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Insect±virus relationships: sifting
by informatics
David Dall,
1
* Teresa Luque,
2
and David O'Reilly
2
Summary
Several groups of large DNA viruses successfully utilise
the rich resource provided by insect hosts. Defining the
mechanisms that enable these pathogens to optimise
their relationships with their hosts is of considerable
scientific and practical importance, but our understand-
ing of the processes involved is, as yet, rudimentary. Here
we describe an informatics-based approach that uses
comparison of viral genomic sequences to identify
candidate genes likely to be specifically involved in this
process. We hypothesise that such genes should satisfy
two essential criteria, namely, that they should be (i)
present in those members of a virus family that infect
insects, but absent from those that infect other hosts, and
(ii) found in at least two unrelated taxa of insect viruses.
These criteria currently identify six groups of viral genes,
including one that encodes the fusolin/gp37 proteins.
Demonstration that the fusolin/gp37 proteins can en-
hance oral infectivity of insect viruses provides a primary
validation of this approach to the examination of insect-
virus relationships. BioEssays 23:184±193, 2001.
ß 2001 John Wiley & Sons, Inc.
Introduction
The availability of genomic sequences for many vertebrate-
infecting viruses and their cognate hosts has allowed
identification of virally encoded proteins that influence the
relationship between host and pathogen. For example, studies
of the interactions between poxviruses and vertebrate hosts
have been greatly advanced by demonstration that the viruses
encode proteins with sequence relationships to host immuno-
modulatory factors, such as elements of the complement
cascade
(1)
and cytokine receptors.
(2)
More recently, database
``mining'' has revealed the presence of homologous inter-
leukin-binding proteins encoded by both vertebrate and
poxvirus genomes.
(3)
Similar approaches have provided
evidence that herpesviruses encode a range of proteins that
are related to host genes, some of which are involved in host
immune function and cell cycle control.
(4)
This productive approach to the investigation of verte-
brate±virus relationships is, however, essentially unavailable
for use in analysis of insect±virus relationships, principally
because of the current dearth of sequence information relating
to the insect hosts. Most of the well-characterised viruses of
insects have been studied with a view to their potential use as
biological control agents of insect pests and, as such, their
hosts are largely caterpillars, beetles, locusts, etc. While these
host taxa are, collectively, among the most abundant on earth,
and certainly of great significance to global agricultural
production, pertinent genomic sequence information is cur-
rently scarce.
Nevertheless, we hypothesise that an alternative infor-
matics-based route can be used to identify genes or gene
products that specifically influence relationships between
invertebrate hosts and viruses, namely, multidirectional
comparisons of viral genomic sequences. We hypothesise
that genes likely to encode such factors should, at the least,
satisfy two criteria, namely, they should be (i) present in insect-
infecting members of a virus family but absent from any
vertebrate-infecting members of the same family, and (ii)
found in at least two unrelated taxa of insect viruses. This
hypothesis is described here in relation to insect-infecting
viruses that possess large double-stranded DNA (dsDNA)
genomes, namely, members of the Baculoviridae, Poxviridae
and Iridoviridae although, in principle, it could be extended to
other groups of insect pathogens as well.
In following sections, we thus consider ``within family'' and
``between family'' comparisons of viral genomic sequences.
The former involves comparison of insect-infecting and other
members of a single virus family (e.g., of the insect- and
vertebrate-infecting poxviruses), in order to satisfy the first
184 BioEssays 23.2 BioEssays 23:184±193, ß 2001 John Wiley & Sons, Inc.
1
CSIRO Entomology, Canberra, Australia.
2
Department of Biology, Imperial College, London, UK.
Funding agencies: The Australian Academy of Science and Australian
Academy of Technical Sciences and Engineering Scientific and
Technological Exchange Program with the Royal Society.
*Correspondence to: Dr. David Dall, CSIRO Entomology, GPO Box
1700, Canberra, ACT 2001, Australia.
Abbreviations: ChPV, chordopoxvirus; EPV, entomopoxvirus; ER,
endoplasmic reticulum; GV, granulovirus; IV, iridovirus; NPV, nucleo-
polyhedrovirus; ORF, open reading frame; SB, spindle bodies.
Taxonomic abbreviations: AcNPV, Autographa californica NPV;
BmNPV, Bombyx mori NPV; CIV, Chilo IV; CbEPV, Choristoneura
biennis EPV; CpGV, Cydia pomonella GV; HaEPV, Heliothis armigera
EPV; HaGV, Helicoverpa armigera GV; HzNPV, Helicoverpa zea
NPV; LdNPV, Lymantria dispar NPV; MsEPV, Melanoplus sangui-
nipes EPV; OpNPV, Orgyia pseudotsugata NPV; PxGV, Plutella
xylostella GV; PuGV, Pseudaletia unipuncta GV; SeNPV, Spodoptera
exigua NPV; TnGV, Trichoplusia ni GV; XcGV, Xestia c-nigrum GV.
Genes and genomes