Coevolution and Hierarchical Interactions of Tomato mosaic virus and the Resistance Gene Tm-1

PLoS Pathogens

Volumn 8, Issue 10, 2012, Pages

  Ishibashi, Kazuhiro ^a   Mawatari, Natsuki ^a   Miyashita, Shuhei ^a,b   Kishino, Hirohisa ^c   Meshi, Tetsuo ^a   Ishikawa, Masayuki ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; TM 1 PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ALLELE; AMINO ACID SEQUENCE; ARTICLE; COEVOLUTION; CONTROLLED STUDY; GENETIC RESISTANCE; INOCULATION; NONHUMAN; PURIFYING SELECTION; SOLANUM; SOLANUM HABROCHAITES; TOBACCO MOSAIC VIRUS; VIRUS REPLICATION;

AMINO ACID SEQUENCE; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; GENES, PLANT; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; MUTATION; PLANT DISEASES; PLANT PROTEINS; PROTEIN BINDING; RNA, VIRAL; SELECTION, GENETIC; TOBAMOVIRUS; VIRUS REPLICATION;

LYCOPERSICON ESCULENTUM; LYCOPERSICON HIRSUTUM; TOMATO MOSAIC VIRUS;

EID: 84868114450     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002975     Document Type: Article

References (54)

1. Ruiz-Ferrer V, Voinnet O, (2009) Roles of Plant Small RNAs in Biotic Stress Responses. Annu Rev Plant Biol 60: 485-510.
2. Csorba T, Pantaleo V, Burgyán J, (2009) RNA silencing: an antiviral mechanism. Adv Virus Res 75: 35-71.
3. Kang B-C, Yeam I, Jahn MM, (2005) Genetics of Plant Virus Resistance. Annu Rev Phytopathol 43: 581-621.
4. Maule AJ, Caranta C, Boulton MI, (2007) Sources of natural resistance to plant viruses: status and prospects. Mol Plant Pathol 8: 223-231.
5. Gómez P, Rodríguez-Hernández AM, Moury B, Aranda MA, (2009) Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability. Eur J Plant Pathol 125: 1-22.
6. Ishikawa M, Meshi T, Motoyoshi F, Takamatsu N, Okada Y, (1986) In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus. Nucleic Acids Res 14: 8291-8305.
7. Ishibashi K, Nishikiori M, Ishikawa M, (2010) Interactions between tobamovirus replication proteins and cellular factors: their impacts on virus multiplication. Mol Plant Microbe Interact 23: 1413-1419.
8. Kurihara Y, Inaba N, Kutsuna N, Takeda A, Tagami Y, et al. (2007) Binding of tobamovirus replication protein with small RNA duplexes. J Gen Virol 88: 2347-2352.
9. Mérai Z, Kerényi Z, Kertész S, Magna M, Lakatos L, et al. (2006) Double-Stranded RNA Binding May Be a General Plant RNA Viral Strategy To Suppress RNA Silencing. J Virol 80: 5747-5756.
10. Csorba T, Bovi A, Dalmay T, Burgyán J, (2007) The p122 Subunit of Tobacco Mosaic Virus Replicase Is a Potent Silencing Suppressor and Compromises both Small Interfering RNA- and MicroRNA-Mediated Pathways. J Virol 81: 11768-11780.
11. Deom CM, Oliver MJ, Beachy RN, (1987) The 30-kilodalton gene product of tobacco mosaic virus potentiates virus movement. Science 237: 389-394.
12. Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, et al. (1987) Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6: 2557-2563.
13. Takamatsu N, Ishikawa M, Meshi T, Okada Y, (1987) Expression of bacterial chloramphenicol acetyltransferase gene in tobacco plants mediated by TMV-RNA. EMBO J 6: 307-311.
14. Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, et al. (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.
15. Ishibashi K, Masuda K, Naito S, Meshi T, Ishikawa M, (2007) An inhibitor of viral RNA replication is encoded by a plant resistance gene. Proc Natl Acad Sci U S A 104: 13833-13838.
