Skip to main content
SpringerLink
Log in

Phylogenetic relationships reveal recombination among isolates of cauliflower mosaic virus

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 19:239–249

    Google Scholar 

  • Blok J, Mackenzie A, Guy P, Gibbs A (1987) Nucleotide sequence comparisons of turnip yellow mosaic virus isolates from Australia and Europe. Arch Virol 97:283–295

    Google Scholar 

  • Chenault KD, Melcher U (1993) The complete nucleotide sequence of cauliflower mosaic virus isolate BBC. Gene 123:255–257

    Google Scholar 

  • Chenault KD, Melcher U (1994) Patterns of nucleotide sequence variation among cauliflower mosaic virus isolates. Biochimie 76:3–8

    Google Scholar 

  • Choe IS, Melcher U, Richards K, Lebeurier G, Essenberg RC (1985) Recombination between mutant cauliflower mosaic virus DNAs. Plant Mol Biol 5:281–289

    Google Scholar 

  • Daubert SD, Schoelz J, Debao L, Shepherd RJ (1984) Expression of disease symptoms in cauliflower mosaic virus genomic hybrids. J Mol Appl Gen 2:537–547

    Google Scholar 

  • Dawson WO (1992) Tobamovirus-plant interactions. Virology 186: 359–367

    Google Scholar 

  • Dixon L, Nyffenegger T, Delley G, Martinez-Izquierdo J, Hohn T (1986) Evidence for replicative recombination in cauliflower mosaic virus. Virology 150:463–468

    Google Scholar 

  • Donis R, Bean WJ, Kawaoka Y, Webster RG (1989) Distinct lineages of influenza virus H4 hemagglutinin genes in different regions of the world. Virology 169:408–417

    Google Scholar 

  • Dykhuizen DE, Green L (1991) Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173:7257–7268

    Google Scholar 

  • Falk BW, Bruening G (1994) Will transgenic crops generate new viruses and new diseases? Science 263:1395–1396

    Google Scholar 

  • Felsenstein J (1989) PHYLIP-phylogeny inference package. Cladistics 5:164–166

    Google Scholar 

  • Franck A, Guilley H, Jonard G, Richards K, Hirth L (1980) Nucleotide sequence of cauliflower mosaic virus DNA. Cell 21:285–294

    Google Scholar 

  • 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 16:8377–8390

    Google Scholar 

  • 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 187:525–533

    Google Scholar 

  • Gojobori T, Moriyama EN, Kimura M (1990) Molecular clock of viral evolution, and the neutral theory. Proc Natl Acad Sci U S A 87: 10015–10018

    Google Scholar 

  • Gracia O, Shepherd RJ (1985) Cauliflower mosaic virus in the nucleus of Nicotiana. Virology 146:141–145

    Google Scholar 

  • Grimsley N, Hohn T, Hohn B (1986) Recombination in a plant virus: template-switching in cauliflower mosaic virus. EMBO J 5:641–646

    Google Scholar 

  • 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 17:9993–10013

    Google Scholar 

  • Holland JJ, De La Torre JC, Steinhauer DA (1992) RNA virus populations as quasispecies. Curr Top Microbiol Immunol 176:1–20

    Google Scholar 

  • Howarth AJ, Gardner RC, Messing J, Shepherd RJ (1981) Nucleotide sequence of naturally occurring deletion mutants of cauliflower mosaic virus. Virology 112:678–685

    Google Scholar 

  • Howarth AJ, Vandemark GJ (1989) Phylogeny of geminiviruses. J Gen Virol 70:2717–2727

    Google Scholar 

  • Howell SH, Walker LL, Walden RM (1981) Rescue of in vitro generated mutants of cloned cauliflower mosaic virus genome in infected plants. Nature 293:483–486

    Google Scholar 

  • Hull R (1980) Structure of the cauliflower mosaic virus genome III. Restriction endonuclease mapping of thirty-three isolates. Virology 100:76–90

    Google Scholar 

  • Hull R, Sadler J, Longstaff M (1986) The sequence of carnation etched ring virus DNA: comparison with cauliflower mosaic virus and retroviruses. EMBO J 5:3083–3090

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    CAS  PubMed  Google Scholar 

  • Li W-H, Tanimura M, Sharp PM (1988) Rates and dates of divergence between AIDS virus nucleotide sequences. Mol Biol Evol 5:313–330

    Google Scholar 

  • Lung MCY, Pirone TP (1972) Datura stramonium, a local lesion host for certain isolates of cauliflower mosaic virus. Phytopathology 62:1473–1474

