#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Analysis of Virion Structural Components Reveals Vestiges of the Ancestral Ichnovirus Genome


Many thousands of endoparasitic wasp species are known to inject polydnavirus (PDV) particles into their caterpillar host during oviposition, causing immune and developmental dysfunctions that benefit the wasp larva. PDVs associated with braconid and ichneumonid wasps, bracoviruses and ichnoviruses respectively, both deliver multiple circular dsDNA molecules to the caterpillar. These molecules contain virulence genes but lack core genes typically involved in particle production. This is not completely unexpected given that no PDV replication takes place in the caterpillar. Particle production is confined to the wasp ovary where viral DNAs are generated from proviral copies maintained within the wasp genome. We recently showed that the genes involved in bracovirus particle production reside within the wasp genome and are related to nudiviruses. In the present work we characterized genes involved in ichnovirus particle production by analyzing the components of purified Hyposoter didymator Ichnovirus particles by LC-MS/MS and studying their organization in the wasp genome. Their products are conserved among ichnovirus-associated wasps and constitute a specific set of proteins in the virosphere. Strikingly, these genes are clustered in specialized regions of the wasp genome which are amplified along with proviral DNA during virus particle replication, but are not packaged in the particles. Clearly our results show that ichnoviruses and bracoviruses particles originated from different viral entities, thus providing an example of convergent evolution where two groups of wasps have independently domesticated viruses to deliver genes into their hosts.


Vyšlo v časopise: Analysis of Virion Structural Components Reveals Vestiges of the Ancestral Ichnovirus Genome. PLoS Pathog 6(5): e32767. doi:10.1371/journal.ppat.1000923
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1000923

Souhrn

Many thousands of endoparasitic wasp species are known to inject polydnavirus (PDV) particles into their caterpillar host during oviposition, causing immune and developmental dysfunctions that benefit the wasp larva. PDVs associated with braconid and ichneumonid wasps, bracoviruses and ichnoviruses respectively, both deliver multiple circular dsDNA molecules to the caterpillar. These molecules contain virulence genes but lack core genes typically involved in particle production. This is not completely unexpected given that no PDV replication takes place in the caterpillar. Particle production is confined to the wasp ovary where viral DNAs are generated from proviral copies maintained within the wasp genome. We recently showed that the genes involved in bracovirus particle production reside within the wasp genome and are related to nudiviruses. In the present work we characterized genes involved in ichnovirus particle production by analyzing the components of purified Hyposoter didymator Ichnovirus particles by LC-MS/MS and studying their organization in the wasp genome. Their products are conserved among ichnovirus-associated wasps and constitute a specific set of proteins in the virosphere. Strikingly, these genes are clustered in specialized regions of the wasp genome which are amplified along with proviral DNA during virus particle replication, but are not packaged in the particles. Clearly our results show that ichnoviruses and bracoviruses particles originated from different viral entities, thus providing an example of convergent evolution where two groups of wasps have independently domesticated viruses to deliver genes into their hosts.


Zdroje

1. VolkoffAN

RavallecM

BossyJP

CeruttiP

RocherJ

1995 The replication of Hyposoter didymator polydnavirus: Cytopathology of the calyx cells in the parasitoid. Biology of the Cell 83 1 13

2. EspagneE

DupuyC

HuguetE

CattolicoL

ProvostB

2004 Genome sequence of a polydnavirus: insights into symbiotic virus evolution. Science 306 286 289

3. LapointeR

TanakaK

BarneyWE

WhitfieldJB

BanksJC

2007 Genomic and morphological features of a banchine polydnavirus: comparison with bracoviruses and ichnoviruses. J Virol 81 6491 6501

4. TanakaK

LapointeR

BarneyWE

MakkayAM

StoltzD

2007 Shared and species-specific features among ichnovirus genomes. Virology 363 26 35

5. WebbBA

StrandMR

DickeySE

BeckMH

HilgarthRS

2006 Polydnavirus genomes reflect their dual roles as mutualists and pathogens. Virology 347 160 174

6. CussonM

LaforgeM

MillerD

CloutierC

StoltzD

2000 Functional significance of parasitism-induced suppression of juvenile hormone esterase activity in developmentally delayed Choristoneura fumiferana larvae. Gen Comp Endocrinol 117 343 354

