Elsevier

Biotechnology Advances

Volume 24, Issue 2, March–April 2006, Pages 143-160
Biotechnology Advances

Baculoviruses — re-emerging biopesticides

https://doi.org/10.1016/j.biotechadv.2005.09.001Get rights and content

Abstract

Biological control of agricultural pests has gained importance in recent years due to increased pressure to reduce the use of agrochemicals and their residues in the environment and food. Viruses of a few families are known to infect insects but only those belonging to the highly specialized family Baculoviridae have been used as biopesticides. They are safe to people and wildlife, their specificity is very narrow. Their application as bioinsecticides was limited until recently because of their slow killing action and technical difficulties for in vitro commercial production. Two approaches for the wider application of baculoviruses as biopesticides will be implemented in future. In countries where use of genetically modified organisms is restricted, the improvements will be mainly at the level of diagnostics, in vitro production and changes in biopesticide formulations. In the second approach, the killing activity of baculoviruses may be augmented by genetic modifications of the baculovirus genome with genes of another natural pathogen. It is expected that the baculoviruses improved by genetic modifications will be gradually introduced in countries which have fewer concerns towards genetically modified organisms.

Introduction

Biological regulation can be defined as a regulation of a species which has reached the level of a pest by another living organism added to the environment to suppress pest densities. So it is ecologically based management of pests by naturally occurring, or genetically modified enemies. Natural enemy choice will vary greatly depending on the target species. Apart from predators, insects have many natural pathogens; these include bacteria, fungi, nematodes and viruses. These pathogens when applied artificially as microbial pesticides may effectively suppress pests. The population of microbial pathogens and/or predators increases because pests are used as a nutritional source and this, in turn, leads to the gradual decline of pest population. Biological control can be potentially permanent because the natural enemies supplied from the outside will establish themselves in the pest population and are likely to exert long-term protection against the target pest species.

The ways to implement biological regulation can be roughly divided into three major groups: importation, conservation/augmentation of natural enemies (which includes predators, parasitoids and causal agents of diseases), and application of microbial pesticides. Importation can be defined as the introduction of a foreign agent for biological regulation of populations while conservation and augmentation comprise the actions which preserve a native agent and provide the conditions for a native agent to increase its number and opportunities to act as homeostatic factor against a pest. Out of these methods, the importation of foreign enemies poses the greatest risk of changing the ecological equilibrium (Myers et al., 2000). On the other hand, one of the most successful attempts to introduce a bioregulatory agent was achieved by introduction of a foreign species. As early as the end of XIXth century, Australian species of a ladybug, Rodalia cardinalis, was introduced into California orange orchards to control cottony cushion scale, Icerya purchasi. Within few years, ladybugs reduced the pest to marginal numbers. The remaining methods are widely used and are relatively safe for the environment. Overall, the benefits from the successes in using biopesticides outweigh by far the money lost on failures which occasionally occur. Economic benefits, though important, are not the only advantages of biocontrol. Animal life, farmers and their families also greatly benefit, as successful biocontrol reduces the exposure to harmful chemicals.

Microbial pesticides are probably the most widely used and cheaper than the other methods of pest bioregulation. Insects can be infected with many species of bacteria but the species belonging to the genus Bacillus are the most widely used pesticides. Of these Bacillus thuringiensis is the most successful. It is a gram-positive, spore-forming bacterium with parasporal crystals. B. thuringiensis has developed an array of molecular mechanisms to produce pesticidal toxins, most of them coded by several cry genes (Agaisse and Lereclus, 1995). There are about 200 registered B. thuringiensis products in the USA and at the end of the last century worldwide sales amounted to about 100 million dollars (about 2% of the total global insecticide market). Though the resistance to Cry proteins may develop after prolonged usage (Schnepf et al., 1998), safety considerations favour the future development of these toxins and their share in pesticide market steadily increases.

