Using genomic analysis to identify tomato Tm-2 resistance-breaking mutations and their underlying evolutionary path in a new and emerging tobamovirus

  • Yonatan Maayan
  • Eswari P. J. Pandaranayaka
  • Dhruv Aditya Srivastava
  • Moshe Lapidot
  • Ilan Levin
  • Aviv Dombrovsky
  • Arye Harel
Original Article
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Abstract

In September 2014, a new tobamovirus was discovered in Israel that was able to break Tm-2-mediated resistance in tomato that had lasted 55 years. The virus was isolated, and sequencing of its genome showed it to be tomato brown rugose fruit virus (ToBRFV), a new tobamovirus recently identified in Jordan. Previous studies on mutant viruses that cause resistance breaking, including Tm-2-mediated resistance, demonstrated that this phenotype had resulted from only a few mutations. Identification of important residues in resistance breakers is hindered by significant background variation, with 9–15% variability in the genomic sequences of known isolates. To understand the evolutionary path leading to the emergence of this resistance breaker, we performed a comprehensive phylogenetic analysis and genomic comparison of different tobamoviruses, followed by molecular modeling of the viral helicase. The phylogenetic location of the resistance-breaking genes was found to be among host-shifting clades, and this, together with the observation of a relatively low mutation rate, suggests that a host shift contributed to the emergence of this new virus. Our comparative genomic analysis identified twelve potential resistance-breaking mutations in the viral movement protein (MP), the primary target of the related Tm-2 resistance, and nine in its replicase. Finally, molecular modeling of the helicase enabled the identification of three additional potential resistance-breaking mutations.

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Conflict of interest

The authors declare that they have no conflict of interest.

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Not applicable.

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References

  1. 1.
    Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM (2014) The evolution and genetics of virus host shifts. PLoS Pathog 10:e1004395CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Moya A, Holmes EC, Gonzalez-Candelas F (2004) The population genetics and evolutionary epidemiology of RNA viruses. Nat Rev Microbiol 2:279–288CrossRefPubMedGoogle Scholar
  3. 3.
    Domingo E, Holland JJ (1997) RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178CrossRefPubMedGoogle Scholar
  4. 4.
    Drake JW (1993) Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci USA 90:4171–4175CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548CrossRefPubMedGoogle Scholar
  6. 6.
    Scholthof KB (2017) Spicing up the N Gene: F. O. Holmes and tobacco mosaic virus resistance in capsicum and nicotiana plants. Phytopathology 107:148–157CrossRefPubMedGoogle Scholar
  7. 7.
    Voinnet O (2005) Induction and suppression of RNA silencing: insights from viral infections. Nat Rev Genet 6:206–220CrossRefPubMedGoogle Scholar
  8. 8.
    Zvereva AS, Pooggin MM (2012) Silencing and innate immunity in plant defense against viral and non-viral pathogens. Viruses 4:2578–2597CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Garcia-Arenal F, McDonald BA (2003) An analysis of the durability of resistance to plant viruses. Phytopathology 93:941–952CrossRefPubMedGoogle Scholar
  10. 10.
    Scholthof KB (2004) Tobacco mosaic virus: a model system for plant biology. Annu Rev Phytopathol 42:13–34CrossRefPubMedGoogle Scholar
  11. 11.
    Craig G, Rosskopf EN, Lucas L, Mellinger HC, Adkins S (2014) First report of tomato mottle mosaic virus infecting tomato in the United States. Plant Health Progress 15:151Google Scholar
  12. 12.
    Li R, Gao S, Fei Z, Ling KS (2013) Complete genome sequence of a new tobamovirus naturally infecting tomatoes in Mexico. Genome Announc 1:e00794-1.  https://doi.org/10.1128/genomeA.00794-13 Google Scholar
  13. 13.
    Li YY, Wang CL, Xiang D, Li RH, Liu Y, Li F (2014) First report of tomato mottle mosaic virus infection of pepper in China. Plant Dis 98:1447CrossRefGoogle Scholar
  14. 14.
    Moreira SR, Eiras M, Chaves ALR, Galleti SR, Colariccio A (2003) Caracterização de uma Nova Estirpe do Tomato mosaic virus isolada de Tomateiro no Estado de São Paulo. Fitopatol bras 28:602–607CrossRefGoogle Scholar
  15. 15.
    Padmanabhan CZY, Li R, Martin GB, Fei Z, Ling K-S (2015) Complete genome sequence of a tomato-Infecting tomato mottle mosaic virus in New York. Genome Announc 3:e01515–e01525Google Scholar
  16. 16.
