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Silencing the triacylglycerol lipase (TGL) gene decreases the number of apyrene sperm and inhibits oviposition in Sitotroga cerealella

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Abstract

Triacylglycerol lipase (TGL) is an essential lipid metabolism enzyme that also plays a critical role in energy metabolism; however, how it regulates other life processes is unknown. To investigate the functional role of TGL in moth reproduction, males Sitotroga cerealella were used as a model. The TGL gene was cloned and analysed. The results showed that the open reading frame of TGL was 1968 bp long and contained three conserved regions. TGL gene expression was higher in the larval and early adult stages than in the pupal stage, with the highest levels observed in the fat body, testis and accessory glands during the early adult stage. Moreover, after TGL in male adults was silenced through RNAi, the protein content in male accessory glands remained unchanged, and the spermatophore transferred into females mated with TGL-silenced males became small and empty; meanwhile, the number of apyrene sperm in the spermatophore was significantly reduced due to the reduction of apyrene sperm in males, which eventually led to the significant reduction of egg-laying amount. All of the findings suggest that TGL regulates the amount of sperm in male moths as well as the morphology and quality of spermatophores transferred to females after mating with treated males, implying that TGL is critical for Sitotroga cerealella’s reproductive process.

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References

  1. Ma M, Chang MM, Lei CL, Yang FL (2016) A garlic substance disrupts odorant-binding protein recognition of insect pheromones released from adults of the angoumois grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insect Mol Biol 25:530–540. https://doi.org/10.1111/imb.12240

    Article  CAS  PubMed  Google Scholar 

  2. Trematerra P (2015) Adult dispersal of Sitotroga cerealella in a conventional small-farm in Southern Italy. Bull Insectol 68:111–118. http://www.bulletinofinsectology.org/

  3. Akinneye JO, Oyeniyi EA (2015) Insecticidal efficacy of Cleistopholis patens (Benth) against Sitotroga cerealella Olivier (Lepidoptera: Gelechiidae) infesting rice grains in Nigeria. J Crop Protect 5:1–10. https://jcp.modares.ac.ir/article-3-7621-en.html

  4. Subramanyam B, Hagstrum DW (1995) Integrated management of insects in stored products. CRC, Florida

    Google Scholar 

  5. Wu MY, Ying YY, Zhang SS et al (2020) Effects of diallyl trisulfide, an active substance from garlic essential oil, on energy metabolism in male moth Sitotroga cerealella (Olivier). Insects. https://doi.org/10.3390/insects11050270

    Article  PubMed  PubMed Central  Google Scholar 

  6. Wu MY (2020) Effect of diallyl trisulfide on sperm quality of Sitotroga cerealella Oliver. Master thesis. Wuhan, P.R.China: Huazhong Agricultural University. https://doi.org/10.27158/d.cnki.ghznu.2020.000524

  7. Ying YY (2019) Regulation of diallyl trisulfide on post-mating effect of Sitotroga cerealella at sublethal concentration. Master thesis. Wuhan, P.R.China: Huazhong Agricultural University. https://doi.org/10.27158/d.cnki.ghznu.2019.000783

  8. Chen X, Firdaus SJ, Fu Z et al (2019) Manduca sexta Perilipin 1B: a new PLIN1 isoform linked to fat storage prior to pupation. Insect Biochem Mol Biol 110:69–79. https://doi.org/10.1016/j.ibmb.2019.05.001

    Article  CAS  PubMed  Google Scholar 

  9. Zimmermann R, Strauss JG, Haemmerle G et al (2004) Fat mobilization in adipose tissue is promoted by adipose triglyceride lipase. Science 306:1383–1386. https://doi.org/10.1126/science.1100747

    Article  CAS  PubMed  Google Scholar 

  10. Arrese EL, Howard AD, Patel RT, Rimoldi OJ, Soulages JL (2010) Mobilization of lipid stores in Manduca sexta: cDNA cloning and developmental expression of fat body triglyceride lipase, TGL. Insect Biochem Mol Biol 40:91–99. https://doi.org/10.1016/j.ibmb.2009.12.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Arrese EL, Wells MA (1994) Purification and properties of a phosphorylatable triacylglycerol lipase from the fat body of an insect Manduca sexta. J Lipid Res 35:1652–1660. https://doi.org/10.1016/S0022-2275(20)41163-0

    Article  CAS  PubMed  Google Scholar 

  12. Rajakumari S, Daum G (2010) Janus-faced enzymes yeast Tgl3p and Tgl5p catalyze lipase and acyltransferase reactions. Mol Biol Cell 21:501–510. https://doi.org/10.1091/mbc.e09-09-0775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Arrese EL, Patel RT, Soulages JL (2006) The main triglyceride-lipase from the insect fat body is an active phospholipase A (1): identification and characterization. J Lipid Res 47:2656–2667. https://doi.org/10.1194/jlr.M600161-JLR200

