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The effect of nucleopolyhedrovirus infection and/or parasitism by Microplitis pallidipes on hemolymph proteins, sugars, and lipids in Spodoptera exigua larvae

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Abstract

We determined the physiological effects of joint and separate nucleopolyhedrovirus (NPV) infection and parasitism by the endoparasitoid Microplitis pallidipes Szepligeti on biochemical events in the noctuid Spodoptera exigua (Hübner). The results indicated that in parasitized larvae, compared to healthy larvae, total protein concentration in host hemolymph began to decline and total sugar concentration significantly increased by the first day, while lipid content in the host body significantly increased by the second day after parasitization. Meanwhile, in jointly infected and parasitized hosts, compared to parasitized larvae, total protein concentration was consistently higher, total sugar concentration was consistently lower, and lipid content became higher by the second day after treatment. In virus-infected larvae, compared to healthy larvae, total protein concentration sharply declined during the first two days but increased by the third, while total sugar concentration increased on the second and third days after virus infection but decreased at other observation times, and lipid content began to increase by the second day after virus infection. Finally, in larvae that were both parasitized and virus-infected, compared to just virus-infected larvae, total protein concentration increased during the first two days but decreased by the third, total sugar concentration increased only on the first and fourth days, and lipid content decreased significantly on the first day but began to increase by the second day after treatment. These findings led us to conclude that parasitization inhibited protein mobilization but stimulated sugar mobilization in host hemolymph, and promoted lipid mobilization in the host body, while Spodoptera exigua NPV infection stimulated protein mobilization induced by parasitization but inhibited sugar mobilization induced by parasitization.

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References

  • Adams JR, Wilcox TA (1968) Histopathology of the almond moth, Cadra cautella infected with a nuclear-polyhedrosis virus. J Invertebr Pathol 12:269–274

    Article  PubMed  CAS  Google Scholar 

  • Barras DJ, Joiner RL, Vinson SB (1970) Neutral lipid composition of the tobacco budworm, Heliothis virescens (Fab.) as affected by its habitual parasite, Cardiochiles nigriceps Viereck. Comp Biochem Phys 36:775–783

    Article  CAS  Google Scholar 

  • Bischof C, Ortel J (1996) The effects of parasitisim by Glyptapanteles liparidis (Braconidae: Hymenoptera) on the hemolymph and total body composition of gypsy moth larvae (Lymantria dispar, Lymantriidae: Lepidoptera. Parasitol Res 82:687–692

    Article  PubMed  CAS  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Büyükgüzel E, Tunaz H, Stanley D, Büyükgüzel K (2007) Eicosanoids mediate Galleria mellonella cellular immune response to viral infection. J Insect Physiol 53:99–105

    Article  PubMed  Google Scholar 

  • Cai Y, Cheng Z, Li C, Wang F, Li G, Pang Y (2010) Biological activity of recombinant Spodoptera exigua multicapsid nucleopolyhedrovirus against Spodoptera exigua larvae. Biol Control 55:178–183

    Article  Google Scholar 

  • Cônsoli FL, Vinson SB (2002) Larval development and feeding behavior of the wing morphs of Melittobia digitata Dahms (Hymenoptera: Eulophidae). J Hymenopt Res 11:188–196

    Google Scholar 

  • Cônsoli FL, Vinson SB (2004) Host regulation and the embryonic development of the endoparasitoid Toxoneuron nigriceps (Hymenoptera: Braconidae). Comp Biochem Phys B 137:463–473

    Article  Google Scholar 

  • Cônsoli FL, Brandt SL, Coudron TA, Vinson SB (2005) Host regulation and release of parasitism-specific proteins in the system Toxoneuron nigriceps–Heliothis virescens. Comp Biochem Phys B 142:181–191

    Article  Google Scholar 

  • Dahlman DL (1975) Trehalose and glucose levels in hemolymph of diet-reared, tobacco leaf-reared and parasitized tobacco hornworm larvae. Comp Biochem Phys A 50:165–167

    Article  CAS  Google Scholar 

  • Dahlman DL, Vinson SB (1976) Trehalose level in the hemolymph of Heliothis virescens parasitized by Campoletis sonorensis. Ann Entomol Soc Am 69:523–524

    CAS  Google Scholar 

  • Dannon EA, Tamò M, van Huis A, Dicke M (2012) Assessing non-target effects and host feeding of the exotic parasitoid Apanteles taragamae, a potential biological control agent of the cowpea pod borer Maruca vitrata. BioControl 57:415–425

