Comprehensive proteome and lysine acetylome analysis after artificial aging reveals the key acetylated proteins involved in wheat seed oxidative stress response and energy production
Bang-Bang Li
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorWei Zhang
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorShan Wei
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorYang-Yong Lv
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorJi-Xu Shang
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorCorresponding Author
Yuan-Sen Hu
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Correspondence
Yuan-Sen Hu, College of Biological Engineering, Henan University of Technology, Zhengzhou, China.
Email: [email protected]
Search for more papers by this authorBang-Bang Li
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorWei Zhang
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorShan Wei
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorYang-Yong Lv
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorJi-Xu Shang
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Search for more papers by this authorCorresponding Author
Yuan-Sen Hu
College of Biological Engineering, Henan University of Technology, Zhengzhou, China
Correspondence
Yuan-Sen Hu, College of Biological Engineering, Henan University of Technology, Zhengzhou, China.
Email: [email protected]
Search for more papers by this authorAbstract
Lysine acetylation is a common post-translational modification of proteins within all organisms. However, quantitative acetylome characterization in wheat seed during aging in storage has not been reported. This study reports the first large-scale acetylome analysis of wheat seeds after artificial aging treatment, using the quantitative proteomic approach. In total, 11,002 acetylation sites, corresponding to 4262 acetylated proteins were identified, of which 1207 acetylated sites, representing 783 acetylated proteins, were significantly more or less acetylated after artificial aging. Functional analysis demonstrated that the majority of the acetylated proteins are closely involved with cellular and metabolic functions. In particular, key enzymes in the oxidative stress response and energy metabolism were significantly differentially acetylated and appear to be heavily involved in wheat seed aging. The acetylome analysis was verified by quantitative real-time PCR and enzyme activity determination. Lysine-acetylation results in a weaker oxidative stress response and lower energy production efficiency, resulting in the apoptosis of wheat seed cells, insufficient energy supply at the germination stage, and consequently, marked loss of seed vigor.
Practical applications
It is known that the loss of protein function is an important reason for the decrease of seed vigor. Therefore, the change of protein function in the process of wheat seed aging was studied by proteome and lysine acetylome analysis technology. The results showed that the oxidation–reduction imbalance and the decrease of energy production efficiency of seeds were the important reasons for the decrease of their vigor. This will provide a new idea for green and safe storage of grain.
CONFLICT OF INTEREST
The authors have declared no conflict of interest for this article.
Supporting Information
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REFERENCES
