三种激发子诱导的过敏性细胞死亡和气孔关闭的分子机制研究
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摘要
植物病原菌产生的激发子和病程相关分子模式(pathogen-associated molecular patterns, PAMP)是一类重要的信号分子,模仿非亲和互作中植物与病原菌的信号交流,启动不同的级联信号途径,诱发植物的抗病性,导致过敏反应(hypersensitive response,HR)和气孔关闭。本研究采用病毒诱导基因沉默(virus inducing gene silencing, VIGS)技术研究了本氏烟(Nicotiana benthamiana)NADPH氧化酶(respiratory burst oxidase homologues, RBOH)、液泡加工酶(vacuolar processing enzyme, VPE)、异三聚体G蛋白(简称G蛋白)及丝裂原活化蛋白激酶(mitogen-activated protein kinase, MAPK)在不同来源的激发子(harpin、Nep1和boehmerin)诱发的过敏反应和气孔关闭中的功能,这些激发子分别是细菌(Xanthomonas oryzae)、真菌(Magnaporthe oryzae)和卵菌(Phytophthora boehmeriae)的PAMPs.试验证明(?)BOH、VPE和G蛋白参与3种激发子诱导的气孔关闭,MAPKKKa-MEK2-WIPK介导激发子Nep1诱发的HR,而Gα、Gβ2和VPEla参与harpin诱导的HR,表明不同激发子诱发的信号传导途径具有一定保守性,同时不同的激发子诱导的信号传导也存在特异性。
RBOH是最重要的活性氧(active oxygen species, AOS)来源之一。NbrbohA、NbrbohB单基因沉默,以及NrbohA和NbrbohB双基因沉默显著抑制了boehmerin、INF1和harpin等3种激发子诱发的叶片中H2O2积累,但不影响激发子诱导的HR,且基因沉默对激发子诱发的PR基因的转录没有影响；而这些基因沉默却抑制激发子诱导的气孔关闭,且保卫细胞内NO积累显著减少,但不影响保卫细胞内Ca2+浓度和AOS积累。说明RBOH参与激发子诱导的气孔关闭,但不参与激发子诱导的过敏反应和PR基因的转录；植物体内其它酶催化产生的AOS及AOS/NO平衡可能参与激发子诱发的过敏性细胞死亡。
VPE是植物液泡的半胱氨酸蛋白酶,具有类似动物caspases-1-like酶活性。本试验发现NbVPE1a和NbVPE1b单基因沉默,及NbVPE1a/1b双基因沉默不影响harpin、boehmerin和Nep1激发子诱发的H2O2积累,NbVPE1a和NbVPE1a/1b沉默却抑制了harpi(?)诱发的HR；而boehmerin和Nep1均可诱发这3种VPE沉默的植株产生正常的HR,表明harpir诱发的HR依赖于VPE,但是VPE不参与boehmerin和Nep1诱发的HR。单基因和双基因沉默均抑制3种激发子诱发的气孔关闭,且抑制了保卫细胞内NO的积累；3种激发子诱导处理后,单基因沉默植株叶片中保卫细胞内活性氧的积累与对照一致,但是双基因沉默植株中保卫细胞内AOS的量显著高于对照和单基因沉默植株中保卫细胞内AOS的量,表明双基因共同作用负调控保卫细胞内AOS的积累。进一步转录分析显示VPE调节了活性氧相关的基因(NbrbohB)和转录因子(WRKY2)的转录。而已证明气孔在植物免疫中具有重要功能,提示VPE参与PAMP触发的抗性(PAMP-triggered immunity,PTI).
