Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-28T07:35:48.697Z Has data issue: false hasContentIssue false
  • English
  • Français

RNA N6-methyladenosine of DHAPAT and PAP involves in regulation of diapause of Bombyx mori via the lipid metabolism pathway

Published online by Cambridge University Press:  09 August 2023

Yan-Hua Chen Open the ORCID record for Yan-Hua Chen [Opens in a new window] ,
Tao Jiang ,
Ayinuer Yasen ,
Bing-Yan Fan ,
Juan Zhu ,
Mei-Xian Wang  and
Xing-Jia Shen Open the ORCID record for Xing-Jia Shen [Opens in a new window]
Yan-Hua Chen
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
Tao Jiang
Affiliation:
Silkworm Egg Institute of Jiangsu Province, Wuxi, Jiangsu 214000, China
Ayinuer Yasen
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
Bing-Yan Fan
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
Juan Zhu
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
Mei-Xian Wang
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
Xing-Jia Shen*
Affiliation:
Jiangsu Key Laboratory of Sericultural Biology and Biotechnology, College of Biotechnology, Jiangsu University of Science and Technology, Zhenjiang, Jiangsu 212100, China Key Laboratory of Silkworm and Mulberry Genetic Improvement, Ministry of Agriculture and Rural Affairs, Sericulture Research Institute, Chinese Academy of Agricultural Sciences, Zhenjiang, Jiangsu 212100, China
*
Corresponding author: Xing-Jia Shen; Email: shenxjsri@163.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Environment-induced epigenetics are involved in diapause regulation, but the molecular mechanism that epigenetically couples nutrient metabolism to diapause regulation remains unclear. In this study, we paid special attention to the significant differences in the level of N6-adenosine methylation (m6A) of dihydroxyacetone phosphate acyltransferase (DHAPAT) and phosphatidate phosphatase (PAP) genes in the lipid metabolism pathway of the bivoltine silkworm (Bombyx mori) strain Qiufeng developed from eggs incubated at a normal temperature (QFHT, diapause egg producer) compared to those from eggs incubated at a low temperature (QFLT, non-diapause egg producer). We knocked down DHAPAT in the pupal stage of the QFLT group, resulting in the non-diapause destined eggs becoming diapausing eggs. In the PAP knockdown group, the colour of the non-diapause destined eggs changed from light yellow to pink 3 days after oviposition, but they hatched as normal. Moreover, we validated that YTHDF3 binds to m6A-modified DHAPAT and PAP mRNAs to promote their stability and translation. These results suggest that RNA m6A methylation participates in the diapause regulation of silkworm by changing the expression levels of DHAPAT and PAP and reveal that m6A epigenetic modification can be combined with a lipid metabolism signal pathway to participate in the regulation of insect diapause traits, which provides a clearer image for exploring the physiological basis of insect diapause.

Keywords

Bombyx moriDHAPATdiapauselipid metabolismPAPpost-transcriptional regulationRNA N6-adenosine methylationYTHDF3
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 5 , October 2023 , pp. 665 - 675
Check for updates
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

*

These authors contributed equally to this work.

