植物病原菌Nep1-Like蛋白研究进展

doi:10.3969/j.issn.1004-1524.2023.03.24

浙江农业学报 ›› 2023, Vol. 35 ›› Issue (3): 708-716.DOI: 10.3969/j.issn.1004-1524.2023.03.24

植物病原菌Nep1-Like蛋白研究进展

向江(), 程建徽, 魏灵珠, 吴江^*()

浙江省农业科学院园艺研究所,浙江杭州 310021

收稿日期:2021-10-11 出版日期:2023-03-25 发布日期:2023-04-07
通讯作者: ^*吴江,E-mail:wujiang@zaas.ac.cn
作者简介:向江(1987—),男,重庆人,博士,助理研究员,主要从事葡萄育种与栽培研究。E-mail:xiangjiang717@163.com
基金资助:
国家自然科学基金(31801822);浙江省农业科学院青年人才培养项目

Progress on Nep1-like proteins (NLPs) of phytopathogens

XIANG Jiang(), CHENG Jianhui, WEI Lingzhu, WU Jiang^*()

Institute of Horticulture, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China

Received:2021-10-11 Online:2023-03-25 Published:2023-04-07

摘要/Abstract

摘要：

NLPs[necrosis-and ethylene-inducing peptide 1 (Nep1)-like proteins]是一类质外体分泌蛋白,存在于多种植物病原菌中,在病原菌侵染植物的过程中发挥着重要的作用。根据结构特点,NLP蛋白分为Ⅰ、Ⅱ和Ⅲ 3种类型,存在有细胞毒性和无细胞毒性两种形态。具有细胞毒性的NLP蛋白与植物的NTCD4蛋白结合后促进自身寡聚化,引起双子叶植物细胞死亡和感病,而对单子叶植物无影响。无细胞毒性的NLP蛋白功能仍不清楚。NLP蛋白还能作为MAMP分子激发植物免疫反应,许多植物已经进化出特异性识别NLP蛋白的免疫系统,例如拟南芥通过受体蛋白RLP23识别类型Ⅰ的NLP蛋白保守多肽nlp20/24,从而激发免疫反应。本文综述了近年来国内外关于NLP蛋白结构、表达模式、致病机理及被寄主识别机制的研究进展,以期为病原菌-寄主互作机制及病害绿色防控研究提供理论依据和参考。

关键词: 植物病原菌, NLP蛋白, 细胞毒性, 免疫反应, 致病机理

Abstract:

NLPs[necrosis-and ethylene-inducing peptide 1 (Nep1)-like proteins] are a type of apoplast secreted protein, which exist in a variety of phytopathogens, and play an important role during plant-pathogen interactions. According to structural characteristics, NLP proteins are divided into three types: Ⅰ, Ⅱ and Ⅲ, with cytotoxic and noncytotoxic forms. Cytotoxic NLPs bind to NTCD4 protein to facilitate oligomerization of NLP proteins, resulting in cell death and disease susceptibility in eudicots, but not monocots. However, the function of noncytotoxic NLP proteins remains unclear. NLPs can also act as microbe-associated molecular patterns(MAMP)to trigger plant immunity. Many plants have evolved immune systems that specifically recognize NLP proteins, e.g., Arabidopsis thaliana recognizes the conserved peptide nlp20/24 of type Ⅰ NLP proteins via the receptor-like protein RLP23, thereby stimulating immune responses. This article reviewed the research progress on NLPs, such as protein structures, gene expression patterns, mechanisms of pathogenicity and host recognition, to provide a theoretical basis and reference for further research on pathogen-host interactions and disease prevention and control.

Key words: phytopathogens, NLPs, cytotoxic, immunity, pathogenic mechanism

中图分类号:

S432.1

向江, 程建徽, 魏灵珠, 吴江. 植物病原菌Nep1-Like蛋白研究进展[J]. 浙江农业学报, 2023, 35(3): 708-716.

XIANG Jiang, CHENG Jianhui, WEI Lingzhu, WU Jiang. Progress on Nep1-like proteins (NLPs) of phytopathogens[J]. Acta Agriculturae Zhejiangensis, 2023, 35(3): 708-716.