    Article  Google Scholar 

  • Durmuş Y, Büyükgüzel E, Terzi B, Tunaz H, Stanley D, Büyükgüzel K (2008) Eicosanoids mediate melanotic nodulation reactions to viral infection in larvae of the parasitic wasp, Pimpla turionellae. J Insect Physiol 54:17–24

    Article  PubMed  Google Scholar 

  • Dushay MS (2009) Insect hemolymph clotting. Cell Mol Life Sci 66:2643–2650

    Article  PubMed  CAS  Google Scholar 

  • Ehler LE (2004) An evaluation of some natural enemies of Spodoptera exigua on sugarbeet in northern California. BioControl 49:121–135

    Article  Google Scholar 

  • Escribano A, Williams T, Goulson D, Cave RD, Caballero P (2000) Parasitoid–pathogen–pest interactions of Chelonus insularis, Campoletis sonorensis, and a nucleopolyhedrovirus in Spodoptera frugiperda larvae. Biol Control 19:265–273

    Article  Google Scholar 

  • Fathi SAA, Bozorg-Amirkalaee M, Sarfraz RM, Rafiee-Dastjerdi H (2012) Parasitism and developmental parameters of the parasitoid Diadegma majale (Gravenhorst) in control of Plutella xylostella (L.) on selected cultivars of canola. BioControl 57:49–59

    Article  Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Gao Y, Luo LZ, Hammond A (2007) Antennal morphology, structure and sensilla distribution in Microplitis pallidipes (Hymenoptera: Braconidae). Micron 38:684–693

    Article  PubMed  Google Scholar 

  • Gatehouse AMR, Butler KJ, Fenton KA, Gatehouse JA (1985) Presence and partial characterisation of a major proteolytic enzyme in the larval gut of Callosobruchus maculatus. Entomol Exp Appl 39:279–286

    Article  CAS  Google Scholar 

  • González-Santoyo I, Córdoba-Aguilar A (2012) Phenoloxidase: a key component of the insect immune system. Entomol Exp Appl 142:1–16

    Article  Google Scholar 

  • Gothama AAA, Sikorowski PP, McLaughlin MR (1998) Replication of nonoccluded baculovirus associated with the parasitoid Microplitis croceipes (Hymenoptera: Braconidae) in Heliothis virescens (Lepidoptera: Noctuidae). Biol Control 12:103–110

    Article  Google Scholar 

  • Grove M, Kimble W, McCarthy WJ (2001) Effects of individual Bacillus thuringiensis insecticidal crystal proteins on adult Heliothis virescens (F.) and Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae). BioControl 46:321–335

    Article  CAS  Google Scholar 

  • Hagner-Holler S, Pick C, Girgenrath S, Marden JH, Burmester T (2007) Diversity of stonefly hexamerins and implication for the evolution of insect storage proteins. Insect Biochem Mol Biol 37:1064–1074

    Article  PubMed  CAS  Google Scholar 

  • Hayakawa Y (1986) Inhibition of lipid transport in insects by a parasite factor. Comp Biochem Phys B 87:279–283

    Google Scholar 

  • Hoch G, Solter LF, Schopf A (2004) Hemolymph melanization and alterations in hemocyte numbers in Lymantria dispar larvae following infections with different entomopathogenic microsporidia. Entomol Exp Appl 113:77–86

    Article  Google Scholar 

  • Ilyinykh A (2011) Analysis of the causes of declines in Western Siberian outbreaks of the nun moth Lymantria monacha. BioControl 56:123–131

    Article  Google Scholar 

  • Jiang JX, Jiang ZR, Lei RH (2004) Cooperative effect of Spodoptera litura nuclear polyhedrosis virus with parasite wasp, Microplitis sp. on the S. litura larvae. Chin J Appl Ecol 15:303–307 (in Chinese)

    Google Scholar 

  • Jiang JX, Zeng AP, Ji XY, Wan NF, Chen XQ (2011) Combined effect of nucleopolyhedrovirus and Microplitis pallidipes for the control of the beet armyworm, Spodoptera exigua. Pest Manag Sci 67:705–713

    Article  PubMed  CAS  Google Scholar 

  • Jôrlfors UE, Dahlman DL, Zhang D (1997) Effects of Microplitis croceipes teratocytes on host haemelymph protein content and fat body proliferation. J Insect Physiol 43:577–585

    Article  Google Scholar 

  • Kaeslina M, Pfister-Wilhelma R, Molinab D, Lanzrein B (2005) Changes in the haemolymph proteome of Spodoptera littoralis induced by the parasitoid Chelonus inanitus or its polydnavirus and physiological implications. J Insect Physiol 51:975–988

    Article  Google Scholar 

  • Keeley LL (1985) Physiology and biochemistry of the fat body. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology, vol 3. Pergamon Press, London, UK, pp 211–248