References

Amsalem, E, Galbraith, D, Cnaani, J, Teal, P and Grozinger, C (2015) Conservation and modification of genetic and physiological toolkits underpinning diapause in bumble bee queens. Molecular Ecology 24, 5596–5615.CrossRefGoogle ScholarPubMed
Arrese, EL and Soulages, JL (2009) Insect fat body: energy, metabolism, and regulation. Annual Review of Entomology 55, 207–225.CrossRefGoogle Scholar
Batz, ZA and Armbruster, PA (2018) Diapause-associated changes in the lipid and metabolite profiles of the Asian tiger mosquito, Aedes albopictus. Journal of Experimental Biology 221, jeb189480.CrossRefGoogle ScholarPubMed
Batz, ZA, Goff, AC and Armbruster, PA (2017) MicroRNAs are differentially abundant during Aedes albopictus diapause maintenance but not diapause induction. Insect Molecular Biology 26, 721–733.CrossRefGoogle Scholar
Boissel, S, Reish, O, Proulx, K, Kawagoe-Takaki, H, Sedgwick, B, Yeo, GS, Meyre, D, Golzio, C, Molinari, F, Kadhom, N, Etchevers, HC, Saudek, V, Farooqi, IS, Froguel, P, Lindahl, T, O'Rahilly, S, Munnich, A and Colleaux, L (2009) Loss-of-function mutation in the dioxygenase-encoding FTO gene causes severe growth retardation and multiple malformations. American Journal of Human Genetics 85, 106–111.CrossRefGoogle ScholarPubMed
Bonasio, R, Tu, S and Reinberg, D (2010) Molecular signals of epigenetic states. Science 330, 612–616.CrossRefGoogle ScholarPubMed
Castellanos-Rubio, A, Santin, I, Olazagoitia-Garmendia, A, Romero-Garmendia, I, Jauregi-Miguel, A, Legarda, M and Bilbao, JR (2019) A novel RT-QPCR-based assay for the relative quantification of residue specific m6A RNA methylation. Scientific Reports 9, 4220.CrossRefGoogle ScholarPubMed
Chen, Y, Fan, B, Yasen, A, Zhu, J, Wang, M and Shen, X (2022) YTHDF3 is involved in the diapause process of bivoltine Bombyx mori strains by regulating the expression of Cyp307a1 and Cyp18a1 genes in the ecdysone synthesis pathway. Biomolecules 12, 1127.CrossRefGoogle ScholarPubMed
Chen, YH, Jiang, T, Yasen, A, Fan, BY, Zhu, J, Wang, MX, Qian, P and Shen, XJ (2023) m(6)A-dependent mevalonate kinase in juvenile hormone synthesis pathway regulates the diapause process of bivoltine silkworm (Bombyx mori). Molecular Biology Reports 50, 5295–5306.CrossRefGoogle Scholar
Denlinger, DL (2002) Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
Dominissini, D, Moshitch-Moshkovitz, S, Schwartz, S, Salmon-Divon, M, Ungar, L, Osenberg, S, Cesarkas, K, Jacob-Hirsch, J, Amariglio, N, Kupiec, M, Sorek, R and Rechavi, G (2012) Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485, 201–206.CrossRefGoogle ScholarPubMed
Du, H, Zhao, Y, He, J, Zhang, Y, Xi, H, Liu, M, Ma, J and Wu, L (2016) YTHDF2 destabilizes m(6)A-containing RNA through direct recruitment of the CCR4-NOT deadenylase complex. Nature Communications 7, 12626.CrossRefGoogle ScholarPubMed
Duan, T-F, Li, L, Wang, H-C and Pang, B-P (2022) MicroRNA miR-2765-3p regulates reproductive diapause by targeting FoxO in Galeruca daurica. Insect Science 30, 279–292.CrossRefGoogle ScholarPubMed
Fischman, BJ, Pitts-Singer, TL and Robinson, GE (2017) Nutritional regulation of phenotypic plasticity in a solitary bee (Hymenoptera: Megachilidae). Environmental Entomology 46, 1070–1079.CrossRefGoogle Scholar
Gebeyew, K, Yang, C, Mi, H, Cheng, Y, Zhang, T, Hu, F, Yan, Q, He, Z, Tang, S and Tan, Z (2022) Lipid metabolism and m(6)A RNA methylation are altered in lambs supplemented rumen-protected methionine and lysine in a low-protein diet. Journal of Animal Science and Biotechnology 13, 85.CrossRefGoogle Scholar