    Salem N, Mansour A, Ciuffo M, Falk BW, Turina M (2016) A new tobamovirus infecting tomato crops in Jordan. Arch Virol 161:503–506CrossRefPubMedGoogle Scholar
  17. 17.
    Sui X, Zheng Y, Li R, Padmanabhan C, Tian T, Groth-Helms D, Keinath AP, Fei Z, Wu Z, Ling KS (2017) Molecular and biological characterization of tomato mottle mosaic virus and development of RT-PCR detection. Plant Dis 101:704–711CrossRefGoogle Scholar
  18. 18.
    Webster CG, Rosskopf EN, Lucas L, Mellinger CH, Adkins S (2014) First report of Tomato mottle mosaic virus infecting tomato in the United States. Plant Health Progress 15:151–152Google Scholar
  19. 19.
    CABI (2017) Pepper mild mottle virus. https://www.cabi.org/isc/datasheet/43826
  20. 20.
    Scholthof K-BG (2008) Tobacco mosaic virus: the beginning of plant pathology. APSnet Features.  https://doi.org/10.1094/APSnetFeatures-2008-0408 Google Scholar
  21. 21.
    Tian T, Posis K, Maroon-Lango CJ, Mavrodieva V, Haymes S, Pitman TL, Falk BW (2014) First report of cucumber green mottle mosaic virus on melon in the United States. Plant Dis 98:1163–1164CrossRefGoogle Scholar
  22. 22.
    Broadbent L (1976) Epidemiology and control of tomato mosaic virus. Annu Rev Phytopathol 14:75–96CrossRefGoogle Scholar
  23. 23.
    Bos L (1999) The natural selection of the chemical elements : the environment and life’s chemistry. Backhuys Publishers, LeidenGoogle Scholar
  24. 24.
    Ishibashi K, Kezuka Y, Kobayashi C, Kato M, Inoue T, Nonaka T, Ishikawa M, Matsumura H, Katoh E (2014) Structural basis for the recognition-evasion arms race between Tomato mosaic virus and the resistance gene Tm-1. Proc Natl Acad Sci USA 111:E3486–E3495CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Meshi T, Motoyoshi F, Adachi A, Watanabe Y, Takamatsu N, Okada Y (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 7:1575–1581PubMedPubMedCentralGoogle Scholar
  26. 26.
    Weber H, Schultze S, Pfitzner AJ (1993) Two amino acid substitutions in the tomato mosaic virus 30-kilodalton movement protein confer the ability to overcome the Tm-2(2) resistance gene in the tomato. J Virol 67:6432–6438PubMedPubMedCentralGoogle Scholar
  27. 27.
    Harrison BD (2002) Virus variation in relation to resistance-breaking in plants. Euphytica 124:181–192CrossRefGoogle Scholar
  28. 28.
    Fabre F, Rousseau E, Mailleret L, Moury B (2015) Epidemiological and evolutionary management of plant resistance: optimizing the deployment of cultivar mixtures in time and space in agricultural landscapes. Evol Appl 8:919–932CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Meshi T, Motoyoshi F, Maeda T, Yoshiwoka S, Watanabe H, Okada Y (1989) Mutations in the tobacco mosaic virus 30-kD protein gene overcome Tm-2 resistance in tomato. Plant Cell 1:515–522CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Strasser M, Pfitzner AJ (2007) The double-resistance-breaking Tomato mosaic virus strain ToMV1-2 contains two independent single resistance-breaking domains. Arch Virol 152:903–914CrossRefPubMedGoogle Scholar
  31. 31.
    Luria N, Smith E, Reingold V, Bekelman I, Lapidot M, Levin I, Elad N, Tam Y, Sela N, Abu-Ras A, Ezra N, Haberman A, Yitzhak L, Lachman O, Dombrovsky A (2017) A New Israeli tobamovirus isolate infects tomato plants harboring Tm-22 resistance genes. PLoS One 12:e0170429CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    International Committee on Taxonomy of Viruses., King AMQ (2012) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Academic Press, London, Waltham, MAGoogle Scholar
  33. 33.
    Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2013) GenBank. Nucl Acid Res 41:D36–D42CrossRefGoogle Scholar
  34. 34.
    Li W, Jaroszewski L, Godzik A (2001) Clustering of highly homologous sequences to reduce the size of large protein databases. Bioinformatics 17:282–283CrossRefPubMedGoogle Scholar
  35. 35.
    Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acid Res 30:3059–3066CrossRefGoogle Scholar
  36. 36.
    Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Adkins S, Kamenova I, Achor D, Lewandowski DJ (2003) Biological and molecular characterization of a novel tobamovirus with a unique host range. Plant Dis 87:1190–1196CrossRefGoogle Scholar
  39. 39.