7. KaeslinM

Pfister-WilhelmR

LanzreinB

2005 Influence of the parasitoid Chelonus inanitus and its polydnavirus on host nutritional physiology and implications for parasitoid development. J Insect Physiol 51 1330 1339

8. MalvaC

VarricchioP

FalabellaP

La ScaleiaR

GrazianiF

2004 Physiological and molecular interaction in the host-parasitoid system Heliothis virescens-Toxoneuron nigriceps: current status and future perspectives. Insect Biochem Mol Biol 34 177 183

9. ShelbyKS

WebbBA

1999 Polydnavirus-mediated suppression of insect immunity. J Insect Physiol 45 507 514

10. FlemingJG

SummersMD

1991 Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proc Natl Acad Sci U S A 88 9770 9774

11. SavaryS

BeckageN

TanF

PeriquetG

DrezenJM

1997 Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastinae) at potential recombinase binding sites. J Gen Virol 78 (Pt 12) 3125 3134

12. BezierA

AnnaheimM

HerbiniereJ

WetterwaldC

GyapayG

2009 Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323 926 930

13. BezierA

HerbiniereJ

LanzreinB

DrezenJM

2009 Polydnavirus hidden face: the genes producing virus particles of parasitic wasps. J Invertebr Pathol 101 194 203

14. MurphyN

BanksJC

WhitfieldJB

AustinAD

2008 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. Mol Phylogenet Evol 47 378 395

15. Abd-AllaAM

VlakJM

BergoinM

MaruniakJE

ParkerA

2009 Hytrosaviridae: a proposal for classification and nomenclature of a new insect virus family. Arch Virol 154 909 918

16. Garcia-MaruniakA

Abd-AllaAM

SalemTZ

ParkerAG

LietzeVU

2009 Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J Gen Virol 90 334 346

17. StoltzDB

VinsonSB

1979 Penetration into caterpillar cells of virus-like particles injected during oviposition by parasitoid ichneumonid wasps. Can J Microbiol 25 207 216

18. WebbBA

1998 Polydnavirus biology, genome structure, and evolution.

MillerLK

BallLA

The insect viruses New York Plenum Publishing Corporation 105 139

19. KrellPJ

StoltzDB

1980 Virus-like particles in the ovary of an ichneumonid wasp: purification and preliminary characterization. Virology 101 408 418

20. KrellPJ

SummersMD

VinsonSB

1982 Virus with a multipartite superhelical DNA genome from the ichneumonid parasitoid Campoletis sonorensis. Journal of Virology 43 859 870

21. DengL

StoltzDB

WebbBA

2000 A gene encoding a polydnavirus structural polypeptide is not encapsidated. Virology 269 440 450

22. DengL

WebbBA

1999 Cloning and expression of a gene encoding a Campoletis sonorensis polydnavirus structural protein. Arch Insect Biochem Physiol 40 30 40

23. BigotY

SamainS

Auge-GouillouC

FedericiBA

2008 Molecular evidence for the evolution of ichnoviruses from ascoviruses by symbiogenesis. BMC Evol Biol 8 253

24. KrellP

1991 Polydnaviridae.

AdamsJR

Atlas of Invertebrate Viruses Boca Raton, FL CRC Press 321 338

25. Suzan-MontiM

La ScolaB

RaoultD

2006 Genomic and evolutionary aspects of Mimivirus. Virus Res 117 145 155

26. DavisonAJ

TrusBL

ChengN

StevenAC

WatsonMS

2005 A novel class of herpesvirus with bivalve hosts. J Gen Virol 86 41 53

27. NegreV

HotelierT

VolkoffAN

GimenezS

CousseransF

2006 SPODOBASE: an EST database for the lepidopteran crop pest Spodoptera. BMC Bioinformatics 7 322

28. MatzMV

2003 Amplification of representative cDNA pools from microscopic amounts of animal tissue. Methods Mol Biol 221 103 116

29. RamakersC

RuijterJM

DeprezRH

MoormanAF

2003 Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339 62 66

30. VolkoffAN

CeruttiP

RocherJ

OhresserMC

DevauchelleG

1999 Related RNAs in lepidopteran cells after in vitro infection with Hyposoter didymator virus define a new polydnavirus gene family. Virology 263 349 363

31. LaemmliUK

1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680 685

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2010 Číslo 5
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#