    Article  CAS  PubMed  Google Scholar 

  14. Jiang YP, Li L, Liu ZY et al (2016) Adipose triglyceride lipase (Atgl) mediates the antibiotic jinggangmycin-stimulated reproduction in the brown planthopper Nilaparvata lugens. Stål Sci Rep 6:18984. https://doi.org/10.1038/srep18984

    Article  CAS  PubMed  Google Scholar 

  15. Wang C, Huang X (2012) Lipid metabolism and Drosophila sperm development. Sci Chin Life Sci 55:35–40. https://doi.org/10.1007/s11427-012-4274-2

    Article  CAS  Google Scholar 

  16. Clifton ME, Correa S, Rivera-Perez C, Nouzova M, Noriega FG (2014) Male Aedes aegypti mosquitoes use JH III transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes. J Insect Physiol 64:40–47. https://doi.org/10.1016/j.jinsphys.2014.03.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Fernando-warnakulasuriya G, Tsuchida K, Wells MA (1988) Effect of dietary lipid content on lipid transport and storage during larval development of Manduca sexta. Insect Biochem 18:211–214. https://doi.org/10.1016/0020-1790(88)90025-X

    Article  CAS  Google Scholar 

  18. Chang MM, Shah S, Wu MY et al (2020) Effect of diallyl trisulfide on the reproductive behavior of the grain moth, Sitotroga cerealella (Lepidoptera: Gelechiidae). Insects 11:21. https://doi.org/10.3390/insects11010021

    Article  Google Scholar 

  19. Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86:1–13. https://doi.org/10.1111/j.1469-185X.2010.00130.x

    Article  PubMed  Google Scholar 

  20. Matthews RW, Matthews JR (2010) Insect behavior. Springer, Dordrecht

    Book  Google Scholar 

  21. Gillott C (2003) Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163–184. https://doi.org/10.1146/annurev.ento.48.091801.112657

    Article  CAS  PubMed  Google Scholar 

  22. Gwynne DT (2008) Sexual conflict over nuptial gifts in insects. Annu Rev Entomol 53:83–101. https://doi.org/10.1146/annurev.ento.53.103106.093423

    Article  CAS  PubMed  Google Scholar 

  23. Chapman RF (1982) The insects: structure and function. Cambridge University, London

    Google Scholar 

  24. Wedell N (2002) Ejaculate size in bushcrickets: the importance of being large. J Evolut Biol 10:315–325. https://doi.org/10.1046/j.1420-9101.1997.10030315.x

    Article  Google Scholar 

  25. Meslina C, Cherwinb ST, Plakke MS et al (2018) Correction: Structural complexity and molecular heterogeneity of a butterfly ejaculate reflect a complex history of selection. Proc Natl Acad Sci USA 114:E5406-5413. https://doi.org/10.1073/pnas.1801459115

    Article  Google Scholar 

  26. Phillips DM (1971) Morphogenesis of the lacinate appendages of Lepidopteran spermatozoa. J Ultrastruct Res 34:67–585. https://doi.org/10.1016/S0022-5320(71)80064-3

    Article  Google Scholar 

  27. Holman L, Freckleton RP, Snook RR (2008) What use is an infertile sperm? A comparative study of sperm-heteromorphic Drosophila. Evolution 62:374–385. https://doi.org/10.1111/j.1558-5646.2007.00280.x

    Article  PubMed  Google Scholar 

  28. Swallow JG, Wilkinson GS (2002) The long and short of sperm polymorphism in insects. Biol Rev 77:153–182. https://doi.org/10.1017/S1464793101005851

    Article  PubMed  Google Scholar 

  29. Osanai M, Kasuga H, Aigaki T (1987) Physiological role of apyrene spermatozoa of Bombyx mori. Experientia 43:593–596. https://doi.org/10.1007/BF02126341

    Article  Google Scholar 

  30. Silberglied RE, Shepherd JG, Dickinson JL (1984) Eunuchs: The role of apyrene sperm in lepidoptera? Am Nat 123:255–265. https://doi.org/10.2307/2461036

    Article  Google Scholar 

  31. Katsuno S (1977) Studies on eupyrene and apyrene spermatozoa in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae): V. The fact related to the separation of eupyrene sperm bundles. Appl Entomol Zool 12:370–371. https://doi.org/10.1303/aez.13.127

    Article  Google Scholar 

  32. Friedländer M, Seth RK, Reynolds SE (2005) Eupyrene and apyrene sperm: dichotomous spermatogenesis in Lepidoptera. Adv Insect Physiol 32:206–308. https://doi.org/10.1016/S0065-2806(05)32003-0

    Article  Google Scholar 

  33. Chen SQ, Liu Y, Yang X et al (2020) Dysfunction of dimorphic sperm impairs male fertility in the silkworm. Cell Discov 6:60. https://doi.org/10.1038/s41421-020-00194-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ram KR, Wolfner MF (2007) Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet 3:2428–2438. https://doi.org/10.1371/journal.pgen.0030238

