Centre for Crop and Disease Management, Curtin University, Bentley, Perth, Western Australia, Australia.
Curtin University, Bentley, Perth, Western Australia, Australia.
PLoS Pathog. 2022 Jan 6;18(1):e1010149. doi: 10.1371/journal.ppat.1010149. eCollection 2022 Jan.
The fungus Parastagonospora nodorum uses proteinaceous necrotrophic effectors (NEs) to induce tissue necrosis on wheat leaves during infection, leading to the symptoms of septoria nodorum blotch (SNB). The NEs Tox1 and Tox3 induce necrosis on wheat possessing the dominant susceptibility genes Snn1 and Snn3B1/Snn3D1, respectively. We previously observed that Tox1 is epistatic to the expression of Tox3 and a quantitative trait locus (QTL) on chromosome 2A that contributes to SNB resistance/susceptibility. The expression of Tox1 is significantly higher in the Australian strain SN15 compared to the American strain SN4. Inspection of the Tox1 promoter region revealed a 401 bp promoter genetic element in SN4 positioned 267 bp upstream of the start codon that is absent in SN15, called PE401. Analysis of the world-wide P. nodorum population revealed that a high proportion of Northern Hemisphere isolates possess PE401 whereas the opposite was observed in representative P. nodorum isolates from Australia and South Africa. The presence of PE401 removed the epistatic effect of Tox1 on the contribution of the SNB 2A QTL but not Tox3. PE401 was introduced into the Tox1 promoter regulatory region in SN15 to test for direct regulatory roles. Tox1 expression was markedly reduced in the presence of PE401. This suggests a repressor molecule(s) binds PE401 and inhibits Tox1 transcription. Infection assays also demonstrated that P. nodorum which lacks PE401 is more pathogenic on Snn1 wheat varieties than P. nodorum carrying PE401. An infection competition assay between P. nodorum isogenic strains with and without PE401 indicated that the higher Tox1-expressing strain rescued the reduced virulence of the lower Tox1-expressing strain on Snn1 wheat. Our study demonstrated that Tox1 exhibits both 'selfish' and 'altruistic' characteristics. This offers an insight into a complex NE-NE interaction that is occurring within the P. nodorum population. The importance of PE401 in breeding for SNB resistance in wheat is discussed.
小麦叶枯病菌利用蛋白营养型坏死效应物（NEs）在侵染过程中诱导小麦叶片坏死，导致叶枯病症状的出现。NEs Tox1 和 Tox3 分别诱导携带显性感病基因 Snn1 和 Snn3B1/Snn3D1 的小麦产生坏死。我们之前观察到 Tox1 对 Tox3 的表达具有上位性，并且在 2A 染色体上存在一个与叶枯病抗性/感病相关的数量性状位点（QTL）。与美国菌株 SN4 相比，澳大利亚菌株 SN15 中 Tox1 的表达水平显著更高。对 Tox1 启动子区域的检查发现，SN4 中的一个 401bp 启动子遗传元件位于起始密码子上游 267bp 处，而在 SN15 中缺失，称为 PE401。对全球 P. nodorum 群体的分析表明，北半球分离株中存在较高比例的 PE401，而在澳大利亚和南非的代表性 P. nodorum 分离株中则相反。PE401 的存在消除了 Tox1 对 SNB 2A QTL 贡献的上位性效应，但对 Tox3 没有影响。将 PE401 引入 SN15 的 Tox1 启动子调控区进行直接调控作用的测试。在存在 PE401 的情况下，Tox1 的表达明显降低。这表明一个抑制分子（s）结合 PE401 并抑制 Tox1 转录。感染测定也表明，缺乏 PE401 的 P. nodorum 对携带 Snn1 的小麦品种的致病性高于携带 PE401 的 P. nodorum。在有无 PE401 的 P. nodorum 同基因菌株之间进行感染竞争测定表明，较高 Tox1 表达株系挽救了较低 Tox1 表达株系在 Snn1 小麦上的毒力降低。我们的研究表明，Tox1 表现出“自私”和“利他”的特征。这为 P. nodorum 群体中发生的复杂 NEs-NEs 相互作用提供了一个见解。讨论了 PE401 在小麦叶枯病抗性育种中的重要性。
