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Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide.

Xu P, Liu Y, Graham RI, Wilson K, Wu K - PLoS Pathog. (2014)

Bottom Line: HaDNV-1 was found to be widespread in wild populations of H. armigera adults (>67% prevalence between 2008 and 2012).Laboratory bioassays revealed that larvae hosting HaDNV-1 had significantly enhanced resistance to HaNPV (and lower viral loads), and that resistance to Bacillus thuringiensis (Bt) toxin was also higher at low doses.We found no evidence for a negative effect of HaDNV-1 infection on H. armigera fitness-related traits, strongly suggesting a mutualistic interaction between the cotton bollworm and its densovirus.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, People's Republic of China.

ABSTRACT
Mutualistic associations between symbiotic bacteria and their hosts are common within insect systems. However, viruses are often considered as pathogens even though some have been reported to be beneficial to their hosts. Herein, we report a novel densovirus, Helicoverpa armigera densovirus-1 (HaDNV-1) that appears to be beneficial to its host. HaDNV-1 was found to be widespread in wild populations of H. armigera adults (>67% prevalence between 2008 and 2012). In wild larval populations, there was a clear negative interaction between HaDNV-1 and H. armigera nucleopolyhedrovirus (HaNPV), a baculovirus that is widely used as a biopesticide. Laboratory bioassays revealed that larvae hosting HaDNV-1 had significantly enhanced resistance to HaNPV (and lower viral loads), and that resistance to Bacillus thuringiensis (Bt) toxin was also higher at low doses. Laboratory assays indicated that the virus was mainly distributed in the fat body, and could be both horizontally- and vertically-transmitted, though the former occurred only at large challenge doses. Densovirus-positive individuals developed more quickly and had higher fecundity than uninfected insects. We found no evidence for a negative effect of HaDNV-1 infection on H. armigera fitness-related traits, strongly suggesting a mutualistic interaction between the cotton bollworm and its densovirus.

No MeSH data available.


Related in: MedlinePlus

Pupal and adult life-history parameters of DNV− and DNV+ cotton bollworms.(A) Pupal period (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (B) Pupal weight (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (C) Number of eggs produced per female (n(DNV+) = 47, n(DNV−) = 48). (D) Egg hatch per female (n(DNV+) = 47, n(DNV−) = 48). (E) Longevity of adult (for male, n(DNV+) = 174, n(DNV−) = 195; for female, n(DNV+) = 174, n(DNV−) = 195). DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01.
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ppat-1004490-g004: Pupal and adult life-history parameters of DNV− and DNV+ cotton bollworms.(A) Pupal period (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (B) Pupal weight (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (C) Number of eggs produced per female (n(DNV+) = 47, n(DNV−) = 48). (D) Egg hatch per female (n(DNV+) = 47, n(DNV−) = 48). (E) Longevity of adult (for male, n(DNV+) = 174, n(DNV−) = 195; for female, n(DNV+) = 174, n(DNV−) = 195). DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01.

Mentions: To quantify the impact of HaDNV-1 infection on H. armigera development, a number of bioassays were performed using neonate larvae orally inoculated with filtered liquid from either HaDNV-1 infected (DNV+) or non-infected (DNV−) individuals (Fig. S3A, S3B). Both male and female DNV+ individuals developed significantly more quickly than the control individuals in both the larval (female: t = 2.732, d.f. = 312, P = 0.0067, male: t = 4.147, d.f. = 379, P<0.001) (Fig. 3A) and pupal stages (female: t = 5.100, d.f. = 312, P<0.001, male: t = 4.057, d.f. = 379, P<0.001) (Fig. 4A). Between 7–11 days post-hatch (approximately 3rd–5th instar) DNV+ larvae weighed significantly more than DNV- larvae by an average of ∼20% (GLMM with larval identity as a random term and log10-transformed larval weight as the dependent variable: Age (days): F = 2386.8, d.f. = 1,127, P<0.0001; HaDNV-1 infection status (+ve or −ve): F = 27.25, d.f. = 1,36, P<0.0001) (Fig. 3B, Fig. S4). However, their growth rates over this period did not differ, suggesting that densovirus effects on larval growth rate occurred prior to day 7 post-hatch (GLMM: interaction between infection status and age: F = 0.01, d.f. = 1,126, P = 0.91) (Fig. S4). A chloroform-wash assay indicated that at 9 days old, DNV+ larvae contained more lipid than DNV− individuals, measured as either lipid mass (t = 2.045, d.f. = 50, P = 0.046) or as a percentage of the whole body (t = 2.342, d.f. = 50, P = 0.023) (Fig. 3C, 4D). Larval mortality of DNV+ was significantly lower than DNV− (Table 3). However, there was no significant difference in pupal weight between DNV+ and DNV− insects (GLM: densovirus infection status: F = 0.99, d.f. = 1,692, P = 0.329; Sex: F = 41.08, d.f. = 1,693, P<0.0001; interaction term: F = 0.064, d.f. = 1,691, P = 0.80; female: t = 0.96, d.f. = 312, P = 0.34, male: t = 0.481, d.f. = 379, P = 0.63) (Fig. 4B), or pupation rate or eclosion rate between HaDNV-1 positive and HaDNV-1 negative insects (Table 3).


Densovirus is a mutualistic symbiont of a global crop pest (Helicoverpa armigera) and protects against a baculovirus and Bt biopesticide.

