The jasmonate receptor COI1 is required for AtPep1-induced immune responses in Arabidopsis thaliana

Abstract

ObjectivePlant cells detect the presence of potentially pathogenic microorganisms in the apoplast via plasma membrane-localized receptors. Activated receptors trigger phosphorylation-mediated signaling cascades that protect the cell from infection. It is thought that signaling triggered by the detection of exogenous signals, such as bacterial flagellin, can be amplified by endogenous signals, such as hormones or debris caused by cell damage, to potentiate robust immune responses. For example, perception of flagellin and other microbial molecules results in increased expression of endogenous PROPEP transcripts that give rise to AtPep peptides which also activate immune signaling. Phytohormones such as methyl-jasmonate also induce PROPEP expression, suggestive of additional hormone-mediated feedback loops that similarly amplify immune signaling. The current study aimed to determine if perception of jasmonate is genetically required for AtPep1-induced immune responses in Arabidopsis thaliana.ResultsWe assessed several AtPep1-induced immune responses in plants expressing a non-functional variant of the jasmonate receptor CORONATINE-INSENSITIVE 1 (COI1). We found that coi1-16 mutants are severely compromised in some AtPep1-induced immune responses, while other AtPep1-induced responses are maintained but reduced. Our findings build on previously published work and suggest that JA perception plays a role in immune responses triggered by AtPep1.Electronic supplementary materialThe online version of this article (10.1186/s13104-018-3628-7) contains supplementary material, which is available to authorized users.

External jasmonic acid isoleucine mediates amplification of plant elicitor peptide receptor (PEPR) and jasmonate‐based immune signalling

“…Loss‐of‐function of PEPRs also impacts the canonical JA‐Ile response pathway. Similar to this data, it is known that perception of flg22 and MeJA results in increased expression of endogenous PROPEP transcripts, suggestive of hormone and MAMP‐mediated feedback loops that amplify Pep‐PEPR mediated immune signalling (Holmes et al, 2018).…”

Spatially distinct phytohormone responses of individualArabidopsis thalianaroot cells to infection and colonization byFusarium oxysporum

“…Importantly, this WRKY-module regulates SA and JA, but has so far not been linked to the regulation of ET. Interestingly, both JA and ET-induced defense signaling has been linked to the PLANT ELICITOR PEPTIDE (PEP) pathway (Liu et al ., 2013; Tintor et al ., 2013; Holmes et al ., 2018). Liu et al .…”

“…(2013) have shown that PEP1, via the PEP RECEPTORs 1 and 2 and phosphorylation of the cytoplasmic BOTRYTIS-INDUCED KINASE 1 (BIK1), induces ethylene-dependent defense genes, including ERF1 . Holmes et al . (2018) demonstrated the requirement of the JA-receptor COI1 for PEP1-induced growth inhibition (as an indirect readout for activated immune signaling) and apoplastic ROS-burst via a member of the RBOH family of NADPH oxidases.…”

“…8). In this case, the PEP pathway would act as an amplifier of both, JA- and ET-signaling (Liu et al ., 2013; Holmes et al ., 2018; Calabria et al ., 2022). RBOHD activation appeared to be strongest in the HR and boundary zones, and this is also where we observed ‘root browning’ (Calabria et al ., 2022).…”

