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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

Relationship between the baculovirus HaNPV and the densovirus HaDNV-1 in cotton bollworm larvae.(A) Effect of HaNPV dose (log10-transformed number of occlusion bodies per ml) on larval survival to pupation. The thick lines are the fitted values and the shaded zones are the standard errors around these fitted values; blue line and shading = DNV− (control) larvae; red line and shading = DNV+ (densovirus-infected) larvae. The numbers of larvae that survived or died at differet concentrations (0, 106, 107, 108, 109 OB/ml) were 46/4, 38/8, 32/14, 20/32, 9/64 for DNV− individuals and 39/2, 31/10, 32/13, 31/17, 10/36 for DNV+ individuals. Temporal variation in (B) survival rate (%) (n = 216) and HaNPV copy numbers (log10-transformed) (C) (for day 2, n = 16; for day 3, n = 24; for day 5, n = 18) at different times after ingesting viruses. The concentrations of HaDNV-1 and HaNPV were 108/µl and 108 OBs/ml, respectively DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01, based on t-tests at each time-point.
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ppat-1004490-g005: Relationship between the baculovirus HaNPV and the densovirus HaDNV-1 in cotton bollworm larvae.(A) Effect of HaNPV dose (log10-transformed number of occlusion bodies per ml) on larval survival to pupation. The thick lines are the fitted values and the shaded zones are the standard errors around these fitted values; blue line and shading = DNV− (control) larvae; red line and shading = DNV+ (densovirus-infected) larvae. The numbers of larvae that survived or died at differet concentrations (0, 106, 107, 108, 109 OB/ml) were 46/4, 38/8, 32/14, 20/32, 9/64 for DNV− individuals and 39/2, 31/10, 32/13, 31/17, 10/36 for DNV+ individuals. Temporal variation in (B) survival rate (%) (n = 216) and HaNPV copy numbers (log10-transformed) (C) (for day 2, n = 16; for day 3, n = 24; for day 5, n = 18) at different times after ingesting viruses. The concentrations of HaDNV-1 and HaNPV were 108/µl and 108 OBs/ml, respectively DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01, based on t-tests at each time-point.

Mentions: To determine the interaction between the densovirus HaDNV-1 and the baculovirus HaNPV, we first confirmed individuals from NONINF strain were NPV-free using PCR with specific primers. Then, NONINF strain neonates were inoculated with either HaDNV-1 (DNV+) or water (DNV− controls), and infections verified using PCR. Survival to pupation in larvae not exposed to HaNPV did not differ between DNV+ (95%) and DNV− (92%) larvae (χ2 = 0.27, d.f. = 1, P = 0.60). However, for those larvae exposed to the baculovirus, there was a significant difference between DNV+ and DNV− larvae in their susceptibility to HaNPV (GLM: HaDNV-1 infection-status: χ2 = 4.04, d.f. = 1, P = 0.044, parameter estimate ± standard error = 0.4645±0.2319), with densovirus-infected larvae suffering lower mortality rates for a given virus dose (GLM: log10 virus dose: χ21 = 98.56, P<0.0001; LC50s = 3.13×107versus 9.10×107 OB per ml, for DNV− and DNV+ larvae, respectively; Fig. 5A); the interaction between viral dose and infection status was marginally non-significant (dose*status: χ2 = 3.72, d.f. = 1, P = 0.054).


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)

Relationship between the baculovirus HaNPV and the densovirus HaDNV-1 in cotton bollworm larvae.(A) Effect of HaNPV dose (log10-transformed number of occlusion bodies per ml) on larval survival to pupation. The thick lines are the fitted values and the shaded zones are the standard errors around these fitted values; blue line and shading = DNV− (control) larvae; red line and shading = DNV+ (densovirus-infected) larvae. The numbers of larvae that survived or died at differet concentrations (0, 106, 107, 108, 109 OB/ml) were 46/4, 38/8, 32/14, 20/32, 9/64 for DNV− individuals and 39/2, 31/10, 32/13, 31/17, 10/36 for DNV+ individuals. Temporal variation in (B) survival rate (%) (n = 216) and HaNPV copy numbers (log10-transformed) (C) (for day 2, n = 16; for day 3, n = 24; for day 5, n = 18) at different times after ingesting viruses. The concentrations of HaDNV-1 and HaNPV were 108/µl and 108 OBs/ml, respectively DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01, based on t-tests at each time-point.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214819&req=5

ppat-1004490-g005: Relationship between the baculovirus HaNPV and the densovirus HaDNV-1 in cotton bollworm larvae.(A) Effect of HaNPV dose (log10-transformed number of occlusion bodies per ml) on larval survival to pupation. The thick lines are the fitted values and the shaded zones are the standard errors around these fitted values; blue line and shading = DNV− (control) larvae; red line and shading = DNV+ (densovirus-infected) larvae. The numbers of larvae that survived or died at differet concentrations (0, 106, 107, 108, 109 OB/ml) were 46/4, 38/8, 32/14, 20/32, 9/64 for DNV− individuals and 39/2, 31/10, 32/13, 31/17, 10/36 for DNV+ individuals. Temporal variation in (B) survival rate (%) (n = 216) and HaNPV copy numbers (log10-transformed) (C) (for day 2, n = 16; for day 3, n = 24; for day 5, n = 18) at different times after ingesting viruses. The concentrations of HaDNV-1 and HaNPV were 108/µl and 108 OBs/ml, respectively DNV− = densovirus negative larvae, DNV+ = densovirus positive larvae. Means ± SE. * = P<0.05, ** = P<0.01, based on t-tests at each time-point.
Mentions: To determine the interaction between the densovirus HaDNV-1 and the baculovirus HaNPV, we first confirmed individuals from NONINF strain were NPV-free using PCR with specific primers. Then, NONINF strain neonates were inoculated with either HaDNV-1 (DNV+) or water (DNV− controls), and infections verified using PCR. Survival to pupation in larvae not exposed to HaNPV did not differ between DNV+ (95%) and DNV− (92%) larvae (χ2 = 0.27, d.f. = 1, P = 0.60). However, for those larvae exposed to the baculovirus, there was a significant difference between DNV+ and DNV− larvae in their susceptibility to HaNPV (GLM: HaDNV-1 infection-status: χ2 = 4.04, d.f. = 1, P = 0.044, parameter estimate ± standard error = 0.4645±0.2319), with densovirus-infected larvae suffering lower mortality rates for a given virus dose (GLM: log10 virus dose: χ21 = 98.56, P<0.0001; LC50s = 3.13×107versus 9.10×107 OB per ml, for DNV− and DNV+ larvae, respectively; Fig. 5A); the interaction between viral dose and infection status was marginally non-significant (dose*status: χ2 = 3.72, d.f. = 1, P = 0.054).

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