George, S and Palli, SR (2020) Histone deacetylase 11 knockdown blocks larval development and metamorphosis in the red flour beetle, Tribolium castaneum. Frontiers in Genetics 11, 683.CrossRefGoogle ScholarPubMed
George, S, Gaddelapati, SC and Palli, SR (2019) Histone deacetylase 1 suppresses Krüppel homolog 1 gene expression and influences juvenile hormone action in Tribolium castaneum. PNAS 116, 17759–17764.CrossRefGoogle ScholarPubMed
Gupta, A.P. (1991) Morphogenetic hormones of arthropodss. In Schooneveld, H (ed.), ecent Advances In Comparative Arthropod Morphology, Physiology, And Development, Vol. 3. New Brunswick: Rutgers University Press.Google Scholar
Hahn, DA and Denlinger, DL (2007) Meeting the energetic demands of insect diapause: nutrient storage and utilization. Journal of Insect Physiology 53, 760–773.CrossRefGoogle ScholarPubMed
Hand, SC, Menze, MA, Borcar, A, Patil, Y, Covi, JA, Reynolds, JA and Toner, M (2011) Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. Journal of Insect Physiology 57, 584–594.CrossRefGoogle ScholarPubMed
Izumi, Y, Sonoda, S and Tsumuki, H (2007) Effects of diapause and cold-acclimation on the avoidance of freezing injury in fat body tissue of the rice stem borer, Chilo suppressalis Walker. Journal of Insect Physiology 53, 685–690.CrossRefGoogle ScholarPubMed
Jiang, T, Li, J, Qian, P, Xue, P, Xu, J, Chen, Y, Zhu, J, Shunming, T, Zhao, Q, Qian, H and Shen, X-J (2019) The role of N6-methyladenosine modification on diapause in silkworm (Bombyx mori) strains that exhibit different voltinism. Molecular Reproduction and Development 86, 1981–1992.CrossRefGoogle ScholarPubMed
Kang, DS, Cotten, MA, Denlinger, DL and Sim, C (2016) Comparative transcriptomics reveals key gene expression differences between diapausing and non-diapausing adults of Culex pipiens. PLoS ONE 11, e0154892.CrossRefGoogle ScholarPubMed
Kitagawa, N, Shiomi, K, Imai, K, Niimi, T, Yaginuma, T and Yamashita, O (2005) Establishment of a sandwich ELISA system to detect diapause hormone, and developmental profile of hormone levels in egg and subesophageal ganglion of the silkworm, Bombyx mori. Zoological Science 22, 213–221.CrossRefGoogle ScholarPubMed
Koštál, V (2006) Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.CrossRefGoogle ScholarPubMed
Lehmann, P, Pruisscher, P, Posledovich, D, Carlsson, M, Käkelä, R, Tang, P, Nylin, S, Wheat, CW, Wiklund, C and Gotthard, K (2016) Energy and lipid metabolism during direct and diapause development in a pierid butterfly. Journal of Experimental Biology 219, 3049–3060.Google Scholar
Li, Y, Zhang, L, Chen, H, Koštál, V, Simek, P, Moos, M and Denlinger, DL (2015) Shifts in metabolomic profiles of the parasitoid Nasonia vitripennis associated with elevated cold tolerance induced by the parasitoid's diapause, host diapause and host diet augmented with proline. Insect Biochemistry and Molecular Biology 63, 34–46.CrossRefGoogle ScholarPubMed
Li, B, Hu, P, Zhang, SZ, Toufeeq, S, Wang, J, Zhao, K, Xu, X, Xu, JP and Huang, SJ (2019) DNA methyltransferase BmDnmt1 and BmDnmt2 in silkworm (Bombyx mori) and the regulation of silkworm embryonic development. Archives of Insect Biochemistry and Physiology 100, e21529.CrossRefGoogle ScholarPubMed
