Spermine-mediated tight sealing of theMagnaporthe oryzaeappressorial pore-rice leaf surface interface

Spermine-mediated tight sealing of theMagnaporthe oryzaeappressorial pore-rice leaf surface interface
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DOI:
10.1038/s41564-020-0786-x
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发表时间:
2020-09-14
影响因子:
28.3
通讯作者:
Wilson, Richard A.
Wilson, Richard A.
中科院分区:
生物学1区
文献类型:
--
作者:
Rocha, Raquel O.;Elowsky, Christian;Wilson, Richard A.

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细胞黏附调节了许多重要的植物-微生物相互作用。在毁灭性的稻瘟病菌(Magnaporthe Oryzae)中(1),强大的富含糖蛋白的粘液粘合剂(2)粘结剂(2)将黑化并加压的圆顶状侵染细胞-附着体--粘合到寄主的水稻叶表面。巨大的内部膨胀压力被引导到从附着体底部(1-4)未黑化的薄壁小孔中冒出的穿透钉上,迫使其穿过叶角质层,在那里它拉长了下面表皮细胞中的入侵菌丝(5)。粘液封闭在附着孔周围有助于肿胀的形成,但粘液分泌和附着体粘连的分子基础尚不清楚。在这里,我们发现在发育中的附着胞中,精胺通过减轻内质网(ER)压力,在促进粘液产生方面发挥了意想不到的唯一作用。缺乏精胺合成酶编码基因SPS1的突变菌株在附着体发育的所有阶段都有进展,包括穿透性附着体的形成,但由于附着体粘附力降低,导致溶质泄漏,角质层穿透不成功。从机制上讲,精胺中和了NADPH氧化酶-1(Nox1)(3,6)产生的偏离靶标的氧自由基,否则会引发内质网应激和未折叠的蛋白质反应,从而严重减少粘液分泌。我们的研究表明,通过内质网氧化还原缓冲的精胺代谢支持附着体附着和水稻细胞入侵,并为了解寄主植物感染的基本过程提供了洞察。蛇床子胺通过减轻发育中的稻瘟菌的内质网胁迫而促进粘液的产生和水稻细胞的入侵。
Cellular adhesion mediates many important plant-microbe interactions. In the devastating blast fungusMagnaporthe oryzae(1), powerful glycoprotein-rich mucilage adhesives(2)cement melanized and pressurized dome-shaped infection cells-appressoria-to host rice leaf surfaces. Enormous internal turgor pressure is directed onto a penetration peg emerging from the unmelanized, thin-walled pore at the appressorial base(1-4), forcing it through the leaf cuticle where it elongates invasive hyphae in underlying epidermal cells(5). Mucilage sealing around the appressorial pore facilitates turgor build-up(2), but the molecular underpinnings of mucilage secretion and appressorial adhesion are unknown. Here, we discovered an unanticipated and sole role for spermine in facilitating mucilage production by mitigating endoplasmic reticulum (ER) stress in the developing appressorium. Mutant strains lacking the spermine synthase-encoding geneSPS1progressed through all stages of appressorial development, including penetration peg formation, but cuticle penetration was unsuccessful due to reduced appressorial adhesion, which led to solute leakage. Mechanistically, spermine neutralized off-target oxygen free radicals produced by NADPH oxidase-1 (Nox1)(3,6)that otherwise elicited ER stress and the unfolded protein response, thereby critically reducing mucilage secretion. Our study reveals that spermine metabolism via redox buffering of the ER underpins appressorial adhesion and rice cell invasion and provides insights into a process that is fundamental to host plant infection.Spermine facilitates mucilage production and rice cell invasion by mitigating endoplasmic reticulum stress in the developingMagnaporthe oryzaeappressorium.