Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens.
Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens.
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DOI：
10.1371/journal.ppat.1002137
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发表时间：
2011-07
期刊：
影响因子：
6.7
通讯作者：
Ma LJ
中科院分区：
文献类型：
--
作者：
Klosterman SJ;Subbarao KV;Kang S;Veronese P;Gold SE;Thomma BP;Chen Z;Henrissat B;Lee YH;Park J;Garcia-Pedrajas MD;Barbara DJ;Anchieta A;de Jonge R;Santhanam P;Maruthachalam K;Atallah Z;Amyotte SG;Paz Z;Inderbitzin P;Hayes RJ;Heiman DI;Young S;Zeng Q;Engels R;Galagan J;Cuomo CA;Dobinson KF;Ma LJ
维管束枯萎病真菌大丽黄萎病菌和白花黄萎病菌感染 200 多种植物，每年造成数十亿美元的农作物损失。典型的枯萎症状是木质部血管中病原体定植和增殖的结果，木质部血管的渗透压发生波动。为了深入了解赋予生物体致病性并使其能够在植物维管系统独特的生态位中增殖的机制，我们对大丽葡萄球菌和白色葡萄球菌的基因组进行了测序，并将它们相互比较，并与另一种真菌枯萎病病原体尖孢镰刀菌的基因组进行比较。我们的分析确定了所有三种枯萎病病原体共有的一组蛋白质，并且存在于少数其他真菌物种中。其中之一是细菌葡萄糖基转移酶的同系物，它在细菌中合成毒力相关的渗透调节周质葡聚糖。相应的大丽弧菌葡萄糖基转移酶基因缺失突变体的致病性测试表明，该基因是澳大利亚烟草物种本塞姆氏烟草中完全毒力所必需的。与其他真菌相比，这两个已测序的黄萎病基因组编码更多的果胶降解酶和其他碳水化合物活性酶，表明其具有非凡的降解植物果胶屏障的能力。两个黄萎病菌组装体之间的高水平同线性突出了大丽黄萎病菌中的四个灵活的基因组岛，这些岛富含转座元件，并且包含重复的基因和在信号/转录调节和铁/脂质代谢中重要的基因。再加上降解植物材料的能力增强，这些基因组岛可能有助于扩大大丽弧菌（黄萎病的主要致病菌）的遗传多样性和毒力。值得注意的是，我们的研究揭示了对真菌枯萎病病原体生态位适应的遗传机制的见解，增进了我们对其发病机制的进化和发展的理解，并揭示了开发新的疾病管理策略以对抗破坏性枯萎病的潜在途径。维管束枯萎病是一种慢性且常常是严重的植物病害，每年造成数十亿美元的农作物损失。典型的枯萎症状是病原微生物在植物木质部（水传导系统）中定殖和增殖引起的水阻塞的结果。我们对两种黄萎病病原体的基因组进行了测序，并将它们与另一种枯萎真菌尖镰孢的基因组进行了比较。这三种枯萎真菌之间共有的基因组特征表明，通过水平转移获得了细菌葡萄糖基转移酶的同源物，参与对渗透胁迫的适应。对大丽黄萎病中葡萄糖基转移酶基因缺失突变体的分析表明，宿主植物本塞姆氏烟草的毒力降低。与其他真菌相比，两种黄萎病基因组编码更多的植物细胞壁降解酶，包括那些能够降解活植物细胞壁的酶。在两个密切相关的黄萎病基因组之间，我们在黄萎病的主要致病因子大丽黄萎病中发现了灵活的基因组岛。再加上令人印象深刻的植物细胞壁降解酶库，这些灵活的基因组岛可能有助于扩大这种生物体的遗传多样性，从而入侵更多的植物宿主。总之，我们的研究揭示了对真菌性枯萎病病原体的进化和生态位适应的见解，并为对抗破坏性枯萎病的新型疾病管理策略的发展提供了线索。
The vascular wilt fungi Verticillium dahliae and V. albo-atrum infect over 200 plant species, causing billions of dollars in annual crop losses. The characteristic wilt symptoms are a result of colonization and proliferation of the pathogens in the xylem vessels, which undergo fluctuations in osmolarity. To gain insights into the mechanisms that confer the organisms' pathogenicity and enable them to proliferate in the unique ecological niche of the plant vascular system, we sequenced the genomes of V. dahliae and V. albo-atrum and compared them to each other, and to the genome of Fusarium oxysporum, another fungal wilt pathogen. Our analyses identified a set of proteins that are shared among all three wilt pathogens, and present in few other fungal species. One of these is a homolog of a bacterial glucosyltransferase that synthesizes virulence-related osmoregulated periplasmic glucans in bacteria. Pathogenicity tests of the corresponding V. dahliae glucosyltransferase gene deletion mutants indicate that the gene is required for full virulence in the Australian tobacco species Nicotiana benthamiana. Compared to other fungi, the two sequenced Verticillium genomes encode more pectin-degrading enzymes and other carbohydrate-active enzymes, suggesting an extraordinary capacity to degrade plant pectin barricades. The high level of synteny between the two Verticillium assemblies highlighted four flexible genomic islands in V. dahliae that are enriched for transposable elements, and contain duplicated genes and genes that are important in signaling/transcriptional regulation and iron/lipid metabolism. Coupled with an enhanced capacity to degrade plant materials, these genomic islands may contribute to the expanded genetic diversity and virulence of V. dahliae, the primary causal agent of Verticillium wilts. Significantly, our study reveals insights into the genetic mechanisms of niche adaptation of fungal wilt pathogens, advances our understanding of the evolution and development of their pathogenesis, and sheds light on potential avenues for the development of novel disease management strategies to combat destructive wilt diseases. Vascular wilts are chronic and very often severe plant diseases that cause billions of dollars in annual crop losses. The characteristic wilt symptom is a result of water blockage caused by the colonization and proliferation of pathogenic microbes in the plant xylem, a water-conducting system. We sequenced genomes of two Verticillium wilt pathogens and compared them to the genome of another wilt fungus, Fusarium oxysporum. The shared genomic features among these three wilt fungi suggest the acquisition of homologs of a bacterial glucosyltransferase, involved in adaptation to osmotic stress, through horizontal transfer. Analyses of glucosyltransferase gene deletion mutants in Verticillium dahliae revealed decreased virulence in the host plant Nicotiana benthamiana. Compared to other fungi, both Verticillium genomes encode more plant cell wall degrading enzymes, including those that are able to degrade cell walls of live plants. Between the two closely related Verticillium genomes, we discovered flexible genomic islands in the primary causal agent of Verticillium wilts, Verticillium dahliae. Coupled with the impressive arsenal of plant cell wall-degrading enzymes, these flexible genomic islands may have contributed to expanding genetic diversity for this organism to invade more plant hosts. In summary, our study reveals insights into the evolution and niche adaptation of fungal wilt pathogens and sheds light on the development of novel disease management strategies for combating the destructive wilt diseases.
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