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

Abstract

Septoria tritici blotch (STB), caused by the fungus Zymoseptoria tritici, 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 (Stb), the recently cloned Stb16q gene encodes a cysteine-rich receptor-like kinase conferring a full broad-spectrum resistance against Z. tritici. Here, we showed that an avirulent Z. tritici inoculated on Stb16q quasi near isogenic lines (NILs) either by infiltration into leaf tissues or by brush inoculation of wounded tissues partially bypasses Stb16q-mediated resistance. To understand this bypass, we monitored the infection of GFP-labeled avirulent and virulent isolates on Stb16q NILs, from germination to pycnidia formation. This quantitative cytological analysis revealed that 95% of the penetration attempts were unsuccessful in the Stb16q incompatible interaction, while almost all succeeded in compatible interactions. Infectious hyphae resulting from the few successful penetration events in the Stb16q incompatible interaction were arrested in the sub-stomatal cavity of the primary-infected stomata. These results indicate that Stb16q-mediated resistance mainly blocks the avirulent isolate during its stomatal penetration into wheat tissue. Analyses of stomatal aperture of the Stb16q NILs during infection revealed that Stb16q triggers a temporary stomatal closure in response to an avirulent isolate. Finally, we showed that infiltrating avirulent isolates into leaves of the Stb6 and Stb9 NILs also partially bypasses resistances, suggesting that arrest during stomatal penetration might be a common major mechanism for Stb-mediated resistances.

Stb6 mediates stomatal immunity, photosynthetic functionality, and the antioxidant system during the Zymoseptoria tritici-wheat interaction

“…This finding was confirmed by measuring the pore width and g s of the treated leaves over time ( Figure 1 ). This outcome was consistent with a recent study that found Stb16q mediates an early and temporary stomatal closure in response to an avirulent Z. tritici isolate ( Battache et al., 2022 ). Typically, each stomatal pore is surrounded by two guard cells, that are extremely specialized in structure and function, and variations in the turgor pressure of these cells regulate the pore aperture size.…”

Effector‐mediated partial and nonhost disease resistance in wheat

“…For example, Z . tritici strains harbouring the avirulence genes AvrStb16q and AvrStb6 were also shown to be mostly arrested at the stomatal penetration step on Stb16q and Stb6 wheat cultivars, respectively (Battache et al ., 2022). This suggests that the stomatal penetration step is key to mediating various forms of disease resistance to Zymoseptoria species.…”

“…This correlates with reduced levels of subsequent disease. Changes in stomatal aperture (transient closure) in resistant wheat cultivars following contact with avirulent fungal hyphae may be a key feature (Battache et al ., 2022). Overall, many of these characteristics are somewhat more reminiscent of events typical of PAMP/MAMP‐triggered plant immunity (Zhang et al ., 2008).…”

A secreted protease-like protein inZymoseptoria triticiis responsible for avirulence onStb9resistance gene in wheat

“…Z. tritici is apoplastic with a biphasic infection process (Petit-Houdenot et al, 2021). After penetration into wheat leaves through stomata, the fungus colonizes the apoplast for 8-11 days while the host remains symptomless (Battache et al, 2022). This long asymptomatic phase is .…”

“…Z. tritici is apoplastic with a biphasic infection process (Petit-Houdenot et al ., 2021). After penetration into wheat leaves through stomata, the fungus colonizes the apoplast for 8-11 days while the host remains symptomless (Battache et al ., 2022). This long asymptomatic phase is followed by a rapid onset of necrotic symptoms, associated with the development of fungal asexual fruiting bodies called pycnidia, which contain the pycnidiospores that further spread the disease (Sánchez-Vallet et al ., 2015).…”