Launay Alban, Patrit Oriane, Wénès Estelle, Fagard Mathilde
CNRS 3559, Institut Jean-Pierre Bourgin, INRA, AgroParisTech, ERL, Université Paris-SaclayVersailles, France; Université Paris-Sud-Université Paris-SaclayOrsay, France.
AgroParisTech Paris, France.
Front Plant Sci. 2016 Apr 26;7:545. doi: 10.3389/fpls.2016.00545. eCollection 2016.
The bacterium Erwinia amylovora is responsible for the fire blight disease of Maleae, which provokes necrotic symptoms on aerial parts. The pathogenicity of this bacterium in hosts relies on its type three-secretion system (T3SS), a molecular syringe that allows the bacterium to inject effectors into the plant cell. E. amylovora-triggered disease in host plants is associated with the T3SS-dependent production of reactive oxygen species (ROS), although ROS are generally associated with resistance in other pathosystems. We showed previously that E. amylovora can multiply transiently in the non-host plant Arabidopsis thaliana and that a T3SS-dependent production of intracellular ROS occurs during this interaction. In the present work we characterize the localization and source of hydrogen peroxide accumulation following E. amylovora infection. Transmission electron microscope (TEM) analysis of infected tissues showed that hydrogen peroxide accumulation occurs in the cytosol, plastids, peroxisomes, and mitochondria as well as in the apoplast. Furthermore, TEM analysis showed that an E. amylovora dspA/E-deficient strain does not induce hydrogen peroxide accumulation in the apoplast. Consistently, a transgenic line expressing DspA/E accumulated ROS in the apoplast. The NADPH oxidase-deficient rbohD mutant showed a very strong reduction in hydrogen peroxide accumulation in response to E. amylovora inoculation. However, we did not find an increase in bacterial titers of E. amylovora in the rbohD mutant and the rbohD mutation did not suppress the toxicity of DspA/E when introgressed into a DspA/E-expressing transgenic line. Co-inoculation of E. amylovora with cycloheximide (CHX), which we found previously to suppress callose deposition and allow strong multiplication of E. amylovora in A. thaliana leaves, led to a strong reduction of apoplastic ROS accumulation but did not affect intracellular ROS. Our data strongly suggest that apoplastic ROS accumulation is one layer of the non-host defense response triggered by the type three effector (T3E) DspA/E, together with callose deposition.
解淀粉欧文氏菌(Erwinia amylovora)是导致苹果属植物火疫病的病原菌,该病会在地上部分引发坏死症状。这种细菌在宿主中的致病性依赖于其三型分泌系统(T3SS),这是一种分子注射器,可使细菌将效应蛋白注入植物细胞。尽管活性氧(ROS)在其他病理系统中通常与抗性相关,但解淀粉欧文氏菌引发的宿主植物病害与T3SS依赖的ROS产生有关。我们之前表明,解淀粉欧文氏菌可以在非宿主植物拟南芥中短暂繁殖,并且在这种相互作用过程中会发生T3SS依赖的细胞内ROS产生。在本研究中,我们对解淀粉欧文氏菌感染后过氧化氢积累的定位和来源进行了表征。对感染组织的透射电子显微镜(TEM)分析表明,过氧化氢积累发生在细胞质、质体、过氧化物酶体和线粒体以及质外体中。此外,TEM分析表明,解淀粉欧文氏菌dspA/E缺陷型菌株不会诱导质外体中过氧化氢的积累。一致地,表达DspA/E的转基因系在质外体中积累了ROS。NADPH氧化酶缺陷型rbohD突变体在接种解淀粉欧文氏菌后,过氧化氢积累显著减少。然而,我们没有发现解淀粉欧文氏菌在rbohD突变体中的细菌滴度增加,并且当将rbohD突变导入表达DspA/E的转基因系时,rbohD突变并未抑制DspA/E的毒性。我们之前发现环己酰亚胺(CHX)可抑制胼胝质沉积并使解淀粉欧文氏菌在拟南芥叶片中大量繁殖,将解淀粉欧文氏菌与CHX共同接种,导致质外体ROS积累显著减少,但不影响细胞内ROS。我们的数据强烈表明,质外体ROS积累是由三型效应蛋白(T3E)DspA/E触发的非宿主防御反应的一层,与胼胝质沉积一起。