The Tomato Yellow Leaf Curl Virus Resistance Genes and Are Allelic and Code for DFDGD-Class RNA–Dependent RNA Polymerases

English version České info

Tomato Yellow Leaf Curl Virus Disease incited by Tomato yellow leaf curl virus (TYLCV) causes huge losses in tomato production worldwide and is caused by different related begomovirus species. Breeding for TYLCV resistance has been based on the introgression of multiple resistance genes originating from several wild tomato species. In this study we have fine-mapped the widely used Solanum chilense–derived Ty-1 and Ty-3 genes by screening nearly 12,000 plants for recombination events and generating recombinant inbred lines. Multiple molecular markers were developed and used in combination with disease tests to fine-map the genes to a small genomic region (approximately 70 kb). Using a Tobacco Rattle Virus–Virus Induced Gene Silencing approach, the resistance gene was identified. It is shown that Ty-1 and Ty-3 are allelic and that they code for a RNA–dependent RNA polymerase (RDR) belonging to the RDRγ type, which has an atypical DFDGD motif in the catalytic domain. In contrast to the RDRα type, characterized by a catalytic DLDGD motif, no clear function has yet been described for the RDRγ type, and thus the Ty-1/Ty-3 gene unveils a completely new class of resistance gene. Although speculative, the resistance mechanism of Ty-1/Ty-3 and its specificity towards TYLCV are discussed in light of the function of the related RDRα class in the amplification of the RNAi response in plants and transcriptional silencing of geminiviruses in plants.

Vyšlo v časopise: The Tomato Yellow Leaf Curl Virus Resistance Genes and Are Allelic and Code for DFDGD-Class RNA–Dependent RNA Polymerases. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003399
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003399

Souhrn

Zdroje

1. JonesJDG, DanglJL (2006) The plant immune system. Nature 444 : 323–329.

2. BrommonschenkelSH, FraryA, FraryA, TanksleySD (2000) The Broad-Spectrum Tospovirus Resistance Gene Sw-5 of Tomato Is a Homolog of the Root-Knot Nematode Resistance Gene Mi. Molecular Plant-Microbe Interactions 13 : 1130–1138.

3. BendahmaneA, QuerciM, KanyukaK, BaulcombeDC (2000) Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: application to the Rx2 locus in potato. The Plant Journal 21 : 73–81.

4. VallejosCE, Astua-MongeG, JonesV, PlylerTR, SakiyamaNS, et al. (2006) Genetic and Molecular Characterization of the I Locus of Phaseolus vulgaris. Genetics 172 : 1229–1242.

5. KangBC, YeamI, JahnMM (2005) Genetics of plant virus resistance. Annual Review of Phytopathology 43 : 581–621.

6. Truniger V, Aranda MA, Gad L, John PC (2009) Chapter 4 -⁠ Recessive Resistance to Plant Viruses. Advances in Virus Research: Academic Press. pp. 119–231.

7. RobagliaC, CarantaC (2006) Translation initiation factors: a weak link in plant RNA virus infection. Trends in Plant Science 11 : 40–45.

8. BernsteinE, CaudyAA, HammondSM, HannonGJ (2001) Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409 : 363–366.

9. SijenT, FleenorJ, SimmerF, ThijssenKL, ParrishS, et al. (2001) On the Role of RNA Amplification in dsRNA-Triggered Gene Silencing. Cell 107 : 465–476.

10. WangX-B, WuQ, ItoT, CilloF, LiW-X, et al. (2010) RNAi-mediated viral immunity requires amplification of virus-derived siRNAs in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 107 : 484–489.

11. Garcia-RuizH, TakedaA, ChapmanEJ, SullivanCM, FahlgrenN, et al. (2010) Arabidopsis RNA-Dependent RNA Polymerases and Dicer-Like Proteins in Antiviral Defense and Small Interfering RNA Biogenesis during Turnip Mosaic Virus Infection. The Plant Cell Online 22 : 481–496.

12. Diaz-PendonJA, LiF, LiW-X, DingS-W (2007) Suppression of Antiviral Silencing by Cucumber Mosaic Virus 2b Protein in Arabidopsis Is Associated with Drastically Reduced Accumulation of Three Classes of Viral Small Interfering RNAs. The Plant Cell Online 19 : 2053–2063.

13. PandeySP, GaquerelE, GaseK, BaldwinIT (2008) RNA-Directed RNA Polymerase3 from Nicotiana attenuata Is Required for Competitive Growth in Natural Environments. Plant Physiology 147 : 1212–1224.

