Abstract
Ascoviruses, iridoviruses, asfarviruses and poxviruses are all cytoplasmic DNA viruses. The evolutionary origins of cytoplasmic DNA viruses have never been fully addressed. Morphological, genetic and molecular data were used to test if all four cytoplasmic virus families (Ascoviridae, Iridoviridae, Asfarviridae, and Poxvirirdae) evolved from nuclear replicating baculoviruses and how the four virus groups are related. Molecular phylogenetic analyses using DNA polymerase predicted that cytoplasmic DNA viruses might have evolved from nuclear replicating baculoviruses, and that poxviruses and asfarviruses share a common ancestor with iridoviruses. These three cytoplasmic viruses again shared a common ancestor with ascoviruses. Morphological and genetic data predicted the same evolutionary trend as molecular data predicted. A genome sequence comparison showed that ascoviruses have more baculovirus protein homologues than do iridoviruses, which suggested that ascoviruses have evolved from baculoviruses and iridoviruses evolved from ascoviruses. Poxviruses showed genetic and morphological similarity to other cytoplamic viruses, such as ascoviruses, suggesting it has undergone reticulate evolution via hybridization, recombination and lateral gene transfer with other viruses. Within the ascovirus family, we tested if molecular phylogenetic analyses agree with biological inference; that is, ascovirus had an evolutionary trend of increasing genome size, expanding host range and widening tissue tropism for these viruses. Both molecular and biological data predicted this evolutionary trend. The phylogenetic relationship among the four species of ascovirus was predicted to be that TnAV-2 and HvAV-3 shared a common ancestor with SfAV-1 and the three virus species again shared a common ancestor with DpAV-4.
Similar content being viewed by others
References
Asgari S. 2006. Replication of Heliothis virescens ascovirus in insect cell lines. Arch Virol. 151: 1689–1699.
Asgaril S, Davis J, Wood D, Wilson P, et al. Sequence and organization of Heliothis virescens ascovirus genome. J Gen Virol, (in press).
Bideshi D K, Demattei. M V, Rouleux-Bonnin F, et al. 2006. Genomic sequence of Spodoptera frugiperda Ascovirus 1a, an enveloped, double-stranded DNA insect virus that manipulates apoptosis for viral reproduction. J Virol, 80: 11791–11805.
Bideshi D K, Tan Y, Bigot Y, et al. 2005. A viral caspase contributes to modified apoptosis for virus transmission. Gene Devel, 19: 1416–1421.
Bigot Y, Rabouille A, Doury G, et al. 1997a. Biological and molecular features of the relationships between Diadromus pulchellus ascovirus, a parasitoid hymenopteran wasp (Diadromus pulchellus) and its lepidopteran host, Acrolepiopsis assectella. J Gen Virol, 78: 1149–1163.
Bigot Y, Rabouille A, Sizaret P Y, et al. 1997b. Particle and genomic characterization of a new member of the Ascoviridae, Diadromus pulchellus ascovirus. J Gen Virol, 78: 1139–1147.
Browning H W, Federici B A, Oatman E R. 1982. Occurrence of a disease caused by a rickettsia-like organism in a larval population of the cabbage looper, Trichoplusia ni, in southern California. Environ Entomol, 11: 550–554.
Carner G R, Hudson J S. 1983. Histopathology of virus-like particles in Heliothis spp. J Invert Pathol, 41: 238–249.
Cheng X-W, Wang L, Carner G R, et al. 2005. Characterization of three ascovirus isolates from cotton insects. J Invertebr Pathol, 89:193–202.
Cheng X-W, Carner G R, Arif B M. 2000. A new ascovirus from Spodoptera exigua and its relatedness to the isolate from Spodoptera frugiperda. J Gen Virol, 81: 3083–3092.
Cheng X-W, Carner G R, Brown T W. 1999. Circular configuration of the genome of ascoviruses. J Gen Virol, 80: 1537–1540.
Federici B A. 1983. Enveloped double-stranded DNA insect virus with novel structure and cytopathology. Proc Natl Acad Sci USA, 80: 7664–7668.
Federici B A, Hamm J J, Styer E L. 1991. Ascoviridae. In: Atlas of Invertebrate Viruses (Adams J R and Bonami J R, eds.), Boca Raton: CRC Press, Fla. p339–349.
Federici B A, Vlak J M, Hamm J J. 1990. Comparative study of virion structure, protein composition and genomic DNA of three ascovirus isolates. J Gen Virol, 71: 1661–1668.
Federici B A, Bigot Y, Granados R R, et al.2005. Family Ascoviridae, In: Virus taxonomy. Eighth report of the International Committee on Taxonomy of Viruses (Fauguet C M, Mayo M A, Maniloff J, Desselberger U, Ball L A. eds.). Amsterdam, The Netherlands: Elsevier. p247–250.
