The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity
The blast pathogen effector AVR-Pik binds and stabilizes rice heavy metal-associated (HMA) proteins to co-opt their function in immunity
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DOI：
10.1101/2020.12.01.406389
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发表时间：
2020-12
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通讯作者：
Kaori Oikawa;K. Fujisaki;Motoki Shimizu;Takumi Takeda;Keiichiro Nemoto;H. Saitoh;Akiko Hirabuchi;Yukie Hiraka;Naomi Miyaji;A. Białas;Thorsten Langner;Ronny Kellner;T. Bozkurt;Stella Cesari;T. Kroj;M. Banfield;S. Kamoun;R. Terauchi
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作者：
Kaori Oikawa;K. Fujisaki;Motoki Shimizu;Takumi Takeda;Keiichiro Nemoto;H. Saitoh;Akiko Hirabuchi;Yukie Hiraka;Naomi Miyaji;A. Białas;Thorsten Langner;Ronny Kellner;T. Bozkurt;Stella Cesari;T. Kroj;M. Banfield;S. Kamoun;R. Terauchi
细胞内核苷酸结合结构域和富含亮氨酸重复序列（NLR）受体在生命多个领域的免疫中起着至关重要的作用。在植物中，NLR的一个子集包含非典型的整合结构域，被认为是从病原体效应子的宿主靶标进化而来的，以充当病原体诱饵。然而，与NLR整合结构域相似的宿主蛋白的功能以及它们被病原体效应物靶向的程度在很大程度上仍然未知。在这里，我们表明，稻瘟菌效应AVR-Pik结合一个子集的相关水稻蛋白含有重金属相关（HMA）结构域，其中一个结构域已反复整合到植物NLR免疫受体。我们发现AVR-Pik结合稳定水稻小HMA（sHMA）蛋白OsHIPP 19和OsHIPP 20。OsHIPP 20的敲除导致对稻瘟病病原体的抗病性增强，表明OsHIPP 20是一个易感基因（S基因）。我们认为AVR-Pik已经进化为结合HMA结构域蛋白并选择它们的功能来抑制免疫。然而，这种结合带来了一个权衡，它触发了携带NLR受体与整合的HMA结构域的植物的免疫力。水稻稻瘟病是由稻瘟病菌（Magnaporthe）引起的水稻病害，是水稻上最具破坏性的病害之一。因此，了解稻瘟病菌的侵染机制和水稻的抗病性对全球粮食安全具有重要意义。在这项研究中，我们表明，M。水稻sHMA效应蛋白AVR-PikD结合水稻sHMA蛋白并使其稳定，推测是为了增强病原体感染。我们发现，水稻sHMA OsHIPP 20中的功能缺失突变体降低了对M.这表明M.入侵需要宿主sHMA来促进入侵。值得注意的是，OsHIPP 20敲除水稻品系没有表现出生长缺陷，这表明编辑sHMA基因可能是抗稻瘟病的新来源。
Intracellular nucleotide-binding domain and leucine-rich repeat-containing (NLR) receptors play crucial roles in immunity across multiple domains of life. In plants, a subset of NLRs contain noncanonical integrated domains that are thought to have evolved from host targets of pathogen effectors to serve as pathogen baits. However, the functions of host proteins with similarity to NLR integrated domains and the extent to which they are targeted by pathogen effectors remain largely unknown. Here, we show that the blast fungus effector AVR-Pik binds a subset of related rice proteins containing a heavy metal-associated (HMA) domain, one of the domains that has repeatedly integrated into plant NLR immune receptors. We find that AVR-Pik binding stabilizes the rice small HMA (sHMA) proteins OsHIPP19 and OsHIPP20. Knockout of OsHIPP20 causes enhanced disease resistance towards the blast pathogen, indicating that OsHIPP20 is a susceptibility gene (S-gene). We propose that AVR-Pik has evolved to bind HMA domain proteins and co-opt their function to suppress immunity. Yet this binding carries a trade-off, it triggers immunity in plants carrying NLR receptors with integrated HMA domains. Significance Statement Rice blast disease, caused by the fungus Magnaporthe oryzae, is one of the most devastating diseases of rice. Therefore, understanding the mechanisms of blast fungus infection and resistance of rice against the disease is important for global food security. In this study, we show that the M. oryzae effector protein AVR-PikD binds rice sHMA proteins and stabilizes them, presumably to enhance pathogen infection. We show that loss-of-function mutants in one rice sHMA, OsHIPP20, reduced the level of susceptibility against a compatible isolate of M. oryzae, suggesting that M. oryzae requires host sHMA to facilitate invasion. Remarkably, OsHIPP20 knockout rice line showed no growth defect, suggesting editing sHMA genes may present a novel source of resistance against blast disease.