    Gibbs AJ, Wood J, Garcia-Arenal F, Ohshima K, Armstrong JS (2015) Tobamoviruses have probably co-diverged with their eudicotyledonous hosts for at least 110 million years. Virus Evol 1:vev019CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755CrossRefPubMedGoogle Scholar
  42. 42.
    Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Rambaut A (2014) FigTree v1.4.1. http://tree.bio.ed.ac.uk/software/figtree/
  44. 44.
    Ferre F, Clote P (2005) DiANNA: a web server for disulfide connectivity prediction. Nucl Acid Res 33:W230–W232CrossRefGoogle Scholar
  45. 45.
    Blom N, Gammeltoft S, Brunak S (1999) Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294:1351–1362CrossRefPubMedGoogle Scholar
  46. 46.
    Drozdetskiy A, Cole C, Procter J, Barton GJ (2015) JPred4: a protein secondary structure prediction server. Nucl Acid Res 43:W389–W394CrossRefGoogle Scholar
  47. 47.
    Feenstra KA, Pirovano W, Krab K, Heringa J (2007) Sequence harmony: detecting functional specificity from alignments. Nucl Acid Res 35:W495–W498CrossRefGoogle Scholar
  48. 48.
    Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucl Acid Res 42:W252–W258CrossRefGoogle Scholar
  49. 49.
    Nishikiori M, Sugiyama S, Xiang H, Niiyama M, Ishibashi K, Inoue T, Ishikawa M, Matsumura H, Katoh E (2012) Crystal structure of the superfamily 1 helicase from Tomato mosaic virus. J Virol 86:7565–7576CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Krissinel E, Henrick K (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60:2256–2268CrossRefPubMedGoogle Scholar
  51. 51.
    Laskowski RA, Macarthur MW, Moss DS, Thornton JM (1993) Procheck—a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26:283–291CrossRefGoogle Scholar
  52. 52.
    Benkert P, Kunzli M, Schwede T (2009) QMEAN server for protein model quality estimation. Nucl Acid Res 37:W510–W514CrossRefGoogle Scholar
  53. 53.
  54. 54.
    Schrodinger LLC (2015) The PyMOL Molecular Graphics System, Version 1.8. https://pymol.org/
  55. 55.
    Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Kadaré G, Haenni AL (1997) Virus-encoded RNA helicases. J Virol 71:2583–2590PubMedPubMedCentralGoogle Scholar
  57. 57.
    Pelham J (1972) Strain-genotype interaction of tobacco mosaic virus in tomato. Ann Appl Biol 71:219–228CrossRefGoogle Scholar
  58. 58.
    Hall TJ (1980) Resistance at the TM-2 locus in the tomato to tomato mosaic virus. Euphytica 29:189–197CrossRefGoogle Scholar
  59. 59.
    Duffy S, Shackelton LA, Holmes EC (2008) Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276CrossRefPubMedGoogle Scholar
  60. 60.
    Gibbs AJ, Fargette D, Garcia-Arenal F, Gibbs MJ (2010) Time–the emerging dimension of plant virus studies. J Gen Virol 91:13–22CrossRefPubMedGoogle Scholar
  61. 61.
    Gibbs A (1999) Evolution and origins of tobamoviruses. Philos Trans R Soc Lond B Biol Sci 354:593–602CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lartey RT, Voss TC, Melcher U (1996) Tobamovirus evolution: gene overlaps, recombination, and taxonomic implications. Mol Biol Evol 13:1327–1338CrossRefPubMedGoogle Scholar
  63. 63.
    Stobbe AH, Melcher U, Palmer MW, Roossinck MJ, Shen GA (2012) Co-divergence and host-switching in the evolution of tobamoviruses. J Gen Virol 93:408–418CrossRefPubMedGoogle Scholar
  64. 64.
    Rodríguez-Cerezo E, Elena SF, Moya A, García-Arenal F (1991) High genetic stability in natural populations of the plant RNA virus tobacco mild green mosaic virus. J Mol Evol 32:328–332CrossRefGoogle Scholar
  65. 65.
    Fraile A, Malpica JM, Aranda MA, Rodriguez-Cerezo E, Garcia-Arenal F (1996) Genetic diversity in tobacco mild green mosaic tobamovirus infecting the wild plant Nicotiana glauca. Virology 223:148–155CrossRefPubMedGoogle Scholar
  66. 66.
    Kim T, Youn MY, Min BE, Choi SH, Kim M, Ryu KH (2005) Molecular analysis of quasispecies of Kyuri green mottle mosaic virus. Virus Res 110:161–167CrossRefPubMedGoogle Scholar
  67. 67.