An extensive number of fungi are associated with a variety of insects and other arthropods, establishing diverse interactions, including the pathogenicity. Approximately 750 species, belonging to 100 genera, of entomopathogenic fungi have been reported, but only about ten of them have been or are now being developed for insect control (Hajek and St. Lager, 1994). According to Benjamin et al. (2004), the entomopathogenic fungi can be classified into two main groups:

  • Biotrophic fungi. These fungi require living cells of their hosts, some of them are commensals that obtain nutrients from the digestive tract of the insect. This class of fungi is wide-spread in many regions, but they are not broadly used for pest control since they are either asymptomatic in insects or the changes caused by pathogens are difficult to observe (Lacey and Kaya, 2000).

  • Necrotrophic fungi. These are the fungi that live at the expense of dead cells; they have to kill their hosts before consuming it. Fungi belonging to this group are very effective in their attack, for this reason many of them are potential agents of biological control of insects. They can attack insects of the orders Coleoptera, Lepidoptera, Hymenoptera, Hemiptera, Orthoptera, Homoptera, Diptera; the attack can occur in several stages of their life cycles (Goettel and Johnson, 1995). Several toxic compounds have been isolated from some species of fungi belonging to the genera Beauveria, Metarhizium, Nomuraea, Aspergillus, Verticillium, Paecilomyces, Isaria, Fusarium, Cordyceps, Entomophthora. One of the substances well studied is the beauverin, a peptide isolated from B. bassiana, with activity against mosquito larvae (Uribe and Khachatourians, 2004). Some species of entomopathogenic fungi possess specificity against their hosts but usually they have a wide spectrum of action. The choice of the host is based on the biochemical affinity to the substrate and not on its morphological characters. This situation has been observed for B. bassiana, N. rileyi and M. anisopliae which can infect about 100 species of insects of a wide variety of orders of insects (Bidochka et al., 2001, Devi, 1994, Fang et al., 2005). Fungi belonging to the genera Beauveria and Metarhizium has been found to be effective against many insect pests including African locust (Langewald et al., 1999). These fungi are formulated as commercial products and are good alternatives to organophosphate and organochlorinated pesticides, mainly because some of them are exerting long-term effect and persistence in the environment. New generation fungi pesticides are often engineered to produce substances significantly improving biocontrol effectiveness (St. Lager et al., 1996).

Some nematodes, mostly those belonging to families Steinerrnematidae and Heterorhabditidae, are successfully used to control insects. In the strict sense of the word nematodes are multicellular eukaryotic organisms which do not belong to the microbial world. However, a close look at the mechanism of action of nematodes on insects justifies the classification of nematodes as microbial pesticides. Entomopathogenic nematodes penetrate insect hosts through natural openings and then defecate symbiotic bacteria belonging to genera Xenorhabdus or Photorhabdus. The bacteria quickly kill the hosts with toxins (Blackburn et al., 1998, Brown et al., 2004) and nematodes then reproduce in decaying host tissues. Nematodes are sensitive to desiccation, so their use is limited to control of pests in moist habitats.

Viruses of fifteen families are known to infect insects but only those belonging to the highly specialized family Baculoviridae have been considered as potential pesticides. They are very safe to people and wildlife. Their specificity is very narrow, often it is limited to only one species. They have been used worldwide but their application as bioinsecticides was limited (a few millions of dollars annually for the end of last century). Expansion of baculoviruses as commercial insecticides was hampered by their slow killing action and technical difficulties for in vitro commercial production. Due to the slow killing action of baculoviruses, primary users (used to fast-killing chemical insecticides) regarded them as ineffective. This attitude changes with time and baculovirus protection becomes a method of choice for long term protection of crops. Up to date the most successful project was implemented in Brazil where over two million hectares of soybean are controlled by baculovirus AgMNPV (Moscardi, 1999, Moscardi and Santos, 2005). The success of Brazilian project revived the interest in baculovirus as a biopesticide and gradually many countries have begun to increase the area of fields and forests to be experimentally protected by baculovirus pesticides.