Li, B, Hu, P, Zhu, LB, You, LL, Cao, HH, Wang, J, Zhang, SZ, Liu, MH, Toufeeq, S, Huang, SJ and Xu, JP (2020) DNA methylation is correlated with gene expression during diapause termination of early embryonic development in the silkworm (Bombyx mori). International Journal of Molecular Sciences 21, 671.CrossRefGoogle ScholarPubMed
Ling, L, Kokoza, VA, Zhang, C, Aksoy, E and Raikhel, AS (2017) MicroRNA-277 targets insulin-like peptides 7 and 8 to control lipid metabolism and reproduction in Aedes aegypti mosquitoes. PNAS 114, E8017–e8024.CrossRefGoogle ScholarPubMed
Meister, P, Schott, S, Bedet, C, Xiao, Y, Rohner, S, Bodennec, S, Hudry, B, Molin, L, Solari, F, Gasser, SM and Palladino, F (2011) Caenorhabditis elegans heterochromatin protein 1 (HPL-2) links developmental plasticity, longevity and lipid metabolism. Genome Biology 12, R123.CrossRefGoogle ScholarPubMed
Meuti, ME, Bautista-Jimenez, R and Reynolds, JA (2018) Evidence that microRNAs are part of the molecular toolkit regulating adult reproductive diapause in the mosquito, Culex pipiens. PLoS ONE 13, e0203015.CrossRefGoogle ScholarPubMed
Pitts-Singer, TL (2020) Photoperiod effect on Megachile rotundata (Hymenoptera: Megachilidae) female regarding diapause status of progeny: the importance of data scrutiny. Environmental Entomology 49, 516–527.CrossRefGoogle ScholarPubMed
Popović, ŽD, Subotić, A, Nikolić, TV, Radojičić, R, Blagojević, DP, Grubor-Lajšić, G and Koštál, V (2015) Expression of stress-related genes in diapause of European corn borer (Ostrinia nubilalis Hbn.). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 186, 1–7.CrossRefGoogle ScholarPubMed
Poupardin, R, Schöttner, K, Korbelová, J, Provazník, J, Dolezel, D, Pavlinic, D, Beneš, V and Kostál, V (2015) Early transcriptional events linked to induction of diapause revealed by RNAseq in larvae of drosophilid fly, Chymomyza costata. BMC Genomics 16, 720.CrossRefGoogle ScholarPubMed
Ragland, GJ and Keep, E (2017) Comparative transcriptomics support evolutionary convergence of diapause responses across Insecta. Physiological Entomology 42, 246–256.CrossRefGoogle Scholar
Ragland, GJ, Denlinger, DL and Hahn, DA (2010) Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. PNAS 107, 14909–14914.CrossRefGoogle ScholarPubMed
Rando, OJ (2012) Daddy issues: paternal effects on phenotype. Cell 151, 702–708.CrossRefGoogle ScholarPubMed
Reynolds, JA (2017) Epigenetic Influences on Diapause. Advances in Insect Physiology 53, 115–144.CrossRefGoogle Scholar
Reynolds, JA and Hand, SC (2009) Embryonic diapause highlighted by differential expression of mRNAs for ecdysteroidogenesis, transcription and lipid sparing in the cricket Allonemobius socius. Journal of Experimental Biology 212, 2075–2084.CrossRefGoogle ScholarPubMed
Reynolds, JA, Poelchau, MF, Rahman, Z, Armbruster, PA and Denlinger, DL (2012) Transcript profiling reveals mechanisms for lipid conservation during diapause in the mosquito, Aedes albopictus. Journal of Insect Physiology 58, 966–973.CrossRefGoogle ScholarPubMed
Reynolds, JA, Peyton, JT and Denlinger, DL (2017) Changes in microRNA abundance may regulate diapause in the flesh fly, Sarcophaga bullata. Insect Biochemistry and Molecular Biology 84, 1–14.CrossRefGoogle ScholarPubMed
Reynolds, JA, Nachman, RJ and Denlinger, DL (2019) Distinct microRNA and mRNA responses elicited by ecdysone, diapause hormone and a diapause hormone analog at diapause termination in pupae of the corn earworm, Helicoverpa zea. General and Comparative Endocrinology 278, 68–78.CrossRefGoogle Scholar