- Alexander, T. E., Dmitry, N. F., Mikhail, V. C., & Abir, U. I. (2021). Effect of salt stress on the expression and promoter methylation of the genes encoding the mitochondrial and cytosolic forms of aconitase and fumarase in maize. International Journal of Molecular Sciences, 22, 6012. https://doi.org/10.3390/ijms22116012
- Bian, Y. W., Deng, X., Yan, X., Zhou, J. X., Yuan, L. L., & Yan, Y. M. (2017). Integrated proteomic analysis of Brachypodium distachyon roots and leaves reveals a synergistic network in the response to drought stress and recovery. Scientific Reports, 7, 46183. https://doi.org/10.1038/srep46183
- Burrell, M. M., Mooney, P. J., Blundy, M., Carter, D., Wilson, F., Green, J., Blundy, K. S., & Rees, T. A. (1994). Genetic manipulation of 6-phosphofructokinase in potato tubers. Planta, 194, 95–101. https://doi.org/10.1007/BF00201039
- Carmelina, S., Stefania, B., Roberto, L., & Isa, G. (2011). Ageing in embryos from wheat grains stored at different temperatures: Oxidative stress and antioxidant response. Functional Plant Biology, 38, 624–631. https://doi.org/10.1071/FP11046
- Chen, Z. J., & Lu, T. (2007). Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochimica et Biophysica Acta, 1769, 295–307. https://doi.org/10.1016/j.bbaexp.2007.04.007
- Christophe, B., Juliette, L., Arnaud, L., Sandra, R., Daniel, C., & FrancËoise, C. (2004). Catalase activity and expression in developing sunflower seeds as related to drying. Journal of Experimental Botany, 396, 475–483. https://doi.org/10.1093/jxb/erh050
- Dayanne, R. D. O., Larissa, F. S., Alcindo, B., Caroline, P. B., Luis, R. P., Catiuscia, M. D. F., Barbara, N. K., Getúlio, N. B., Aline, A. B., Margareth, L. A., Irwin, R. A. D. M., & Roselei, F. (2015). Silymarin has antioxidant potential and changes the activity of Na+/K+-ATPase and monoamine oxidase in vitro. Industrial Crops and Products, 70, 347–355. https://doi.org/10.1016/j.indcrop.2015.03.06052
- Fan, W. W., Yuan, G. Q., Li, Q. Q., & Lin, W. (2014). Antibacterial mechanisms of methyl gallate against Ralstonia solanacearum. Australasian Plant Pathology, 43, 1–7. https://doi.org/10.1007/s13313-013-0234-y
- Fang, X. P., Chen, W. Y., Zhao, Y., Ruan, S. L., Zhang, H. M., Yan, C. Q., Jin, L., Cao, L. L., Zhu, J., Ma, H. S., & Cheng, Z. Y. (2015). Global analysis of lysine acetylation in strawberry leaves. Frontiers in Plant Science, 6, 739. https://doi.org/10.3389/fpls.2015.00739
- Guo, G. F., Lv, D. W., Yan, X., Subburaj, S., Ge., P., Li, X. H., Hu, Y. K., & Yan, Y. M. (2012). Proteome characterization of developing grains in bread wheat cultivars (Triticum aestivum L.). BMC Plant Biology, 12, 147. https://doi.org/10.1186/1471-2229-12-147
- Guo, W., Han, L., Li, X., Wang, H., Mu, P., Lin, Q., Liu, Q. C., & Zhang, Y. M. (2020). Proteome and lysine acetylome analysis reveals insights into the molecular mechanism of seed germination in wheat. Scientific Reports, 10, 13454. https://doi.org/10.1038/s41598-020-70230-8
- Hart, G. W., & Ball, L. E. (2013). Post-translational modifications: A major focus for the future of proteomics. Molecular & Cell Proteomics, 12, 3443. https://doi.org/10.1074/mcp.E113.036491
- Hartl, M., Fussl, M., Boersema, P. J., Jost, J. O., Kramer, K., Bakirbas, A., Sindlinger, J., Plöchinger, M., Leister, D., Uhrig, G., Moorhead, G. B., Cox, J., Salvucci, M. E., Schwarzer, D., Mann, M., & Finkemeier, I. (2017). Lysine acetylome profiling uncovers novel histone deacetylase substrate proteins in Arabidopsis. Molecular Systems Biology, 13, 949. https://doi.org/10.15252/msb.20177819
