Enveloped double-stranded DNA insect virus with novel structure and cytopathology

Abstract

An unusual type of virus has been isolated from larvae of the cabbage looper, Trichoplusia ni (Lepidoptera; Noctuidae). The virus infects a variety of tissues, including fat body, epidermis, and tracheal matrix, causing a chronic, fatal disease. Viral replication begins in the nucleus and is accompanied by invagination of the nuclear envelope and extensive nuclear and cellular hypertrophy. The nuclear envelope eventually ruptures and fragments, after which viral-induced membranes are assembled along planes through the cell and around its periphery. Subsequently, these membranes coalesce, partitioning most of the cell, including viroplasms and virions in various stages of assembly, among a cluster of vesicles. The vesicles dissociate and are liberated into the hemolymph where they accumulate in large numbers (>108 vesicles per ml), causing the blood to become opaque white. The virus has been isolated from T. ni and transmitted per os and by injection to T. ni and several other species of the family Noctuidae. The virions produced by this virus are large (ca. 130 X 400 nm), enveloped, and allantoid in shape with complex symmetry and contain apparently linear, double-stranded DNA of M, of 1.00 x 108. The envelope contains subunits arranged in a hexagonal pattern that impart a distinctive reticular appearance to virions in negatively stained preparations. The unique structural and developmental properties of this virus indicate that it is a member of a group of enveloped, double-stranded DNA viruses not observed previously.An unusual type of virus not observed previously has been found causing a chronic but ultimately fatal disease in larvae of the noctuid moths Scotogramma trifolii (1), Trichoplusia ni (2), and Heliothis zea (3) (order, Lepidoptera; family, Noctuidae). The most unusual feature of this virus is that it induces the host cell to cleave into a cluster of virion-containing vesicles. These vesicles are highly refractile, typically range in diameter from 2 to 12 gm and, after cleavage of the host cell, dissociate and are liberated into the hemolymph where they accumulate in large numbers (>108 vesicles per ml) as the disease progresses. An additional unusual feature of this virus is the unique structure of the virion, which is a large enveloped particle, essentially allantoid in shape, with an envelope that exhibits a distinctive hexagonal pattern in negatively stained preparations.In two initial reports on the disease caused by this virus, the identity of the pathogen was not confirmed (1, 2). It was suggested that the causative agent was either a new type of virus or, because of its large size, shape, and occurrence in membrane-bound vesicles, a peculiar type of Rickettsia. A more definitive characterization of the disease in S. trifolii was not undertaken because attempts to transmit the virus in the laboratory were unsuccessful. However, the occurrence of the virus in populations of T. ni throughout the year permitted the collection of diseased insects on a regular basis and enabled the devel...

Evidence for the evolution of ascoviruses from iridoviruses

“…An unusual property not found in other insect viruses but shared by iridoviruses and ascoviruses is that both are poorly infectious per os (Federici, 1983;. How iridoviruses are transmitted in nature is not well understood.…”

“…This relationship was unexpected owing to significant differences between the structure of their virions and genomes, and because of major differences in their cell biology. Ascoviruses destroy the cell nucleus, assemble virions in the anucleate cell, and subsequently induce cell cleavage resulting in virion-containing vesicles (Federici, 1983;. In contrast, iridoviruses leave the nucleus intact, assemble virions in the cytoplasm, and cause comparatively little gross cellular pathology other than hypertrophy (Federici, 1993;Williams et al, 2000).…”

“…Ascoviruses studied were Spodoptera frugiperda ascovirus (SfAV-1a), Trichoplusia ni ascovirus (TnAV-2a), Heliothis virescens ascovirus (HvAV-3b and c) and Diadromus pulchellus ascovirus (DpAV-4a), all described previously (Bigot et al, 1997a, b;Federici, 1983;Pellock et al, 1996;Stasiak et al, 2000). Regular mosquito iridovirus (RMIV; Invertebrate iridescent virus 3) was provided by J. Becnel (USDA, Gainesville, FL, USA).…”

“…Mechanisms of transmission are not well understood, though transmission horizontally through wounds and vertically through eggs is known. Alternatively, ascoviruses cause a chronic fatal disease restricted to larvae and pupae of lepidopteran insects (Bigot et al, 1997a, b;Federici, 1983;Federici et al, , 2000. The disease is unique in that ascoviruses induce host cells to cleave into clusters of virion-containing vesicles (Federici, 1983).…”

“…Alternatively, ascoviruses cause a chronic fatal disease restricted to larvae and pupae of lepidopteran insects (Bigot et al, 1997a, b;Federici, 1983;Federici et al, , 2000. The disease is unique in that ascoviruses induce host cells to cleave into clusters of virion-containing vesicles (Federici, 1983). Virions are large, 300-400 nm long by 100-150 nm in diameter, enveloped, and vary in shape from ovoidal to allantoid to bacilliform among different species.…”