14. SchwachF, VaistijFE, JonesL, BaulcombeDC (2005) An RNA-Dependent RNA Polymerase Prevents Meristem Invasion by Potato Virus X and Is Required for the Activity But Not the Production of a Systemic Silencing Signal. Plant Physiology 138 : 1842–1852.

15. FauquetC, BriddonR, BrownJ, MorionesE, StanleyJ, et al. (2008) Geminivirus strain demarcation and nomenclature. Archives of Virology 153 : 783–821.

16. ScholthofKBG, AdkinsS, CzosnekH, PalukaitisP, JacquotE, et al. (2011) Top 10 plant viruses in molecular plant pathology. Molecular Plant Pathology 12 : 938–954.

17. Gronenborn B (2007) The Tomato Yellow Leaf Curl Virus Genome and Function of its Proteins. In: Czosnek H, editor. Tomato Yellow Leaf Curl Virus Disease: Springer Netherlands. pp. 67–84.

18. Hanley-BowdoinL, SettlageSB, RobertsonD (2004) Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Molecular Plant Pathology 5 : 149–156.

19. ZamirD, Ekstein MichelsonI, ZakayY, NavotN, ZeidanM, et al. (1994) Mapping and introgression of a tomato yellow leaf curl virus tolerance gene, Ty-1. Theoretical and Applied Genetics 88 : 141–146.

20. HansonP, GreenS, KuoG (2006) Ty-2, a gene on chromosome 11 conditioning geminivirus resistance in tomato. Report of the Tomato Genetics Cooperative 56 : 17–18.

21. JiY, SchusterDJ, ScottJW (2007) Ty-3, a begomovirus resistance locus near the Tomato yellow leaf curl virus resistance locus Ty-1 on chromosome 6 of tomato. Molecular Breeding 20 : 271–284.

22. JiY, ScottJW, SchusterDJ, MaxwellDP (2009) Molecular mapping of Ty-4, a new Tomato yellow leaf curl virus resistance locus on chromosome 3 of Tomato. Journal of the American Society for Horticultural Science 134 : 281–288.

23. AnbinderI, ReuveniM, AzariR, ParanI, NahonS, et al. (2009) Molecular dissection of Tomato leaf curl virus resistance in tomato line TY172 derived from Solanum peruvianum. Theoretical and Applied Genetics 119 : 519–530.

24. HuttonSF, ScottJW, SchusterDJ (2012) Recessive Resistance to Tomato yellow leaf curl virus from the Tomato Cultivar Tyking Is Located in the Same Region as Ty-5 on Chromosome 4. HortScience 47 : 324–327.

25. Narasegowda MaruthiM, CzosnekH, VidavskiF, TarbaS-Y, MiloJ, et al. (2003) Comparison of Resistance to Tomato Leaf Curl Virus (India) and Tomato Yellow Leaf Curl Virus (Israel) among Lycopersicon Wild Species, Breeding Lines and Hybrids. 109 : 1–11.

26. Perez de CastroA, DiezMJ, NuezF (2005) Evaluation of breeding tomato lines partially resistant to Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus derived from Lycopersicon chilense. Canadian Journal of Plant Pathology 27 : 268–275.

27. PicoB, FerriolM, iezMJD, NuezF (1999) Developing tomato breeding lines resistant to Tomato yellow leaf curl virus. Plant Breeding 118 : 537–542.

28. PicoB, SifresA, EliaM, Jose DiezM, NuezF (2000) Searching for new resistance sources to Tomato yellow leaf curl virus within a highly variable wild Lycopersicon genetic pool. Acta Physiologiae Plantarum 22 : 344–350.

29. Pérez de Castro A, Julián O, Díez M Genetic control and mapping of Solanum chilense LA1932, LA1960 and LA1971-derived resistance to Tomato yellow leaf curl disease. Euphytica: 1–12.

30. LapidotM, FriedmannM, LachmanO, YehezkelA, NahonS, et al. (1997) Comparison of resistance level to Tomato yellow leaf curl virus among commercial cultivars and breeding lines. Plant Disease 81 : 1425–1428.

31. FargetteD, LeslieM, HarrisonBD (1996) Serological studies on the accumulation and localisation of three tomato leaf curl geminiviruses in resistant and susceptible Lycopersicon species and tomato cultivars. Annals of Applied Biology 128 : 317–328.