G蛋白连接着细胞表面的受体和下游的效应因子,在植物多种信号途径中具有重要的作用。本研究克隆了N.benthamiana G蛋白Gα、Gβ1和Gβ2等基因及腺苷酸环化酶基因(adenylyl cyclase,AC),Gα和Gβ2沉默抑制细菌蛋白激发子harpin诱导的过敏反应;Gα、Gβ2、AC削弱了3种激发子诱发的H2O2积累。Gα、Gβ1、Gβ2沉默抑制激发子诱发的气孔关闭,且保卫细胞中NO的积累减少。但是AC因沉默对3种激发子诱发过敏反应和气孔关闭及保卫细胞内NO的积累均没有影响。结果表明G蛋白的Gα、Gβ亚基在不同激发子激发过敏反应和气孔关闭及NO和H2O2积累中作用存在差异。
MAPK信号级联途径包含三个保守的激酶,MAPK kinase kinase(MAPKKK或MEKK)磷酸化MAPK kinase(MAPKK或MEK)又磷酸化MAPK,调节荷尔蒙和其它环境刺激或外源信号。MAPKKKα.MEK2和WIPK沉默烟草抑制了Nep1诱导的HR；MEK1、SIPK和NTF6沉默的本氏烟不影响harpin、Nep1和boehmerin诱导的HR.Nep1处理的基因沉默植株内,转录因子(WRKY2)和防卫基因(PR2b)的表达受抑制。WRKY2沉默后也抑制了Nep1诱导的HR,但不影响boehmerin和harpin诱导的HR。另外,MEK2-NTF6调节激发子诱导的H2O2积累；MEK2-WIPK调节Nep1诱导的NO积累,SIPK沉默削弱了激发子诱导的保卫细胞内NO积累。基因沉默烟草不影响激发子诱导的保卫细胞内Ca2+浓度和AOS积累。结果表明,MAPKKKα、MEK1、MEK2、WIPK、SIPK、NTF6和WRKY2参与调节激发子信号。综上,RBOH.VPE.G蛋白及MAPK调节激发子诱发的信号传递,揭示了不同激发子信号的保守性及复杂性。
Elicitors or pathogen-associated molecular patterns (PAMP) can trigger the plant immune system, leading to rapid programmed cell death (hypersensitive response, HR) and stomatal closure. Here, we describe the role of plant respiratory burst oxidase homologs (RBOH), vacuolar processing enzyme (VPE), heterotrimeric G-proteins (G proteins), and mitogen-activated protein kinase (MAPK) from Nicotiana benthamiana in response to three PAMPs:bacterial harpin, fungal Nepl, and oomycete boehmerin, induced HR and stomatal closure via virus-induced gene silencing. RBOH, VPE, and G protein can function in elicitor-induced stomatal closure. MAPKKKa-MEK2-WIPK play a role in Nepl-triggered HR. Ga, Gβ2, and VPE la are involved in harpin-induced HR. These results indicate signaling component is conserved in different elicitor-triggered stomatal closure. Despite this conservation, the complexity of elicitor signaling also exists.
RBOH play a prominent role in AOS production. NbrbohA was constitutively expressed at a low level, whereas NbrbohB was induced when protein elicitors exist (such as boehmerin, harpin, or INF1). We examined the HR cell death and pathogenesis-related (PR) gene expression of these single-silenced (NbrbohA or NbrbohB) and double-silenced (NbrbohA and NbrbohB) N. benthamiana plants, induced by various elicitors. The HR cell death and transcript accumulation of genes related to the defense response (PR1) were slightly affected, suggesting that RBOH are not essential for elicitor-induced HR and activation of these genes. Interestingly, gene-silenced plants impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production, but not elicitor-induced cytosolic calcium ion accumulation and elicitor-triggered AOS production in guard cells. These results indicate that RBOH from N. benthamiana function in elicitor-induced stomatal closure, but not in elicitor-induced HR.
VPE is a cysteine proteinase with the caspase-1-like activity. Although NbVPE silencing didn't affect H2O2 accumulation triggered by boehmerin, harpin, or Nep1, the HR was absent in NbVPE 1a-and NbVPEl a/1b-silenced plants treated with harpin alone. However, NbVPE-silenced plants developed a normal HR after boehmerin and Nepl treatment. These results suggest that harpin-triggered HR is VPE-dependent. Surprisingly, all gene-silenced plants showed significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. Dual-silenced plants showed elicitor-triggered AOS production in guard cells. The accumulation of transcripts associated with defense and cell redox was examined using semi-quantitive RT-PCR, and it was found that an Nbrboh gene and WKRY transcription factor are VPE-regulated. Overall, these results indicate that VPE from N. benthamiana functions not only in elicitor-induced HR, but also in elicitor-induced stomatal closure, suggesting that VPE may be involved in PAMP-triggered immunity (PTI).
Signaling through G proteins is a conserved mechanism found in all eukaryotes. Here, Ga, Gβ1, Gβ2, and AC cDNA were isolated. The HR was absent in Gα-and Gβ2-silenced plants treated with harpin alone. However, all the gene silenced plants developed a normal HR after boehmerin and Nep1 treatment. These results suggest that harpin-triggered HR is Ga and G02 dependent. Surprisingly, Gα, Gβ1, and Gβ2-silenced plants showed significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. It suggests elicitors signaling mechanisms are different. We show that both Gβsubunits, each provides functional selectivity to the plant heterotrimeric G proteins, revealing a mechanism underlying the complexity of G protein-mediated signaling in plants.
