Characterization of seminal fluid peptides/proteins of male Helicoverpa armigera and their plausible role in post-copulatory modulation of female reproductive behaviour
DOI:
https://doi.org/10.22364/eeb.22.18Keywords:
accessory reproductive glands, acyl-CoA-binding proteins, elongation factor, fecundity, Helicoverpa armigera, juvenile hormone, longevity, odorant binding protein, pheromone, post mating receptivityAbstract
In many insect species, female reproductive output is determined by male ejaculate components such as seminal fluid, plasma, and male accessory gland (MAG) peptides. These elements have additional roles in affecting insect receptivity and mating physiology. Studies indicate that the peptides/proteins of the male insects’ seminal fluid are responsible for these behavioural changes in female Helicoverpa armigera insects. In particular, the virgin male’s MAG peptide induces mating receptivity inhibition approximately 12 h after eclosion (emergence), which reaches peak concentration approximately at 24 h. This time coincides with the male’s mating time, and is transferred to female moths during copulation. The aim of the study was to purify and characterize the virgin male’s MAG-duplex peptides/proteins by biochemical and bioinformatics analysis. Analysis yielded a peptide of 5 kDa molecular weight. In insects several conserved proteins belonging to members of multigene families control a wide range of reproduction and related physiological processes. Data mining of the MAG‑duplex peptides utilizing the public protein repository identified six proteins (heat shock proteins, diazepam-binding inhibitor, elongation factor 1 alpha, odorant-binding protein, serpin, and thioredoxin) with diverse functions. The diazepam-binding inhibitor protein, which binds coenzyme A and thiol esters of long fatty acids, was unique to H. armigera. The molecular evolutionary analysis of the proteins independently supports the widely accepted theory that genes in gene families with roles in reproduction have evolved over a generational time scale.
References
Andres J.A., Maroja L.S., Harrison R.G. 2008. Searching for candidate speciation genes using a proteomic approach: seminal proteins in field crickets. Proc. Royal Soc. London Ser. B Biol. Sci. 275: 1975–1983.
Antony B., Ding B.J., Moto K., Aldosari S.A., Aldawood A.S. 2016. Two fatty acyl reductases involved in moth pheromone biosynthesis. Sci. Rep. 6: 29927.
Apger-McGlaughon J., Wolfner M.F. 2013. Post-mating change in excretion by mated Drosophila melanogaster females is a long-term response that depends on sex peptide and sperm. J. Insect Physiol. 59:1024–1030.
Asquith K.L., Harman A.J., McLaughlin E.A., Nixon B., Aitken R.J. 2005. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction. Biol. Reprod. 72: 328–337.
Avila F.W., Sirot L.K., LaFlamme B.A., Rubinstein C.D., Wolfner M.F. 2011. Insect seminal fluid proteins: identification and function. Annu .Rev. Entomol. 56: 21-40.
Azevedo R.V., Dias D.B., Bretãs J.A., Mazzoni C.J., Souza N.A., Albano R.M., Wagner G., Davila A.M.R., Peixoto A.A. 2012. The transcriptome of Lutzomyia longipalpis (Diptera: Psychodidae) male reproductive organs. PLoS One 7: e34495.
Baer B., Heazlewood J.L., Taylor N.L., Eubel H., Millar A.H. 2009. The seminal fluid proteome of the honeybee Apis mellifera. Proteomics 9: 2085–2097.
Baldini F., Gabrieli P., Rogers D.W., Catteruccia F. 2012. Function and composition of male accessory gland secretions in Anopheles gambiae: a comparison with other insect vectors of infectious diseases. Pathog. Global Health 106: 82–93.
Barrozo R.B., Gadenne C., Anton S. 2010. Switching attraction to inhibition: mating-induced reversed role of sex pheromone in an insect. J. Exp. Biol. 213: 2933–2939.
Betzel C., Gourinath S., Kumar P., Kaur P., Perbandt M., Eschenburg S., Singh TP. 2001. Structure of a serine protease proteinase K from Tritirachium album limber at 0.98 A resolution. Biochemistry 40: 3080-3080.