32. SadeD, EybishtzA, GorovitsR, SobolI, CzosnekH (2012) A developmentally regulated lipocalin-like gene is overexpressed in Tomato yellow leaf curl virus-resistant tomato plants upon virus inoculation, and its silencing abolishes resistance. Plant Molecular Biology 80 : 273–287.

33. EybishtzA, PeretzY, SadeD, GorovitsR, CzosnekH (2009) Tomato yellow leaf curl virus infection of a resistant tomato line with a silenced sucrose transporter gene LeHT1 results in inhibition of growth, enhanced virus spread, and necrosis. Planta 231 : 537–548.

34. EybishtzA, PeretzY, SadeD, AkadF, CzosnekH (2009) Silencing of a single gene in tomato plants resistant to Tomato yellow leaf curl virus renders them susceptible to the virus. Plant Molecular Biology 71 : 157–171.

35. VerlaanMG, SzinayD, HuttonSF, de JongH, KormelinkR, et al. (2011) Chromosomal rearrangements between tomato and Solanum chilense hamper mapping and breeding of the TYLCV resistance gene Ty-1. The Plant Journal 68 : 1093–1103.

36. BombarelyA, MendaN, TecleIY, BuelsRM, StricklerS, et al. (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Research 39: D1149–D1155.

37. Lozano-DuránR, Rosas-DíazT, LunaAP, BejaranoER (2011) Identification of Host Genes Involved in Geminivirus Infection Using a Reverse Genetics Approach. PLoS ONE 6: e22383 doi:10.1371/journal.pone.0022383.

38. PochO, BlumbergBM, BougueleretL, TordoN (1990) Sequence comparison of five polymerases (L proteins) of unsegmented negative-strand RNA viruses: theoretical assignment of functional domains. Journal of General Virology 71 : 1153–1162.

39. ZongJ, YaoX, YinJ, ZhangD, MaH (2009) Evolution of the RNA-dependent RNA polymerase (RdRP) genes: Duplications and possible losses before and after the divergence of major eukaryotic groups. Gene 447 : 29–39.

40. WasseneggerM, KrczalG (2006) Nomenclature and functions of RNA-directed RNA polymerases. Trends in Plant Science 11 : 142–151.

41. DingS-W, VoinnetO (2007) Antiviral Immunity Directed by Small RNAs. Cell 130 : 413–426.

42. ChellappanP, MasonaM, VanitharaniR, TaylorN, FauquetC (2004) Broad Spectrum Resistance to ssDNA Viruses Associated with Transgene-Induced Gene Silencing in Cassava. Plant Molecular Biology 56 : 601–611.

43. RibeiroSG, LohuisH, GoldbachR, PrinsM (2007) Tomato Chlorotic Mottle Virus Is a Target of RNA Silencing but the Presence of Specific Short Interfering RNAs Does Not Guarantee Resistance in Transgenic Plants. Journal of Virology 81 : 1563–1573.

44. YadavRK, ChattopadhyayD (2011) Enhanced viral intergenic region-specific short interfering RNA accumulation and DNA methylation correlates with resistance against a geminivirus. Molecular Plant-Microbe Interactions 24 : 1189–1197.

45. YangX, XieY, RajaP, LiS, WolfJN, et al. (2011) Suppression of Methylation-Mediated Transcriptional Gene Silencing by βC1-SAHH Protein Interaction during Geminivirus-Betasatellite Infection. PLoS Path 7: e1002329 doi:10.1371/journal.pgen.1002329.

46. VanitharaniR, ChellappanP, FauquetCM (2005) Geminiviruses and RNA silencing. Trends in Plant Science 10 : 144–151.

47. RajaP, SanvilleBC, BuchmannRC, BisaroDM (2008) Viral Genome Methylation as an Epigenetic Defense against Geminiviruses. Journal of Virology 82 : 8997–9007.

48. BroughCL, GardinerWE, InamdarNM, ZhangX-Y, EhrlichM, et al. (1992) DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Molecular Biology 18 : 703–712.

49. VanitharaniR, ChellappanP, PitaJS, FauquetCM (2004) Differential roles of AC2 and AC4 of cassava geminiviruses in mediating synergism and suppression of posttranscriptional gene silencing. Journal of Virology 78 : 9487–9498.

