First Comprehensive Analysis of Lysine Succinylation in Paper Mulberry (Broussonetia Papyrifera)

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2021 Apr 11

PMID 33838656

Citations 9

Authors

YiBo Dong

Ping Li

Chao Chen

Affiliations

Soon will be listed here.

Abstract

Background: Lysine succinylation is a naturally occurring post-translational modification (PTM) that is ubiquitous in organisms. Lysine succinylation plays important roles in regulating protein structure and function as well as cellular metabolism. Global lysine succinylation at the proteomic level has been identified in a variety of species; however, limited information on lysine succinylation in plant species, especially paper mulberry, is available. Paper mulberry is not only an important plant in traditional Chinese medicine, but it is also a tree species with significant economic value. Paper mulberry is found in the temperate and tropical zones of China. The present study analyzed the effects of lysine succinylation on the growth, development, and physiology of paper mulberry.

Results: A total of 2097 lysine succinylation sites were identified in 935 proteins associated with the citric acid cycle (TCA cycle), glyoxylic acid and dicarboxylic acid metabolism, ribosomes and oxidative phosphorylation; these pathways play a role in carbon fixation in photosynthetic organisms and may be regulated by lysine succinylation. The modified proteins were distributed in multiple subcellular compartments and were involved in a wide variety of biological processes, such as photosynthesis and the Calvin-Benson cycle.

Conclusion: Lysine-succinylated proteins may play key regulatory roles in metabolism, primarily in photosynthesis and oxidative phosphorylation, as well as in many other cellular processes. In addition to the large number of succinylated proteins associated with photosynthesis and oxidative phosphorylation, some proteins associated with the TCA cycle are succinylated. Our study can serve as a reference for further proteomics studies of the downstream effects of succinylation on the physiology and biochemistry of paper mulberry.

Citing Articles

Systematic qualitative proteome-wide analysis of lysine malonylation profiling in Platycodon grandiflorus.

Yang Q, Xu S, Jiang W, Meng F, Wang S, Sun Z Amino Acids. 2025; 57(1):9.

PMID: 39812870 PMC: 11735498. DOI: 10.1007/s00726-024-03432-3.

Post-translational modulation of cell signalling through protein succinylation.

Kubatzky K, Gao Y, Yu D Explor Target Antitumor Ther. 2024; 4(6):1260-1285.

PMID: 38213532 PMC: 10776603. DOI: 10.37349/etat.2023.00196.

Silage preparation and sustainable livestock production of natural woody plant.

Du Z, Yang F, Fang J, Yamasaki S, Oya T, Nguluve D Front Plant Sci. 2023; 14:1253178.

PMID: 37746011 PMC: 10514673. DOI: 10.3389/fpls.2023.1253178.

Comprehensive analysis of the lysine succinylome in fish oil-treated prostate cancer cells.

Jiang Y, He C, Ye H, Xu Q, Chen X, Chen Y Life Sci Alliance. 2023; 6(11).

PMID: 37684043 PMC: 10487806. DOI: 10.26508/lsa.202302131.

Protein post-translational modification by lysine succinylation: Biochemistry, biological implications, and therapeutic opportunities.

Zhao G, Zhen J, Liu X, Guo J, Li D, Xie J Genes Dis. 2023; 10(4):1242-1262.

PMID: 37397549 PMC: 10310984. DOI: 10.1016/j.gendis.2022.03.009.

References

Zhou H, Finkemeier I, Guan W, Tossounian M, Wei B, Young D . Oxidative stress-triggered interactions between the succinyl- and acetyl-proteomes of rice leaves. Plant Cell Environ. 2017; 41(5):1139-1153. DOI: 10.1111/pce.13100. View

Meng X, Mujahid H, Zhang Y, Peng X, Redona E, Wang C . Comprehensive Analysis of the Lysine Succinylome and Protein Co-modifications in Developing Rice Seeds. Mol Cell Proteomics. 2019; 18(12):2359-2372. PMC: 6885699. DOI: 10.1074/mcp.RA119.001426. View

Jin W, Wu F . Proteome-Wide Identification of Lysine Succinylation in the Proteins of Tomato (Solanum lycopersicum). PLoS One. 2016; 11(2):e0147586. PMC: 4734689. DOI: 10.1371/journal.pone.0147586. View

Wan Y, Liao L, Liu Y, Yang H, Song X, Wang L . Allosteric regulation of protein 14-3-3ζ scaffold by small-molecule editing modulates histone H3 post-translational modifications. Theranostics. 2020; 10(2):797-815. PMC: 6929985. DOI: 10.7150/thno.38483. View