Blankers T., Fruitet E., Burdfield‐Steel E., Groot A.T. 2022. Experimental evolution of a pheromone signal. Ecol. Evol. 12: e8941.
Bräutigam A., Shrestha R.P., Whitten D., Wilkerson C.G., Carr K.M., Froehlich J.E., Weber A.P.M. 2008. Comparison of the use of a species-specific database generated by pyrosequencing with databases from related species for proteome analysis of pea chloroplast envelopes. J. Biotechnol. 136: 44–53.
Burton M., Rose T.M., Færgeman N.J., Knudsen K. 2005. Evolution of the acyl-CoA binding protein (ACBP). Biochem. J. 392: 299–307.
Cai L.J., Zheng L.S., Huang Y.P., Xu W., You M.S. 2021. Identification and characterization of odorant binding proteins in the diamondback moth, Plutella xylostella. Insect Sci. 28: 987–1004.
CABI. 2018. Helicoverpa armigera. Center for Agriculture and Bioscience International Wallingford, UK.
Chakraborty A., Halder S., Kishore P., Saha D., Saha S., Sikder K., Basu A. 2022. The structure-function analysis of Obg-like GTPase proteins along the evolutionary tree from bacteria to humans. Genes Cells 27: 469–481.
Chang H., Liu Y., Ai D., Jiang X., Dong S., Wang G. 2017. Pheromone antagonist regulates optimal mating time in the moth Helicoverpa armigera. Curr. Biol. 27: 1610–1615.
Choi M.Y., Fuerst E.J., Rafaeli A., Jurenka R. 2003. Identification of a G protein-coupled receptor for pheromone biosynthesis activating neuropeptide from pheromone glands of the moth Helicoverpa zea. Proc. Natl. Acad. Sci. USA 100: 9721–9726.
Ding Z., Haussmann I., Ottiger M., Kubli E. 2003. Sex-peptides bind to two molecularly different targets in Drosophila melanogaster females. J. Neurobiol. 55: 372–384.
Domanitskaya E.V., Liu H., Chen S., Kubli E. 2007. The hydroxyproline motif of male sex peptide elicits the innate immune response in Drosophila females. FEBS J. 274: 5659–5668.
Dong J., Song Y., Li W., Shi J., Wang Z. 2016. Identification of putative chemosensory receptor genes from the Athetis dissimilis antennal transcriptome. PLoS One 11: e0147768.
Druart X., de Graaf S. 2018. Seminal plasma proteomes and sperm fertility. Anim. Reprod. Sci. 194: 33–40.
Duvall L.B., Basrur N.S., Molina H., McMeniman C.J., Vosshall L.B. 2017. A peptide signaling system that rapidly enforces paternity in the Aedes aegypti mosquito. Curr. Biol. 27: 3734–3742.
Eliyahu D., Nagalakshmi V., Kubli E., Choffat Y., Applebaum S.W., Rafaeli A. 2003. Inhibition of pheromone biosynthesis in Helicoverpa armigera by pheromonostatic peptides. J. Insect Physiol. 49: 569-574.
Emelyanov A.V., Fyodorov D.V. 2016. Thioredoxin-dependent disulfide bond reduction is required for protamine eviction from sperm chromatin. Genes Dev. 30: 2651–2656.
Evans J.P., Wilson A.J., Pilastro A., Garcia-Gonzalez F. 2019. Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications. Reproduction 157: R109-R126.
Fan Y., Rafaeli A., Moshitzky P., Kubli E., Choffat Y., Applebaum S.W. 2000. Common functional elements of Drosophila melanogaster seminal peptides involved in reproduction of Drosophila melanogaster and Helicoverpa armigera females. Insect Biochem. Mol. Biol. 30: 805–812.
Fedorka K.M., Winterhalter W.E., Ware B. 2011. Perceived sperm competition intensity influences seminal fluid protein production prior to courtship and mating. Evolution 65: 584–90.
