Université Clermont Auvergne, INRAE, GDEC, Clermont-Ferrand, France.
Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM), Instituto Nacional de Investigación y Technología Agraria y Alimentaria (INIA), Pozuelo de Alarcón, Madrid, 28223, Spain.
BMC Plant Biol. 2024 Aug 2;24(1):736. doi: 10.1186/s12870-024-05426-5.
Septoria tritici blotch (STB), caused by the foliar fungus Zymoseptoria tritici, is one of the most damaging disease of wheat in Europe. Genetic resistance against this fungus relies on different types of resistance from non-host resistance (NHR) and host species specific resistance (HSSR) to host resistance mediated by quantitative trait loci (QTLs) or major resistance genes (Stb). Characterizing the diversity of theses resistances is of great importance for breeding wheat cultivars with efficient and durable resistance. While the functional mechanisms underlying these resistance types are not well understood, increasing piece of evidence suggest that fungus stomatal penetration and early establishment in the apoplast are both crucial for the outcome of some interactions between Z. tritici and plants. To validate and extend these previous observations, we conducted quantitative comparative phenotypical and cytological analyses of the infection process corresponding to 22 different interactions between plant species and Z. tritici isolates. These interactions included four major bread wheat Stb genes, four bread wheat accessions with contrasting quantitative resistance, two species resistant to Z. tritici isolates from bread wheat (HSSR) and four plant species resistant to all Z. tritici isolates (NHR).
Infiltration of Z. tritici spores into plant leaves allowed the partial bypass of all bread wheat resistances and durum wheat resistance, but not resistances from other plants species. Quantitative comparative cytological analysis showed that in the non-grass plant Nicotiana benthamiana, Z. tritici was stopped before stomatal penetration. By contrast, in all resistant grass plants, Z. tritici was stopped, at least partly, during stomatal penetration. The intensity of this early plant control process varied depending on resistance types, quantitative resistances being the least effective. These analyses also demonstrated that Stb-mediated resistances, HSSR and NHR, but not quantitative resistances, relied on the strong growth inhibition of the few Z. tritici penetrating hyphae at their entry point in the sub-stomatal cavity.
In addition to furnishing a robust quantitative cytological assessment system, our study uncovered three stopping patterns of Z. tritici by plant resistances. Stomatal resistance was found important for most resistances to Z. tritici, independently of its type (Stb, HSSR, NHR). These results provided a basis for the functional analysis of wheat resistance to Z. tritici and its improvement.
由叶部真菌叶点霉引起的叶锈病是欧洲小麦最具破坏性的病害之一。对这种真菌的遗传抗性依赖于非寄主抗性（NHR）和寄主种特异性抗性（HSSR）等不同类型的抗性，以及由数量性状位点（QTL）或主要抗性基因（Stb）介导的寄主抗性。这些抗性的多样性特征对于培育具有高效和持久抗性的小麦品种非常重要。虽然这些抗性类型的功能机制尚不清楚，但越来越多的证据表明，真菌的气孔穿透和在质外体中的早期定殖对于一些叶点霉与植物之间相互作用的结果都是至关重要的。为了验证和扩展这些先前的观察结果，我们对 22 种不同的植物种与叶点霉分离株之间的相互作用的感染过程进行了定量比较表型和细胞学分析。这些相互作用包括四个主要的面包小麦叶锈病基因、四个具有不同数量抗性的面包小麦品系、两个对来自面包小麦的叶点霉分离株具有抗性的物种（HSSR）和四个对所有叶点霉分离株具有抗性的植物物种（NHR）。
叶点霉孢子渗透到植物叶片中，使所有的面包小麦抗性和硬粒小麦抗性部分失效，但对其他植物物种的抗性无效。定量比较细胞学分析表明，在非禾本科植物烟草原生质体中，叶点霉在气孔穿透之前就被阻止。相比之下，在所有具有抗性的禾本科植物中，叶点霉在气孔穿透时至少部分被阻止。这个早期植物控制过程的强度取决于抗性类型，数量抗性的效果最差。这些分析还表明，Stb 介导的抗性、HSSR 和 NHR，但不是数量抗性，依赖于在亚气孔腔中的进入点处穿透菌丝的少量叶点霉的强烈生长抑制。
除了提供一个稳健的定量细胞学评估系统外，我们的研究还揭示了植物抗性阻止叶点霉的三种模式。气孔抗性对于大多数叶锈病抗性都很重要，而与抗性类型无关（Stb、HSSR、NHR）。这些结果为小麦对叶点霉的功能分析及其改良提供了依据。
