Journal of Molecular Evolution

, Volume 39, Issue 5, pp 496–505 | Cite as

Phylogenetic relationships reveal recombination among isolates of cauliflower mosaic virus

  • Chenault Kelly D. 
  • Ulrich Melcher


Isolates of cauliflower mosaic virus (CaMV) differ in host range and symptomatology. Knowledge of their sequence relationships should assist in identifying nucleotide sequences responsible for isolate-specific characters. Complete nucleotide sequences of the DNAs of eight isolates of CaMV were aligned and the aligned sequences were used to analyze phylogenetic relationships by maximum likelihood, bootstrapped parsimony, and distance methods. Isolates found in North America clustered separately from those isolated from other parts of the world. Additional isolates, for which partial sequences were available, were incorporated into phylogenetic analysis of the sequences of genome segments corresponding to individual protein coding regions or the large intergenic region of CaMV DNA. The analysis revealed several instances where the position of an isolate on a tree for one coding region did not agree with the position of the isolate on the tree for the complete genome or with its position on trees for other coding regions. Examination of the distribution of shared residue types of phylogenetically informative positions in anomalous regions suggested that most of the anomalies were due to recombination events during the evolution of the isolates. Application of an algorithm that searches for segments of significant length that are identical between pairs of isolates or contain a significantly high concentration of polymorphisms suggested two additional recombination events between progenitors of the isolates studied and an event between the XinJing isolate and a CaMV not represented in the data set. An earlier phylogenetic origin for CaMV than for carnation etched ring virus, the caulimovirus used as outgroup in these analyses, was deduced from the position of the outgroup with North American isolates in some trees, but with non-North American isolates in other trees.