Fónagy A., Ohnishi A., Esumi Y., Suzuki Y., Matsumoto S. 2005. Further studies of lipid droplets in the bombykol-producing pheromone gland of Bombyx mori. Ann. NY Acad. Sci. 1040: 310–314.
Fraaije M.W., Berkel W.J.V., Benen J.A., Visser J., Mattevi A. 1998. A novel oxidoreductase family sharing a conserved FAD-binding domain. Trends Biochem. Sci. 23: 206–207.
Gillott C. 2003. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev. Entomol. 48: 163–184.
Gioti A., Wigby S., Wertheim B., Schuster E., Martinez P., Pennington C.J, Partridge L., Chapman T. 2012. Sex peptide of Drosophila melanogaster males is a global regulator of reproductive processes in females. Proc. Biol. Sci. 279: 4423–4432.
Guang X.G., Yu X.P., Li D.T. 2023. Post-mating responses in insects induced by seminal fluid proteins and octopamine. Biology 12: 1283.
Hagström A.K., Liénard M.A., Groot A.T., Hedenström E., Löfstedt C. 2012. Semi-selective fatty acyl reductases from four heliothine moths influence the specific pheromone composition. PLoS One 7: e37230.
Hanin O., Azrielli A., Applebaum S.W., Rafaeli A. 2012. Functional impact of silencing the Helicoverpa armigera sex-peptide receptor on female reproductive behaviour. Insect Mol. Biol. 21: 161–167.
Hendrick J.P., Hartl F.U. 1993. Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62: 349–384.
Hosseini S.A., van Wijk M., Ke G., Goldansaz S.H., Schal C., Groot A.T. 2016. Experimental evidence for chemical mate guarding in a moth. Sci. Rep. 6: 38567.
Hou M.L. 1998. Adult population dynamics and reproductive ecology of the cotton bollworm, Helicoverpa armigera (Hüber) (Lepidoptera: Noctuidae). PhD thesis, Institute of Zoology Academia Sinica, Beijing China, 118 p.
Hughes G.P., Carde R.T. 2020. Do Helicoverpa armigera moths signal their fecundity by emission of an antagonist? J. Chem. Ecol. 46: 21–29.
Huntington J.A. 2011. Serpin structure, function and dysfunction. J. Thromb. Haemost. 9: 26–34.
Islinger M., Costello J.L., Kors S., Soupene E., Levine T.P., Kuypers F.A., Schrader M. 2020. The diversity of ACBD proteins-from lipid binding to protein modulators and organelle tethers. Biochim. Biophys. Acta Mol. Cell Res. 1867: 118675.
Jarriault D., Barrozo R.B., de Carvalho Pinto C., Greiner B., Dufour M., Masante-Roca I., Gramsbergen J.B., Anton S., Gadenne C. 2009. Age-dependent plasticity of sex pheromone response in the moth, Agrotis ipsilon: combined effects of octopamine and juvenile hormone. Horm. Behav. 56: 85–191.
Jin Z.Y., Gong H. 2001. Male accessory gland derived factors can stimulate oogenesis and enhance oviposition in Helicoverpa armigera (Lepidoptera: Noctuidae). Arch. Insect Biochem. Physiol. 46: 175–185.
Jurenka R. 2004. Insect pheromone biosynthesis. Top. Curr. Chem. 239: 97–132.
Jurenka R. 2017. Regulation of pheromone biosynthesis in moths. Curr. Opin. Insect Sci. 24: 29–35.
Kankare M., Salminen T., Laiho A., Vesala L., Hoikkala A. 2010. Changes in gene expression linked with adult reproductive diapause in a northern malt fly species: a candidate gene microarray study. BMC Ecol. 10: 3.
Karr T.L. 2008. Application of proteomics to ecology and population biology. Heredity 100: 200–206.
Kingan T.G., Thomas-Laemont P.A., Raina A.K. 1993. Male accessory gland factors elicit change from ‘virgin’ to ‘mated’ behaviour in the female corn earworm moth Helicoverpa zea. J. Exp. Biol. 183: 61–76.