    Article  CAS  Google Scholar 

  35. Ram KR, Wolfner MF (2007) Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol 47:427–445. https://doi.org/10.1093/icb/icm046

    Article  CAS  Google Scholar 

  36. Happ GM (1992) Maturation of the male reproductive system and its endocrine regulation. Annu Rev Entomol 37:303–320. https://doi.org/10.1146/annurev.en.37.010192.001511

    Article  CAS  PubMed  Google Scholar 

  37. Herndon LA, Wolfner MF (1995) A Drosophila seminal fluid protein, Acp26Aa, stimulates egg laying in females for 1 day after mating. PNAS 92:10114–10118. https://doi.org/10.1073/pnas.92.22.10114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Wolfner MF (2002) The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88:85–93. https://doi.org/10.1038/sj.hdy.6800017

    Article  CAS  PubMed  Google Scholar 

  39. Marchini D, Del Bene G, Cappelli L, Dallai R (2003) Ultrastructure of the male reproductive accessory glands in the medfly Ceratitis capitata (Diptera: Tephritidae) and preliminary characterization of their secretions. Arthropod Struct Dev 31:313–327. https://doi.org/10.1016/S1467-8039(03)00003-3

    Article  CAS  PubMed  Google Scholar 

  40. Davies SJ, Chapman T (2006) Identification of genes expressed in the accessory glands of male mediterranean fruit flies (Ceratitis capitata). Insect Biochem Mol Biol 36:846–856. https://doi.org/10.1016/j.ibmb.2006.08.009

    Article  CAS  PubMed  Google Scholar 

  41. Adams EM, Wolfner MF (2007) Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage. J Insect Physiol 53:319–331. https://doi.org/10.1016/j.jinsphys.2006.12.003

    Article  CAS  PubMed  Google Scholar 

  42. Abry MF, Kimenyi KM, Masiga D, Kulohoma BW (2017) Comparative genomics identifies male accessory gland proteins in five species. Welcome Open Res 2:73. https://doi.org/10.12688/wellcomeopenres.12445.2

  43. Avila FW, Sirot LK, Laflamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Ann Entomol 56:21. https://doi.org/10.1603/AN12079

    Article  CAS  Google Scholar 

  44. Friedländer M, Gitay H (1972) The fate of the normal-anucleated spermatozoa in inseminated females of the silkworm Bombyx mori. J Morphol 138:121–129. https://doi.org/10.1002/jmor.1051380104

    Article  PubMed  Google Scholar 

  45. Kawamura N, Bando YN, H, (1998) Behavior of mitochondria during eupyrene and apyrene spermatogenesis in the silkworm, Bombyx mori (Lepidoptera), investigated by fluorescence in situ hybridization and electron microscopy. Protoplasma 202:223–231. https://doi.org/10.1007/BF01282550

    Article  CAS  Google Scholar 

  46. Friedländer M (1997) Control of the eupyrene-apyrene sperm dimorphism in Lepidoptera. J Insect Physiol 43:1085–1092. https://doi.org/10.1016/S0022-1910(97)00044-9

    Article  PubMed  Google Scholar 

  47. Boggs CL (1990) A general model of the role of male-donated nutrients in female insects’ reproduction. Am Nat 136:598–617. https://doi.org/10.1086/285118

    Article  Google Scholar 

  48. Boggs CL, Gilbert LE (1979) Male contribution to egg production in butterflies: Evidence for transfer of nutrients at mating. Science 206:83–84. https://doi.org/10.1126/science.206.4414.83

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (31871955), the National Key Research and Development Program of China (2018YFD0201009), Hubei Provincial Natural Science Foundation of China (2017CFB541), Fundamental Research Funds for the Central Universities (No. 2662017JC032).

Funding

This work was supported by the National Natural Science Foundation of China (31871955), the National Key Research and Development Program of China (2018YFD0201009), Hubei Provincial Natural Science Foundation of China (2017CFB541), Fundamental Research Funds for the Central Universities (No. 2662017JC032).

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Conceived of and designed the experiments: W-HY, M-YW, and F-LY. Performed the experiments: W-HY, M-YW, NT; Analysis of the data: W-HY and GW; Drafted and revised manuscript: W-HY, SS, Y-CY, KKE, and F-LY. All authors approved the final version of the article, including the authorship list.

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Correspondence to Feng-Lian Yang.

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Yan, Wh., Wu, MY., Shah, S. et al. Silencing the triacylglycerol lipase (TGL) gene decreases the number of apyrene sperm and inhibits oviposition in Sitotroga cerealella. Cell. Mol. Life Sci. 79, 44 (2022). https://doi.org/10.1007/s00018-021-04048-6

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