Polydnaviruses of Braconid Wasps Derive from an Ancestral Nudivirus

Many species of parasitoid wasps inject polydnavirus particles in order to manipulate host defenses and development. Because the DNA packaged in these particles encodes almost no viral structural proteins, their relation to viruses has been debated. Characterization of complementary DNAs derived from braconid wasp ovaries identified genes encoding subunits of a viral RNA polymerase and structural components of polydnavirus particles related most closely to those of nudiviruses—a sister group of baculoviruses. The conservation of this viral machinery in different braconid wasp lineages sharing polydnaviruses suggests that parasitoid wasps incorporated a nudivirus-related genome into their own genetic material. We found that the nudiviral genes themselves are no longer packaged but are actively transcribed and produce particles used to deliver genes essential for successful parasitism in lepidopteran hosts.

[1]  R. Kleespies,et al.  Sequencing of the large dsDNA genome of Oryctes rhinoceros nudivirus using multiple displacement amplification of nanogram amounts of virus DNA. , 2008, Journal of virological methods.

[2]  J. Banks,et al.  Phylogeny of the parasitic microgastroid subfamilies (Hymenoptera: Braconidae) based on sequence data from seven genes, with an improved time estimate of the origin of the lineage. , 2008, Molecular phylogenetics and evolution.

[3]  Nicolas J. Parker,et al.  Genome Analysis of a Glossina pallidipes Salivary Gland Hypertrophy Virus Reveals a Novel, Large, Double-Stranded Circular DNA Virus , 2008, Journal of Virology.

[4]  Passarelli Al,et al.  Baculovirus late and very late gene regulation. , 2007 .

[5]  G. Rohrmann,et al.  Baculovirus DNA replication and processing. , 2007, Current drug targets.

[6]  M. Summers,et al.  Molecular biology of the baculovirus occlusion-derived virus envelope. , 2007, Current drug targets.

[7]  M. Annaheim,et al.  Transcriptional analysis of polydnaviral genes in the course of parasitization reveals segment-specific patterns. , 2007, Archives of insect biochemistry and physiology.

[8]  B. Haas,et al.  Structure and evolution of a proviral locus of Glyptapanteles indiensis bracovirus , 2007, BMC Microbiology.

[9]  N. Moran,et al.  Colloquium Papers: Symbiosis as an adaptive process and source of phenotypic complexity , 2007 .

[10]  R. Kleespies,et al.  The Genome of Gryllus bimaculatus Nudivirus Indicates an Ancient Diversification of Baculovirus-Related Nonoccluded Nudiviruses of Insects , 2007, Journal of Virology.

[11]  M. Annaheim,et al.  Genome organization of the Chelonus inanitus polydnavirus: excision sites, spacers and abundance of proviral and excised segments. , 2007, The Journal of general virology.

[12]  Supporting Online Material: Material and Methods , 2007 .

[13]  M. Strand,et al.  Inhibitor κB-like proteins from a polydnavirus inhibit NF-κB activation and suppress the insect immune response , 2005 .

[14]  L. Cattolico,et al.  A Virus Essential for Insect Host-Parasite Interactions Encodes Cystatins , 2005, Journal of Virology.

[15]  刘金明,et al.  IL-13受体α2降低血吸虫病肉芽肿的炎症反应并延长宿主存活时间[英]/Mentink-Kane MM,Cheever AW，Thompson RW，et al//Proc Natl Acad Sci U S A , 2005 .

[16]  B. Webb.  6.10 – The Biology and Genomics of Polydnaviruses , 2005 .

[17]  L. Cattolico,et al.  Bracoviruses Contain a Large Multigene Family Coding for Protein Tyrosine Phosphatases , 2004, Journal of Virology.

[18]  L. Cattolico,et al.  Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution , 2004, Science.

[19]  L. Duret,et al.  The endogenous retroviral locus ERVWE1 is a bona fide gene involved in hominoid placental physiology. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  L. Gilbert,et al.  Comprehensive molecular insect science (seven-volume set). , 2004 .

[21]  B. Webb,et al.  Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. , 2004, Annual review of entomology.

[22]  E. Herniou,et al.  The genome sequence and evolution of baculoviruses. , 2003, Annual review of entomology.

[23]  Y. Bigot,et al.  Origin and evolution of polydnaviruses by symbiogenesis of insect DNA viruses in endoparasitic wasps. , 2003, Journal of insect physiology.

[24]  S. Asgari,et al.  Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. , 2003, Journal of insect physiology.

[25]  F. Blank,et al.  Fate of polydnavirus DNA of the egg-larval parasitoid Chelonus inanitus in the host Spodoptera littoralis. , 2003, Journal of insect physiology.

[26]  Hong-Hwa Chen,et al.  Analysis of the Complete Genome Sequence of the Hz-1 Virus Suggests that It Is Related to Members of the Baculoviridae , 2002 .

[27]  E. Huguet,et al.  Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. , 2002, The Journal of general virology.

[28]  J. Whitfield.  Estimating the age of the polydnavirus/braconid wasp symbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Raina,et al.  Further characterization of the gonad-specific virus of corn earworm, Helicoverpa zea. , 2000, Journal of invertebrate pathology.

[30]  B. Webb,et al.  A gene encoding a polydnavirus structural polypeptide is not encapsidated. , 2000, Virology.

[31]  Vincent C. Emery,et al.  J. Virol. Methods , 1996 .

[32]  T. Nguyen,et al.  An insect cell line persistently infected with a baculovirus-like particle. , 1978, Intervirology.

[33]  K. Cheng.  Theory of Superconductivity , 1948, Nature.