Horizontal gene transfer of a syp homolog contributes to the virulence of Burkholderia glumae

doi:10.1016/S2095-3119(20)63553-5

Journal of Integrative Agriculture ›› 2021, Vol. 20 ›› Issue (12): 3222-3229.DOI: 10.1016/S2095-3119(20)63553-5

所属专题：植物抗病遗传合辑Plant Disease-resistance Genetics

收稿日期:2020-09-29 出版日期:2021-12-01 发布日期:2021-10-20

Horizontal gene transfer of a syp homolog contributes to the virulence of Burkholderia glumae

WANG Sai^1*, WANG Pei-hong^1*, NIE Wen-han¹, CUI Zhou-qi², LI Hong-yu¹, WU Yan¹, Ayizekeranmu YIMING¹, FU Luo-yi¹, Iftikhar AHMAD^{1, 3}, CHEN Gong-you¹, ZHU Bo¹

¹School of Agriculture and Biology, Shanghai Jiao Tong University/Key Laboratory of Urban Agriculture of the Ministry of Agriculture and Rural Affairs, Shanghai 200240, P.R.China
² Department of Plant Pathology & Ecology, the Connecticut Agricultural Experiment Station, New Haven 06504, CT, USA
³ Department of Environmental Sciences, COMSATS University Islamabad, Vehari-Campus, Vehari 61100, Pakistan

Received:2020-09-29 Online:2021-12-01 Published:2021-10-20
Contact: Correspondence ZHU Bo, E-mail: bzhu1981@sjtu.edu.cn
About author:WANG Sai, E-mail: wangsai@sjtu.edu.cn; * These authors contributed equally to this study.
Supported by:
This work was supported by the National Key R&D Program of China (2018YFD0201202 and 2017YFD0201108), the Agri-X Interdisciplinary Fund of Shanghai Jiao Tong University, China (Agri-X2017010), the State Key Laboratory for Biology of Plant Diseases and Insect Pests of Shanghai Jiao Tong University (SKLOF201802), the Shanghai Committee of Science and Technology (19390743300), the National Natural Science Foundation of China (31200003 and 31770772), and Joint Research Funds for Translational Medicine at Shanghai Jiao Tong University (ZH2018ZDA06).

摘要/Abstract

摘要：

水稻细菌性穗枯病又称水稻细菌性谷枯病，是一种由颖壳伯克氏菌 (Burkholderia glumae) 引起的严重的水稻种传病害，对全球水稻生产和食品安全造成了巨大威胁。由于缺乏对B. glumae在植物宿主中的适应性和发病机制的深入了解，迄今生产上还没有有效的防治措施。水平基因转移 (HGT) 已被证明是原核生物进化的主要驱动力。先前对60个Burkholderia全基因组的比较分析推断，大多数Burkholderia基因在其进化过程中至少经历过一次HGT，并在其菌株分化和致病性决定因素中起着重要作用。在本研究中，我们通过对LMG 2196菌株进行全基因组分析，鉴定到了42个潜在的水平转移基因。其中，一个注释为非核糖体肽合成酶(KS03_RS09665)的基因被确定为候选基因。进一步通过系统进化树的建立，发现该基因仅出现在与植物致病相关的Burkholderia菌属，并且在进化分枝上更接近于假单胞菌(Pseudomonas)中编码丁香肽合成酶(SypA)的sypA基因。为研究该基因在B. glumae致病性中的潜在作用，我们构建了syp基因缺失突变株。表型观察结果表明，sypA基因参与调控了该病菌的游动性、生物膜的形成、类似丁香肽代谢物的合成和致病性等重要生理表型。其中，与野生型菌株接种稻穗相比，sypA突变体接种稻穗后发病指数降低了20%。另外，与野生型菌株相比，sypA缺失突变菌株表现为游动能力显著下降、生物膜形成和类似丁香肽代谢物的合成受到抑制。综上所述，本研究探讨了水平转移基因sypA在颖壳伯克氏菌毒力中的作用。结果表明，sypA基因可能参与了颖壳伯克氏菌毒性物质丁香肽的合成，并且正向调控了其游动性和生物膜的形成，从而参与了颖壳伯克氏菌的致病力。本研究的结果强调了在颖壳伯克氏菌进化过程中，HGT现象对其毒力和适应性影响的可能性。

Abstract:

Horizontal gene transfer (HGT) has been proved a major driving force in prokaryotic evolution. However, the molecular functions of these transferred genes in pathogenic bacteria especially plant pathogenic bacteria are still not fully investigated. In this study, the whole-genome in silico analysis was performed and found a syringopeptin synthetase (syp) homolog in Burkholderia glumae, which can cause bacterial panicle blight in rice, was predicted to be horizontally transferred from Pseudomonas ancestor with solid confidence by phylogenetic analysis. The comprehensive molecular experiments were performed to study the potential role of this gene in B. glumae. Inoculation of rice panicles with the syp mutant resulted in 60% lower disease index compared with the wild type (WT) parent strain, suggesting the requirement of syp for the full virulence of B. glumae. Chromatography analysis of exudates from B. glumae showed suppression of synthesis of metabolites analogous to syringopeptin in the mutants. All these data raise the possibility of HGT phenomenon in shaping the virulence and adaptation of B. glumae over evolutionary time.

Key words: horizontal gene transfer , burkholderia glumae , syringopeptin synthetase

. [J]. Journal of Integrative Agriculture, 2021, 20(12): 3222-3229.

WANG Sai, WANG Pei-hong, NIE Wen-han, CUI Zhou-qi, LI Hong-yu, WU Yan, Ayizekeranmu YIMING, FU Luo-yi, Iftikhar AHMAD, CHEN Gong-you, ZHU Bo. Horizontal gene transfer of a syp homolog contributes to the virulence of Burkholderia glumae[J]. Journal of Integrative Agriculture, 2021, 20(12): 3222-3229.

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Horizontal gene transfer of a syp homolog contributes to the virulence of Burkholderia glumae

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