参考文献 58

[1]	KAMOUN S. A catalogue of the effector secretome of plant pathogenic oomycetes[J]. Annual Review of Phytopathology, 2006, 44: 41-60. PMID
[2]	CHISHOLM S T, COAKER G, DAY B, et al. Host-microbe interactions: shaping the evolution of the plant immune response[J]. Cell, 2006, 124(4): 803-814. DOI PMID
[3]	ROCAFORT M, FUDAL I, MESARICH C H. Apoplastic effector proteins of plant-associated fungi and oomycetes[J]. Current Opinion in Plant Biology, 2020, 56: 9-19. DOI PMID
[4]	BAILEY B A. Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca[J]. Phytopathology, 1995, 85(10): 1250. DOI URL
[5]	PEMBERTON C L, SALMOND G P C. The Nep1-like proteins—a growing family of microbial elicitors of plant necrosis[J]. Molecular Plant Pathology, 2004, 5(4): 353-359. DOI URL
[6]	LENARČIČ T, PIRC K, HODNIK V, et al. Molecular basis for functional diversity among microbial Nep1-like proteins[J]. PLoS Pathogens, 2019, 15(9): e1007951.
[7]	QUTOB D, KEMMERLING B, BRUNNER F, et al. Phytotoxicity and innate immune responses induced by Nep1-like proteins[J]. The Plant Cell, 2006, 18(12): 3721-3744. DOI URL
[8]	TYLER B M, TRIPATHY S, ZHANG X M, et al. Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis[J]. Science, 2006, 313(5791): 1261-1266. DOI URL
[9]	QUTOB D, KAMOUN S, GIJZEN M. Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy[J]. The Plant Journal, 2002, 32(3): 361-373. DOI URL
[10]	BÖHM H, ALBERT I, OOME S, et al. A conserved peptide pattern from a widespread microbial virulence factor triggers pattern-induced immunity in Arabidopsis[J]. PLoS Pathogens, 2014, 10(11): e1004491.
[11]	OTTMANN C, LUBERACKI B, KÜFNER I, et al. A common toxin fold mediates microbial attack and plant defense[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(25): 10359-10364. DOI PMID
[12]	GIJZEN M, NÜRNBERGER T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP₁ domain across taxa[J]. Phytochemistry, 2006, 67(16): 1800-1807. DOI URL
[13]	OOME S, RAAYMAKERS T M, CABRAL A, et al. Nep1-like proteins from three kingdoms of life act as a microbe-associated molecular pattern in Arabidopsis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(47): 16955-16960.
[14]	MCGOWAN J, FITZPATRICK D A. Genomic, network, and phylogenetic analysis of the oomycete effector arsenal[J]. mSphere, 2017, 2(6): e00408-17.
[15]	HORNER N R, GRENVILLE-BRIGGS L J, VAN WEST P. The oomycete Pythium oligandrum expresses putative effectors during mycoparasitism of Phytophthora infestans and is amenable to transformation[J]. Fungal Biology, 2012, 116(1): 24-41. DOI URL
[16]	OOME S, VAN DEN ACKERVEKEN G. Comparative and functional analysis of the widely occurring family of Nep1-like proteins[J]. Molecular Plant-Microbe Interactions: MPMI, 2014, 27(10): 1081-1094. DOI PMID
[17]	FELLBRICH G, ROMANSKI A, VARET A, et al. NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis[J]. The Plant Journal, 2002, 32(3): 375-390. DOI URL
[18]	NELSON A J, APEL-BIRKHOLD P C, BAILEY B A. Sequence announcements: GenBank accession No. AF036580[J]. Plant Molecular Biology, 1998, 38: 911-912. DOI URL
[19]	DEAN R A, TALBOT N J, EBBOLE D J, et al. The genome sequence of the rice blast fungus Magnaporthe grisea[J]. Nature, 2005, 434 (7036): 980-986. DOI
[20]	KANNEGANTI T D, HUITEMA E, CAKIR C, et al. Synergistic interactions of the plant cell death pathways induced by Phytophthora infestans Nep1-like protein PiNPP1.1 and INF1 elicitin[J]. Molecular Plant-Microbe Interactions, 2006, 19(8): 854-863. DOI URL
[21]	FENG B Z, LI P Q. Molecular characterization and functional analysis of the Nep1-like protein-encoding gene from Phytophthora capsici[J]. Genetics and Molecular Research, 2013, 12(2): 1468-1478. DOI URL
