A monocot-specific hydroxycinnamoylputrescine gene cluster contributes to immunity and cell death in rice  

单子叶植物特异的羟基肉桂酰腐胺基因簇调控水稻免疫反应及细胞死亡

作　　者：Hong Fang Shuangqian Shen Dan Wang Fan Zhang Chongyang Zhang Zixuan Wang Qianqian Zhou Ruyi Wang Hui Tao Feng He Chenkun Yang Meng Peng Xinyu Jing Zeyun Hao Xionglun Liu Jie Luo Guo-Liang Wang Yuese Ning 方红;沈双欠;王丹;张帆;张重阳;王梓烜;周蒨蒨;王如意;陶辉;何峰;杨陈坤;彭梦;靖鑫宇;郝泽芸;刘雄伦;罗杰;王国梁;宁约瑟(State Key Laboratory for Biology of Plant Diseases and Insect Pests,Institute of Plant Protection,Chinese Academy of Agricultural Sciences,Beijing 100193,China;College of Agronomy,Hunan Agricultural University,Changsha 410128,China;National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research(Wuhan),Huazhong Agricultural University,Wuhan 430070,China;Department of Plant Pathology,The Ohio State University,Columbus OH 43210,USA;College of Tropical Crops,Hainan University,Haikou 572208,China)

机构地区：[1]State Key Laboratory for Biology of Plant Diseases and Insect Pests,Institute of Plant Protection,Chinese Academy of Agricultural Sciences,Beijing 100193,China [2]College of Agronomy,Hunan Agricultural University,Changsha 410128,China [3]National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research(Wuhan),Huazhong Agricultural University,Wuhan 430070,China [4]Department of Plant Pathology,The Ohio State University,Columbus OH 43210,USA [5]College of Tropical Crops,Hainan University,Haikou 572208,China

出　　处：《Science Bulletin》2021年第23期2381-2393,共13页科学通报（英文版）

基　　金：supported by grants from the National Natural Science Foundation of China (31822041 and 31972225);the National Key Research and Development Program of China (2016YFD0100600) to Yuese Ning;the National Natural Science Foundation of China (U20A2021) to Ruyi Wang;the National Natural Science Foundation of China (31801692) to Fan Zhang;the State Key Program of National Natural Science Foundation of China (31530052);the National Science Fund for Distinguished Young Scholars (31625021);the Foundation for Innovative Research Groups of the National Natural Science Foundation of China (31821005);the Hainan University Start up Fund (KYQD(ZR)1866 to Jie Luo。

摘　　要：Phenolamides(PAs), a diverse group of specialized metabolites, including hydroxycinnamoylputrescine(HP), hydroxycinnamoylagmatine, and hydroxycinnamoyltryptamine, are important in plant resistance to biotic stress. However, the genes involved in the biosynthesis and modulation of PAs have not been fully elucidated. This study identified an HP biosynthetic gene cluster in rice(Oryza sativa) comprising one gene(Os ODC) encoding a decarboxylase and two tandem-duplicated genes(Os PHT3 and Os PHT4)encoding putrescine hydroxycinnamoyl acyltransferases coexpressed in different tissues. Os ODC catalyzes the conversion of ornithine to putrescine, which is used in HP biosynthesis involving Os PHT3 and Os PHT4. Os PHT3 or Os PHT4 overexpression causes HP accumulation and cell death and putrescine hydroxycinnamoyl acyltransferases(PHT) activity-dependent resistance against the fungal pathogen Magnaporthe oryzae. Os ODC overexpression plants also confer enhanced resistance to M. oryzae.Notably, the basic leucine zipper transcription factor APIP5, a negative regulator of cell death, directly binds to the Os PHT4 promoter, repressing its transcription. Moreover, APIP5 suppression induces Os PHT4 expression and HP accumulation. Comparative genomic analysis revealed that the HP biosynthetic gene cluster is conserved in monocots. These results characterized a previously unidentified monocot-specific gene cluster that is involved in HP biosynthesis and contributes to defense and cell death in rice.酚胺代谢物是一类丰富多样的次级代谢物,主要包括羟基肉桂酰腐胺、羟基肉桂酰胍丁胺和羟基肉桂酰色胺,在生物胁迫中扮演着至关重要的角色.然而,其生物合成和调控机制尚不清楚.本研究利用基于代谢物的全基因关联分析(m GWAS)鉴定了一个水稻(Oryza sativa)脂肪族酚胺代谢基因簇-羟基肉桂酰腐胺(HP)基因簇,该基因簇由1个鸟氨酸脱羧酶(Os ODC)和2个串联的腐胺羟基肉桂酰转移酶(Os PHT3和Os PHT4)组成.超量表达Os PHT3和Os PHT4促进了HP的显著积累,诱发了强烈的植物细胞死亡,同时显著提高了水稻对稻瘟菌的抗病性,且它们的表型依赖于其酰基转移酶活性. Os ODC过表达植物也增强了水稻对稻瘟菌的抗病性.进一步研究发现,水稻免疫及细胞死亡负调控转录因子APIP5直接结合Os PHT4的启动子并抑制其表达,进而影响HP的积累.比较基因组学分析表明, HP生物合成基因簇在单子叶植物中具有保守性,暗示HP基因簇在单子叶植物中可能有相似的生物学功能.本研究揭示了单子叶植物特异的脂肪族酚胺代谢基因簇调控水稻免疫及细胞死亡的新机制,为植物细胞死亡及免疫在代谢水平上的研究提供了新的见解.

关 键 词：Secondary metabolites Plant immunity Cell death HP gene cluster bZIP transcription factor Oryza sativa Magnaporthe oryzae 

分 类 号：S511[农业科学—作物学]