    Google Scholar 

  • Mason WS, Taylor JM, Hull R (1987) Retroid virus genome replication. Adv Virus Res 32:35–96

    Google Scholar 

  • Matthews R (1991) Plant virology, 3rd ed. Academic Press, New York

    Google Scholar 

  • Melcher U, Choe IS, Lebeurier G, Richards K, Essenberg RC (1986) Selective allele loss and interference between cauliflower mosaic virus DNAs. Mol Gen Genet 203:230–236

    CAS  Google Scholar 

  • Melcher U (1989) Symptoms of cauliflower mosaic virus infection in Arabidopsis thaliana and turnip. Bot Gazette 150:139–147

    Google Scholar 

  • Melcher U (1990) Similarities between putative transport proteins of plant viruses. J Gen Virol 71:1009–1018

    Google Scholar 

  • Melcher U, Lartey RT, Pennington RE (1992) Isolate-specific synergy in symptom production between a caulimo- and a tobamovirus. Phytopathology 82:1173–1174

    Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pennington RE, Melcher U (1993) In planta deletion of DNA inserts from the large intergenic region of cauliflower mosaic virus DNA. Virology 192:188–196

    Google Scholar 

  • 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 155–183

    Google Scholar 

  • 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 73:1449–1456

    Google Scholar 

  • 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 1:247–256

    Google Scholar 

  • Sanger M, Daubert S, Goodman RM (1991) The regions of sequence variation in caulimovirus gene VI. Virology 182:830–834

    Google Scholar 

  • Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:526–538

    Google Scholar 

  • Schoelz J, Shepherd RJ, Daubert S (1986) Region VI of cauliflower mosaic virus encodes a host range determinant. Mol Cell Biol 6: 2632–2637

    Google Scholar 

  • Schoelz JE, Shepherd RJ (1988) Host range control of cauliflower mosaic virus. Virology 162:30–37

    Google Scholar 

  • Shepherd RJ (1989) Biochemistry of DNA plant viruses. In: Marcus A (ed) The biochemistry of plants. Academic Press, New York, pp 563–616

    Google Scholar 

  • Shepherd RJ, Bruening GE, Wakeman RJ (1970) Double-stranded DNA from cauliflower mosaic virus. Virology 41:339–347

    Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Taxonomic congruence in the Leptodomorpha reexamined. Syst Zool 30:309–325

    Google Scholar 

  • Steinhauer DA, Holland JJ (1987) Rapid evolution of RNA viruses. Annu Rev Microbiol 41:409–433

    Google Scholar 

  • Stenger DC, Mullin RH, Morris TJ (1988) Isolation, molecular cloning, and detection of strawberry vein banding virus DNA. Phytopathology 78:154–159

    Google Scholar 

  • Stratford R, Covey SN (1989) Segregation of cauliflower mosaic virus symptom genetic determinants. Virology 172:451–459

    Google Scholar 

  • Vaden VR, Melcher U (1990) Recombination sites in cauliflower mosaic virus DNAs: implications for mechanisms of recombination. Virology 177:717–726

    Google Scholar 

  • Walden RM, Howell SH (1983) Uncut recombinant plasmids bearing nested cauliflower mosaic virus genomes infect plants by intragenomic recombination. Plant Mol Biol 2:27–31

    Google Scholar 

  • Wintermantel WM, Schoelz JE (1992) Cauliflower mosaic virus is capable of recombination with transgenic Nicotiana bigelovii that contain CaMV coding sequences. Phytopathology 82:1110

    Google Scholar 

  • 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 23:15–23

    Google Scholar 

  • Zhang XS, Melcher U (1989) Competition between isolates and variants of cauliflower mosaic virus in infected turnip plants. J Gen Virol 70:3427–3437

    Google Scholar 

Download references

Author information

Author notes

  1. Chenault Kelly D.

    Present address: Department of Plant Pathology, Oklahoma State University, 74078, Stillwater, OK, USA

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, Oklahoma State University, 74078, Stillwater, OK, USA

    Chenault Kelly D. & Ulrich Melcher

Authors
  1. Chenault Kelly D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulrich Melcher
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Correspondence to: U. Melcher

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chenault, K., Melcher, U. Phylogenetic relationships reveal recombination among isolates of cauliflower mosaic virus. J Mol Evol 39, 496–505 (1994). https://doi.org/10.1007/BF00173419

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00173419

Key words

Search

Navigation