Rice blast, caused by the fungal pathogen Magnaporthe oryzae, is one of the most devastating diseases in rice (Oryza sativa L.). Plant annexins are calcium- and lipid-binding proteins that have multiple functions; however, the biological roles of annexins in plant disease resistance remain unknown. Here, we report a rice annexin gene, OsANN1 (Rice annexin 1), that was induced by M. oryzae infection and negatively regulated blast disease resistance in rice. By yeast 2-hybrid screening, we found that OsANN1 interacted with a cytochrome P450 monooxygenase, HAN1 (“HAN” termed “chilling” in Chinese), which has been reported to catalyze the conversion of biologically active jasmonoyl-L-isoleucine (JA-Ile) to the inactive form 12-hydroxy-JA-Ile. Pathogen inoculation assays revealed that HAN1 was also a negative regulator in rice blast resistance. Genetic evidence showed that OsANN1 acts upstream of HAN1. OsANN1 stabilizes HAN1 in planta, resulting in the inactivation of the endogenous biologically active JA-Ile. Taken together, our study unravels a mechanism where an OsANN1–HAN1 module impairs blast disease resistance via inactivating biologically active JA-Ile and JA signaling in rice.
由稻瘟菌引起的稻瘟病是水稻極其嚴重的真菌病害，嚴重影響稻米產(chǎn)量和品質(zhì)。植物激素調(diào)控的免疫信號傳遞是植物基礎抗性的重要組成部分，如茉莉酸是植物應對病蟲侵害的重要植物激素，植物通過激活茉莉酸信號通路產(chǎn)生有效的防御反應。但是茉莉酸的過度積累會影響植物的生長和發(fā)育，因此，茉莉酸信號的適時消減至關重要。但是，植物是如何調(diào)控體內(nèi)茉莉酸水平來平衡其生長和免疫尚不清楚。本揭示了膜聯(lián)蛋白OsANN1通過調(diào)節(jié)體內(nèi)茉莉酸代謝途徑來調(diào)控水稻對稻瘟病抗性的新機制。
植物膜聯(lián)蛋白（Annexins）是一種多功能的鈣離子和磷脂分子結(jié)合蛋白，通過調(diào)節(jié)離子運輸、鈣通道形成和氧化還原反應等方式來調(diào)控植物生長發(fā)育和環(huán)境應答，但是其在水稻抗病過程中的作用還不明確。該研究發(fā)現(xiàn)一個水稻Annexin家族基因OsANN1在侵染水稻時誘導表達，并且負調(diào)控了水稻的抗病性。通過互作蛋白篩選鑒定到一個細胞色素P450單加氧酶HAN1，該蛋白與OsANN1直接互作。HAN1可以催化生物活性的JA-Ile轉(zhuǎn)化為非活性形式的12OH-JA-Ile（Mao et al., 2019）。進一步研究發(fā)現(xiàn)HAN1負調(diào)控了水稻抗病性，并在遺傳學上作用于OsANN1下游。OsANN1可以穩(wěn)定HAN1蛋白，促進該蛋白的積累，進而加劇了水稻JA-Ile的氧化失活，導致水稻的抗病性減弱。值得注意的是，該研究還發(fā)現(xiàn)病菌侵染可以使OsANN1與HAN1的互作顯著減弱。
基于以上結(jié)果，作者提出一個OsANN1通過調(diào)節(jié)體內(nèi)活性茉莉酸水平來調(diào)控免疫反應的分子模型：水稻未被病菌侵染時，OsANN1與茉莉酸合成途徑中的關鍵氧化酶HAN1結(jié)合，阻止其被泛素化降解，進而導致水稻茉莉酸的氧化失活，促進水稻生長；而當水稻識別病菌侵染時，HAN1與OsANN1解離并降解，進而導致活性茉莉酸積累，增強了水稻的抗病性。