    Schneider WL, Roossinck MJ (2000) Evolutionarily related Sindbis-like plant viruses maintain different levels of population diversity in a common host. J Virol 74:3130–3134CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Marco CF, Aranda MA (2005) Genetic diversity of a natural population of Cucurbit yellow stunting disorder virus. J Gen Virol 86:815–822CrossRefPubMedGoogle Scholar
  69. 69.
    Hamamoto H, Watanabe Y, Kamada H, Okada Y (1997) Amino acid changes in the putative replicase of tomato mosaic tobamovirus that overcome resistance in Tm-1 tomato. J Gen Virol 78:461–464CrossRefPubMedGoogle Scholar
  70. 70.
    Yamafuji R, Watanabe Y, Meshi T, Okada Y (1991) Replication of TMV-L and Lta1 RNAs and their recombinants in TMV-resistant Tm-1 tomato protoplasts. Virology 183:99–105CrossRefPubMedGoogle Scholar
  71. 71.
    Meshi T, Watanabe Y, Saito T, Sugimoto A, Maeda T, Okada Y (1987) Function of the 30 kd protein of tobacco mosaic virus: involvement in cell-to-cell movement and dispensability for replication. EMBO J 6:2557–2563PubMedPubMedCentralGoogle Scholar
  72. 72.
    Weber H, Pfitzner AJ (1998) Tm-2(2) resistance in tomato requires recognition of the carboxy terminus of the movement protein of tomato mosaic virus. Mol Plant Microb Interact 11:498–503CrossRefGoogle Scholar
  73. 73.
    Lanfermeijer FC, Dijkhuis J, Sturre MJ, de Haan P, Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum. Plant Mol Biol 52:1037–1049CrossRefPubMedGoogle Scholar
  74. 74.
    Lanfermeijer FC, Warmink J, Hille J (2005) The products of the broken Tm-2 and the durable Tm-2(2) resistance genes from tomato differ in four amino acids. J Exp Bot 56:2925–2933CrossRefPubMedGoogle Scholar
  75. 75.
    Kobayashi M, Yamamoto-Katou A, Katou S, Hirai K, Meshi T, Ohashi Y, Mitsuhara I (2011) Identification of an amino acid residue required for differential recognition of a viral movement protein by the Tomato mosaic virus resistance gene Tm-2(2). J Plant Physiol 168:1142–1145CrossRefPubMedGoogle Scholar
  76. 76.
    Citovsky V, Wong ML, Shaw AL, Prasad BV, Zambryski P (1992) Visualization and characterization of tobacco mosaic virus movement protein binding to single-stranded nucleic acids. Plant Cell 4:397–411CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Waigmann E, Lucas WJ, Citovsky V, Zambryski P (1994) Direct functional assay for tobacco mosaic virus cell-to-cell movement protein and identification of a domain involved in increasing plasmodesmal permeability. Proc Natl Acad Sci USA 91:1433–1437CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Waigmann E, Chen MH, Bachmaier R, Ghoshroy S, Citovsky V (2000) Regulation of plasmodesmal transport by phosphorylation of tobacco mosaic virus cell-to-cell movement protein. EMBO J 19:4875–4884CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Citovsky V, Knorr D, Schuster G, Zambryski P (1990) The P30 movement protein of tobacco mosaic virus is a single-strand nucleic acid binding protein. Cell 60:637–647CrossRefPubMedGoogle Scholar
  80. 80.
    Brill LM, Nunn RS, Kahn TW, Yeager M, Beachy RN (2000) Recombinant tobacco mosaic virus movement protein is an RNA-binding, alpha-helical membrane protein. Proc Natl Acad Sci USA 97:7112–7117CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Fujiki M, Kawakami S, Kim RW, Beachy RN (2006) Domains of tobacco mosaic virus movement protein essential for its membrane association. J Gen Virol 87:2699–2707CrossRefPubMedGoogle Scholar
  82. 82.
    Peiro A, Martinez-Gil L, Tamborero S, Pallas V, Sanchez-Navarro JA, Mingarro I (2014) The tobacco mosaic virus movement protein associates with but does not integrate into biological membranes. J Virol 88:3016–3026CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Chen MH, Sheng J, Hind G, Handa AK, Citovsky V (2000) Interaction between the tobacco mosaic virus movement protein and host cell pectin methylesterases is required for viral cell-to-cell movement. EMBO J 19:913–920CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Hirashima K, Watanabe Y (2003) RNA helicase domain of tobamovirus replicase executes cell-to-cell movement possibly through collaboration with its nonconserved region. J Virol 77:12357–12362CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Schoelz JE, Harries PA, Nelson RS (2011) Intracellular transport of plant viruses: finding the door out of the cell. Mol Plant 4:813–831CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Wang LY, Lin SS, Hung TH, Li TK, Lin NC, Shen TL (2012) Multiple domains of the tobacco mosaic virus p126 protein can independently suppress local and systemic RNA silencing. Mol Plant Microb Interact 25:648–657CrossRefGoogle Scholar
  87. 87.