Sahoo, A, Dutta, A, Dandapat, J and Samanta, L (2018) Low H2O2 and enhanced oxidative resistance in the diapause-destined pupa of silkworm, Antheraea mylitta (Lepidoptera:Saturniidae) suggest their possible involvement in dormancy and lifespan extension. BMC Zoology 3, 1.CrossRefGoogle Scholar
Slobodin, B, Han, R, Calderone, V, Vrielink, J, Loayza-Puch, F, Elkon, R and Agami, R (2017) Transcription impacts the efficiency of mRNA translation via co-transcriptional N6-adenosine methylation. Cell 169, 326–337, e312.CrossRefGoogle ScholarPubMed
Smemo, S, Tena, JJ, Kim, KH, Gamazon, ER, Sakabe, NJ, Gómez-Marín, C, Aneas, I, Credidio, FL, Sobreira, DR, Wasserman, NF, Lee, JH, Puviindran, V, Tam, D, Shen, M, Son, JE, Vakili, NA, Sung, HK, Naranjo, S, Acemel, RD, Manzanares, M, Nagy, A, Cox, NJ, Hui, CC, Gomez-Skarmeta, JL and Nóbrega, MA (2014) Obesity-associated variants within FTO form long-range functional connections with IRX3. Nature 507, 371–375.CrossRefGoogle ScholarPubMed
Stoll, S, Wang, C and Qiu, H (2018) DNA methylation and histone modification in hypertension. International Journal of Molecular Sciences 19, 703–715.CrossRefGoogle ScholarPubMed
Süess, P, Dircksen, H, Roberts, KT, Gotthard, K, Nässel, DR, Wheat, CW, Carlsson, MA and Lehmann, P (2022) Time- and temperature-dependent dynamics of prothoracicotropic hormone and ecdysone sensitivity co-regulate pupal diapause in the green-veined white butterfly Pieris napi. Insect Biochemistry and Molecular Biology 149, 103833.CrossRefGoogle ScholarPubMed
Takemoto, S, Nakano, M, Fukami, T and Nakajima, M (2021) m(6)A modification impacts hepatic drug and lipid metabolism properties by regulating carboxylesterase 2. Biochemical Pharmacology 193, 114766.CrossRefGoogle ScholarPubMed
Taylor, LR (1987) Review of Seasonal Adaptations of Insects.Journal of Animal Ecology 56, 374–375.Google Scholar
Vukašinović, EL, Pond, DW, Worland, MR, Kojić, D, Purać, J, Popović Ž, D and Grubor-Lajšić, G (2015) Diapause induces remodeling of the fatty acid composition of membrane and storage lipids in overwintering larvae of Ostrinia nubilalis, Hubn. (Lepidoptera: Crambidae). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 184, 36–43.CrossRefGoogle ScholarPubMed
Vukašinović, EL, Pond, DW, Grubor-Lajšić, G, Worland, MR, Kojić, D, Purać, J, Popović, ŽD and Blagojević, DP (2018) Temperature adaptation of lipids in diapausing Ostrinia nubilalis: an experimental study to distinguish environmental versus endogenous controls. Journal of Comparative Physiology B 188, 27–36.CrossRefGoogle ScholarPubMed
Wadsworth, C and Dopman, E (2015) Transcriptome profiling reveals mechanisms for the evolution of insect seasonality. Journal of Experimental Biology 218, 3611–3622.Google ScholarPubMed
Wang, X, Zhu, L, Chen, J and Wang, Y (2015) mRNA m6A methylation downregulates adipogenesis in porcine adipocytes. Biochemical and Biophysical Research Communications 459, 201–207.CrossRefGoogle ScholarPubMed
Wang, Y, Wang, Y, Gu, J, Su, T, Gu, X and Feng, Y (2022) The role of RNA m6A methylation in lipid metabolism. Frontiers in Endocrinology 13, 866116.CrossRefGoogle ScholarPubMed
Zhong, X, Yu, J, Frazier, K, Weng, X, Li, Y, Cham, CM, Dolan, K, Zhu, X, Hubert, N, Tao, Y, Lin, F, Martinez-Guryn, K, Huang, Y, Wang, T, Liu, J, He, C, Chang, EB and Leone, V (2018) Circadian clock regulation of hepatic lipid metabolism by modulation of m6A mRNA methylation. Cell Reports 25, 1816–1828, e1814.CrossRefGoogle Scholar