16. Lanfermeijer FC, Dijkhuis J, Sturre MJ, de Haan P, Hille J, (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-22 from Lycopersicon esculentum. Plant Mol Biol 52: 1037-1049.
17. Lanfermeijer FC, Warmink J, Hille J, (2005) The products of the broken Tm-2 and the durable Tm-22 resistance genes from tomato differ in four amino acids. J Exp Bot 56: 2925-2933.
18. Tomita R, Sekine K-T, Mizumoto H, Sakamoto M, Murai J, et al. (2011) Genetic Basis for the Hierarchical Interaction Between Tobamovirus spp. and L Resistance Gene Alleles from Different Pepper Species. Mol Plant Microbe Interact 24: 108-117.
19. Padgett HS, Beachy RN, (1993) Analysis of a Tobacco Mosaic Virus Strain Capable of Overcoming N Gene-Mediated Resistance. Plant Cell 5: 577-586.
20. Meshi T, Motoyoshi F, Adachi A, Watanabe Y, Takamatsu N, et al. (1988) Two concomitant base substitutions in the putative replicase genes of tobacco mosaic virus confer the ability to overcome the effects of a tomato resistance gene, Tm-1. EMBO J 7: 1575-1581.
21. Padgett HS, Watanabe Y, Beachy RN, (1997) Identification of the TMV Replicase Sequence That Activates the N Gene-Mediated Hypersensitive Response. Mol Plant Microbe Interact 10: 709-715.
22. Meshi T, Motoyoshi F, Maeda T, Yoshiwoka S, Watanabe H, et al. (1989) Mutations in the Tobacco Mosaic Virus 30-kD Protein Gene Overcome Tm-2 Resistance in Tomato. Plant Cell 1: 515-522.
23. Weber H, Schultze S, Pfitzner AJP, (1993) Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-22 resistance gene in the tomato. J Virol 67: 6432-6438.
24. Berzal-Herranz A, De La Cruz A, Tenllado F, Díaz-Ruíz JR, López L, et al. (1995) The Capsicum L3 gene-mediated resistance against the tobamoviruses is elicited by the coat protein. Virology 209: 498-505.
25. De La Cruz A, López L, Tenllado F, Díaz-Ruíz J, Sanz A, et al. (1997) The coat protein is required for the elicitation of the Capsicum L2 gene-mediated resistance against the tobamoviruses. Mol Plant Microbe Interact 10: 107-113.
26. Gilardi P, García-Luque I, Serra MT, (1998) Pepper mild mottle virus coat protein alone can elicit the Capsicum spp. L3 gene-mediated resistance. Mol Plant Microbe Interact 11: 1253-1257.
27. Pelham J, (1966) Resistance in tomato to tobacco mosaic virus. Euphytica 15: 258-267.
28. Strasser M, Pfitzner AJP, (2007) The double-resistance-breaking Tomato mosaic virus strain ToMV1-2 contains two independent single resistance-breaking domains. Arch Virol 152: 903-914.
29. Nishikiori M, Sugiyama S, Xiang H, Niiyama M, Ishibashi K, et al. (2012) Crystal Structure of the Superfamily 1 Helicase from Tomato Mosaic Virus. J Virol 86: 7565-7576.
30. Ishibashi K, Naito S, Meshi T, Ishikawa M, (2009) An inhibitory interaction between viral and cellular proteins underlies the resistance of tomato to nonadapted tobamoviruses. Proc Natl Acad Sci U S A 106: 8778-8783.
31. Fraile A, García-Arenal F, (2010) The Coevolution of Plants and Viruses: Resistance and Pathogenicity. Adv Virus Res 76: 1-32.
32. Elena SF, Lenski RE, (2003) Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4: 457-469.
33. Wilson DJ, McVean G, (2006) Estimating diversifying selection and functional constraint in the presence of recombination. Genetics 172: 1411.
34. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, et al. (2011) CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39: D225-D229.
35. Tajima F, (1989) Statistical Method for Testing the Neutral Mutation Hypothesis by DNA Polymorphism. Genetics 123: 585-595.
