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Proteomic investigation of Peristenus spretus ovary and characterization of an ovary-enriched heat shock protein

Published online by Cambridge University Press:  30 September 2020

Miaomiao Tian Open the ORCID record for Miaomiao Tian [Opens in a new window] ,
Yayun Xia ,
Ducheng Cai ,
Jianjun Mao  and
Shuping Luo
Miaomiao Tian
Affiliation:
IPPCAAS – State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China College of Plant Protection, Hainan University, Hainan Haikou, China
Yayun Xia
Affiliation:
IPPCAAS – State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China College of Plant Protection, Hainan University, Hainan Haikou, China
Ducheng Cai
Affiliation:
College of Plant Protection, Hainan University, Hainan Haikou, China
Jianjun Mao*
Affiliation:
IPPCAAS – State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
Shuping Luo*
Affiliation:
IPPCAAS – State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection (IPP), Chinese Academy of Agricultural Sciences (CAAS), Beijing, China
*
Author for correspondence: Jianjun Mao, Email: [email protected]; Shuping Luo, Email: [email protected]
Author for correspondence: Jianjun Mao, Email: [email protected]; Shuping Luo, Email: [email protected]
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Abstract

Peristenus spretus (Hymenoptera: Braconidae) is one of the most important endoparasitoids used for biological control of the green mirid bug, Apolygus lucorum Meyer-Dür (Heteroptera: Miridae). However, what we know about its reproductive genetics is very limited. Here, the composition of ovarian proteins in P. spretus was analyzed. Mass spectrum data searched against the non-redundant NCBI protein and UniProt protein database identified 1382 proteins and revealed an enrichment of the heat shock protein 83 (HSP83) in P. spretus ovary. The Pshsp83 complete cDNA is 2175 bp in length and encodes a protein of 724 amino acids with a calculated molecular mass of 83.4 kDa and a theoretical isoelectric point of 4.87. Transcription of Pshsp83 appeared from days 1 to 13 post-emergence and peaked at 13th day. Immuno-localization showed that the HSP83 protein was present in cytoplasm of germarium and in egg chambers of the whole ovariole. The transcript abundance of Pshsp83 fluctuated drastically after heat shocks at different temperatures and the maximum emerged at 35°C. The exposure to 35°C caused no dramatic effects on reproductive parameters of adult females such as pupation rate, cocoon weight, emergence rate, sex ratio and developmental duration, but did on longevity. These results suggested that the HSP83 protein is involved in life-span regulation in the P. spretus.

Keywords

Heat shock proteinhsp83longevityOvary proteomePeristenus spretus
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 3 , June 2021 , pp. 270 - 281
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Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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References

Berg, CA (2008) Tube formation in Drosophila Egg chambers. Tissue Engineering Part A 14, 1479–1488.CrossRefGoogle ScholarPubMed
Blanckenhorn, WU and Henseler, C (2005) Temperature-dependent ovariole and testis maturation in the yellow dung fly. Entomologia Experimentalis et Applicata 116, 159–165.CrossRefGoogle Scholar
Chen, B and Wagner, A (2012) Hsp90 is important for fecundity, longevity, and buffering of cryptic deleterious variation in wild fly populations. BMC Evolutionary Biology 12, 25.CrossRefGoogle ScholarPubMed
Chen, XX and van Achterberg, C (1997) Revision of the subfamily Euphorinae (excluding the tribe Meteorini Cresson) (Hymenoptera: Braconidae) from China. Zoologische Verhandelingen 313, 1–217.Google Scholar