Kiran T., Mangala J.N., Anjana K., Manjulakumari D. 2021. Heterologous expression of a substance which inhibits receptivity and calling in Helicoverpa armigera (Hübner). Insect Mol. Biol. 30: 472–479.
Koppik M., Fricke C. 2017. Gene expression changes in male accessory glands during ageing are accompanied by reproductive decline in Drosophila melanogaster. Mol. Ecol. 26: 6704–6716.
Laemmli U.K. 1970. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227: 680–685.
Le Bourg E., Valenti P., Lucchetta P., Payre F. 2001. Effects of mild heat shocks at young age on aging and longevity in Drosophila melanogaster. Biogerontology 2: 155–164.
Lee S.K., Kim B.Y., Choo Y.M., Jin B.R. 2018. Dual role of the serine protease homolog BmSPH-1 in the development and immunity of the silkworm Bombyx mori. Dev. Comp. Immunol. 85: 170–176.
Mack P.D., Kapelnikov A., Heifetz Y., Bender M. 2006. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 103: 10358–10363.
Mamtha R., Kiran T., Manjulakumari D. 2019. Accessory gland proteome of male tobacco cutworm, Spodoptera litura (F.) – an approach to identify proteins influencing reproductive physiology and behaviour. J. Asia-Pacific Entomol. 22: 778–785.
Martinez-Goikoetxea M., Lupas A.N. 2023. New protein families with hendecad coiled coils in the proteome of life. J. Struct. Biol. 215: 108007.
Matsumoto S. 2010. Molecular mechanisms underlying sex pheromone production in moths. Biosci. Biotechnol. Biochem. 74: 223–231.
Matsumoto S., Yoshiga T., Yokoyama N., Iwanaga M., Koshiba S., Kigawa T., Hirota H., Yokoyama S., Okano K., Mita K., Shimada T., Tatsuki S. 2001. Characterization of acyl-CoA-binding protein (ACBP) in the pheromone gland of the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 31: 603–609.
Michaud S., Marin R., Tanguay R.M. 1997. Regulation of heat shock gene induction and expression during Drosophila development. Cell. Mol. Life Sci. 53: 104–113.
Moehle K., Freund A., Kubli E., Robinson J.A. 2011. NMR studies of the solution conformation of the sex peptide from Drosophila melanogaster. FEBS Lett. 585: 1197–1202.
Moshitzky P., Fleischmann I., Chaimov N., Saudan P., Klauser S., Kubli E., Applebaum S.W. 1996. Sex-peptide activates juvenile hormone biosynthesis in the Drosophila melanogaster corpus allatum. Arch. Insect Biochem. Physiol. 32: 363–374.
Mueller J.L., Ripoll D.R., Aquadro C.F., Wolfner M.F. 2004. Comparative structural modeling and inference of conserved protein classes in Drosophila seminal fluid. Biol. Sci. 101: 13542–13547
Nagalakshmi V.K., Applebaum S.W., Kubli E., Choffat Y., Rafaeli A. 2004. The presence of Drosophila melanogaster sex peptide-like immunoactivity in the accessory glands of male Helicoverpa armigera. J. Insect Physiol. 50: 241–248.
Newell N.R., Ray S., Dalton J.E., Fortier J.C., Kao J.Y., Chang P.L., Nuzhdin S.V., Arbeitman M.N. 2020. The Drosophila post-mating response: Gene expression and behavioral changes reveal perdurance and variation in cross-tissue interactions. G3 Genes Genomes Genet. 10: 967–983.
Pagán O.R. 2021. Endozepines in insect development and metamorphosis. In: Raffa R.B., Amantea D. (Eds.) Naturally Occurring Benzodiazepines, Endozepines, and their Receptors. CRC Press, Boca Raton, pp. 9.
Pedro J.M.B., Sica V., Madeo F., Kroemer G. 2019. Acyl-CoA-binding protein (ACBP): the elusive ‘hunger factor’ linking autophagy to food intake. Cell Stress 3: 312–318.
