Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1.
Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1.
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DOI：
10.1371/journal.ppat.1002975
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发表时间：
2012
期刊：
影响因子：
6.7
通讯作者：
Ishikawa M
中科院分区：
文献类型：
--
作者：
Ishibashi K;Mawatari N;Miyashita S;Kishino H;Meshi T;Ishikawa M
在病毒与其宿主之间的对抗性共同进化过程中，病毒因进化速度更快而具有主要优势。然而，病毒和它们的宿主共存并共同进化，尽管这一过程在很大程度上仍然未知。我们之前鉴定了 Tm-1，它赋予对番茄花叶病毒 (ToMV) 的抗性，并揭示它编码一种结合 ToMV 复制蛋白并抑制 RNA 复制的蛋白质。 Tm-1 是从野生番茄品种 Solanum habrochaites 渗入到栽培番茄品种 Solanum lycopersicum 中的。在这项研究中，我们分析了 S. habrochaites 中的 Tm-1 等位基因。尽管该基因的大部分处于纯化选择之下，但在一个小区域中发现了对抑制活性很重要的一组非同义取代，这表明该区域处于正选择之下。然后我们检查了 S. habrochaites 植物对 ToMV 的抗性。来自 24 个品种的 149 个个体中，大约 60% 对 ToMV 具有抗性，而其他个体在接种后积累了可检测水平的外壳蛋白。出乎意料的是，观察到许多 S. habrochaites 植物，其中甚至破坏 Tm-1 抗性的 ToMV 突变体 LT1 的增殖也受到抑制。 Tm-1 蛋白正选区域的氨基酸变化导致了 LT1 增殖的抑制。这种氨基酸变化使得 Tm-1 能够结合 LT1 复制蛋白，而不会失去结合野生型 ToMV 复制蛋白的能力。抗病毒谱和生化特性表明，Tm-1 的进化是通过改变其抑制活性的强度，而不是使识别谱多样化。在接种 LT1 的 LT1 抗性 S. habrochaites 植物中，出现了突变病毒，其增殖不受赋予 LT1 抗性的 Tm-1 等位基因抑制。然而，在缺乏 Tm-1 的情况下，抗性破坏突变体的竞争力低于亲本菌株。基于这些结果，我们讨论了 ToMV 和 Tm-1 可能的共同进化过程。病毒快速进化并适应其宿主生物，并且进化过程可以在实验室中重现（实验进化）。相比之下，细胞生物（可以是病毒宿主）的进化速度比病毒慢得多，但它们具有抗病毒系统的事实表明病毒和它们的宿主是共同进化的。为了探索病毒及其宿主的共同进化历史，我们重点关注了 Tm-1，这是一种赋予番茄花叶病毒 (ToMV) 抗性的 Solanum habrochaites 基因。基于对 S. habrochaites 中 Tm-1 基因序列的分析，我们证明该基因的一部分处于正选择之下。生化研究表明，Tm-1 的进化是为了增强其抑制活性，而不是为了使识别光谱多样化。此外，实验进化分析表明，通过 ToMV 克服 Tm-1 介导的抗性与适应成本相关。基于这些结果，我们讨论了 ToMV 和植物抗性基因如何共同进化。
During antagonistic coevolution between viruses and their hosts, viruses have a major advantage by evolving more rapidly. Nevertheless, viruses and their hosts coexist and have coevolved, although the processes remain largely unknown. We previously identified Tm-1 that confers resistance to Tomato mosaic virus (ToMV), and revealed that it encodes a protein that binds ToMV replication proteins and inhibits RNA replication. Tm-1 was introgressed from a wild tomato species Solanum habrochaites into the cultivated tomato species Solanum lycopersicum. In this study, we analyzed Tm-1 alleles in S. habrochaites. Although most part of this gene was under purifying selection, a cluster of nonsynonymous substitutions in a small region important for inhibitory activity was identified, suggesting that the region is under positive selection. We then examined the resistance of S. habrochaites plants to ToMV. Approximately 60% of 149 individuals from 24 accessions were resistant to ToMV, while the others accumulated detectable levels of coat protein after inoculation. Unexpectedly, many S. habrochaites plants were observed in which even multiplication of the Tm-1-resistance-breaking ToMV mutant LT1 was inhibited. An amino acid change in the positively selected region of the Tm-1 protein was responsible for the inhibition of LT1 multiplication. This amino acid change allowed Tm-1 to bind LT1 replication proteins without losing the ability to bind replication proteins of wild-type ToMV. The antiviral spectra and biochemical properties suggest that Tm-1 has evolved by changing the strengths of its inhibitory activity rather than diversifying the recognition spectra. In the LT1-resistant S. habrochaites plants inoculated with LT1, mutant viruses emerged whose multiplication was not inhibited by the Tm-1 allele that confers resistance to LT1. However, the resistance-breaking mutants were less competitive than the parental strains in the absence of Tm-1. Based on these results, we discuss possible coevolutionary processes of ToMV and Tm-1. Viruses rapidly evolve and adapt to their host organisms, and the evolutionary processes can be reproduced in the laboratory (experimental evolution). In contrast, cellular organisms (that can be viral hosts) evolve much more slowly than viruses, but the fact that they have antiviral systems suggests that viruses and their hosts have coevolved. To explore the coevolutionary histories of viruses and their hosts, we focused on Tm-1, a Solanum habrochaites gene that confers resistance to Tomato mosaic virus (ToMV). Based on analyses of the Tm-1 gene sequences in S. habrochaites, we demonstrated that a part of the gene has been under positive selection. Biochemical studies suggested that Tm-1 has evolved to strengthen its inhibitory activity rather than to diversify recognition spectra. In addition, experimental evolution analyses suggested that overcoming the Tm-1-mediated resistance by ToMV is associated with fitness costs. Based on these results, we discuss how ToMV and the plant resistance gene have coevolved.
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