Key words

Caulimovirus Pararetroviruses Recombination Reverse transcription Viral isolates 


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  1. Balàzs E, Guilley H, Jonard G, Richards K (1982) Nucleotide sequence of DNA from an altered-virulence isolate D/H of the cauliflower mosaic virus. Gene 19:239–249Google Scholar
  2. Blok J, Mackenzie A, Guy P, Gibbs A (1987) Nucleotide sequence comparisons of turnip yellow mosaic virus isolates from Australia and Europe. Arch Virol 97:283–295Google Scholar
  3. Chenault KD, Melcher U (1993) The complete nucleotide sequence of cauliflower mosaic virus isolate BBC. Gene 123:255–257Google Scholar
  4. Chenault KD, Melcher U (1994) Patterns of nucleotide sequence variation among cauliflower mosaic virus isolates. Biochimie 76:3–8Google Scholar
  5. Choe IS, Melcher U, Richards K, Lebeurier G, Essenberg RC (1985) Recombination between mutant cauliflower mosaic virus DNAs. Plant Mol Biol 5:281–289Google Scholar
  6. Daubert SD, Schoelz J, Debao L, Shepherd RJ (1984) Expression of disease symptoms in cauliflower mosaic virus genomic hybrids. J Mol Appl Gen 2:537–547Google Scholar
  7. Dawson WO (1992) Tobamovirus-plant interactions. Virology 186: 359–367Google Scholar
  8. Dixon L, Nyffenegger T, Delley G, Martinez-Izquierdo J, Hohn T (1986) Evidence for replicative recombination in cauliflower mosaic virus. Virology 150:463–468Google Scholar
  9. Donis R, Bean WJ, Kawaoka Y, Webster RG (1989) Distinct lineages of influenza virus H4 hemagglutinin genes in different regions of the world. Virology 169:408–417Google Scholar
  10. Dykhuizen DE, Green L (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268Google Scholar
  11. Falk BW, Bruening G (1994) Will transgenic crops generate new viruses and new diseases? Science 263:1395–1396Google Scholar
  12. Felsenstein J (1989) PHYLIP-phylogeny inference package. Cladistics 5:164–166Google Scholar
  13. Franck A, Guilley H, Jonard G, Richards K, Hirth L (1980) Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21:285–294Google Scholar
  14. Fütterer J, Gordon K, Bonneville JM, Sanfaçon H, Pisan B, Penswick J, Hohn T (1988) The leading sequence of caulimovirus large RNA can be folded into a large stem-loop structure. Nucleic Acids Res 16:8377–8390Google Scholar
  15. Gal S, Pisan B, Hohn T, Grimsley N, Hohn B (1992) Agroinfection of transgenic plants leads to viable cauliflower mosaic virus by intermolecular recombination. Virology 187:525–533Google Scholar
  16. Gojobori T, Moriyama EN, Kimura M (1990) Molecular clock of viral evolution, and the neutral theory. Proc Natl Acad Sci U S A 87: 10015–10018Google Scholar
  17. Gracia O, Shepherd RJ (1985) Cauliflower mosaic virus in the nucleus of Nicotiana. Virology 146:141–145Google Scholar
  18. Grimsley N, Hohn T, Hohn B (1986) Recombination in a plant virus: template-switching in cauliflower mosaic virus. EMBO J 5:641–646Google Scholar
  19. Hasegawa A, Verver J, Shimada A, Saito M, Goldbach R, Van Kammen A, Miki K, Kameya-Jwaki M, Hibi T (1989) The complete sequence of soybean chlorotic mottle virus DNA and the identification of a novel promoter. Nucleic Acids Res 17:9993–10013Google Scholar
  20. Holland JJ, De La Torre JC, Steinhauer DA (1992) RNA virus populations as quasispecies. Curr Top Microbiol Immunol 176:1–20Google Scholar
  21. Howarth AJ, Gardner RC, Messing J, Shepherd RJ (1981) Nucleotide sequence of naturally occurring deletion mutants of cauliflower mosaic virus. Virology 112:678–685Google Scholar
  22. Howarth AJ, Vandemark GJ (1989) Phylogeny of geminiviruses. J Gen Virol 70:2717–2727Google Scholar
  23. Howell SH, Walker LL, Walden RM (1981) Rescue of in vitro generated mutants of cloned cauliflower mosaic virus genome in infected plants. Nature 293:483–486Google Scholar
  24. Hull R (1980) Structure of the cauliflower mosaic virus genome III. Restriction endonuclease mapping of thirty-three isolates. Virology 100:76–90Google Scholar
  25. Hull R, Sadler J, Longstaff M (1986) The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO J 5:3083–3090Google Scholar
  26. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedGoogle Scholar
  27. Li W-H, Tanimura M, Sharp PM (1988) Rates and dates of divergence between AIDS virus nucleotide sequences. Mol Biol Evol 5:313–330Google Scholar
  28. Lung MCY, Pirone TP (1972) Datura stramonium, a local lesion host for certain isolates of cauliflower mosaic virus. Phytopathology 62:1473–1474Google Scholar
  29. Mason WS, Taylor JM, Hull R (1987) Retroid virus genome replication. Adv Virus Res 32:35–96Google Scholar
  30. Matthews R (1991) Plant virology, 3rd ed. Academic Press, New YorkGoogle Scholar
  31. Melcher U, Choe IS, Lebeurier G, Richards K, Essenberg RC (1986) Selective allele loss and interference between cauliflower mosaic virus DNAs. Mol Gen Genet 203:230–236Google Scholar
  32. Melcher U (1989) Symptoms of cauliflower mosaic virus infection in Arabidopsis thaliana and turnip. Bot Gazette 150:139–147Google Scholar
  33. Melcher U (1990) Similarities between putative transport proteins of plant viruses. J Gen Virol 71:1009–1018Google Scholar
  34. Melcher U, Lartey RT, Pennington RE (1992) Isolate-specific synergy in symptom production between a caulimo- and a tobamovirus. Phytopathology 82:1173–1174Google Scholar
  35. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  36. Pennington RE, Melcher U (1993) In planta deletion of DNA inserts from the large intergenic region of cauliflower mosaic virus DNA. Virology 192:188–196Google Scholar
  37. Penny D, Hendy MD, Steel MA (1991) Testing the theory of descent. In: Miyamoto MM, Cracraft J (eds) Phylogenetic analysis of DNA sequences. Oxford University Press, New York, pp 155–183Google Scholar
  38. Riederer MA, Grimsley NH, Hohn B, Jiricny J (1992) The mode of cauliflower mosaic virus propagation in the plant allows rapid amplification of viable mutant strains. J Gen Virol 73:1449–1456Google Scholar
  39. Rongxiang F, Xiacjun W, Ming B, Yingchuan T, Faxing C, Kequiang M (1985) Complete nucleotide sequence of cauliflower mosaic virus (Xinjing isolate) genomic DNA. Chin J Virol 1:247–256Google Scholar
  40. Sanger M, Daubert S, Goodman RM (1991) The regions of sequence variation in caulimovirus gene VI. Virology 182:830–834Google Scholar
  41. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538Google Scholar
  42. Schoelz J, Shepherd RJ, Daubert S (1986) Region VI of cauliflower mosaic virus encodes a host range determinant. Mol Cell Biol 6: 2632–2637Google Scholar
  43. Schoelz JE, Shepherd RJ (1988) Host range control of cauliflower mosaic virus. Virology 162:30–37Google Scholar
  44. Shepherd RJ (1989) Biochemistry of DNA plant viruses. In: Marcus A (ed) The biochemistry of plants. Academic Press, New York, pp 563–616Google Scholar
  45. Shepherd RJ, Bruening GE, Wakeman RJ (1970) Double-stranded DNA from cauliflower mosaic virus. Virology 41:339–347Google Scholar
  46. Sokal RR, Rohlf FJ (1981) Taxonomic congruence in the Leptodomorpha reexamined. Syst Zool 30:309–325Google Scholar
  47. Steinhauer DA, Holland JJ (1987) Rapid evolution of RNA viruses. Annu Rev Microbiol 41:409–433Google Scholar
  48. Stenger DC, Mullin RH, Morris TJ (1988) Isolation, molecular cloning, and detection of strawberry vein banding virus DNA. Phytopathology 78:154–159Google Scholar
  49. Stratford R, Covey SN (1989) Segregation of cauliflower mosaic virus symptom genetic determinants. Virology 172:451–459Google Scholar
  50. Vaden VR, Melcher U (1990) Recombination sites in cauliflower mosaic virus DNAs: implications for mechanisms of recombination. Virology 177:717–726Google Scholar
  51. Walden RM, Howell SH (1983) Uncut recombinant plasmids bearing nested cauliflower mosaic virus genomes infect plants by intragenomic recombination. Plant Mol Biol 2:27–31Google Scholar
  52. Wintermantel WM, Schoelz JE (1992) Cauliflower mosaic virus is capable of recombination with transgenic Nicotiana bigelovii that contain CaMV coding sequences. Phytopathology 82:1110Google Scholar
  53. Woolston CJ, Covey SN, Penswick JR, Davies JW (1983) Aphid transmission and a polypeptide are specified by a defined region of the cauliflower mosaic virus genome. Gene 23:15–23Google Scholar
  54. Zhang XS, Melcher U (1989) Competition between isolates and variants of cauliflower mosaic virus in infected turnip plants. J Gen Virol 70:3427–3437Google Scholar

Copyright information

© Springer-Verlag New York Inc 1994

Authors and Affiliations

  • Chenault Kelly D. 
    • 1
  • Ulrich Melcher
    • 1
  1. 1.Department of Biochemistry and Molecular BiologyOklahoma State UniversityStillwaterUSA
  2. 2.Department of Plant PathologyOklahoma State UniversityStillwaterUSA

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