Section snippets

Molecular biology of baculoviruses

Baculoviruses are the major group of arthropod viruses well known due to their potential as agents of biological control of pests in agriculture and forestry. They are also widely used as expression vectors in biotechnology. The family Baculoviridae comprises two genera: the Nucleopolyhedrovirus (NPVs) and the Granulovirus (GVs) (Van Regenmortel et al., 2000). NPVs can be phylogenetically subdivided into group I and group II. These viruses produce a large number of occlusion bodies in infected

Baculovirus pesticides — past and present

The attempts to use baculoviruses for the protection of European forests date back to 19th century but the first introduction of baculovirus into the environment which resulted in successful regulation of the pest in a large area occurred accidentally in 1930 s (reviewed by Moscardi, 1999). A parasitoid was imported from Scandinavia to Canada to control spruce sawfly Diprion hercyniae. Along with a parasitoid, an NPV specific for spruce sawfly was introduced which established itself in Canada (

Future prospects

In the preceding chapter many naturally occurring baculoviruses were described which have been used as pesticides in a number of cropping systems worldwide. The most spectacular success—protection of over 2 million hectares of soybean fields against velvet bean caterpillar was a breakthrough which proved that the baculovirus protection is feasible and can be done at relatively low cost. Therefore, we can expect that after a lag period lasting for many years, more and more attempts will be made

References (147)

  • R. Eldridge et al.

    Expression of an eclosion hormone gene in insect cells using baculovirus vectors

    Insect Biochem

    (1991)
  • P.F. Entwistle et al.

    Avian dispersal of nuclear polyhedrosis virus after induced epizootics in the pine beauty moth, Panolis flammea (Lepidoptera: Noctuidae)

    Biol Control

    (1993)
  • J.R. Fuxa et al.

    Vertical transmission of TnSNPV, TnCPV, AcMNPV, and possibly recombinant NPV in Trichoplusia ni

    J Invertebr Pathol

    (2002)
  • E. Gershburg et al.

    Baculovirus-mediated expression of a scorpion depressant toxin improves the insecticidal efficacy achieved with excitatory toxins

    FEBS Lett

    (1998)
  • R.R. Granados et al.

    A new insect cell line from Trichoplusia ni (BTI-Tn-5B1-4) susceptible to Trichoplusia ni single nuclear polyhedrosis virus

    J Invertebr Pathol

    (1994)
  • R.L. Harrison et al.

    Use of scorpion neurotoxins to improve the insecticidal activity of Rachiplusia ou multicapsid nucleopolyhedrovirus

    Biol Control

    (2000)
  • R.L. Harrison et al.

    Use of proteases to improve the insecticidal activity of baculoviruses

    Biol Control

    (2001)
  • R.E. Hawtin et al.

    Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes

    Virology

    (1997)
  • K.L. Hefferon et al.

    Host cell receptor binding by baculovirus GP64 and kinetics of virion entry

    Virology

    (1999)
  • P.R. Hughes et al.

    Enhanced bioactivity of recombinant baculoviruses expressing insect-specific spider toxins in lepidopteran crop pests

    J Invertebr Pathol

    (1997)
  • R. Ichinose et al.

    Pharmacokinetic studies of the recombinant juvenile hormone esterase in Manduca sexta

    Pestic Biochem Physiol

    (1992)
  • C.M. Ignoffo et al.

    The relation of pH to the activity of inclusion bodies of a Heliothis nuclear polyhedrosis

    J Invertebr Pathol

    (1966)
  • W.F. Ijkel et al.

    A novel baculovirus envelope fusion protein with a proprotein convertase cleavage site

    Virology

    (2000)
  • J.D. Knell et al.

    Investigation of genetic heterogeneity in wild isolates of Spodoptera frugiperda nuclear polyhedrosis virus by restriction endonuclease analysis of plaque-purified variants

    Virology

    (1981)
  • D. Kreutzweiser et al.

    Comparative effects of a genetically engineered insect virus and a growth-regulating insecticide on microbial communities in aquatic microcosms

    Ecotoxicol Environ Saf

    (2001)
  • B. Kukan

    Vertical transmission of nucleopolyhedrovirus in insects

    J Invertebr Pathol

    (1999)
  • L.A. Lacey et al.