Research progress on the function of plant elicitor peptides

“…AtPep1 的敏感性 [55][56] 。Collins 等发现网格蛋白衔接子 EPS1 可以调节 AtPEPR1 和 BAK1 在细胞膜上的丰度，调控植物免疫信号 [57] 。AtPep1-AtPEPR1 从质膜通 过内吞转运到液泡前体， 这一途径不依赖于反面高尔基网/早期核内体 (trans golgi network/early endosome，TGN/EE)转运 [55] [43][58] 。 自然界中大多数病原菌主要通过植物表面的伤口或者自然开口进入植物体 [59] 。植物叶表面的气孔是病原菌进入植物体内的主要路径。植物通过先天免疫 系统感知病原菌并通过一系列精细调控机制来关闭气孔以阻止病原菌进入植物 叶组织 [60] 。Zheng 等发现 Peps-PEPRs 系统能够调控气孔关闭来阻止病原菌向叶 片组织扩散。Pep1 诱导气孔关闭主要通过激活慢阴离子通道(Slow-type Anion Channel 1，SLAC1)及其同源蛋白 SLAH3 的活性，促使保卫细胞阴离子外流， 降低细胞膨压来关闭气孔(图 3) [37] 。Open Stomata 1(OST1)是控制气孔关闭 的核心调控因子，同时也是气孔对抗病原菌及相关 PAMPs 所必需的组分 [60]- [62] 。 Zheng 等发现 Pep1 调控气孔关闭不依赖于 OST1 途径， 而 BIK1 在该信号途径中 起正调控作用 [37] 。 Peps 在植物系统免疫中也发挥重要作用，利用 AtPeps 预处理拟南芥叶片或 过表达 AtPROPEP1 和 AtPROPEP2 时均能增强植物对 Pst. DC3000 和 Pythium irregulare 的抗性， PEPRs 功能突变后植物体对多种致病菌的抗性减弱 [13][43][47][63] 。 Peps 信号主要与植物防御激素如 ET、JA 和 SA 信号相关联调控植物系统 A c c e p t e d https://engine.scichina.com/doi/10.1360/SSV-2021-0137 [13][43][47][63] 。ET 可诱导 PROPEPs 的表达并合成 Peps，Peps-PEPRs 进一步磷酸化 激活 BIK1 及其同源蛋白 PBL1，调控植物对 Botrytis cinerea 的抗性 [13][43][47][63] ， PEPRs 位于 ET 信号下游调控植物免疫，当 ET 信号缺失时，PEPRs 也可弥补 ET 的作用以增强植物免疫信号 [63] 。 同时 Peps-PEPRs 可促进 ET 合成并对 ET 诱导的 免疫信号做出反馈调节，进一步放大植物免疫信号 [43] 。ET 和 JA 能协同调控植 物对死体营养菌的免疫 [64][65] 。Peps 的识别能诱导 JA 合成和 JA 信号通路基因 PDF1.2 的表达，启动植物系统免疫 [43][64] [66], JA 合成酶 Allene oxide synthase [13] 。Peps 处理也能诱导 SA 信号相关基因 pathogenesis related 1(PR1)的转录上调，SA 合成关键基因 SID2 的突变降低了 Peps 对植物系统免疫的调控 [13] ，说明 SA 信号 在 Peps 调控的系统免疫中也发挥重要作用。在 Peps 调控的 ETI 过程中，Peps 主要依赖水杨酸信号诱导程序性细胞死亡 [54] 。 Peps 在抵抗食草类动物的危害中也发挥重要作用，研究者们分别利用甜菜 夜蛾(Spodoptera exigua)或斜纹夜蛾(Spodoptera littoralis larvae)口腔分泌物 处理玉米或者拟南芥叶片，发现均能促进 AtPROPEP3 和 AtPEPRs 基因的表达， 同时叶片组织中 JA 和 ET 显著积累 [11][15] 。直接用叶片饲喂斜纹夜蛾幼虫，发现 AtPEPRs 功能突变降低了对幼虫的抗性 [11] 。 而利用 ZmPep3 处理玉米叶片发现能 诱导挥发性萜烯和苯并恶唑嗪酮类物质的生成，有助于抑制甜菜夜蛾幼虫的生 长，同时也能够间接吸引甜菜夜蛾天敌寄生蜂，起到防御虫害作用 [15] 。 4.2 调控植物非生物逆境胁迫 非生物逆境胁迫也是影响植物正常生长的重要因素之一。Nakaminami 等发 现 AtPep3 可作为一类激素信号调控植物高盐胁迫 [20] 。高盐处理后，AtPROPEP3 的表达量显著上调。外源施加 AtPep3 或过表达 AtPROPEP3 均能提高植物耐盐 性 [20] 。AtPep3 C 末端 11-23 个氨基酸残基决定植物的抗盐能力。AtPEPR1 作为 [20] 。 AtPEPR2 也 可 作 为 CLAVATA3/Endosperm surrounding region 14(CLE14)小肽的受体来调控低磷响 应信号 [67] 。植物感受低磷信号后，分泌 CLE14 小肽，然后被其受体 CLAVATA2 (CLV2)和 PEPR...…”