MAPK cascades are composed of three protein kinase modules:MAPKK kinases (MAPKKKs), MAPK kinases (MAPKKs), and MAPKs, which are linked in various ways to upstream receptors and downstream targets. Silencing of genes encoding a motigen-activated protein kinase (MAPK) WIPK, an MAPK kinase (MAPKK) MEK2, or an MAPK kinase kinase (MAPKKK) MAPKKKa attenuated Nepl-induced hypersensitive response (HR); two MAPK, SIPK and NTF6, an MAPKK, MEK1-silenced plants developed the normal HR after boehmerin, harpin or Nepl treatment. We also found the transcript accumulations of a WRKY2 transcription factor and a defense-related gene (PR2b) were down-regulated in all the gene-silenced plants after Nepl treatment. WRKY2-silencing also abolished Nepl-triggered HR, but not boehmerin and harpin. We also found MEK2-NTF6 participated in elicitor-induced H2O2 production and SIPK-silencing attenuated elicitor-induced NO production in guard cells.
Above all, the identification of these genes that play a role in elicitor signaling advances our knowledge of elicitor signaling, and it provides further evidence for the convergence and divergence of downstream signaling of different elicitors.
RBOH是最重要的活性氧(active oxygen species, AOS)来源之一。NbrbohA、NbrbohB单基因沉默,以及NrbohA和NbrbohB双基因沉默显著抑制了boehmerin、INF1和harpin等3种激发子诱发的叶片中H2O2积累,但不影响激发子诱导的HR,且基因沉默对激发子诱发的PR基因的转录没有影响；而这些基因沉默却抑制激发子诱导的气孔关闭,且保卫细胞内NO积累显著减少,但不影响保卫细胞内Ca2+浓度和AOS积累。说明RBOH参与激发子诱导的气孔关闭,但不参与激发子诱导的过敏反应和PR基因的转录；植物体内其它酶催化产生的AOS及AOS/NO平衡可能参与激发子诱发的过敏性细胞死亡。
VPE是植物液泡的半胱氨酸蛋白酶,具有类似动物caspases-1-like酶活性。本试验发现NbVPE1a和NbVPE1b单基因沉默,及NbVPE1a/1b双基因沉默不影响harpin、boehmerin和Nep1激发子诱发的H2O2积累,NbVPE1a和NbVPE1a/1b沉默却抑制了harpi(?)诱发的HR；而boehmerin和Nep1均可诱发这3种VPE沉默的植株产生正常的HR,表明harpir诱发的HR依赖于VPE,但是VPE不参与boehmerin和Nep1诱发的HR。单基因和双基因沉默均抑制3种激发子诱发的气孔关闭,且抑制了保卫细胞内NO的积累；3种激发子诱导处理后,单基因沉默植株叶片中保卫细胞内活性氧的积累与对照一致,但是双基因沉默植株中保卫细胞内AOS的量显著高于对照和单基因沉默植株中保卫细胞内AOS的量,表明双基因共同作用负调控保卫细胞内AOS的积累。进一步转录分析显示VPE调节了活性氧相关的基因(NbrbohB)和转录因子(WRKY2)的转录。而已证明气孔在植物免疫中具有重要功能,提示VPE参与PAMP触发的抗性(PAMP-triggered immunity,PTI).
G蛋白连接着细胞表面的受体和下游的效应因子,在植物多种信号途径中具有重要的作用。本研究克隆了N.benthamiana G蛋白Gα、Gβ1和Gβ2等基因及腺苷酸环化酶基因(adenylyl cyclase,AC),Gα和Gβ2沉默抑制细菌蛋白激发子harpin诱导的过敏反应;Gα、Gβ2、AC削弱了3种激发子诱发的H2O2积累。Gα、Gβ1、Gβ2沉默抑制激发子诱发的气孔关闭,且保卫细胞中NO的积累减少。但是AC因沉默对3种激发子诱发过敏反应和气孔关闭及保卫细胞内NO的积累均没有影响。结果表明G蛋白的Gα、Gβ亚基在不同激发子激发过敏反应和气孔关闭及NO和H2O2积累中作用存在差异。
MAPK信号级联途径包含三个保守的激酶,MAPK kinase kinase(MAPKKK或MEKK)磷酸化MAPK kinase(MAPKK或MEK)又磷酸化MAPK,调节荷尔蒙和其它环境刺激或外源信号。MAPKKKα.MEK2和WIPK沉默烟草抑制了Nep1诱导的HR；MEK1、SIPK和NTF6沉默的本氏烟不影响harpin、Nep1和boehmerin诱导的HR.Nep1处理的基因沉默植株内,转录因子(WRKY2)和防卫基因(PR2b)的表达受抑制。WRKY2沉默后也抑制了Nep1诱导的HR,但不影响boehmerin和harpin诱导的HR。另外,MEK2-NTF6调节激发子诱导的H2O2积累；MEK2-WIPK调节Nep1诱导的NO积累,SIPK沉默削弱了激发子诱导的保卫细胞内NO积累。基因沉默烟草不影响激发子诱导的保卫细胞内Ca2+浓度和AOS积累。结果表明,MAPKKKα、MEK1、MEK2、WIPK、SIPK、NTF6和WRKY2参与调节激发子信号。综上,RBOH.VPE.G蛋白及MAPK调节激发子诱发的信号传递,揭示了不同激发子信号的保守性及复杂性。
Elicitors or pathogen-associated molecular patterns (PAMP) can trigger the plant immune system, leading to rapid programmed cell death (hypersensitive response, HR) and stomatal closure. Here, we describe the role of plant respiratory burst oxidase homologs (RBOH), vacuolar processing enzyme (VPE), heterotrimeric G-proteins (G proteins), and mitogen-activated protein kinase (MAPK) from Nicotiana benthamiana in response to three PAMPs:bacterial harpin, fungal Nepl, and oomycete boehmerin, induced HR and stomatal closure via virus-induced gene silencing. RBOH, VPE, and G protein can function in elicitor-induced stomatal closure. MAPKKKa-MEK2-WIPK play a role in Nepl-triggered HR. Ga, Gβ2, and VPE la are involved in harpin-induced HR. These results indicate signaling component is conserved in different elicitor-triggered stomatal closure. Despite this conservation, the complexity of elicitor signaling also exists.