Chen, XX, He, JH and Ma, Y (2004) China Fauna Insect Class: Hymenoptera: Braconidae. BeiJing: Science Press.Google Scholar
Clouse, KN, Ferguson, SB and Schupbach, T (2008) Squid, Cup, and PABP55B function together to regulate gurken translation in Drosophila. Developmental Biology 313, 713–724.CrossRefGoogle ScholarPubMed
Denlinger, DL, Rinehart, JP and Yocum, GD (2001) Insect Timing: Circadian Rhythmicity to Seasonality – Stress Proteins: A Role in Insect Diapause? Amsterdam: Elsevier.Google Scholar
Ding, D, Parkhurst, SM, Halsell, SR and Lipshitz, HD (1993) Dynamic hsp83 RNA localization during Drosophila Oogenesis and embryogenesis. Molecular and Cellular Biology 13, 3773–3781.Google ScholarPubMed
Dong, SZ, Ye, GY and Hu, C (2009) Detection and immunological relationship of yolk proteins from different parasitoid wasps. Acts Entomologica Sinica 52, 1024–1027.Google Scholar
Feder, ME and Hofmann, GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annual Review of Physiology 61: 243–282.CrossRefGoogle ScholarPubMed
Gancz, D and Gilboa, L (2013) Insulin and target of rapamycin signaling orchestrate niche-stem cell units in Drosophila. Development (Cambridge, England) 140, 4145–4154.CrossRefGoogle ScholarPubMed
Gilbert, C, Schaack, S, Pace, JK, Brindley, PJ and Feschotte, C (2010) A role for hostparasite interactions in the horizontal transfer of transposons across phyla. Nature 464, 1347–1350.CrossRefGoogle Scholar
Gilbert, C, Chateigner, A, Ernenwein, L, Barbe, V, Bézier, A, Herniou, EA and Cordaux, R (2014) Population genomics supports baculoviruses as vectors of horizontal transfer of insect transposons. Nature Communications 5, 3348.CrossRefGoogle ScholarPubMed
Gruntenko, NE, Bownes, M, Terashima, J, Sukhanova, M and Raushenbach, IY (2003) Heat stress affects oogenesis differently in wild-type Drosophila virilis and a mutant with altered juvenile hormone and 20-hydroxyecdysone levels. Insect Molecular Biology 12, 393–404.CrossRefGoogle Scholar
Hoffmann, AA, Sørensen, JG and Loeschcke, V (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology 28, 175–216.CrossRefGoogle Scholar
Huang, LH and Kang, L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Molecular Biology 16, 491–500.CrossRefGoogle ScholarPubMed
Jia, D, Huang, YC and Deng, WM (2015) Analysis of cell cycle switches in Drosophila Oogenesis. Methods in Molecular Biology 1328, 207–216.CrossRefGoogle ScholarPubMed
Johnson, JL (2012) Evolution and function of diverse hsp90 homologs and cochaperone proteins. BBA – Molecular Cell Research 1823, 607–613.Google ScholarPubMed
Knorr, E and Vilcinskas, A (2011) Post-embryonic functions of hsp90 in Tribolium castaneum include the regulation of compound eye development. Development Genes and Evolution 221, 357–362.CrossRefGoogle ScholarPubMed
Lindquist, S and Craig, EA (1988) The heat-shock proteins. Annual Review of Genetics 22, 631–677.CrossRefGoogle ScholarPubMed
Liu, YH, Ye, GY and XH, L (2006) The effect of different temperature on ovarian development and oogenesis of Telenomus Theophilae Wu Et Chen (Hymenoptera: Scelionidae). Natural Enemies of Insects 28, 126–131.Google Scholar
Liu, SS, Li, SS, Zhang, Y and Wang, Y (2017) Purification of a polyclonal antibody against CD147 for ELISA using antigen–immuno affinity chromatography. Molecular Medicine Reports 15, 4035–4040.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods (San Diego, California) 25, 402–408.CrossRefGoogle Scholar
Lu, YH, Wu, KM, Cai, XM and Liu, YQ (2008) A rearing method for mirids using the green bean, Phaseolus vulgaris in the laboratory. Acta Phytophylacica Sinica 35, 215–219.Google Scholar
