN=1664-462X

ABSTRACT=<p>Septoria tritici blotch (STB), caused by the fungus <italic>Zymoseptoria tritici</italic>, is among the most threatening wheat diseases in Europe. Genetic resistance remains one of the main environmentally sustainable strategies to efficiently control STB. However, the molecular and physiological mechanisms underlying resistance are still unknown, limiting the implementation of knowledge-driven management strategies. Among the 22 known major resistance genes (<italic>Stb</italic>), the recently cloned <italic>Stb16q</italic> gene encodes a cysteine-rich receptor-like kinase conferring a full broad-spectrum resistance against <italic>Z. tritici</italic>. Here, we showed that an avirulent <italic>Z. tritici</italic> inoculated on <italic>Stb16q</italic> quasi near isogenic lines (NILs) either by infiltration into leaf tissues or by brush inoculation of wounded tissues partially bypasses <italic>Stb16q</italic>-mediated resistance. To understand this bypass, we monitored the infection of GFP-labeled avirulent and virulent isolates on <italic>Stb16q</italic> NILs, from germination to pycnidia formation. This quantitative cytological analysis revealed that 95% of the penetration attempts were unsuccessful in the <italic>Stb16q</italic> incompatible interaction, while almost all succeeded in compatible interactions. Infectious hyphae resulting from the few successful penetration events in the <italic>Stb16q</italic> incompatible interaction were arrested in the sub-stomatal cavity of the primary-infected stomata. These results indicate that <italic>Stb16q</italic>-mediated resistance mainly blocks the avirulent isolate during its stomatal penetration into wheat tissue. Analyses of stomatal aperture of the <italic>Stb16q</italic> NILs during infection revealed that <italic>Stb16q</italic> triggers a temporary stomatal closure in response to an avirulent isolate. Finally, we showed that infiltrating avirulent isolates into leaves of the <italic>Stb6</italic> and <italic>Stb9</italic> NILs also partially bypasses resistances, suggesting that arrest during stomatal penetration might be a common major mechanism for <italic>Stb</italic>-mediated resistances.</p>