50. BuchmannRC, AsadS, WolfJN, MohannathG, BisaroDM (2009) Geminivirus AL2 and L2 Proteins Suppress Transcriptional Gene Silencing and Cause Genome-Wide Reductions in Cytosine Methylation. Journal of Virology 83 : 5005–5013.

51. VoinnetO, PintoYM, BaulcombeDC (1999) Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants. Proceedings of the National Academy of Sciences 96 : 14147–14152.

52. WangH, BuckleyKJ, YangX, BuchmannRC, BisaroDM (2005) Adenosine Kinase Inhibition and Suppression of RNA Silencing by Geminivirus AL2 and L2 Proteins. Journal of Virology 79 : 7410–7418.

53. WangH, HaoL, ShungC-Y, SunterG, BisaroDM (2003) Adenosine Kinase Is Inactivated by Geminivirus AL2 and L2 Proteins. The Plant Cell Online 15 : 3020–3032.

54. van WezelWR, DongX, LiuH, TienP, StanleyJ, et al. (2002) Mutation of three cysteine residues in Tomato yellow leaf curl virus-China C2 protein causes dysfunction in pathogenesis and posttranscriptional gene-silencing suppression. Molecular Plant-Microbe Interactions 15 : 203–208.

55. ZhangZ, ChenH, HuangX, XiaR, ZhaoQ, et al. (2011) BSCTV C2 Attenuates the Degradation of SAMDC1 to Suppress DNA Methylation-Mediated Gene Silencing in Arabidopsis. The Plant Cell Online 23 : 273–288.

56. LunaAP, MorillaG, VoinnetO, BejaranoER (2012) Functional analysis of gene silencing suppressors from Tomato yellow leaf curl disease viruses. Molecular Plant-Microbe Interactions 25 : 1294–1306.

57. MuangsanN, BeclinC, VaucheretH, RobertsonD (2004) Geminivirus VIGS of endogenous genes requires SGS2/SDE1 and SGS3 and defines a new branch in the genetic pathway for silencing in plants. The Plant Journal 38 : 1004–1014.

58. VoinnetO (2008) Use, tolerance and avoidance of amplified RNA silencing by plants. Trends in Plant Science 13 : 317–328.

59. PandeySP, BaldwinIT (2007) RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. The Plant Journal 50 : 40–53.

60. Olmedo-MonfilV, Duran-FigueroaN, Arteaga-VazquezM, Demesa-ArevaloE, AutranD, et al. (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. 464 : 628–632.

61. PeragineA, YoshikawaM, WuG, AlbrechtHL, PoethigRS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes & Development 18 : 2368–2379.

62. LeibmanD, WolfD, SaharanV, ZelcerA, AraziT, et al. (2011) A High Level of Transgenic Viral Small RNA Is Associated with Broad Potyvirus Resistance in Cucurbits. Molecular Plant-Microbe Interactions 24 : 1220–1238.

63. WuQ, WangX, DingS-W (2010) Viral Suppressors of RNA-Based Viral Immunity: Host Targets. Cell Host & Microbe 8 : 12–15.

64. WillmannMR, EndresMW, CookRT, GregoryBD (2011) The Functions of RNA-Dependent RNA Polymerases in Arabidopsis. The Arabidopsis Book e0146.

65. GriffithsP, ScottJ (2001) Inheritance and linkage of tomato mottle virus resistance genes derived from Lycopersicon chilense accession LA 1932. Journal of the American Society for Horticultural Science 126 : 462–467.

66. DoyleJJ, DoyleJL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical bulletin 19 : 11–15.

67. FultonTM, ChunwongseJ, TanksleySD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Molecular Biology Reporter 13 : 207–209.

68. RozenS, SkaletskyH (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132 : 365–386.

69. HuttonSF, ScottJW (2011) A collection of polymorphic markers useful for fine-mapping the Ty-3 locus from Solanum chilense accession LA2779. Report of the Tomato Genetics Cooperative 61 : 12–14.

70. LiuY, SchiffM, Dinesh-KumarS (2002) Virus-induced gene silencing in tomato. The Plant Journal 31 : 777–786.

71. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution 28 : 2731–2739.

72. LameschP, BerardiniTZ, LiD, SwarbreckD, WilksC, et al. (2011) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Research

73. LøvdalT, LilloC (2009) Reference gene selection for quantitative real-time PCR normalization in tomato subjected to nitrogen, cold, and light stress. Analytical Biochemistry 387 : 238–242.

74. LivakKJ, SchmittgenTD (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method. Methods 25 : 402–408.