Luo, SP, Li, HM, Lu, YH, Zhang, F, Haye, T, Kuhlmann, U and Wu, KM (2014) Functional response and mutual interference of Peristenus spretus (Hymenoptera: Braconidae), a parasitoid of Apolygus lucorum (Heteroptera: Miridae). Biocontrol Science and Technology 24, 247–256.CrossRefGoogle Scholar
Luo, SP, Zhang, F and Wu, KM (2015) Effect of temperature on the reproductive biology of Peristenus spretus (Hymenoptera: Braconidae), a biological control agent of the plant bug Apolygus lucorum (Hemiptera: Miridae). Biocontrol Science and Technology 25, 1–29.CrossRefGoogle Scholar
Luo, SP, Zhang, F and Wu, KG (2018) Interspecific competition between Peristenus spretus and Peristenus relictus (Hymenoptera: Braconidae), larval parasitoids of Apolygus lucorum (Hemiptera: Miridae). Biological Control 117, 115–122.CrossRefGoogle Scholar
Ma, J, Chen, T, Wu, S, Yang, C, Bai, M, Shu, KX, Li, KL, Zhang, GQ, Jin, Z, He, FC, Hermjakob, HN and Zhu, YP (2019) Iprox: an integrated proteome resource. Nucleic Acids Research 47, 1211–1217.CrossRefGoogle ScholarPubMed
Mahroof, R, Subramanyam, B and Flinn, P (2005) Reproductive performance of Tribolium castaneum (Coleoptera: Tenebrionidae) exposed to the minimum heat treatment temperature as pupae and adults. Journal of Economic Entomology 98, 626–633.CrossRefGoogle ScholarPubMed
Minami, Y, Kimura, Y, Kawasaki, H, Suzuki, K and Yahara, I (1994) The carboxy-terminal region of mammalian HSP90 is required for its dimerization and function in vivo. Molecular and Cellular Biology 14, 1459–1464.Google ScholarPubMed
Minami, MM, Nakamura, M, Emori, Y and Minami, Y (2001) Both the N- and C-terminal chaperone sites of hsp90 participate in protein refolding. European Journal of Biochemistry 268, 2520–2524.CrossRefGoogle Scholar
Moseley, PL (1997) Heat shock proteins and heat adaptation of the whole organism. Journal of Applied Physiology 83, 1413–1417.CrossRefGoogle ScholarPubMed
Nakamura, A, Sato, K and Hanyu-Nakamura, K (2004) Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Developmental Cell 6, 69–78.CrossRefGoogle ScholarPubMed
Nelson, MR, Leidal, AM and Smibert, CA (2004) Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO Journal 23, 150–159.CrossRefGoogle ScholarPubMed
Nemoto, T, Ohara-Nemoto, Y, Ota, M, Takagi, T and Yokoyama, K (1995) Mechanism of dimer formation of the 90-kDa heat shock protein. European Journal of Biochemistry 233, 1–8.CrossRefGoogle ScholarPubMed
Neuer, A, Spandorfer, SD, Giraldo, P, Dieterle, S, Rosenwaks, Z and Witkin, SS (2000) The role of heat shock proteins in reproduction. Human Reproduction Update 6, 149–159.CrossRefGoogle ScholarPubMed
Pearl, LH and Prodromou, C (2006) Structure and mechanism of the hsp90 molecular chaperone machinery. Annual Review of Biochemistry 75, 271–294.CrossRefGoogle ScholarPubMed
Pisa, V, Cozzolino, M, Gargiulo, S, Ottone, C, Piccioni, F, Monti, M, Gigliotti, S, Talamo, F, Graziani, F, Pucci, P and Verrotti, AC (2009) The molecular chaperone hsp90 is a component of the cap-binding complex and interacts with the translational repressor cup during Drosophila oogenesis. Gene 432, 67–74.CrossRefGoogle ScholarPubMed
Roberts, RH (1980) The effect of temperature on the duration of oogenesis and embryonic development in tabanidae (Diptera). Journal of Medical Entomology 17, 8–14.CrossRefGoogle Scholar
Sato, S, Fujita, N and Tsuruo, T (2000) Modulation of Akt kinase activity by binding to hsp90. Proceedings of the National Academy of Sciences of the USA 97, 10832–10837.CrossRefGoogle ScholarPubMed
Schneider, SE and Thomas, JH (2014) Accidental genetic engineers: horizontal sequence transfer from parasitoid wasps to their Lepidopteran hosts. PLoS ONE 9, 109446.CrossRefGoogle ScholarPubMed