Pelosi P., Iovinella I., Felicioli A., Dani F.R. 2014. Soluble proteins of chemical communication: an overview across arthropods. Front. Physiol. 27: 320.
Peng J., Chen S., Büsser S., Liu H., Honegger T., Kubli E. 2005. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr. Biol. 15: 207–213.
Petrova B., Liu K., Tian C., Kitaoka M., Freinkman E., Yang J., Orr-Weaver T.L. 2018. Dynamic redox balance directs the oocyte-to-embryo transition via developmentally controlled reactive cysteine changes. Proc. Natl. Acad. Sci. USA 115: E7978-E7986.
Poole L.B. 2015. The basics of thiols and cysteines in redox biology and chemistry. Free Radic. Biol. Med. 80: 148–157.
Rafaeli A. 2009. Pheromone biosynthesis activating neuropeptide (PBAN): regulatory role and mode of action. Gen. Com. Endocrinol. 162: 69–78.
Rafaeli A., Hanin O. 2013. The influence of photoperiod and mating on the profiles of seminal fluid peptides from male accessory glands of Helicoverpa armigera. Israel J. Entomol. 43: 51–79.
Rama, T., Tannavi K., Manjulakumari D. 2021. Do male-derived substances affect female reproductive physiology? A study on oviposition, fecundity and longevity aspects in female Helicoverpa armigera (Hubner) moths. Res. J. Agric. Sci. 12: 790–797.
Reinhardt K., Wong C.H., Georgiou A.S. 2009. Detection of seminal fluid proteins in the bed bug, Cimex lectularius, using two-dimensional gel electrophoresis and mass spectrometry. Parasitology 136: 283–292.
Rubinstein C.D., Wolfner M.F. 2013. Drosophila seminal protein ovulin mediates ovulation through female octopamine neuronal signaling. Proc. Natl. Acad. Sci. USA 110: 17420–17425.
Saraswathi S., Chaitra B.S., Tannavi K., Mamtha R., Sowrabha R., Karthik V.R., Manjulakumari D. 2021. A comparative protein profile of accessory glands of virgin and mated Leucinodes orbonalis males. Physiol. Entomol. 46: 60–69.
Schmidt T., Choffat Y., Klauser S., Kubli E. 1993. The Drosophila melanogaster sex-peptide: A molecular analysis of structure-function relationships. J. Insect Physiol. 39: 361–368.
Schmidt T., Choffat Y., Schneider M., Hunziker P., Fuyama Y., Kubli E. 1993. Drosophila suzukii contains a peptide homologous to the Drosophila melanogaster sex-peptide and functional in both species. Insect Biochem. Mol. Biol. 23: 571–579..
Schönfelder J., Alonso-Caballero A., Perez-Jimenez R. 2022. Mechanochemical evolution of disulfide bonds in proteins. Methods Mol. Biol. 2376: 283–300.
Scolari F., Khamis F.M., Pérez-Staples D. 2021. Beyond sperm and male accessory gland proteins: Exploring insect reproductive metabolomes. Front. Physiol. 12: 729440.
Snyder M.J., Antwerpen R.V. 1998. Evidence for a diazepam-binding inhibitor (DBI) benzodiazepine receptor-like mechanism in ecdysteroidogenesis by the insect prothoracic gland. Cell Tissue Res. 294: 161–168.
Stawiski E.W., Baucom A.E., Lohr S.C., Gregoret L.M. 2000. Predicting protein function from structure: unique structural features of proteases. Proc. Natl. Acad. Sci. USA 97: 3954–3958.
Steen H., Mann M. 2004. The ABC’s (and XYZ’s) of peptide sequencing. Nature Rev. Mol. Cell. Biol. 5: 699–711.
Takahashi S., Hasumi K., Ohnishi A., Koshino H., Matsumoto S. 2007. Synthesis and biological activities of analogs of D-glucosyl-l-tyrosine, a humoral factor that stimulates transcription of the acyl-CoA binding protein in the pheromone gland of the Silkmoth, Bombyx mori. Bioorg. Med. Chem. 15: 97–103.