    Padmanabhan MS, Kramer SR, Wang X, Culver JN (2008) Tobacco mosaic virus replicase-auxin/indole acetic acid protein interactions: reprogramming the auxin response pathway to enhance virus infection. J Virol 82:2477–2485CrossRefPubMedGoogle Scholar
  88. 88.
    Lapidot M, Karniel U, Gelbart D, Fogel D, Evenor D, Kutsher Y, Makhbash Z, Nahon S, Shlomo H, Chen L, Reuveni M, Levin I (2015) A novel route controlling begomovirus resistance by the messenger RNA surveillance factor pelota. PLoS Genet 11:e1005538CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Navratil V, de Chassey B, Meyniel L, Delmotte S, Gautier C, Andre P, Lotteau V, Rabourdin-Combe C (2009) VirHostNet: a knowledge base for the management and the analysis of proteome-wide virus-host interaction networks. Nucl Acid Res 37:D661–D668CrossRefGoogle Scholar
  90. 90.
    Schoelz JE, Angel CA, Nelson RS, Leisner SM (2016) A model for intracellular movement of Cauliflower mosaic virus: the concept of the mobile virion factory. J Exp Bot 67:2039–2048CrossRefPubMedGoogle Scholar
  91. 91.
    Daubert SD, Schoelz J, Debao L, Shepherd RJ (1984) Expression of disease symptoms in cauliflower mosaic virus genomic hybrids. J Mol Appl Genet 2:537–547PubMedGoogle Scholar
  92. 92.
    Schoelz J, Shepherd RJ, Daubert S (1986) Region VI of cauliflower mosaic virus encodes a host range determinant. Mol Cell Biol 6:2632–2637CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Haas G, Azevedo J, Moissiard G, Geldreich A, Himber C, Bureau M, Fukuhara T, Keller M, Voinnet O (2008) Nuclear import of CaMV P6 is required for infection and suppression of the RNA silencing factor DRB4. EMBO J 27:2102–2112CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Laird J, McInally C, Carr C, Doddiah S, Yates G, Chrysanthou E, Khattab A, Love AJ, Geri C, Sadanandom A, Smith BO, Kobayashi K, Milner JJ (2013) Identification of the domains of cauliflower mosaic virus protein P6 responsible for suppression of RNA silencing and salicylic acid signalling. J Gen Virol 94:2777–2789CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Love AJ, Geri C, Laird J, Carr C, Yun BW, Loake GJ, Tada Y, Sadanandom A, Milner JJ (2012) Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS One 7:e47535CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Bonneville JM, Sanfacon H, Futterer J, Hohn T (1989) Posttranscriptional trans-activation in cauliflower mosaic virus. Cell 59:1135–1143CrossRefPubMedGoogle Scholar
  97. 97.
    Angel CA, Lutz L, Yang XH, Rodriguez A, Adair A, Zhang Y, Leisner SM, Nelson RS, Schoelz JE (2013) The P6 protein of Cauliflower mosaic virus interacts with CHUP1, a plant protein which moves chloroplasts on actin microfilaments. Virology 443:363–374CrossRefPubMedGoogle Scholar
  98. 98.
    Harries PA, Palanichelvam K, Yu W, Schoelz JE, Nelson RS (2009) The cauliflower mosaic virus protein P6 forms motile inclusions that traffic along actin microfilaments and stabilize microtubules. Plant Physiol 149:1005–1016CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771CrossRefPubMedGoogle Scholar
  100. 100.
    Sarkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Yonatan Maayan
    • 1
  • Eswari P. J. Pandaranayaka
    • 1
  • Dhruv Aditya Srivastava
    • 1
  • Moshe Lapidot
    • 1
  • Ilan Levin
    • 1
  • Aviv Dombrovsky
    • 2
  • Arye Harel
    • 1
  1. 1.Department of Vegetable and Field Crop Research, Institute of Plant SciencesAgricultural Research Organization, Volcani CenterRishon LeZionIsrael
  2. 2.Department of Plant Pathology and Weed Research, Institute of Plant ProtectionAgricultural Research Organization, Volcani CenterRishon LeZionIsrael

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