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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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A small region of the Tm-1 gene is under positive selection in S. habrochaites.(A) Predicted domain structure of the Tm-1 protein by the NCBI Conserved Domain Database. A region encoded by the alternative exon (46–263) is underlined. (B) Detection of natural selection in the Tm-1 alleles from S. habrochaites. The ratio of nonsynonymous/synonymous substitutions (ω) in each codon was inferred by omegaMap [33]. ω>1, ω = 1, and ω<1 suggest positive selection, neutral evolution, and negative selection, respectively. The region where posterior probability of positive selection (ω>1) exceeds 95% is indicated (from 79th to 112th codon). (C) Sliding window analysis of Tajima's D of the Tm-1 alleles from S. habrochaites. The confidence limits of D for neutral evolution [35] are shown as dashed lines.
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ppat-1002975-g002: A small region of the Tm-1 gene is under positive selection in S. habrochaites.(A) Predicted domain structure of the Tm-1 protein by the NCBI Conserved Domain Database. A region encoded by the alternative exon (46–263) is underlined. (B) Detection of natural selection in the Tm-1 alleles from S. habrochaites. The ratio of nonsynonymous/synonymous substitutions (ω) in each codon was inferred by omegaMap [33]. ω>1, ω = 1, and ω<1 suggest positive selection, neutral evolution, and negative selection, respectively. The region where posterior probability of positive selection (ω>1) exceeds 95% is indicated (from 79th to 112th codon). (C) Sliding window analysis of Tajima's D of the Tm-1 alleles from S. habrochaites. The confidence limits of D for neutral evolution [35] are shown as dashed lines.

Mentions: To analyze the Tm-1 gene of S. habrochaites, we obtained seeds of 24 S. habrochaites accessions from the Germplasm Resources Information Network (GRIN). All accessions were collected in South America (Peru, Ecuador, or Venezuela). From each accession, one plant was randomly chosen and the Tm-1 cDNA was sequenced. In the obtained 48 sequences, a significant negative correlation was observed between linkage disequilibrium (r2) and distance between sites in the sequences (r = −0.2975, p<0.001), suggestive of intragenic recombination between alleles. Since this result indicated that the samples were not amenable for phylogenetic analyses, we used omegaMap [33] to analyze whether the evidence of natural selection is detected from the sequences in the presence of recombination. Remarkably, positive selection (ω = ratio of the rate of nonsynonymous/synonymous substitutions >1) was detected in a small region while most of the other parts of the gene were under purifying selection (ω<1) (Figure 2). An interdomain region (residues 432–483, predicted by NCBI Conserved Domain Database [34]) likely evolved neutrally (ω = 1) (Figure 2). The posterior probability of positive selection is >95% at residues 79–112. Consistently, Tajima's D, a test of neutral evolution [35], was significantly high (p<0.001) in the positively selected region based on a sliding window analysis (Figure 2C), also indicating that the region has not evolved neutrally. Importantly, the region is located in the alternative exon (encoding amino acids 46–263) of the Tm-1 gene that is required for inhibitory activity (Figure 2) [15].


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)

A small region of the Tm-1 gene is under positive selection in S. habrochaites.(A) Predicted domain structure of the Tm-1 protein by the NCBI Conserved Domain Database. A region encoded by the alternative exon (46–263) is underlined. (B) Detection of natural selection in the Tm-1 alleles from S. habrochaites. The ratio of nonsynonymous/synonymous substitutions (ω) in each codon was inferred by omegaMap [33]. ω>1, ω = 1, and ω<1 suggest positive selection, neutral evolution, and negative selection, respectively. The region where posterior probability of positive selection (ω>1) exceeds 95% is indicated (from 79th to 112th codon). (C) Sliding window analysis of Tajima's D of the Tm-1 alleles from S. habrochaites. The confidence limits of D for neutral evolution [35] are shown as dashed lines.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3475678&req=5

ppat-1002975-g002: A small region of the Tm-1 gene is under positive selection in S. habrochaites.(A) Predicted domain structure of the Tm-1 protein by the NCBI Conserved Domain Database. A region encoded by the alternative exon (46–263) is underlined. (B) Detection of natural selection in the Tm-1 alleles from S. habrochaites. The ratio of nonsynonymous/synonymous substitutions (ω) in each codon was inferred by omegaMap [33]. ω>1, ω = 1, and ω<1 suggest positive selection, neutral evolution, and negative selection, respectively. The region where posterior probability of positive selection (ω>1) exceeds 95% is indicated (from 79th to 112th codon). (C) Sliding window analysis of Tajima's D of the Tm-1 alleles from S. habrochaites. The confidence limits of D for neutral evolution [35] are shown as dashed lines.
Mentions: To analyze the Tm-1 gene of S. habrochaites, we obtained seeds of 24 S. habrochaites accessions from the Germplasm Resources Information Network (GRIN). All accessions were collected in South America (Peru, Ecuador, or Venezuela). From each accession, one plant was randomly chosen and the Tm-1 cDNA was sequenced. In the obtained 48 sequences, a significant negative correlation was observed between linkage disequilibrium (r2) and distance between sites in the sequences (r = −0.2975, p<0.001), suggestive of intragenic recombination between alleles. Since this result indicated that the samples were not amenable for phylogenetic analyses, we used omegaMap [33] to analyze whether the evidence of natural selection is detected from the sequences in the presence of recombination. Remarkably, positive selection (ω = ratio of the rate of nonsynonymous/synonymous substitutions >1) was detected in a small region while most of the other parts of the gene were under purifying selection (ω<1) (Figure 2). An interdomain region (residues 432–483, predicted by NCBI Conserved Domain Database [34]) likely evolved neutrally (ω = 1) (Figure 2). The posterior probability of positive selection is >95% at residues 79–112. Consistently, Tajima's D, a test of neutral evolution [35], was significantly high (p<0.001) in the positively selected region based on a sliding window analysis (Figure 2C), also indicating that the region has not evolved neutrally. Importantly, the region is located in the alternative exon (encoding amino acids 46–263) of the Tm-1 gene that is required for inhibitory activity (Figure 2) [15].

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