Böhm Hannah, Albert Isabell, Oome Stan, Raaymakers Tom M, Van den Ackerveken Guido, Nürnberger Thorsten
Center of Plant Molecular Biology (ZMBP)-Plant Biochemistry, Eberhard-Karls-University Tübingen, Tübingen, Germany.
Plant-Microbe Interactions, Department of Biology, Utrecht University, Utrecht, The Netherlands; Centre for BioSystems Genomics (CBSG), Wageningen, The Netherlands.
PLoS Pathog. 2014 Nov 6;10(11):e1004491. doi: 10.1371/journal.ppat.1004491. eCollection 2014 Nov.
Microbe- or host damage-derived patterns mediate activation of pattern-triggered immunity (PTI) in plants. Microbial virulence factor (effector)-triggered immunity (ETI) constitutes a second layer of plant protection against microbial attack. Various necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) produced by bacterial, oomycete and fungal microbes are phytotoxic virulence factors that exert immunogenic activities through phytotoxin-induced host cell damage. We here show that multiple cytotoxic NLPs also carry a pattern of 20 amino acid residues (nlp20) that triggers immunity-associated plant defenses and immunity to microbial infection in Arabidopsis thaliana and related plant species with similar characteristics as the prototype pattern, bacterial flagellin. Characteristic differences in flagellin and nlp20 plant responses exist however, as nlp20s fail to trigger extracellular alkalinization in Arabidopsis cell suspensions and seedling growth inhibition. Immunogenic nlp20 peptide motifs are frequently found in bacterial, oomycete and fungal NLPs. Such an unusually broad taxonomic distribution within three phylogenetic kingdoms is unprecedented among microbe-derived triggers of immune responses in either metazoans or plants. Our findings suggest that cytotoxic NLPs carrying immunogenic nlp20 motifs trigger PTI in two ways as typical patterns and by inflicting host cell damage. We further propose that conserved structures within a microbial virulence factor might have driven the emergence of a plant pattern recognition system mediating PTI. As this is reminiscent of the evolution of immune receptors mediating ETI, our findings support the idea that there is a continuum between PTI and ETI.
微生物或宿主损伤衍生的模式介导植物中模式触发免疫(PTI)的激活。微生物毒力因子(效应子)触发的免疫(ETI)构成了植物抵御微生物攻击的第二层保护。细菌、卵菌和真菌微生物产生的各种坏死和乙烯诱导肽1(Nep1)样蛋白(NLPs)是具有植物毒性的毒力因子,它们通过植物毒素诱导的宿主细胞损伤发挥免疫原性活性。我们在此表明,多种细胞毒性NLPs还携带一种20个氨基酸残基的模式(nlp20),该模式可触发拟南芥及具有与原型模式(细菌鞭毛蛋白)相似特征的相关植物物种中与免疫相关的植物防御反应及对微生物感染的免疫。然而,鞭毛蛋白和nlp20在植物反应中存在特征差异,因为nlp20无法在拟南芥细胞悬浮液中触发细胞外碱化以及抑制幼苗生长。免疫原性nlp20肽基序在细菌、卵菌和真菌的NLPs中经常被发现。在后生动物或植物的免疫反应的微生物来源触发因子中,这种在三个系统发育界内异常广泛的分类分布是前所未有的。我们的研究结果表明,携带免疫原性nlp20基序的细胞毒性NLPs以两种方式触发PTI,一种是作为典型模式,另一种是通过造成宿主细胞损伤。我们进一步提出,微生物毒力因子内的保守结构可能推动了介导PTI的植物模式识别系统的出现。由于这让人联想到介导ETI的免疫受体的进化,我们的研究结果支持了PTI和ETI之间存在连续性的观点。