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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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ToMV-L-resistant and -susceptible S. habrochaites have distinct amino acid sequences in the positively selected region of Tm-1.Deduced amino acid sequences of the Tm-1 protein of five ToMV-L-resistant and -susceptible S. habrochaites plants from the indicated accessions were aligned. The positively selected region (79–112) is indicated. Identical amino acid residues to those of Tm-1GCR237 are indicated by dots.
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ppat-1002975-g003: ToMV-L-resistant and -susceptible S. habrochaites have distinct amino acid sequences in the positively selected region of Tm-1.Deduced amino acid sequences of the Tm-1 protein of five ToMV-L-resistant and -susceptible S. habrochaites plants from the indicated accessions were aligned. The positively selected region (79–112) is indicated. Identical amino acid residues to those of Tm-1GCR237 are indicated by dots.

Mentions: We next examined the ToMV resistance of 149 S. habrochaites plants from the 24 accessions by mechanically inoculating ToMV-L onto leaves. The accumulation of CP in the inoculated leaves was examined by SDS-PAGE, followed by Coomassie blue staining at 7 or 8 days postinoculation (dpi). Since S. habrochaites plants are self-incompatible, the accessions would not be genetically uniform. Indeed, in some accessions, both ToMV-resistant (CP undetectable) and -susceptible (CP detectable) plants were found (Table 1). Of the 149 plants tested, 94 did not accumulate detectable amounts of ToMV CP (Table 1). We then sequenced Tm-1 cDNA of randomly chosen five plants that did not accumulate ToMV CP (i.e., ToMV-resistant plants) and five plants that accumulated ToMV CP at high levels (i.e., ToMV-susceptible plants). The amino acid sequences of the positively selected region were clearly divided into two classes, consistent with their ToMV-resistant or -susceptible phenotypes (Figure 3). In this region, each of the 48 Tm-1 amino acid sequences obtained above was similar to either one of the two groups (29 to the resistant type and 19 to the susceptible type; Figure S1). These results suggest that both types of alleles were maintained by balancing selection.


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)

ToMV-L-resistant and -susceptible S. habrochaites have distinct amino acid sequences in the positively selected region of Tm-1.Deduced amino acid sequences of the Tm-1 protein of five ToMV-L-resistant and -susceptible S. habrochaites plants from the indicated accessions were aligned. The positively selected region (79–112) is indicated. Identical amino acid residues to those of Tm-1GCR237 are indicated by dots.
© Copyright Policy
Related In: Results  -  Collection

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

ppat-1002975-g003: ToMV-L-resistant and -susceptible S. habrochaites have distinct amino acid sequences in the positively selected region of Tm-1.Deduced amino acid sequences of the Tm-1 protein of five ToMV-L-resistant and -susceptible S. habrochaites plants from the indicated accessions were aligned. The positively selected region (79–112) is indicated. Identical amino acid residues to those of Tm-1GCR237 are indicated by dots.
Mentions: We next examined the ToMV resistance of 149 S. habrochaites plants from the 24 accessions by mechanically inoculating ToMV-L onto leaves. The accumulation of CP in the inoculated leaves was examined by SDS-PAGE, followed by Coomassie blue staining at 7 or 8 days postinoculation (dpi). Since S. habrochaites plants are self-incompatible, the accessions would not be genetically uniform. Indeed, in some accessions, both ToMV-resistant (CP undetectable) and -susceptible (CP detectable) plants were found (Table 1). Of the 149 plants tested, 94 did not accumulate detectable amounts of ToMV CP (Table 1). We then sequenced Tm-1 cDNA of randomly chosen five plants that did not accumulate ToMV CP (i.e., ToMV-resistant plants) and five plants that accumulated ToMV CP at high levels (i.e., ToMV-susceptible plants). The amino acid sequences of the positively selected region were clearly divided into two classes, consistent with their ToMV-resistant or -susceptible phenotypes (Figure 3). In this region, each of the 48 Tm-1 amino acid sequences obtained above was similar to either one of the two groups (29 to the resistant type and 19 to the susceptible type; Figure S1). These results suggest that both types of alleles were maintained by balancing selection.

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