Fan B, Li Y, Li L, Peng X, Bu C, Wu X . Malonylome analysis of rhizobacterium Bacillus amyloliquefaciens FZB42 reveals involvement of lysine malonylation in polyketide synthesis and plant-bacteria interactions. J Proteomics. 2016; 154:1-12. DOI: 10.1016/j.jprot.2016.11.022. View

Zhang Z, Tan M, Xie Z, Dai L, Chen Y, Zhao Y . Identification of lysine succinylation as a new post-translational modification. Nat Chem Biol. 2010; 7(1):58-63. PMC: 3065206. DOI: 10.1038/nchembio.495. View

Zhang Y, Wang G, Song L, Mu P, Wang S, Liang W . Global analysis of protein lysine succinylation profiles in common wheat. BMC Genomics. 2017; 18(1):309. PMC: 5397794. DOI: 10.1186/s12864-017-3698-2. View

Colak G, Xie Z, Zhu A, Dai L, Lu Z, Zhang Y . Identification of lysine succinylation substrates and the succinylation regulatory enzyme CobB in Escherichia coli. Mol Cell Proteomics. 2013; 12(12):3509-20. PMC: 3861704. DOI: 10.1074/mcp.M113.031567. View

Zhang N, Gao R, Yang J, Zhu Y, Zhang Z, Xu X . Quantitative Global Proteome and Lysine Succinylome Analyses Reveal the Effects of Energy Metabolism in Renal Cell Carcinoma. Proteomics. 2018; 18(19):e1800001. DOI: 10.1002/pmic.201800001. View

10.

Xu Z, Dong M, Peng X, Ku W, Zhao Y, Yang G . New insight into the molecular basis of cadmium stress responses of wild paper mulberry plant by transcriptome analysis. Ecotoxicol Environ Saf. 2019; 171:301-312. DOI: 10.1016/j.ecoenv.2018.12.084. View

11.

Yang Q, Liu X, Chen J, Wen Y, Liu H, Peng Z . Lead-mediated inhibition of lysine acetylation and succinylation causes reproductive injury of the mouse testis during development. Toxicol Lett. 2019; 318:30-43. DOI: 10.1016/j.toxlet.2019.10.012. View

12.

Li X, Hu X, Wan Y, Xie G, Li X, Chen D . Systematic identification of the lysine succinylation in the protozoan parasite Toxoplasma gondii. J Proteome Res. 2014; 13(12):6087-95. DOI: 10.1021/pr500992r. View

13.

Omena-Garcia R, Araujo W, Gibon Y, Fernie A, Nunes-Nesi A . Measurement of Tricarboxylic Acid Cycle Enzyme Activities in Plants. Methods Mol Biol. 2017; 1670:167-182. DOI: 10.1007/978-1-4939-7292-0_14. View

14.

Kanehisa M . The KEGG database. Novartis Found Symp. 2003; 247:91-101; discussion 101-3, 119-28, 244-52. View

15.

Yang M, Wang Y, Chen Y, Cheng Z, Gu J, Deng J . Succinylome analysis reveals the involvement of lysine succinylation in metabolism in pathogenic Mycobacterium tuberculosis. Mol Cell Proteomics. 2015; 14(4):796-811. PMC: 4390261. DOI: 10.1074/mcp.M114.045922. View

16.

Wang Y, Hou Y, Qiu J, Li Z, Zhao J, Tong X . A Quantitative Acetylomic Analysis of Early Seed Development in Rice (Oryza sativa L.). Int J Mol Sci. 2017; 18(7). PMC: 5535869. DOI: 10.3390/ijms18071376. View

17.

Khadivi F, Razavi S, Hashemi F . Protective effects of zinc on rat sperm chromatin integrity involvement: DNA methylation, DNA fragmentation, ubiquitination and protamination after bleomycin etoposide and cis-platin treatment. Theriogenology. 2019; 142:177-183. DOI: 10.1016/j.theriogenology.2019.09.039. View

18.

Jensen R, Bassham J . Photosynthesis by isolated chloroplasts. Proc Natl Acad Sci U S A. 1966; 56(4):1095-101. PMC: 220006. DOI: 10.1073/pnas.56.4.1095. View

19.

Xie L, Yang W, Fan X, Xie J . Comprehensive analysis of protein acetyltransferases of human pathogen Mycobacterium tuberculosis. Biosci Rep. 2019; 39(12). PMC: 6923341. DOI: 10.1042/BSR20191661. View

20.

Zhang K, Xiong Y, Sun W, Wang G, Liu W . Global Proteomic Analysis Reveals Widespread Lysine Succinylation in Rice Seedlings. Int J Mol Sci. 2019; 20(23). PMC: 6929033. DOI: 10.3390/ijms20235911. View