Felsenstein J. 1993. Phylogeny inference package(PHYLIP), Version 3.5. Department of Genetics, University of Washington, Seattle.
Flint S J, Enquist L W, Racaniello V R, et al. 2004. Principles of Virology, Molecular Biology, Pathogenesis, and control of animal viruses. Washington DC: ASM press. p 918.
Granados R P. 1973. Entry of an insect poxvirus by fusion of the virus envelope with the host cell membrane. Virology, 52: 305–309.
Granados R P, Lawler K A. 1981. In vivo pathway of Autographa californica baculovirus invasion and infection. Virology, 108: 297–308.
Hamm J J, Nordlung D A, Marti O G. 1985. Effects of a nonoccluded virus of Spodoptera frugiperda (Lepidoptera: Noctuidae) on the development of a parasitoid, Cotesia marginiventris (Hymenoptera: Braconidae). Environ Entomol, 14: 258–261.
Hamm J J, Pair S D, Jr Marti O G. 1986. Incidence and host range of a new ascovirus isolated from fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae) Fla. Entomol. 69: 524–541.
Jakob N J, MuÈller K, Bahr U, et al. 2001. Analysis of the First Complete DNA Sequence of an Invertebrate Iridovirus: Coding Strategy of the Genome of Chilo Iridescent Virus. Virology, 286: 182–196.
Kusumah Y M. 2004. Biological and molecular characterization of ascovirus isolates from Indonesia and the United States (PhD. Dissertation). Clemson University. p99.
Labandeira C C, Sepkoski J. 1993. Insect diversity in the fossil record. Science, 261: 310–314.
Lauzon H A, Lucarotti C J, Krell P J, et al. 2004. Sequence and organization of the Neodiprion lecontei nucleopolyhedrovirus genome. J Virol, 78: 7023–7035.
Lopez M J, Rojas C, Vandame R, et al. 2002. Parasitoid-mediated transmission of an iridescent virus. JInvert Pathol, 80: 160–170.
Nalcacioglu R, Marks H, Vlak J M, et al. 2003. Promoter analysis of the Chilo iridescent virus DNA polymerase and major capsid protein genes. Virology, 317: 321–329.
Newton I R. 2003. The biology and characterisation of the ascoviruses (Ascoviridae: Ascovirus) of Helicoverpa armigera Hübner and Helicoverpa punctigera Wallengren (Lepidoptera: Noctuidae) in Australia. School of Life Sciences. Brisbane, University of Queensland. p191.
O’Reilly D R. 1997. Auxiliary genes of baculoviruses, In: The baculoviruses (Miller L K. ed.). New York: Plenum Press, p 267–300.
Peter M, Nakagawa J, Doree M, et al. 1990. In vitro disassembly of the nuclear lamina and M phase-specific phosphoylation of lamins by cdc2 kinase. Cell, 61: 591–602.
Salas J, Salas M L, Vinuela E. 1999. A African swine fever virus: a missing link between poxviruses and iridoviruses. In: Origin and evolution of viruses (Domingo E, Webster R and Holland J. eds.), Bath Great Britain: Academic Press, p 467–480
Stasiak K, Renault S, Demattei M, et al. 2003. Evidence for the evolution of ascoviruses from irido-viruses. J Gen Virol, 84: 2999–3009.
Swofford D L. 2002. PAUP Phylogenetic Analysis Using Parsimony (and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates
Tillman P G, Hamm J J, Styer E L, et al. 2004. Transmission of an ascovirus of Heliothis virescens (Lepidoptera: Noctuidae) and effects of the pathogen on the survival of a parasitoid, Cardiochiles nigriceps (Hymenoptera: Braconidae). Environ Entomol, 33: 633–643.
Villarreal L P. 1999. DNA virus contribution to host evolution. In: Origin and evolution of viruses (Domingo E, Webster R and Holland J. ed), Bath Great Britain: Academic Press, p 391–420.
Villarreal L P. 2005. Viruses and the evolution of life. Washington DC: ASM Press, p395
Wang L, Xue J, Seaborn C P, et al. 2006. Sequence and organization of the Trichoplusia ni ascovirus 2c (Ascoviridae) genome. Virology, 354: 167–177.
Wickens M. 1990. How the messenger got its tail: Addition of poly (A) in the nucleus. Trends in Biochemical Sciences 15: 277–281.
Williams T. 1998. Insect iridescent viruses. In: The insect viruses. (Miller L K and Ball L A ed.), New York: Plenum Press, p31–68.
Wrigley N G. 1969. An electron microscope study of the structure of Sericesthis iridescent virus. J Gen Virol, 5: 123–134.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Cheng, XW., Wan, XF., Xue, J. et al. Ascovirus and its evolution. Virol. Sin. 22, 137–147 (2007). https://doi.org/10.1007/s12250-007-0015-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12250-007-0015-2