    Comparative activity of baculoviruses against codling moth Cydia pomonella and three other tortricid pests of tree fruits

    J Invertebr Pathol

    (2002)
  • J. Li et al.

    Effects of recombinant baculoviruses on three nontarget heliothine predators

    Biol Contr

    (1999)
  • A. Lu et al.

    Signal sequence and promoter effects on the efficacy of toxin-expressing baculoviruses as biopesticides

    Biol Control

    (1996)
  • S. Maeda

    Increased insecticidal effect by a recombinant baculovirus carrying a synthetic diuretic hormone gene

    Biochem Biophys Res Commun

    (1989)
  • J.H. Myers et al.

    Eradication revisited: dealing with exotic species

    Trends Ecol Evol

    (2000)
  • D.T. Petrik et al.

    Improving baculovirus resistance to UV inactivation: increased virulence resulting from expression of a DNA repair enzyme

    J Invertebr Pathol

    (2003)
  • H. Agaisse et al.

    How does Bacillus thuringiensis produce so much insecticidal crystal protein?

    J Bacteriol

    (1995)
  • B. Arif

    Scientific description of genetically modified baculoviruses for forest insect management applications

  • A.C. Bellotti

    Recent advances in cassava pest management

    Annu Rev Entomol

    (1999)
  • M.J. Bidochka et al.

    Habitat association in two genetic groups of the insect–pathogenic fungus Metarhizium anisopliae: uncovering cryptic species

    Appl Environ Microbiol

    (2001)
  • F.T. Bird et al.

    Artificial disseminated virus as a factor controlling the European spruce sawfly, Diprion hercyniae (Htg) in the absence of introduced parasites

    Can Entomol

    (1961)
  • B.C. Black et al.

    Commercialization of baculovirus insecticides

  • M. Blackburn et al.

    A novel insecticidal toxin from Photorhabdus luminescens, toxin complex a (Tca), and its histopathological effects on the midgut of Manduca sexta

    Appl Environ Microbiol

    (1998)
  • G.W. Blissard

    Baculovirus–insect cell interactions

    Cytotechnology

    (1996)
  • J.R. Bloomquist

    Ion channels as targets for insecticides

    Annu Rev Entomol

    (1996)
  • B.C. Bonning et al.

    Development of recombinant baculoviruses for insect control

    Annu Rev Entomol

    (1996)
  • B.C. Bonning et al.

    Superior expression of juvenile hormone esterase and β-galactosidase from the basic promoter of Autographa californica nuclear polyhedrosis virus compared to the p10 and polyhedrin promoters

    J Gen Virol

    (1994)
  • F.M. Boyce et al.

    Baculovirus-mediated gene transfer into mammalian cells

    Proc Natl Acad Sci U S A

    (1996)
  • S.C. Braunagel et al.

    Determination of protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus

    Proc Natl Acad Sci U S A

    (2003)
  • C.S. Brown et al.

    Assembly of empty capsids by using baculovirus recombinants expressing human parvovirus B19 structural proteins

    J Virol

    (1991)
  • M.E.B. Castro et al.

    Host-specific transcription of nucleopolyhedrovirus gene homologues in productive and abortive Anticarsia gemmatalis MNPV infections

    Arch Virol

    (1999)
  • M.E.B. Castro et al.

    Análise fenotípica de dois variantes de Anticarsia gemmatalis MNPV multiplicados durante passagem seriada em cultura de células

    Boletim de Pesquisa e Desenvolvimento da Embrapa Recursos Genéticos e Biotecnologia

    (2002)
  • X. Chen et al.

    Comparative analysis of the complete sequences of Helicoverpa zea and Helicoverpa armigera single-nucleocapsid nucleopolyhedroviruses

    J Gen Virol

    (2002)
  • L.G. Copping et al.

    Biopesticides: a review of their action, applications and efficacy

    Pest Manag Sci

    (2000)
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