{"title":"A Comprehensive Review on Oxidative Stress and ROS-Related Resistance Strategies in Compatible Interaction Between Erwinia amylovora and Host Plants","authors":"Hamid Abdollahi, Jaber Nasiri, Sadegh Mohajer","doi":"10.1007/s00344-024-11482-w","DOIUrl":null,"url":null,"abstract":"<p>The fire blight, a withering and scorched appearance of trees infected with <i>Erwinia amylovora</i>, is assumed as one of the most destructive and contagious disease adversely affecting pome fruit trees worldwide. The bacterium of <i>E. amylovora</i> elicits reactive oxygen species (ROS) generation followed by rapid oxidative bursts during both compatible and incompatible interactions in host and non-host plants, respectively. These interactions occur because of the stimulation and expression of numerous <i>hrp</i>, <i>hrc</i>, <i>dsp</i>, <i>eop</i>, and <i>avr</i> genes in the pathogen's Hrp pathogenicity island followed by the subsequent secretion of effector proteins into host cells via type three secretion systems (T3SS). The <i>E. amylovora’s</i> secretome triggers oxidative burst in host and non-host tissues with different range of severities and various spatiotemporal patterns. Subsequently, numerous responses including hypersensitive reactions (HR) as absolute resistance in non-host plants (owing to the suppression of systemic acquired resistance; SAR) together with a range of disease resistance in host plants rating from highly resistance to fully susceptible (because of SAR suppression/activation) are normally appeared. In the battle between the hosts and <i>E. amylovora</i>, the former try to neutralize destructive effects of the pathogen via applying enzymatic and/or non-enzymatic ROS scavenging mechanisms, while the latter try to overcome the hosts mainly through recruiting two pathogenicity mechanisms of “ROS (oxidative burst)-independent pathogenicity factors” (i.e., levan, sucrose, and sorbitol) and “ROS (oxidative burst)-dependent pathogenicity elements” (i.e., secretion of effector proteins followed by protective mechanisms such as amylovoran and siderophores biosynthesis). In host plants, the activation/suppression of defense mechanisms regularly results in a multilateral of responses including ROS generation, particularly OH<sup>·−</sup> formation from H<sub>2</sub>O<sub>2</sub>, lipid peroxidation, electrolyte leakage and ultimately tissue necrosis. Depending on the host ability either to produce higher amounts of H<sub>2</sub>O<sub>2</sub> or to scavenge O<sub>2</sub><sup>·−</sup> and H<sub>2</sub>O<sub>2</sub>, two different resistance mechanisms of I and II could be concluded, respectively. This review was aimed to systematically detail the aforesaid two different pathogenicity mechanisms of <i>E. amylovora</i> in host tissues. Furthermore, diverse roles of ROS generation/scavenging during compatible interactions between hosts and <i>E. amylovora</i>, with an emphasis on various ROS sources in host cells (i.e., chloroplast and mitochondria organelles), the distinct functions of the various ROS, and ultimately their dual roles in acquiring diverse ranges of resistancibility to susceptibility to fire blight are discussed. Finally, the potential antioxidative function and protective actions of plant enzymes together with plant secondary metabolites to moderate/minimize deleterious side effects of the pathogen in the course of invasion are explained as “enzymatic/non-enzymatic ROS scavenging mechanisms”.</p>","PeriodicalId":16842,"journal":{"name":"Journal of Plant Growth Regulation","volume":null,"pages":null},"PeriodicalIF":3.9000,"publicationDate":"2024-09-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Plant Growth Regulation","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1007/s00344-024-11482-w","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
The fire blight, a withering and scorched appearance of trees infected with Erwinia amylovora, is assumed as one of the most destructive and contagious disease adversely affecting pome fruit trees worldwide. The bacterium of E. amylovora elicits reactive oxygen species (ROS) generation followed by rapid oxidative bursts during both compatible and incompatible interactions in host and non-host plants, respectively. These interactions occur because of the stimulation and expression of numerous hrp, hrc, dsp, eop, and avr genes in the pathogen's Hrp pathogenicity island followed by the subsequent secretion of effector proteins into host cells via type three secretion systems (T3SS). The E. amylovora’s secretome triggers oxidative burst in host and non-host tissues with different range of severities and various spatiotemporal patterns. Subsequently, numerous responses including hypersensitive reactions (HR) as absolute resistance in non-host plants (owing to the suppression of systemic acquired resistance; SAR) together with a range of disease resistance in host plants rating from highly resistance to fully susceptible (because of SAR suppression/activation) are normally appeared. In the battle between the hosts and E. amylovora, the former try to neutralize destructive effects of the pathogen via applying enzymatic and/or non-enzymatic ROS scavenging mechanisms, while the latter try to overcome the hosts mainly through recruiting two pathogenicity mechanisms of “ROS (oxidative burst)-independent pathogenicity factors” (i.e., levan, sucrose, and sorbitol) and “ROS (oxidative burst)-dependent pathogenicity elements” (i.e., secretion of effector proteins followed by protective mechanisms such as amylovoran and siderophores biosynthesis). In host plants, the activation/suppression of defense mechanisms regularly results in a multilateral of responses including ROS generation, particularly OH·− formation from H2O2, lipid peroxidation, electrolyte leakage and ultimately tissue necrosis. Depending on the host ability either to produce higher amounts of H2O2 or to scavenge O2·− and H2O2, two different resistance mechanisms of I and II could be concluded, respectively. This review was aimed to systematically detail the aforesaid two different pathogenicity mechanisms of E. amylovora in host tissues. Furthermore, diverse roles of ROS generation/scavenging during compatible interactions between hosts and E. amylovora, with an emphasis on various ROS sources in host cells (i.e., chloroplast and mitochondria organelles), the distinct functions of the various ROS, and ultimately their dual roles in acquiring diverse ranges of resistancibility to susceptibility to fire blight are discussed. Finally, the potential antioxidative function and protective actions of plant enzymes together with plant secondary metabolites to moderate/minimize deleterious side effects of the pathogen in the course of invasion are explained as “enzymatic/non-enzymatic ROS scavenging mechanisms”.
期刊介绍:
The Journal of Plant Growth Regulation is an international publication featuring original articles on all aspects of plant growth and development. We welcome manuscripts reporting question-based research on various aspects of plant growth and development using hormonal, physiological, environmental, genetic, biophysical, developmental and/or molecular approaches.
The journal also publishes timely reviews on highly relevant areas and/or studies in plant growth and development, including interdisciplinary work with an emphasis on plant growth, plant hormones and plant pathology or abiotic stress.
In addition, the journal features occasional thematic issues with special guest editors, as well as brief communications describing novel techniques and meeting reports.
The journal is unlikely to accept manuscripts that are purely descriptive in nature or reports work with simple tissue culture without attempting to investigate the underlying mechanisms of plant growth regulation, those that focus exclusively on microbial communities, or deal with the (elicitation by plant hormones of) synthesis of secondary metabolites.