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Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1.

Ishibashi K, Mawatari N, Miyashita S, Kishino H, Meshi T, Ishikawa M - PLoS Pathog. (2012)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Division of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba, Japan. bashi@affrc.go.jp

ABSTRACT
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.

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Model of the hierarchical interactions between ToMV and Tm-1.The horizontal axis indicates the insensitivity (i.e., weakness of binding to) of the tobamovirus replication proteins to Tm-1. The vertical axis indicates fitness of tobamoviruses in Tm-1-lacking hosts. The dashed lines represent thresholds that determine whether viruses can infect plants harboring tm-1GCR26, Tm-1GCR237, or Tm-1I91T. Schematic representation of the inhibitory activities of tm-1GCR26, Tm-1GCR237, and Tm-1I91T are shown at the bottom. Whether ToMV-L evolved from a tm-1-sensitive prototype remains unknown, although TMGMV evolved to TMGMV-T894M,F970Y in the presence of tm-1GCR26 with apparent fitness costs [30], [41].
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ppat-1002975-g008: Model of the hierarchical interactions between ToMV and Tm-1.The horizontal axis indicates the insensitivity (i.e., weakness of binding to) of the tobamovirus replication proteins to Tm-1. The vertical axis indicates fitness of tobamoviruses in Tm-1-lacking hosts. The dashed lines represent thresholds that determine whether viruses can infect plants harboring tm-1GCR26, Tm-1GCR237, or Tm-1I91T. Schematic representation of the inhibitory activities of tm-1GCR26, Tm-1GCR237, and Tm-1I91T are shown at the bottom. Whether ToMV-L evolved from a tm-1-sensitive prototype remains unknown, although TMGMV evolved to TMGMV-T894M,F970Y in the presence of tm-1GCR26 with apparent fitness costs [30], [41].

Mentions: We demonstrated that interactions between ToMV mutants and Tm-1 variants are hierarchical. The hierarchical classification may also apply to other tobamoviruses; the multiplication of tm-1GCR26-sensitive TMGMV and PMMoV are also inhibited by Tm-1GCR237[30], and a TMGMV mutant that can replicate in the presence of tm-1GCR26 (TMGMV-T894M,F970Y) cannot overcome the resistance by Tm-1GCR237 (K.I. and M.I., unpublished result). Thus, wild-type TMGMV and TMGMV-T894M,F970Y are categorized into the TLIle class and ToMV-L class, respectively (Figure 8). Based on these considerations and the results of in vitro RNA replication inhibition by Tm-1 variants, we suggest that the relative strengths of binding to the replication proteins and inhibition of RNA replication by each Tm-1 protein variant decreases in the order of TLIle, TMGMV>ToMV-L, TMGMV-T894M,F970Y>LT1>T21, LT1E979K, and LT1D1097Y (Figure 8). Additionally, for each ToMV variant, the binding strengths to the replication proteins and inhibition of RNA replication by Tm-1 variants decrease in the order of Tm-1I91T>Tm-1GCR237>tm-1GCR26 (Figure 8). Under selective pressure by tobamoviruses, Tm-1 may have modified the strength of its inhibitory activity, but not diversified the recognition spectra.


Coevolution and hierarchical interactions of Tomato mosaic virus and the resistance gene Tm-1.

Ishibashi K, Mawatari N, Miyashita S, Kishino H, Meshi T, Ishikawa M - PLoS Pathog. (2012)

Model of the hierarchical interactions between ToMV and Tm-1.The horizontal axis indicates the insensitivity (i.e., weakness of binding to) of the tobamovirus replication proteins to Tm-1. The vertical axis indicates fitness of tobamoviruses in Tm-1-lacking hosts. The dashed lines represent thresholds that determine whether viruses can infect plants harboring tm-1GCR26, Tm-1GCR237, or Tm-1I91T. Schematic representation of the inhibitory activities of tm-1GCR26, Tm-1GCR237, and Tm-1I91T are shown at the bottom. Whether ToMV-L evolved from a tm-1-sensitive prototype remains unknown, although TMGMV evolved to TMGMV-T894M,F970Y in the presence of tm-1GCR26 with apparent fitness costs [30], [41].
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3475678&req=5

ppat-1002975-g008: Model of the hierarchical interactions between ToMV and Tm-1.The horizontal axis indicates the insensitivity (i.e., weakness of binding to) of the tobamovirus replication proteins to Tm-1. The vertical axis indicates fitness of tobamoviruses in Tm-1-lacking hosts. The dashed lines represent thresholds that determine whether viruses can infect plants harboring tm-1GCR26, Tm-1GCR237, or Tm-1I91T. Schematic representation of the inhibitory activities of tm-1GCR26, Tm-1GCR237, and Tm-1I91T are shown at the bottom. Whether ToMV-L evolved from a tm-1-sensitive prototype remains unknown, although TMGMV evolved to TMGMV-T894M,F970Y in the presence of tm-1GCR26 with apparent fitness costs [30], [41].
Mentions: We demonstrated that interactions between ToMV mutants and Tm-1 variants are hierarchical. The hierarchical classification may also apply to other tobamoviruses; the multiplication of tm-1GCR26-sensitive TMGMV and PMMoV are also inhibited by Tm-1GCR237[30], and a TMGMV mutant that can replicate in the presence of tm-1GCR26 (TMGMV-T894M,F970Y) cannot overcome the resistance by Tm-1GCR237 (K.I. and M.I., unpublished result). Thus, wild-type TMGMV and TMGMV-T894M,F970Y are categorized into the TLIle class and ToMV-L class, respectively (Figure 8). Based on these considerations and the results of in vitro RNA replication inhibition by Tm-1 variants, we suggest that the relative strengths of binding to the replication proteins and inhibition of RNA replication by each Tm-1 protein variant decreases in the order of TLIle, TMGMV>ToMV-L, TMGMV-T894M,F970Y>LT1>T21, LT1E979K, and LT1D1097Y (Figure 8). Additionally, for each ToMV variant, the binding strengths to the replication proteins and inhibition of RNA replication by Tm-1 variants decrease in the order of Tm-1I91T>Tm-1GCR237>tm-1GCR26 (Figure 8). Under selective pressure by tobamoviruses, Tm-1 may have modified the strength of its inhibitory activity, but not diversified the recognition spectra.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Division of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba, Japan. bashi@affrc.go.jp

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus