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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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Schematic representation of ToMV mutant genomes with different sensitivities to Tm-1 alleles.Positions of amino acid residue changes in Tm-1-resistance-breaking mutants are shown. Amino acid residues identical to ToMV-L are indicated by dots. LT1 and T21 are Tm-1GCR237-breaking mutants [20], [28] and TLIle is a tm-1GCR26-sensitive mutant [30], [50]. LT1E979K and LT1D1097Y were characterized in this study. MT: methyltransferase domain, Hel: helicase domain, Pol: RNA-dependent RNA polymerase domain, CP: coat protein.
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ppat-1002975-g001: Schematic representation of ToMV mutant genomes with different sensitivities to Tm-1 alleles.Positions of amino acid residue changes in Tm-1-resistance-breaking mutants are shown. Amino acid residues identical to ToMV-L are indicated by dots. LT1 and T21 are Tm-1GCR237-breaking mutants [20], [28] and TLIle is a tm-1GCR26-sensitive mutant [30], [50]. LT1E979K and LT1D1097Y were characterized in this study. MT: methyltransferase domain, Hel: helicase domain, Pol: RNA-dependent RNA polymerase domain, CP: coat protein.

Mentions: Tobacco mosaic virus, Tomato mosaic virus (ToMV), Tobacco mild green mosaic virus (TMGMV), and Pepper mild mottle virus (PMMoV) are positive-strand RNA viruses belonging to the genus Tobamovirus. The tobamovirus genome encodes at least four proteins, namely, the 130K protein, the 180K protein (translational read-through product of the 130K protein), the 30K protein, and the coat protein (CP) (Figure 1). The 130K and 180K proteins are involved in RNA replication [6] and are collectively referred to here as replication proteins. The 130K protein is a multifunctional protein that interacts with many host proteins [7], as well as small RNA duplexes to function as a suppressor of RNA silencing [8]–[10]. The 30K protein is required for cell-to-cell movement [11], [12]. The CP is the only structural protein and required for systemic spread of the virus [13].


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)

Schematic representation of ToMV mutant genomes with different sensitivities to Tm-1 alleles.Positions of amino acid residue changes in Tm-1-resistance-breaking mutants are shown. Amino acid residues identical to ToMV-L are indicated by dots. LT1 and T21 are Tm-1GCR237-breaking mutants [20], [28] and TLIle is a tm-1GCR26-sensitive mutant [30], [50]. LT1E979K and LT1D1097Y were characterized in this study. MT: methyltransferase domain, Hel: helicase domain, Pol: RNA-dependent RNA polymerase domain, CP: coat protein.
© Copyright Policy
Related In: Results  -  Collection

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

ppat-1002975-g001: Schematic representation of ToMV mutant genomes with different sensitivities to Tm-1 alleles.Positions of amino acid residue changes in Tm-1-resistance-breaking mutants are shown. Amino acid residues identical to ToMV-L are indicated by dots. LT1 and T21 are Tm-1GCR237-breaking mutants [20], [28] and TLIle is a tm-1GCR26-sensitive mutant [30], [50]. LT1E979K and LT1D1097Y were characterized in this study. MT: methyltransferase domain, Hel: helicase domain, Pol: RNA-dependent RNA polymerase domain, CP: coat protein.
Mentions: Tobacco mosaic virus, Tomato mosaic virus (ToMV), Tobacco mild green mosaic virus (TMGMV), and Pepper mild mottle virus (PMMoV) are positive-strand RNA viruses belonging to the genus Tobamovirus. The tobamovirus genome encodes at least four proteins, namely, the 130K protein, the 180K protein (translational read-through product of the 130K protein), the 30K protein, and the coat protein (CP) (Figure 1). The 130K and 180K proteins are involved in RNA replication [6] and are collectively referred to here as replication proteins. The 130K protein is a multifunctional protein that interacts with many host proteins [7], as well as small RNA duplexes to function as a suppressor of RNA silencing [8]–[10]. The 30K protein is required for cell-to-cell movement [11], [12]. The CP is the only structural protein and required for systemic spread of the virus [13].

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