36. Fraser RSS, Loughlin SAR, (1980) Resistance to Tobacco Mosaic Virus in Tomato: Effects of the Tm-1 Gene on Virus Multiplication. J Gen Virol 48: 87-96.
37. Komoda K, Naito S, Ishikawa M, (2004) Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc Natl Acad Sci U S A 101: 1863-1867.
38. Komoda K, Mawatari N, Hagiwara-Komoda Y, Naito S, Ishikawa M, (2007) Identification of a Ribonucleoprotein Intermediate of Tomato Mosaic Virus RNA Replication Complex Formation. J Virol 81: 2584-2591.
39. Pelham J, Fletcher JT, Hawkins JH, (1970) The establishment of a new strain of tobacco mosaic virus resulting from the use of resistant varieties of tomato. Ann Appl Biol 65: 293-297.
40. Fraser RSS, Gerwitz A (1987) The genetics of resistance and virulence in plant virus disease. In: Day PR, Jellis GJ, editors. Genetics and Plant Pathogenesis. Oxford: Blackwell. pp. 33-44.
41. Ishibashi K, Meshi T, Ishikawa M, (2011) Gaining Replicability in a Nonhost Compromises the Silencing Suppression Activity of Tobacco Mild Green Mosaic Virus in a Host. J Virol 85: 1893-1895.
42. Charron C, Nicolaï M, Gallois J-L, Robaglia C, Moury B, et al. (2008) Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J 54: 56-68.
43. Cavatorta JR, Savage AE, Yeam I, Gray SM, Jahn MM, (2008) Positive Darwinian Selection at Single Amino Acid Sites Conferring Plant Virus Resistance. J Mol Evol 67: 551-559.
44. Hofinger BJ, Russell JR, Bass CG, Baldwin T, Dos Reis M, et al. (2011) An exceptionally high nucleotide and haplotype diversity and a signature of positive selection for the eIF4E resistance gene in barley are revealed by allele mining and phylogenetic analyses of natural populations. Mol Ecol 20: 3653-3668.
45. Salvaudon L, Giraud T, Shykoff JA, (2008) Genetic diversity in natural populations: a fundamental component of plant-microbe interactions. Curr Opin Plant Biol 11: 135-143.
46. Brown JKM, Tellier A, (2011) Plant-parasite coevolution: bridging the gap between genetics and ecology. Annu Rev Phytopathol 49: 345-367.
47. Bergelson J, Dwyer G, Emerson J, (2001) Models and data on plant-enemy coevolution. Annu Rev Genet 35: 469-499.
48. Fraile A, Pagán I, Anastasio G, Sáez E, García-Arenal F, (2011) Rapid Genetic Diversification and High Fitness Penalties Associated with Pathogenicity Evolution in a Plant Virus. Mol Biol Evol 28: 1425-1437.
49. Kubota K, Tsuda S, Tamai A, Meshi T, (2003) Tomato Mosaic Virus Replication Protein Suppresses Virus-Targeted Posttranscriptional Gene Silencing. J Virol 77: 11016-11026.
50. Hamamoto H, Watanabe Y, Kamada H, Okada Y, (1997) A Single Amino Acid Substitution in the Virus-Encoded Replicase of Tomato Mosaic Tobamovirus Alters Host Specificity. Mol Plant Microbe Interact 10: 1015-1018.
51. Ishibashi K, Komoda K, Ishikawa M (2006) In Vitro Translation and Replication of Tobamovirus RNA in a Cell-Free Extract of Evacuolated Tobacco BY-2 Protoplasts. In: Nagata T, Matsuoka K, Inzé D, editors. Tobacco BY-2 Cells: From Cellular Dynamics to Omics: Springer Berlin Heidelberg. pp. 183-194.
52. Hagiwara Y, Komoda K, Yamanaka T, Tamai A, Meshi T, et al. (2003) Subcellular localization of host and viral proteins associated with tobamovirus RNA replication. EMBO J 22: 344-353.
53. Librado P, Rozas J, (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451-1452.
54. Watanabe Y, Meshi T, Okada Y, (1987) Infection of tobacco protoplasts with in vitro transcribed tobacco mosaic virus RNA using an improved electroporation method. FEBS Lett 219: 65-69.