Talapatra S., Wagner J.D., Thompson C.B. 2002. Elongation factor-1 alpha is a selective regulator of growth factor withdrawal and ER stress-induced apoptosis. Cell Death Differ. 9: 856–861.
Tillman J.A., Seybold S.J., Jurenka R.A., Blomquist G.J. 1999. Insect pheromones-an overview of biosynthesis and endocrine regulation. Insect Biochem. Mol. Biol. 29: 481–514.
Walters J.R., Harrison R.G. 2010. Combined EST and proteomic analysis identify rapidly evolving seminal fluid proteins in Heliconius butterflies. Mol. Biol. Evol. 27: 2000–2013.
Wang C., Li Q., Redden D.T., Weindruch R., Allison D.B. 2004. Statistical methods for testing effects on “maximum lifespan”. Mech. Ageing Dev. 125: 629–632.
Wedell N. 2005. Female receptivity in butterflies and moths. Rev. J. Exp. Biol. 208: 3433–3440.
Wiese S., Gronemeyer T., Ofman R., Kunze M., Grou C.P., Almeida J.A., Eisenacher M., Stephan C., Hayen H., Schollenberger L., Korosec T., Waterham H.R., Schliebs W., Erdmann R., Berger J., Meyer H., Just W., Azevedo J., Wanders R.J.A., Warscheid B. 2007. Proteomics characterization of mouse kidney peroxisomes by tandem mass spectrometry and protein correlation profiling. Mol. Cell. Proteom. 6: 2045–2057.
Wolfner M.F., Applebaum S.W. 2005. Reproduction and development. In: Atkinson P.W., Yamanaka N. (Eds.) Comprehensive Molecular Insect Science. 2nd Ed. Elsevier.
Xu J., Baulding J., Palli S.R. 2013. Proteomics of Tribolium castaneum seminal fluid proteins: identification of an angiotensin-converting enzyme as a key player in regulation of reproduction. J. Proteom. 14: 83–93.
Xu X., Wang Y., Bi H., Xu J., Liu Z., Niu C., et al. 2020. Mutation of the seminal protease gene, serine protease 2, results in male sterility in diverse lepidopterans. Insect Mol. Biol. 116: 103243.
Yang L., Mei Y., Fang Q., Wang J., Yan Z., Song Q., Lin Z., Ye G. 2017. Identification and characterization of serine protease inhibitors in a parasitic wasp, Pteromalus puparum. Sci. Rep. 7: 15755.
Zhang S., Liu X., Zhu B., Yin X., Du M., Song Q., An S.2014. Identification of differentially expressed genes in the pheromone glands of mated and virgin Bombyx mori by digital gene expression profiling. PLoS One 10: e111003.
Zhang S.F., Zhang Z., Kong X.B., Wang H.B., Liu F. 2018. Dynamic changes in chemosensory gene expression during the Dendrolimus punctatus mating process. Front. Physiol. 10: 1127.
Zhang Y., Dong Z., Gu P., Zhang W., Wang D., Guo X., Zhao P., Xia Q. 2014. Proteomics analysis of adult testis from Bombyx mori. Proteomics 14: 2345–2349.
Zhao L.N., Qin Z., Wei P., Guo H., Dang X., Wang S., Guo X., 2012. Elongation factor 1β’ gene from Spodoptera exigua: characterization and function identification through RNA interference. Int. J. Mol. Sci. 13: 8126–8141.
Zhou S., Zhang J., Fam M.D., Wyatt G.R., Walker V.K. 2002. Sequences of elongation factors-1 alpha and -1 gamma and stimulation by juvenile hormone in Locusta migratoria. Insect Biochem. Mol. Biol. 32: 1567–1576.
Downloads
Published
Issue
Section
License
Copyright (c) 2024 University of LatviaThis is an open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles in this journal without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access. Author(s) of the published papers retain copyright, the papers are made freely available for non-commercial purposes, allowing download, reuse, reprint and distribution of the material as long as the original authors and the source are cited. This license is equivalent to the CC BY-NC-ND.
