Evolution of Immunosuppressive Organelles from DNA Viruses in Insects
Endoparasitic wasps inject particles into their lepidopteran hosts that enable these parasitoids to evade or directly suppress the hosts’ innate immune response, especially encapsulation by hemocytes. For decades, these particles have been considered viri
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Evolution of Immunosuppressive Organelles from DNA Viruses in Insects Brian A. Federici and Yves Bigot
Abstract Endoparasitic wasps inject particles into their lepidopteran hosts that enable these parasitoids to evade or directly suppress the hosts’ innate immune response, especially encapsulation by hemocytes. For decades, these particles have been considered virions produced by DNA viruses known as polydnaviruses (family Polydnaviridae). Structurally, there are two main types of particles, those resembling, respectively, virions of baculoviruses or ascoviruses. These particles contain double-stranded DNA in the form of multiple small circular molecules that are transcribed but not replicated in cells of the lepidopteran hosts. Instead particle DNA is replicated from the wasp genome and selectively amplified for packaging into the particles in the reproductive tract of female wasps. Once assembled and secreted into calyx lumen, the particles become mixed with eggs and injected into caterpillars during wasp oviposition. Particle DNA, referred to as the “viral genome,” has now been sequenced for several polydnaviruses. Annotation shows that most of this DNA consists of noncoding DNA or wasp genes, not viral genes. More significantly, recent studies have shown that particle structural proteins are coded by the wasp genome, not by particle DNA, but are of viral origin. Together, these findings provide strong evidence that these particles originated from viruses, but through symbiogenesis followed by gene deletion and acquisition evolved into transducing organelles that shuttle wasp immunosuppressive genes into their hosts, thereby enhancing wasp progeny survival and species radiation.
B.A. Federici Department of Entomology, University of California, Riverside 900 University Avenue, Riverside, California 92521, USA Laboratoire d’Etude des Parasites Ge´ne´tiquesParc Grandmont, Universite´ de Tours, U.F.R. des Sciences et Techniques, 37200, Tours, France e-mail: [email protected] Y. Bigot Laboratoire d’Etude des Parasites Ge´ne´tiquesParc Grandmont, Universite´ de Tours, U.F.R. des Sciences et Techniques, 37200 Tours, France
P. Pontarotti (ed.), Evolutionary Biology – Concepts, Molecular and Morphological Evolution, DOI 10.1007/978-3-642-12340-5_14, # Springer-Verlag Berlin Heidelberg 2010
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B.A. Federici and Y. Bigot
Introduction
14.1.1 Background George Salt at the University of Cambridge published a series of pioneering studies during the 1960s aimed at understanding how endoparasitic wasps circumvented the innate immune response of their caterpillar hosts. Based on studies of the ichneumonid parasitoid, Venturia (then Nemeritis) canescens and its lepidopteran host, larvae of the Mediterranean flower moth, Ephestia kuehniella, he determined that parasitoid eggs gained protection as they passed through the calyx (egg storage region) of the female wasp’s reproductive tract (Salt 1965, 1966, 1968). This protection was due to a coating added to the eggs in the calyx. Subsequently, Susan Rotheram,
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