A fungal effector suppresses plant immunity by manipulating DAHPS-mediated metabolic flux in chloroplasts

IF 8.3 1区 生物学 Q1 PLANT SCIENCES New Phytologist Pub Date : 2024-09-26 DOI:10.1111/nph.20117
Shengping Shang, Xiaofei Liang, Guangli Liu, Youwei Du, Song Zhang, Yanan Meng, Junming Zhu, Jeffrey A. Rollins, Rong Zhang, Guangyu Sun
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Abstract

  • Plant secondary metabolism represents an important and ancient form of defense against pathogens. Phytopathogens secrete effectors to suppress plant defenses and promote infection. However, it is largely unknown, how fungal effectors directly manipulate plant secondary metabolism.
  • Here, we characterized a fungal defense-suppressing effector CfEC28 from Colletotrichum fructicola. Gene deletion assays showed that ∆CfEC28-mutants differentiated appressoria normally on plant surface but were almost nonpathogenic due to increased number of plant papilla accumulation at attempted penetration sites. CfEC28 interacted with a family of chloroplast-localized 3-deoxy-d-arabinose-heptulonic acid-7-phosphate synthases (DAHPSs) in apple. CfEC28 inhibited the enzymatic activity of an apple DAHPS (MdDAHPS1) and suppressed DAHPS-mediated secondary metabolite accumulation through blocking the manganese ion binding region of DAHPS. Dramatically, transgene analysis revealed that overexpression of MdDAHPS1 provided apple with a complete resistance to C. fructicola.
  • We showed that a novel effector CfEC28 can be delivered into plant chloroplasts and contributes to the full virulence of C. fructicola by targeting the DAHPS to disrupt the pathway linking the metabolism of primary carbohydrates with the biosynthesis of aromatic defense compounds.
  • Our study provides important insights for understanding plant–microbe interactions and a valuable gene for improving plant disease resistance.
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一种真菌效应物通过操纵叶绿体中由 DAHPS 介导的代谢通量来抑制植物免疫。
植物次生代谢是抵御病原体的一种重要而古老的防御方式。植物病原体会分泌效应物来抑制植物防御系统并促进感染。然而,人们对真菌效应物如何直接操纵植物次生代谢还知之甚少。在这里,我们研究了一种来自 Colletotrichum fructicola 的真菌防御抑制效应子 CfEC28。基因缺失试验表明,ΔCfEC28-突变体在植物表面正常分化出附属物,但由于尝试穿透部位的植物乳头积累数量增加,因此几乎不致病。CfEC28 与苹果中叶绿体定位的 3-脱氧-d-阿拉伯糖-庚酮酸-7-磷酸合成酶(DAHPSs)家族相互作用。CfEC28 可抑制苹果 DAHPS(MdDAHPS1)的酶活性,并通过阻断 DAHPS 的锰离子结合区抑制 DAHPS 介导的次生代谢物积累。引人注目的是,转基因分析表明,过量表达 MdDAHPS1 能使苹果完全抵抗果蝇疫霉菌。我们的研究表明,一种新型效应物 CfEC28 可被传递到植物叶绿体中,并通过靶向 DAHPS 破坏连接初级碳水化合物代谢与芳香防御化合物生物合成的途径,从而增强果蝇科细菌的完全毒力。我们的研究为了解植物与微生物之间的相互作用提供了重要启示,也为提高植物抗病性提供了一个有价值的基因。
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来源期刊
New Phytologist
New Phytologist 生物-植物科学
自引率
5.30%
发文量
728
期刊介绍: New Phytologist is an international electronic journal published 24 times a year. It is owned by the New Phytologist Foundation, a non-profit-making charitable organization dedicated to promoting plant science. The journal publishes excellent, novel, rigorous, and timely research and scholarship in plant science and its applications. The articles cover topics in five sections: Physiology & Development, Environment, Interaction, Evolution, and Transformative Plant Biotechnology. These sections encompass intracellular processes, global environmental change, and encourage cross-disciplinary approaches. The journal recognizes the use of techniques from molecular and cell biology, functional genomics, modeling, and system-based approaches in plant science. Abstracting and Indexing Information for New Phytologist includes Academic Search, AgBiotech News & Information, Agroforestry Abstracts, Biochemistry & Biophysics Citation Index, Botanical Pesticides, CAB Abstracts®, Environment Index, Global Health, and Plant Breeding Abstracts, and others.
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