Comparative Proteomics and Metabonomics Analysis of Different Diapause Stages Revealed a New Regulation Mechanism of Diapause in (Lepidoptera: Pyralidae)

Overview

Journal Molecules

Publisher MDPI

Specialty Biology

Date 2024 Aug 10

PMID 39124877

Authors

Lijun Shao

Fangzheng Yue

Jinfu Fan

Qin Su

Hairui Liu

Quanyi Zhang

Linbo Xu

Affiliations

Soon will be listed here.

Abstract

Histone acetylation is an important epigenetic mechanism that has been shown to play a role in diapause regulation. To explore the physiological and molecular mechanisms of histone deacetylase in the diapause process, LC-MS/MS analysis was used to perform TMT proteomic and metabolomic analysis on non-diapause (ND), pre-diapause (PreD), diapause (D), cold treatment (CT), and post-diapause (RD) stages of the meadow moth. A total of 5367 proteins were identified by proteomics, including 1179 differentially expressed proteins. We found 975 (602 up-regulated and 373 down-regulated), 997 (608 up-regulated and 389 down-regulated), 1119 (726 up-regulated and 393 down-regulated), 1179 (630 up-regulated and 549 down-regulated), 94 (51 up-regulated and 43 down-regulated), 111 (63 up-regulated and 48 down-regulated), 533 (243 up-regulated and 290 down-regulated), 58 (31 up-regulated and 27 down-regulated), and 516 (228 up-regulated and 288 down-regulated) proteins in ND and PreD, ND and D, ND and CT, ND and RD, PreD and D, PreD and CT, PreD and RD, D and CT, D and RD, and CT and RD stages, respectively. A total of 1255 differentially expressed metabolites were annotated by metabolomics. Through KEGG analysis and time series analysis of differentially expressed metabolites, we found that phospholipids were annotated in significantly different modules, demonstrating their important role in the diapause process of the meadow moth. Using phospholipids as an indicator for weighted gene co-expression network analysis, we analyzed the most relevant differentially expressed proteins in the module and found that ribosomal 40s and 60s subunits were the most relevant proteins for diapause. Because there have been studies that have shown that histone deacetylase is associated with the diapause of meadow moths, we believe that histone deacetylase regulates the 40s and 60s subunits of ribosomes, which in turn affects the diapause of meadow moths. This finding expands our understanding of the regulation of meadow moth diapause and provides new insights into its control mechanism.

Citing Articles

Enhancing Biomedicine: Proteomics and Metabolomics in Action.

Costanzo M, Caterino M, Santorelli L Proteomes. 2025; 13(1.

PMID: 39846636 PMC: 11755564. DOI: 10.3390/proteomes13010005.

References

Bian J, Liao Y, Liu R, An X, Hu C, Liu H . Synergy of cyano groups and cobalt single atoms in graphitic carbon nitride for enhanced bio-denitrification. Water Res. 2022; 218:118465. DOI: 10.1016/j.watres.2022.118465. View

Saunders D . Dormancy, Diapause, and the Role of the Circadian System in Insect Photoperiodism. Annu Rev Entomol. 2019; 65:373-389. DOI: 10.1146/annurev-ento-011019-025116. View

Urwanisch L, Unger M, Sieberer H, Dang H, Neuper T, Regl C . The Class IIA Histone Deacetylase (HDAC) Inhibitor TMP269 Downregulates Ribosomal Proteins and Has Anti-Proliferative and Pro-Apoptotic Effects on AML Cells. Cancers (Basel). 2023; 15(4). PMC: 9953883. DOI: 10.3390/cancers15041039. View

Hahn D, Denlinger D . Energetics of insect diapause. Annu Rev Entomol. 2010; 56:103-21. DOI: 10.1146/annurev-ento-112408-085436. View

Reynolds J, Bautista-Jimenez R, Denlinger D . Changes in histone acetylation as potential mediators of pupal diapause in the flesh fly, Sarcophaga bullata. Insect Biochem Mol Biol. 2016; 76:29-37. DOI: 10.1016/j.ibmb.2016.06.012. View

