A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling.
A Phytophthora sojae CRN effector mediates phosphorylation and degradation of plant aquaporin proteins to suppress host immune signaling.
复制标题
大豆疫霉CRN效应物介导植物水通道蛋白的磷酸化和降解，抑制宿主免疫信号。
DOI：
10.1371/journal.ppat.1009388
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发表时间：
2021-03
期刊：
影响因子：
6.7
通讯作者：
Dou D
中科院分区：
文献类型：
--
作者：
Ai G;Xia Q;Song T;Li T;Zhu H;Peng H;Liu J;Fu X;Zhang M;Jing M;Xia A;Dou D
疫霉基因组编码无数的 Crinkler (CRN) 效应子，其中一些包含推定的激酶结构域。人们对这些含有激酶结构域的 CRN 的宿主靶点及其促进感染的机制知之甚少。在这里，我们报告了臭名昭著的卵菌病原体大豆疫霉中名为 CRN78 的保守激酶 CRN 效应子的宿主靶点和功能机制。 CRN78 通过抑制植物 H2O2 积累和免疫相关基因表达，促进烟草疫霉感染，并增强大豆疫霉对宿主植物大豆的毒力。进一步研究表明，CRN78 与植物质膜上的 PIP2 家族水通道蛋白（包括来自本塞姆氏烟草的 NbPIP2;2 和来自大豆的 GmPIP2-13）相互作用，膜定位对于 CRN78 的毒力是必要的。接下来，CRN78 在体内利用其激酶结构域促进 NbPIP2;2 或 GmPIP2-13 的磷酸化，从而导致它们随后在 26S 依赖性途径中发生蛋白质降解。我们的数据还表明，NbPIP2;2 作为 H2O2 转运蛋白，可以积极调节植物免疫力和活性氧 (ROS) 积累。系统发育分析表明，PIP2 蛋白的磷酸化位点和 CRN78 同源物的激酶结构域分别在高等植物和卵菌病原体中高度保守。因此，本研究阐明了效应蛋白通过靶向和劫持植物水通道蛋白的磷酸化来抑制宿主细胞防御的保守且新颖的途径。 CRN 效应子在植物、动物和昆虫的多种病原体中是保守的，并且在疫霉属物种中高度扩展。然而，人们对它们的功能、目标和作用机制知之甚少。在这里，我们表征了臭名昭著的卵菌病原体 P. sojae 中含有激酶结构域的 CRN 效应子 (CRN78)。 CRN78 是酱油假单胞菌感染的毒力必需效应子，通过抑制植物 H2O2 积累和防御基因表达发挥作用。我们证明，CRN78 可能与植物 PIP2 家族水通道蛋白（包括本塞姆氏烟草 NbPIP2;2 和大豆 GmPIP2-13）相互作用，并调节其磷酸化，导致随后的 26S 依赖性蛋白质降解。此外，我们发现 NbPIP2;2 是一种质外体到细胞质的 H2O2 转运蛋白，可正向调节植物免疫和 ROS 积累。重要的是，这种磷酸化在许多植物水通道蛋白中可能高度保守。因此，本研究鉴定了酱油假单胞菌的毒力相关效应子和新型植物免疫相关基因，并揭示了效应子介导的植物水通道蛋白磷酸化和降解的详细机制。
Phytophthora genomes encode a myriad of Crinkler (CRN) effectors, some of which contain putative kinase domains. Little is known about the host targets of these kinase-domain-containing CRNs and their infection-promoting mechanisms. Here, we report the host target and functional mechanism of a conserved kinase CRN effector named CRN78 in a notorious oomycete pathogen, Phytophthora sojae. CRN78 promotes Phytophthora capsici infection in Nicotiana benthamiana and enhances P. sojae virulence on the host plant Glycine max by inhibiting plant H2O2 accumulation and immunity-related gene expression. Further investigation reveals that CRN78 interacts with PIP2-family aquaporin proteins including NbPIP2;2 from N. benthamiana and GmPIP2-13 from soybean on the plant plasma membrane, and membrane localization is necessary for virulence of CRN78. Next, CRN78 promotes phosphorylation of NbPIP2;2 or GmPIP2-13 using its kinase domain in vivo, leading to their subsequent protein degradation in a 26S-dependent pathway. Our data also demonstrates that NbPIP2;2 acts as a H2O2 transporter to positively regulate plant immunity and reactive oxygen species (ROS) accumulation. Phylogenetic analysis suggests that the phosphorylation sites of PIP2 proteins and the kinase domains of CRN78 homologs are highly conserved among higher plants and oomycete pathogens, respectively. Therefore, this study elucidates a conserved and novel pathway used by effector proteins to inhibit host cellular defenses by targeting and hijacking phosphorylation of plant aquaporin proteins. CRN effectors are conserved in diverse pathogens of plants, animals, and insects, and highly expanded in Phytophthora species. Nevertheless, little is known about their functions, targets, and action mechanisms. Here, we characterized a kinase-domain-containing CRN effector (CRN78) in a notorious oomycete pathogen, P. sojae. CRN78 is a virulence-essential effector of P. sojae infection, and acts via suppression of plant H2O2 accumulation and defense gene expressions. We demonstrated that CRN78 might interact with plant PIP2-family aquaporin proteins, including N. benthamiana NbPIP2;2 and soybean GmPIP2-13, and regulate their phosphorylation, resulting in subsequent 26S-dependent protein degradation. Furthermore, we revealed that NbPIP2;2 was an apoplast-to-cytoplast H2O2 transporter and positively regulated plant immunity and ROS accumulation. Importantly, this phosphorylation may be highly conserved in many plant aquaporin proteins. Thus, this study identifies a virulence-related effector from P. sojae and a novel plant immunity-related gene, and reveals a detailed mechanism of effector-mediated phosphorylation and degradation of plant aquaporin proteins.
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