The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.

The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity.
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DOI:
10.1371/journal.ppat.1002130
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发表时间:
2011-08
期刊:
影响因子:
6.7
通讯作者:
Vinatzer BA
Vinatzer BA
中科院分区:
医学1区
文献类型:
--
作者:
Cai R;Lewis J;Yan S;Liu H;Clarke CR;Campanile F;Almeida NF;Studholme DJ;Lindeberg M;Schneider D;Zaccardelli M;Setubal JC;Morales-Lizcano NP;Bernal A;Coaker G;Baker C;Bender CL;Leman S;Vinatzer BA

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最近,基因单态细菌人类病原体的许多分离株的基因组测序提供了新的见解病原体微进化和微地理。在这里,我们报告了一个基于基因组的微进化研究的细菌植物病原体,假单胞菌pv。番茄在5个测序的分离株中,在3,543,009 nt的基因组序列中仅鉴定出267个突变,这表明该病原体的进化起源较近。对89个全球分离株的基因组衍生标记的进一步分析表明,北美和欧洲存在几种基因型,表明这些世界地区之间的病原体频繁移动。基因组衍生的标记和分子分析的关键病原体位点的重要毒力和运动都表明正在进行的适应番茄宿主。在III型分泌的效应基因hopM 1中发现突变热点。这些突变消除了全长蛋白质的细胞死亡触发活性,表明对该效应子功能丧失的强烈选择,该效应子先前被认为是毒力因子。鞭毛蛋白编码基因fliC中的两个非同义突变允许在与已知的MAMP flg 22不同的区域中鉴定新的微生物相关分子模式(MAMP)。有趣的是,该MAMP的祖先等位基因比衍生的等位基因诱导更强的番茄免疫应答。祖先的等位基因已经基本上从今天的Pto人群中消失,这表明鞭毛蛋白触发的免疫限制了病原体的适应性,即使是在高毒力的病原体中。在南美分离株中,在flg 22中鉴定出另外的非同义突变。因此,MAMP比预期的更易变,甚至在相同病原体菌株的其他几乎相同的分离株之间也不同。在过去的五年里,我们对细菌性人类病原体的最新进化的了解急剧增加。相比之下,对细菌性植物病原体的最新进化知之甚少。在这里,我们分析了大量收集的经济上重要的植物病原体假单胞菌pv。番茄与标记来自比较五个基因组的这种病原体。我们发现,这种病原体可能在相对较近的时间尺度上进化,并通过最大限度地减少番茄免疫系统对其的识别来继续适应番茄。我们发现,鞭毛蛋白亚基fliC的等位基因在20世纪80年代首次出现在病原体群体中,并且是该基因在北美和欧洲最常见的等位基因,其引发的番茄免疫反应比20世纪60年代和70年代发现的fliC等位基因弱。这些结果不仅影响了我们对病原体-植物相互作用和病原体进化的理解,而且对疾病预防也有重要的影响。鉴于新的病原体菌株传播和取代现有菌株的速度,限制特定菌株在地理区域之间的移动至关重要,即使对于已知具有全球分布的病原体也是如此。
Recently, genome sequencing of many isolates of genetically monomorphic bacterial human pathogens has given new insights into pathogen microevolution and phylogeography. Here, we report a genome-based micro-evolutionary study of a bacterial plant pathogen, Pseudomonas syringae pv. tomato. Only 267 mutations were identified between five sequenced isolates in 3,543,009 nt of analyzed genome sequence, which suggests a recent evolutionary origin of this pathogen. Further analysis with genome-derived markers of 89 world-wide isolates showed that several genotypes exist in North America and in Europe indicating frequent pathogen movement between these world regions. Genome-derived markers and molecular analyses of key pathogen loci important for virulence and motility both suggest ongoing adaptation to the tomato host. A mutational hotspot was found in the type III-secreted effector gene hopM1. These mutations abolish the cell death triggering activity of the full-length protein indicating strong selection for loss of function of this effector, which was previously considered a virulence factor. Two non-synonymous mutations in the flagellin-encoding gene fliC allowed identifying a new microbe associated molecular pattern (MAMP) in a region distinct from the known MAMP flg22. Interestingly, the ancestral allele of this MAMP induces a stronger tomato immune response than the derived alleles. The ancestral allele has largely disappeared from today's Pto populations suggesting that flagellin-triggered immunity limits pathogen fitness even in highly virulent pathogens. An additional non-synonymous mutation was identified in flg22 in South American isolates. Therefore, MAMPs are more variable than expected differing even between otherwise almost identical isolates of the same pathogen strain. Our knowledge of the recent evolution of bacterial human pathogens has increased dramatically over the last five years. By comparison, relatively little is known about recent evolution of bacterial plant pathogens. Here, we analyze a large collection of isolates of the economically important plant pathogen Pseudomonas syringae pv. tomato with markers derived from the comparison of five genomes of this pathogen. We find that this pathogen likely evolved on a relatively recent time scale and continues to adapt to tomato by minimizing its recognition by the tomato immune system. We find that an allele of the flagellin subunit fliC that appeared in the pathogen population for the first time in the 1980s, and which is the most common allele of this gene in North America and Europe today, triggers a weaker tomato immune response than the fliC allele found in the 1960s and 1970s. These results not only impact our understanding of pathogen – plant interactions and pathogen evolution but also have important ramifications for disease prevention. Given the speed with which new pathogen strains spread and replace existing strains, limiting the movement of specific strains between geographic regions is critically important, even for pathogens known to have worldwide distribution.
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期刊: PloS one
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