RBOH play a prominent role in AOS production. NbrbohA was constitutively expressed at a low level, whereas NbrbohB was induced when protein elicitors exist (such as boehmerin, harpin, or INF1). We examined the HR cell death and pathogenesis-related (PR) gene expression of these single-silenced (NbrbohA or NbrbohB) and double-silenced (NbrbohA and NbrbohB) N. benthamiana plants, induced by various elicitors. The HR cell death and transcript accumulation of genes related to the defense response (PR1) were slightly affected, suggesting that RBOH are not essential for elicitor-induced HR and activation of these genes. Interestingly, gene-silenced plants impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production, but not elicitor-induced cytosolic calcium ion accumulation and elicitor-triggered AOS production in guard cells. These results indicate that RBOH from N. benthamiana function in elicitor-induced stomatal closure, but not in elicitor-induced HR.
VPE is a cysteine proteinase with the caspase-1-like activity. Although NbVPE silencing didn't affect H2O2 accumulation triggered by boehmerin, harpin, or Nep1, the HR was absent in NbVPE 1a-and NbVPEl a/1b-silenced plants treated with harpin alone. However, NbVPE-silenced plants developed a normal HR after boehmerin and Nepl treatment. These results suggest that harpin-triggered HR is VPE-dependent. Surprisingly, all gene-silenced plants showed significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. Dual-silenced plants showed elicitor-triggered AOS production in guard cells. The accumulation of transcripts associated with defense and cell redox was examined using semi-quantitive RT-PCR, and it was found that an Nbrboh gene and WKRY transcription factor are VPE-regulated. Overall, these results indicate that VPE from N. benthamiana functions not only in elicitor-induced HR, but also in elicitor-induced stomatal closure, suggesting that VPE may be involved in PAMP-triggered immunity (PTI).
Signaling through G proteins is a conserved mechanism found in all eukaryotes. Here, Ga, Gβ1, Gβ2, and AC cDNA were isolated. The HR was absent in Gα-and Gβ2-silenced plants treated with harpin alone. However, all the gene silenced plants developed a normal HR after boehmerin and Nep1 treatment. These results suggest that harpin-triggered HR is Ga and G02 dependent. Surprisingly, Gα, Gβ1, and Gβ2-silenced plants showed significantly impaired elicitor-induced stomatal closure and elicitor-promoted nitric oxide (NO) production in guard cells. It suggests elicitors signaling mechanisms are different. We show that both Gβsubunits, each provides functional selectivity to the plant heterotrimeric G proteins, revealing a mechanism underlying the complexity of G protein-mediated signaling in plants.
MAPK cascades are composed of three protein kinase modules:MAPKK kinases (MAPKKKs), MAPK kinases (MAPKKs), and MAPKs, which are linked in various ways to upstream receptors and downstream targets. Silencing of genes encoding a motigen-activated protein kinase (MAPK) WIPK, an MAPK kinase (MAPKK) MEK2, or an MAPK kinase kinase (MAPKKK) MAPKKKa attenuated Nepl-induced hypersensitive response (HR); two MAPK, SIPK and NTF6, an MAPKK, MEK1-silenced plants developed the normal HR after boehmerin, harpin or Nepl treatment. We also found the transcript accumulations of a WRKY2 transcription factor and a defense-related gene (PR2b) were down-regulated in all the gene-silenced plants after Nepl treatment. WRKY2-silencing also abolished Nepl-triggered HR, but not boehmerin and harpin. We also found MEK2-NTF6 participated in elicitor-induced H2O2 production and SIPK-silencing attenuated elicitor-induced NO production in guard cells.
Above all, the identification of these genes that play a role in elicitor signaling advances our knowledge of elicitor signaling, and it provides further evidence for the convergence and divergence of downstream signaling of different elicitors.
引文
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