Liu M, Pile L . The Transcriptional Corepressor SIN3 Directly Regulates Genes Involved in Methionine Catabolism and Affects Histone Methylation, Linking Epigenetics and Metabolism. J Biol Chem. 2016; 292(5):1970-1976. PMC: 5290966. DOI: 10.1074/jbc.M116.749754. View

van Delft J, Mathijs K, Staal Y, van Herwijnen M, Brauers K, Boorsma A . Time series analysis of benzo[A]pyrene-induced transcriptome changes suggests that a network of transcription factors regulates the effects on functional gene sets. Toxicol Sci. 2010; 117(2):381-92. DOI: 10.1093/toxsci/kfq214. View

Huang Q, Ma Q, Li F, Zhu-Salzman K, Cheng W . Metabolomics Reveals Changes in Metabolite Profiles among Pre-Diapause, Diapause and Post-Diapause Larvae of (Diptera: Cecidomyiidae). Insects. 2022; 13(4). PMC: 9032936. DOI: 10.3390/insects13040339. View

Hu S, Hu C, Luo L, Zhang H, Zhao S, Liu Z . Pu-erh tea increases the metabolite Cinnabarinic acid to improve circadian rhythm disorder-induced obesity. Food Chem. 2022; 394:133500. DOI: 10.1016/j.foodchem.2022.133500. View

10.

Ren Y, Yu G, Shi C, Liu L, Guo Q, Han C . Majorbio Cloud: A one-stop, comprehensive bioinformatic platform for multiomics analyses. Imeta. 2024; 1(2):e12. PMC: 10989754. DOI: 10.1002/imt2.12. View

11.

El-Sharkawy I, Liang D, Xu K . Transcriptome analysis of an apple (Malus × domestica) yellow fruit somatic mutation identifies a gene network module highly associated with anthocyanin and epigenetic regulation. J Exp Bot. 2015; 66(22):7359-76. PMC: 4765799. DOI: 10.1093/jxb/erv433. View

12.

Xu Q, Liu Q, Chen Z, Yue Y, Liu Y, Zhao Y . Histone deacetylases control lysine acetylation of ribosomal proteins in rice. Nucleic Acids Res. 2021; 49(8):4613-4628. PMC: 8096213. DOI: 10.1093/nar/gkab244. View

13.

Batz Z, Armbruster P . Diapause-associated changes in the lipid and metabolite profiles of the Asian tiger mosquito, . J Exp Biol. 2018; 221(Pt 24). PMC: 6307873. DOI: 10.1242/jeb.189480. View

14.

Birgbauer E, Chun J . New developments in the biological functions of lysophospholipids. Cell Mol Life Sci. 2006; 63(23):2695-701. PMC: 11136021. DOI: 10.1007/s00018-006-6155-y. View

15.

Ju Z, Liang L, Zheng Y, Shi H, Zhao W, Sun W . Full-Length Transcriptome Sequencing and RNA-Seq Analysis Offer Insights into Terpenoid Biosynthesis in (L.) DC. Genes (Basel). 2024; 15(3). PMC: 10970515. DOI: 10.3390/genes15030285. View

16.

Lennartsson A, Ekwall K . Histone modification patterns and epigenetic codes. Biochim Biophys Acta. 2009; 1790(9):863-8. DOI: 10.1016/j.bbagen.2008.12.006. View

17.

Hickner P, Mori A, Zeng E, Tan J, Severson D . Whole transcriptome responses among females of the filariasis and arbovirus vector mosquito Culex pipiens implicate TGF-β signaling and chromatin modification as key drivers of diapause induction. Funct Integr Genomics. 2015; 15(4):439-47. PMC: 4492872. DOI: 10.1007/s10142-015-0432-5. View

18.

Jiang X, Huang S, Luo L, Liu Y, Zhang L . Diapause termination, post-diapause development and reproduction in the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). J Insect Physiol. 2010; 56(9):1325-31. DOI: 10.1016/j.jinsphys.2010.04.016. View

19.

Wen J, Niu X, Chen S, Chen Z, Wu S, Wang X . Chitosan oligosaccharide improves the mucosal immunity of small intestine through activating SIgA production in mice: Proteomic analysis. Int Immunopharmacol. 2022; 109:108826. DOI: 10.1016/j.intimp.2022.108826. View

20.

Reynolds J, Hand S . Decoupling development and energy flow during embryonic diapause in the cricket, Allonemobius socius. J Exp Biol. 2009; 212(Pt 13):2065-74. PMC: 2702453. DOI: 10.1242/jeb.027359. View