    Google Scholar 

  • Kobayashi M, Kawase S (1981) Quantitative analysis of the metabolism in the isolated pupal abdomens of the silkworm, Bombyx mori, infected with nuclear polyhedrosis virus. J Invertebr Pathol 38:4–11

    Article  CAS  Google Scholar 

  • Kostal V, Sula J, Simek P (1998) Physiology of drought tolerance and cold hardiness of the Mediterranean tiger moth Cymbalophora pudica during summer diapause. J Insect Physiol 44:165–173

    Article  PubMed  CAS  Google Scholar 

  • Kumar NS, Murugan K, Zhang W (2008) Additive interaction of Helicoverpa armigera, Nucleopolyhedrovirus and Azadirachtin. BioControl 53:869–880

    Article  Google Scholar 

  • Lasa R, Ruiz-Portero C, Alcázar MD, Belda JE, Caballero P, Williams T (2007) Efficacy of optical brightener formulations of Spodoptera exigua multiple nucleopolyhedrovirus (SeMNPV) as a biological insecticide in greenhouses in southern Spain. Biol Control 40:89–96

    Article  CAS  Google Scholar 

  • Lu HP, Cai J, Ye GY, Xu HX, Hu C (2000) Effect of parasitism by Petranalus puparum on hemolymph protein and carbohydrate metabolism in overwintering pupae of Pieris rapae. J Zhejiang Univ (Agric Life Sci) 26:611–615

    CAS  Google Scholar 

  • Mascarin GM, Alves SB, Rampelotti-Ferreira FT (2010) Potential of a granulovirus isolate to control Phthorimaea operculella (Lepidoptera: Gelechiidae). BioControl 55:657–671

    Article  Google Scholar 

  • Mori H, Ohyane M, Ito M, Iwamoto SI, Matsumoto T, Sumida M, Matsubara F (1989) Induction of a hemagglutinating activity in the hemolymph of the silkworm, Bombyx mori, infected with cytoplasmic polyhedrosis virus. J Invertebr Pathol 54:112–116

    Article  Google Scholar 

  • Nakai M, Kunimi Y (1997) Granulosis virus infection of the smaller tea tortrix (Lepidoptera: Tortricidae): effect on the development of the endoparasitoid, Ascogaster reticulatus (Hymenoptera: Braconidae). Biol Control 8:74–80

    Article  Google Scholar 

  • Nakamatsu Y, Tanaka T (2004) Correlation between concentration of hemolymph nutrients and amount of fat body consumed in lightly and heavily parasitized hosts (Pseudaletia separata). J Insect Physiol 50:135–141

    Article  PubMed  CAS  Google Scholar 

  • Nakamatsu Y, Gyotoku Y, Tanaka T (2001) The endoparasitoid Cotesia kariyai (Ck) regulates the growth and metabolic efficiency of Pseudaletia separata larvae by venom and Ck polydnavirus. J Insect Physiol 47:573–584

    Article  PubMed  CAS  Google Scholar 

  • Park Y, Stanley D (2006) The entomopathogenic bacterium, Xenorhabdus nematophila, impairs hemocytic immunity by inhibition of eicosanoid biosynthesis in adult crickets, Gryllus firmus. Biol Control 38:247–253

    Article  CAS  Google Scholar 

  • Pérez J, Rojas JC, Montoya P, Liedo P, González FJ, Castillo A (2012) Size, shape and hue modulate attraction and landing responses of the braconid parasitoid Fopius arisanus to fruit odour-baited visual targets. BioControl 55:405–414

    Article  Google Scholar 

  • Roe JH (1955) The determination of sugar in blood fluid and spinal fluid with anthrone reagent. J Biol Chem 212:335–343

    PubMed  CAS  Google Scholar 

  • Salvador G, Cônsoli FL (2008) Changes in the hemolymph and fat body metabolites of Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) parasitized by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae). Biol Control 45:103–110

    Article  CAS  Google Scholar 

  • Shelby KS, Webb BA (1997) Polydnavirus infection inhibits translation of specific growth-associated host proteins. Insect Biochem Mol Biol 27:263–270

    Article  PubMed  CAS  Google Scholar 

  • Smits PH, Vlak JM (1988) Selection of nuclear polyhedrosis viruses as biological control agents of Spodoptera exigua [Lep.: Noctuidae]. BioControl 33:299–308

    Google Scholar 

  • Stark DM, Mills NJ, Purcell AH (1999) Interactions between the parasitoid Ametadoria misella (Diptera: Tachinidae) and the granulovirus of Harrisina brillians (Lepidoptera: Zygaenidae). Biol Control 14:146–151