Xu P, Liu Y, Graham RI, Wilson K, Wu K - PLoS Pathog. (2014)

Pupal and adult life-history parameters of DNV− and DNV+ cotton bollworms.(A) Pupal period (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (B) Pupal weight (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (C) Number of eggs produced per female (n(DNV+) = 47, n(DNV−) = 48). (D) Egg hatch per female (n(DNV+) = 47, n(DNV−) = 48). (E) Longevity of adult (for male, n(DNV+) = 174, n(DNV−) = 195; for female, n(DNV+) = 174, n(DNV−) = 195). DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01.
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ppat-1004490-g004: Pupal and adult life-history parameters of DNV− and DNV+ cotton bollworms.(A) Pupal period (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (B) Pupal weight (for male, n(DNV+) = 204, n(DNV−) = 177; for female, n(DNV+) = 169, n(DNV−) = 145). (C) Number of eggs produced per female (n(DNV+) = 47, n(DNV−) = 48). (D) Egg hatch per female (n(DNV+) = 47, n(DNV−) = 48). (E) Longevity of adult (for male, n(DNV+) = 174, n(DNV−) = 195; for female, n(DNV+) = 174, n(DNV−) = 195). DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01.
Mentions: To quantify the impact of HaDNV-1 infection on H. armigera development, a number of bioassays were performed using neonate larvae orally inoculated with filtered liquid from either HaDNV-1 infected (DNV+) or non-infected (DNV−) individuals (Fig. S3A, S3B). Both male and female DNV+ individuals developed significantly more quickly than the control individuals in both the larval (female: t = 2.732, d.f. = 312, P = 0.0067, male: t = 4.147, d.f. = 379, P<0.001) (Fig. 3A) and pupal stages (female: t = 5.100, d.f. = 312, P<0.001, male: t = 4.057, d.f. = 379, P<0.001) (Fig. 4A). Between 7–11 days post-hatch (approximately 3rd–5th instar) DNV+ larvae weighed significantly more than DNV- larvae by an average of ∼20% (GLMM with larval identity as a random term and log10-transformed larval weight as the dependent variable: Age (days): F = 2386.8, d.f. = 1,127, P<0.0001; HaDNV-1 infection status (+ve or −ve): F = 27.25, d.f. = 1,36, P<0.0001) (Fig. 3B, Fig. S4). However, their growth rates over this period did not differ, suggesting that densovirus effects on larval growth rate occurred prior to day 7 post-hatch (GLMM: interaction between infection status and age: F = 0.01, d.f. = 1,126, P = 0.91) (Fig. S4). A chloroform-wash assay indicated that at 9 days old, DNV+ larvae contained more lipid than DNV− individuals, measured as either lipid mass (t = 2.045, d.f. = 50, P = 0.046) or as a percentage of the whole body (t = 2.342, d.f. = 50, P = 0.023) (Fig. 3C, 4D). Larval mortality of DNV+ was significantly lower than DNV− (Table 3). However, there was no significant difference in pupal weight between DNV+ and DNV− insects (GLM: densovirus infection status: F = 0.99, d.f. = 1,692, P = 0.329; Sex: F = 41.08, d.f. = 1,693, P<0.0001; interaction term: F = 0.064, d.f. = 1,691, P = 0.80; female: t = 0.96, d.f. = 312, P = 0.34, male: t = 0.481, d.f. = 379, P = 0.63) (Fig. 4B), or pupation rate or eclosion rate between HaDNV-1 positive and HaDNV-1 negative insects (Table 3).

Bottom Line: HaDNV-1 was found to be widespread in wild populations of H. armigera adults (>67% prevalence between 2008 and 2012).Laboratory bioassays revealed that larvae hosting HaDNV-1 had significantly enhanced resistance to HaNPV (and lower viral loads), and that resistance to Bacillus thuringiensis (Bt) toxin was also higher at low doses.We found no evidence for a negative effect of HaDNV-1 infection on H. armigera fitness-related traits, strongly suggesting a mutualistic interaction between the cotton bollworm and its densovirus.

View Article: PubMed Central - PubMed

Affiliation: State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, People's Republic of China; Tobacco Research Institute, Chinese Academy of Agricultural Sciences, Qingdao, People's Republic of China.

ABSTRACT
Mutualistic associations between symbiotic bacteria and their hosts are common within insect systems. However, viruses are often considered as pathogens even though some have been reported to be beneficial to their hosts. Herein, we report a novel densovirus, Helicoverpa armigera densovirus-1 (HaDNV-1) that appears to be beneficial to its host. HaDNV-1 was found to be widespread in wild populations of H. armigera adults (>67% prevalence between 2008 and 2012). In wild larval populations, there was a clear negative interaction between HaDNV-1 and H. armigera nucleopolyhedrovirus (HaNPV), a baculovirus that is widely used as a biopesticide. Laboratory bioassays revealed that larvae hosting HaDNV-1 had significantly enhanced resistance to HaNPV (and lower viral loads), and that resistance to Bacillus thuringiensis (Bt) toxin was also higher at low doses. Laboratory assays indicated that the virus was mainly distributed in the fat body, and could be both horizontally- and vertically-transmitted, though the former occurred only at large challenge doses. Densovirus-positive individuals developed more quickly and had higher fecundity than uninfected insects. We found no evidence for a negative effect of HaDNV-1 infection on H. armigera fitness-related traits, strongly suggesting a mutualistic interaction between the cotton bollworm and its densovirus.

No MeSH data available.


Related in: MedlinePlus