Sejerkilde, M, Sørensen, JG and Loeschcke, V (2003) Effects of cold-and heat hardening on thermal resistance in Drosophila melanogaster. Journal of Insect Physiology 49, 719–726.CrossRefGoogle ScholarPubMed
Song, Y, Fee, L, Lee, TH and Wharton, RP (2007) The molecular chaperone hsp90 is required for mRNA localization in Drosophila Melanogaster embryos. Genetics 176, 2213–2222.CrossRefGoogle ScholarPubMed
Sonoda, S, Ashfaq, M and Tsumuki, H (2006) Cloning and nucleotide sequencing of three heat shock protein genes (hsp90, hsc70, and hsp19.5) from the diamondback moth, Plutella Xylotella (L.) and their expression in relation to developmental stage and temperature. Archives of Insect Biochemistry and Physiology 62, 80–90.CrossRefGoogle Scholar
Theodoraki, MA and Mintzas, AC (2006) cDNA cloning, heat shock regulation and developmental expression of the hsp83 gene in the Mediterranean fruit fly Ceratitis capitata. Insect Molecular Biology 15, 839–852.CrossRefGoogle ScholarPubMed
Tootle, TL, Williams, D, Hubb, A, Frederick, R and Spradling, A (2011) Drosophila eggshell production: identification of new genes and coordination by pxt. PLoS ONE 6, 19943.CrossRefGoogle ScholarPubMed
Tufail, M and Takeda, M (2008) Molecular characteristics of insect vitellogenins. Journal of Insect Physiology 54, 1447–1458.CrossRefGoogle ScholarPubMed
Walsh, AM, Kortschak, RD, Gardner, MG, Bertozzi, T and Adelson, DL (2013) Widespread horizontal transfer of retrotransposons. Proceedings of the National Academy of Sciences of the USA 110, 1012–1016.CrossRefGoogle ScholarPubMed
Wilhelm, JE, Hilton, M, Amos, Q and Henzel, WJ (2003) Cup is an eIF4E binding protein required for both the translational repression of oskar and the recruitment of Barentsz. Journal of Cell Biology 163, 1197–1204.CrossRefGoogle ScholarPubMed
Will, T, Schmidtberg, H, Skaljac, M and Vilcinskas, A (2017) Heat shock protein 83 plays pleiotropic roles in embryogenesis, longevity, and fecundity of the pea aphid Acyrthosiphon pisum. Development Genes and Evolution 227, 1–9.CrossRefGoogle ScholarPubMed
Wu, X, Tanwar, PS and Raftery, LA (2008) Drosophila follicle cells: morphogenesis in an eggshell. Seminars in Cell & Developmental Biology 19, 271–282.CrossRefGoogle Scholar
Xavier, B and Maria-Dolors, P (2015) Ecdysone signalling and ovarian development in insects: from stemcells to ovarian follicle formation. BBA – Gene Regulatory Mechanisms 1849, 181–186.Google Scholar
Xi, GS, Liang, KD, Fan, DF, Zhang, WH and Zhang, WN (2010) Study progress on regulation factors of insect oogenesis. Chinese Bulletin of Entomology 47, 848–855.Google Scholar
Xu, J, Shu, J, Qiu, X, Wang, Z, Zhao, F, Zhang, Z and Zhang, Q (2009) Effects of heat shock on ovary development and hsp83 expression in Tribolium castaneum (Coleoptera: Tenebrionidae). Archives of Insect Biochemistry and Physiology 70, 204–216.CrossRefGoogle Scholar
Xu, JJ, Shu, J and Zhang, Q (2010) Expression of the Tribolium castaneum (Coleoptera: Tenebrionidae) hsp83 gene and its relation to oogenesis during ovarian maturation. Journal of Genetics and Genomics 37, 513–522.CrossRefGoogle ScholarPubMed
Young, JC, Moarefi, I and Hartl, FU (2001) HSP90: a specialized but essential protein-folding tool. Journal of Cell Biology 154, 267–273.CrossRefGoogle ScholarPubMed
Yu, RX, Shi, M, Huang, F and Chen, XX (2008) Immature development of Cotesia Vestalis (Hymenoptera: Braconidae), an endoparasitoid of Plutella Xylostella (Lepidoptera: Plutellidae). Annals of the Entomological Society of America 101, 189–196.CrossRefGoogle Scholar
Yue, L, Karr, TL, Nathan, DF, Swift, H, Srinivasan, S and Lindquist, S (1999) Genetic analysis of viable hsp90 alleles reveals a critical role in Drosophila Spermatogenesis. Genetics 151, 1065–1079.CrossRefGoogle ScholarPubMed
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