[22]	IRIEDA H, MAEDA H, AKIYAMA K, et al. Colletotrichum orbiculare secretes virulence effectors to a biotrophic interface at the primary hyphal neck via exocytosis coupled with SEC22-mediated traffic[J]. The Plant Cell, 2014, 26(5): 2265-2281. DOI URL
[23]	AZMI N S A, SINGKARAVANIT-OGAWA S, IKEDA K, et al. Inappropriate expression of an NLP effector in Colletotrichum orbiculare impairs infection on Cucurbitaceae cultivars via plant recognition of the C-terminal region[J]. Molecular Plant-Microbe Interactions, 2018, 31(1): 101-111. DOI URL
[24]	CABRAL A, OOME S, SANDER N, et al. Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis: repression of necrosis-inducing activity by a surface-exposed region[J]. Molecular Plant-Microbe Interactions, 2012, 25(5): 697-708. DOI URL
[25]	SCHUMACHER S, GROSSER K, VOEGELE R T, et al. Identification and characterization of Nep1-like proteins from the grapevine downy mildew pathogen Plasmopara viticola[J]. Frontiers in Plant Science, 2020, 11: 65. DOI URL
[26]	FENG B Z, ZHU X P, FU L, et al. Characterization of necrosis-inducing NLP proteins in Phytophthora capsici[J]. BMC Plant Biology, 2014, 14: 126. DOI
[27]	SANTHANAM P, VAN ESSE H P, ALBERT I, et al. Evidence for functional diversification within a fungal NEP1-like protein family[J]. Molecular Plant-Microbe Interactions, 2013, 26(3): 278-286. DOI PMID
[28]	DONG S M, KONG G H, QUTOB D, et al. The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity[J]. Molecular Plant-Microbe Interactions, 2012, 25(7): 896-909. DOI URL
[29]	ZHOU B J, JIA P S, GAO F, et al. Molecular characterization and functional analysis of a necrosis-and ethylene-inducing, protein-encoding gene family from Verticillium dahliae[J]. Molecular Plant-Microbe Interactions, 2012, 25(7): 964-975. DOI URL
[30]	CUESTA ARENAS Y, KALKMAN E R I C, SCHOUTEN A, et al. Functional analysis and mode of action of phytotoxic Nep1-like proteins of Botrytis cinerea[J]. Physiological and Molecular Plant Pathology, 2010, 74(5/6): 376-386. DOI URL
[31]	DALLAL BASHI Z, HEGEDUS D D, BUCHWALDT L, et al. Expression and regulation of Sclerotinia sclerotiorum necrosis and ethylene-inducing peptides (NEPs)[J]. Molecular Plant Pathology, 2010, 11(1): 43-53. DOI URL
[32]	STAATS M, VAN BAARLEN P, SCHOUTEN A, et al. Functional analysis of NLP genes from Botrytis elliptica[J]. Molecular Plant Pathology, 2007, 8(2): 209-214. DOI URL
[33]	BAXTER L, TRIPATHY S, ISHAQUE N, et al. Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome[J]. Science, 2010, 330(6010): 1549-1551. DOI URL
[34]	BAILEY B A, BAE H H, STREM M D, et al. Developmental expression of stress response genes in Theobroma cacao leaves and their response to Nep1 treatment and a compatible infection by Phytophthora megakarya[J]. Plant Physiology and Biochemistry, 2005, 43(6): 611-622. DOI URL
[35]	JENNINGS J C, APEL-BIRKHOLD P C, MOCK N M, et al. Induction of defense responses in tobacco by the protein Nep1 from Fusarium oxysporum[J]. Plant Science, 2001, 161(5): 891-899. DOI URL
[36]	KEATES S E, KOSTMAN T A, ANDERSON J D, et al. Altered gene expression in three plant species in response to treatment with Nep1, a fungal protein that causes necrosis[J]. Plant Physiology, 2003, 132(3): 1610-1622. PMID
[37]	VEIT S, WÖRLE J M, NÜRNBERGER T, et al. A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco[J]. Plant Physiology, 2001, 127(3): 832-841. DOI URL
[38]	SCHOUTEN A, VAN BAARLEN P, KAN J A L V. Phytotoxic Nep1-like proteins from the necrotrophic fungus Botrytis cinerea associate with membranes and the nucleus of plant cells[J]. New Phytologist, 2008, 177(2): 493-505. DOI URL
[39]	TEH C Y, PANG C L, TOR X Y, et al. Molecular cloning and functional analysis of a necrosis and ethylene inducing protein (NEP) from Ganoderma boninense[J]. Physiological and Molecular Plant Pathology, 2019, 106: 42-48. DOI URL