- Hu, W. Y., Zhang, X. Y., Godana, E. A., Gu, X. Y., Zhao, L. N., & Zhang, H. Y. (2021). Yarrowia lipolytica reduces the disease incidence of asparagus infected by fusarium proliferatum by affecting respiratory metabolism and energy status. Biological Control, 159, 104625. https://doi.org/10.1016/j.biocontrol.2021.104625
- Jiang, J. T., Gai, Z. S., Wang, Y., Fan, K., Sun, L. T., Wang, H., & Ding, Z. T. (2018). Comprehensive proteome analyses of lysine acetylation in tea leaves by sensing nitrogen nutrition. BMC Genomics, 19, 840. https://doi.org/10.1186/s12864-018-5250-4
- Jin, P., Zhu, H., Wang, L., Shan, T. M., & Zheng, Y. H. (2014). Oxalic acid alleviates chilling injury in peach fruit by regulating energy metabolism and fatty acid contents. Food Chemistry, 161, 87–93. https://doi.org/10.1016/j.foodchem.2014.03.103
- Lei, K. Q., Sun, S. Z., Zhong, K. T., Li, S. Y., Hu, H., Sun, C. J., Zheng, Q., M., Tian, Z. W., Dai, T. B., & Sun, J. Y. (2021). Seed soaking with melatonin promotes seed germination under chromium stress via enhancing reserve mobilization and antioxidant metabolism in wheat. Ecotoxicology and Environmental Safety, 220, 112241. https://doi.org/10.1016/j.ecoenv.2021.112241
- Li, B. B., Zhang, S. B., Lv, Y. Y., Wei, S., & Hu, Y. S. (2022). Reactive oxygen species-induced protein carbonylation promotes deterioration of physiological activity of wheat seeds. PLoS ONE, 17, e0263553. https://doi.org/10.1371/journal.pone.0263553
- Li, L., Lv, F. Y., Guo, Y. Y., & Wang, Z. Q. (2016). Respiratory pathway metabolism and energy metabolism associated with senescence in postharvest broccoli (Brassica oleracea L. var. italica) florets in response to O2/CO2 controlled atmospheres. Postharvest Biology and Technology, 111, 330–336. https://doi.org/10.1016/jposthavorbio.2015.09.032
- Li, S. G., Jiang, H., Wang, Y., Lyu, L., Prusky, D., Ji, Y., Zhang, X. L., & Bi, Y. (2020). Effect of benzothiadiazole treatment on improving the mitochondrial energy metabolism involved in induced resistance of apple fruit during postharvest storage. Food Chemistry, 302, 125288. https://doi.org/10.1016/j.foodchem.2019.125288
- Li, X. J., Ye, J. Y., Ma, H., & Lu, P. L. (2018). Proteomic analysis of lysine acetylation provides strong evidence for involvement of acetylated proteins in plant meiosis and tapetum function. The Plant Journal, 93, 142–154. https://doi.org/10.1111/tpj.1376624
- Liu, Z., Wang, Y., Gao, T., Pan, Z., Cheng, H., Yang, Q., Cheng, Z., Guo, A., Ren, J., & Xue, Y. (2014). CPLM: A database of protein lysine modifications. Nucleic Acids Research, 42, 531–536. https://doi.org/10.1093/nar/gkt1093
- Liu, Z. B., Song, J. S., Miao, W., Yang, B. Z., Zhang, Z. Q., Chen, W. C., Tan, F. J., Suo, H., Dai, X. Z., Zou, X. X., & Ou, L. J. (2021). Comprehensive proteome and lysine acetylome analysis reveals the widespread involvement of acetylation in cold resistance of pepper (Capsicum annuum L.). Frontiers in Plant Science, 12, 730489. https://doi.org/10.3389/fpls.2021.730489
- Liu, Z. L., Li, L., Luo, Z. S., Zeng, F. F., Jiang, L., & Tang, K. C. (2016). Effect of brassinolide on energy status and proline metabolism in postharvest bamboo shoot during chilling stress. Postharvest Biology and Technology, 111, 240–246. https://doi.org/10.1016/j.postharvbio.2015.09.016
- Meng, X., Lv, Y., Mujahid, H., Edelmann, M. J., Zhao, H., Peng, X., & Peng, Z. (2018). Proteome-wide lysine acetylation identification in developing rice (Oryza sativa) seeds and protein co-modification by acetylation, succinylation, ubiquitination, and phosphorylation. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1866, 451–463. https://doi.org/10.1016/j.bbapap.2017.12.001