    Article  Google Scholar 

  • Strand MR, Witherell RA, Trudeau D (1997) Two Microplitis demolitor polydnavirus mRNAs expressed in hemocytes of Pseudoplusia includens contain a common cysteine-rich domain. J Virol 71:2146–2156

    PubMed  CAS  Google Scholar 

  • Takei GH, Tamashiro M (1975) Changes observed in hemolymph proteins of the lawn armyworm, Spodoptera mauritia acronyctoides, during growth, development, and exposures to a nuclear polyhedrosis. J Invertebr Pathol 26:147–158

    Article  Google Scholar 

  • Thompson SN (1982a) Effects of parasitization by the insect parasite Hyposoter exiguiae on the growth, development and physiology of its host Trichoplusia ni. Parasitology 84:491–510

    Article  Google Scholar 

  • Thompson SN (1982b) Effects of parasitization by the insect parasite Hyposoter exiguiae on the total body glycogen and lipid levels of its host Trichoplusia ni. Comp Biochem Phys B 72:233–237

    Google Scholar 

  • Thompson SN (1993) Redirection of host metabolism and effects on parasite nutrition. In: Beckage NE, Thompson SN, Federici BA (eds) Parasites and pathogens of insects, vol 1. Academic Press, San Diego, USA, pp 125–144

    Chapter  Google Scholar 

  • Vail PV, Hall IM (1969) The histopathology of a nuclear polyhedral infection in larvae of the cabbage looper, Trichoplusia ni, related to symptoms and mortality. J Invertebr Pathol 13:188–198

    Article  PubMed  CAS  Google Scholar 

  • van der Geest LPS, Craig R (1967) Biochemical changes in the larvae of the variegated cutworm, Peridroma saucia, after infection with a nuclear-polyhedrosis virus. J Invertebr Pathol 9:43–54

    Article  Google Scholar 

  • Vinson SB, Iwantsch GF (1980) Host regulation by insect parasitoids. Q Rev Biol 55:143–165

    Article  CAS  Google Scholar 

  • Young SY, Lovel J (1971) Hemcaymph protein of Trichoptusia ni during the course of a nuclear polyhedrosis virus infection. J Invertebr Pathol 17:410–418

    Article  CAS  Google Scholar 

  • Young SY, Scott HA (1970) Immunoelectrophoresis of hemolymph of the cabbage looper, Trichoplusia ni, during the course of a nuclear polyhedrosis virus infection. J Invertebr Pathol 16:57–62

    Article  PubMed  CAS  Google Scholar 

  • Zeng AP, Wang KW, Jiang JX, Ji XY, You LS (2005) On the bionomics of Microplitis pallidipes. J Hunan Agric Univ 31:502–505 (in Chinese)

    Google Scholar 

  • Zeng AP, Jiang JX, Ji XY, Huang ZY, You LS (2010) Changes in physiology for Spodoptera exigua larvae parasitized by Microplitis pallidipe. Chin Agric Sci Bull 26:216–220 (in Chinese)

    Google Scholar 

  • Zhang T, Zhang Z, Li K, Ye GY, Hu C (2005) Physiological effects of parasitization by Nasonia vitripennis on its host pupae of Boettcherisca peregrina. J Zhejiang Univ (Agric Life Sci) 31:71–75

    Google Scholar 

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Acknowledgments

We thank Prof. Roy van Driesche at University of Massachusetts, USA for improving the English of this manuscript and providing constructive comments that greatly improved the quality of our paper. We thank the anonymous reviewers and editors who gave us useful suggestions and also thank Prof. Weidong Tian (Institute of Biostatistics, School of Life Sciences, Fudan University, China) who gave us constructive guidance in dealing with the data. This study was funded by the grants from the National Natural Science Foundation of China (31171904, 30771450) and Shanghai Municipal Science and Technology Commission (11JC1411500, 123919N0400, 12QB1402500, 08dz1900401).

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  1. Eco-environment Protection Research Institute, Shanghai Academy of Agricultural Sciences, Shanghai Key Laboratory of Protected Horticultural Technology, 1000#, Jinqi Road, Fengxian District, Shanghai, 201403, China

    Jie-Xian Jiang, Xiang-Yun Ji, Yang-Yi Yin & Nian-Feng Wan

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  1. Jie-Xian Jiang
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Jiang, JX., Ji, XY., Yin, YY. et al. The effect of nucleopolyhedrovirus infection and/or parasitism by Microplitis pallidipes on hemolymph proteins, sugars, and lipids in Spodoptera exigua larvae. BioControl 58, 777–788 (2013). https://doi.org/10.1007/s10526-013-9538-7

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