[40]	KAPILA J, DE RYCKE R, VAN MONTAGU M, et al. An Agrobacterium-mediated transient gene expression system for intact leaves[J]. Plant Science, 1997, 122(1): 101-108. DOI URL
[41]	BAILEY B A, JENNINGS J C, ANDERSON J D. The 24-kDa protein from Fusarium oxysporum f.sp. erythroxyli: occurrence in related fungi and the effect of growth medium on its production[J]. Canadian Journal of Microbiology, 1997, 43(1): 45-55. DOI URL
[42]	MATTINEN L, TSHUIKINA M, MÄE A, et al. Identification and characterization of nip, necrosis-inducing virulence protein of Erwinia carotovora subsp. carotovora[J]. Molecular Plant-Microbe Interactions, 2004, 17(12): 1366-1375. DOI URL
[43]	JENNINGS J C, APEL-BIRKHOLD P C, BAILEY B A, et al. Induction of ethylene biosynthesis and necrosis in weed leaves by a Fusarium oxysporum protein[J]. Weed Science, 2000, 48(1): 7-14. DOI URL
[44]	MOTTERAM J, KÜFNER I, DELLER S, et al. Molecular characterization and functional analysis of MgNLP, the sole NPP₁ domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola[J]. Molecular Plant-Microbe Interactions: MPMI, 2009, 22(7): 790-799. DOI URL
[45]	KÜFNER I, OTTMANN C, OECKING C, et al. Cytolytic toxins as triggers of plant immune response[J]. Plant Signaling & Behavior, 2009, 4(10): 977-979.
[46]	ROJKO N, DALLA SERRA M, MAČEK P, et al. Pore formation by actinoporins, cytolysins from sea anemones[J]. Biochimica et Biophysica Acta (BBA) -Biomembranes, 2016, 1858(3): 446-456. DOI PMID
[47]	LENARČIČ T, ALBERT I, BÖHM H, et al. Eudicot plant-specific sphingolipids determine host selectivity of microbial NLP cytolysins[J]. Science, 2017, 358(6369): 1431-1434. DOI PMID
[48]	CHEN J B, BAO S W, FANG Y L, et al. An LRR-only protein promotes NLP-triggered cell death and disease susceptibility by facilitating oligomerization of NLP in Arabidopsis[J]. New Phytologist, 2021, 232(4): 1808-1822. DOI URL
[49]	PEMBERTON C L, WHITEHEAD N A, SEBAIHIA M, et al. Novel quorum-sensing-controlled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium[J]. Molecular Plant-Microbe Interactions, 2005, 18(4): 343-353. DOI URL
[50]	AMSELLEM Z, COHEN B A, GRESSEL J. Engineering hypervirulence in a mycoherbicidal fungus for efficient weed control[J]. Nature Biotechnology, 2002, 20 (10): 1035-1039. PMID
[51]	BAILEY B A, APEL-BIRKHOLD P C, LUSTER D G. Expression of NEP 1 by Fusarium oxysporum f. sp. erythroxyli after gene replacement and overexpression using polyethylene glycol-mediated transformation[J]. Phytopathology, 2002, 92(8): 833-841. DOI URL
[52]	FANG Y L, PENG Y L, FAN J. The Nep1-like protein family of Magnaporthe oryzae is dispensable for the infection of rice plants[J]. Scientific Reports, 2017, 7: 4372. DOI
[53]	ZHANG H J, LI D Q, WANG M F, et al. The Nicotiana benthamiana mitogen-activated protein kinase cascade and WRKY transcription factor participate in Nep1(Mo)-triggered plant responses[J]. Molecular Plant-Microbe Interactions, 2012, 25(12): 1639-1653. DOI URL
[54]	YANG K, DONG X H, LI J L, et al. Type 2 Nep1-like proteins from the biocontrol oomycete Pythium oligandrum suppress Phytophthora capsici infection in solanaceous plants[J]. Journal of Fungi (Basel, Switzerland), 2021, 7(7): 496. DOI URL
[55]	MACHO A P, ZIPFEL C. Plant PRRs and the activation of innate immune signaling[J]. Molecular Cell, 2014, 54(2): 263-272. DOI PMID
[56]	ALBERT I, BÖHM H, ALBERT M, et al. An RLP23-SOBIR1-BAK1 complex mediates NLP-triggered immunity[J]. Nature Plants, 2015, 1: 15140. DOI PMID
[57]	RAAYMAKERS T M. Activation of plant immunity by microbial Nep1-like protein patterns[D]. Utrecht: Utrecht University, 2018.
[58]	REYES-CHIN-WO S, WANG Z, YANG X, et al. Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce[J]. Nature Communications, 2017, 8: 14953. DOI URL

植物病原菌Nep1-Like蛋白研究进展

Progress on Nep1-like proteins (NLPs) of phytopathogens

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