{"title":"N-Hydroxypipecolic acid and salicylic acid play key roles in autoimmunity induced by loss of the callose synthase PMR4","authors":"Baofang Fan, Zizhang Li, Amber S Jannasch, Shunyuan Xiao, Zhixiang Chen","doi":"10.1093/plphys/kiaf163","DOIUrl":null,"url":null,"abstract":"In Arabidopsis thaliana, the POWDERY MILDEW RESISTANT4 (PMR4)/GLUCAN SYNTHASE LIKE5 (GSL5) callose synthase is required for pathogen-induced callose deposition in cell wall defense. Paradoxically, pmr4/gsl5 mutants exhibit strong resistance to both powdery and downy mildew. The powdery mildew resistance of pmr4/gsl5 has been attributed to up-regulated salicylic acid (SA) signaling based on its dependence on PHYTOALEXIN DEFICIENT4 (PAD4), which controls SA accumulation, and its abolishment by bacterial NahG salicylate hydroxylase. Our study revealed that disruption of PMR4/GSL5 also leads to early senescence. Suppressor analysis uncovered that PAD4 and N-hydroxypipecolic acid (NHP) biosynthetic genes ABERRANT GROWTH AND DEATH2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1) and FLAVIN-DEPENDENT MONOXYGENASE1 (FMO1) are required for early senescence of pmr4/gsl5 mutants. The critical role of NHP in the early senescence of pmr4/gsl5 was supported by greatly increased accumulation of pipecolic acid in pmr4/gsl5 mutants. In contrast, disruption of the SA biosynthetic gene ISOCHORISMATE SYNTHASE1/SA-INDUCTION DIFFICIENT 2 (ICS1/SID2), which greatly reduces SA accumulation, had little effect on impaired growth of pmr4/gsl5. Furthermore, while disruption of PAD4 completely abolished the powdery mildew resistance in pmr4/gsl5, mutations in ICS1/SID2, ALD1, or FMO1 had only a minor effect on the resistance of the mutant plants. However, disruption of both ICS1/SID2 and FMO1 abolished the enhanced immunity of the callose synthase mutants against the fungal pathogen. Therefore, while NHP plays a crucial role in the early senescence of pmr4/gsl5 mutants, both SA and NHP have important roles in the strong powdery mildew resistance induced by the loss of the callose synthase.","PeriodicalId":20101,"journal":{"name":"Plant Physiology","volume":"13 1","pages":""},"PeriodicalIF":6.5000,"publicationDate":"2025-05-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Plant Physiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/plphys/kiaf163","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
In Arabidopsis thaliana, the POWDERY MILDEW RESISTANT4 (PMR4)/GLUCAN SYNTHASE LIKE5 (GSL5) callose synthase is required for pathogen-induced callose deposition in cell wall defense. Paradoxically, pmr4/gsl5 mutants exhibit strong resistance to both powdery and downy mildew. The powdery mildew resistance of pmr4/gsl5 has been attributed to up-regulated salicylic acid (SA) signaling based on its dependence on PHYTOALEXIN DEFICIENT4 (PAD4), which controls SA accumulation, and its abolishment by bacterial NahG salicylate hydroxylase. Our study revealed that disruption of PMR4/GSL5 also leads to early senescence. Suppressor analysis uncovered that PAD4 and N-hydroxypipecolic acid (NHP) biosynthetic genes ABERRANT GROWTH AND DEATH2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1) and FLAVIN-DEPENDENT MONOXYGENASE1 (FMO1) are required for early senescence of pmr4/gsl5 mutants. The critical role of NHP in the early senescence of pmr4/gsl5 was supported by greatly increased accumulation of pipecolic acid in pmr4/gsl5 mutants. In contrast, disruption of the SA biosynthetic gene ISOCHORISMATE SYNTHASE1/SA-INDUCTION DIFFICIENT 2 (ICS1/SID2), which greatly reduces SA accumulation, had little effect on impaired growth of pmr4/gsl5. Furthermore, while disruption of PAD4 completely abolished the powdery mildew resistance in pmr4/gsl5, mutations in ICS1/SID2, ALD1, or FMO1 had only a minor effect on the resistance of the mutant plants. However, disruption of both ICS1/SID2 and FMO1 abolished the enhanced immunity of the callose synthase mutants against the fungal pathogen. Therefore, while NHP plays a crucial role in the early senescence of pmr4/gsl5 mutants, both SA and NHP have important roles in the strong powdery mildew resistance induced by the loss of the callose synthase.
期刊介绍:
Plant Physiology® is a distinguished and highly respected journal with a rich history dating back to its establishment in 1926. It stands as a leading international publication in the field of plant biology, covering a comprehensive range of topics from the molecular and structural aspects of plant life to systems biology and ecophysiology. Recognized as the most highly cited journal in plant sciences, Plant Physiology® is a testament to its commitment to excellence and the dissemination of groundbreaking research.
As the official publication of the American Society of Plant Biologists, Plant Physiology® upholds rigorous peer-review standards, ensuring that the scientific community receives the highest quality research. The journal releases 12 issues annually, providing a steady stream of new findings and insights to its readership.