- Nallamilli, B. R. R., Edelmann, M. J., Zhong, X. X., Tan, F., Mujahid, H., Zhang, J., Nanduri, B., Peng, Z. H., & Soberón, M. (2014). Global analysis of lysine acetylation suggests the involvement of protein acetylation in diverse biological processes in rice (Oryza sativa). PLoS ONE, 9, e89283. https://doi.org/10.1371/journal.pone.0089283
- Narita, T., Weinert, B. T., & Choudhary, C. (2019). Functions and mechanisms of non-histone protein acetylation. Nature Reviews Molecular Cell Biology, 20, 156–174. https://doi.org/10.1038/s41580-018-0081-3
- Qiu, Z. B., Guo, J. L., Zhu, A. J., Zhang, L., & Zhang, M. M. (2014). Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicology and Environmental Safety, 104, 202–208. https://doi.org/10.1016/j.ecoenv.2014.03.014
- Sheng, Y., Abreu, I. A., Cabelli, D. E., Maroney, M. J., Miller, A. F., Teixeira, M., & Valentine, J. S. (2014). Superoxide dismutases and superoxide reductases. Chemical Reviews, 114, 3854–3918. https://doi.org/10.1021/cr4005296
- Smith-Hammond, C. L., Swatek, K. N., Johnston, M. L., Thelen, J. J., & Miernyk, J. A. (2014). Initial description of the developing soybean seed protein Lys-N(ε)-acetylome. Journal of Proteomics, 96, 56–66. https://doi.org/10.1016/j.jprot.2013.10.038
- Sweetlove, L. J., Beard, K. F., Nunes-Nesi, A., Fernie, A. R., & Ratcliffe, R. G. (2010). Not just a circle: Flux modes in the plant TCA cycle. Trends in Plant Science, 15, 462–470. https://doi.org/10.1016/j.tplants.2010.05.006
- Tyagi, S., Shumayla., Verma, P. C., Singh, K., & Upadhyay, S. K. (2020). Molecular characterization of ascorbate peroxidase (APX) and APX-related (APX-R) genes in Triticum aestivum L. Genomics, 112, 4208–4223. https://doi.org/10.1016/j.ygeno.2020.07.023
- Verdin, E., & Ott, M. (2015). 50 years of protein acetylation: From gene regulation to epigenetics, metabolism and beyond. Nature Reviews Molecular Cell Biology, 16, 258–264. https://doi.org/10.1038/nrm3931
- Wang, Q. J., Zhang, Y. K., Yang, C., Xiong, H., Lin, Y., Yao, J., Li, H., Xie, L., Zhao, W., Yao, Y., Ning, Z. B., Zeng, R., Xiong, Y., Guan, K. L., Zhao, S., & Zhao, G. P. (2010). Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science, 327, 1004–1007. https://doi.org/10.1126/science.1179687
- Wang, X., Cai, J. A., Jiang, D., Liu, F. L., Dai, T. B., & Cao, W. X. (2011). Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. Journal of Plant Physiology, 168, 585–593. https://doi.org/10.1016/j.jplph.2010.09.016
- Wang, Y. F., Hou, Y. X., Qiu, J. H., Li, Z. Y., Tong, X. H., & Zhao, J. (2017). A quantitative acetylomic analysis of early seed development in rice (Oryza sativa L.). International Journal of Molecular Sciences, 18, 1376. https://doi.org/10.3390/ijms18071376
- Wang, Y. S., Luo, Z. S., Khan, Z. U., Mao, L. C., & Ying, T. J. (2015). Effect of nitric oxide on energy metabolism in postharvest banana fruit in response to chilling stress. Postharvest Biology and Technology, 108, 21–27. https://doi.org/10.1016/j.postharvbio.2015.05.007
- Wang, Z. C., Zhu, J. F., Li, W. T., Li, R. F., Wang, X. Q., Qiao, H. Z., Sun, Q., & Zhang, H. R. (2020). Antibacterial mechanism of the polysaccharide produced by Chaetomium globosum CGMCC 6882 against Staphylococcus aureus. International Journal of Biological Macromolecules, 59, 231–235. https://doi.org/10.1016/j.ijbiomac.2020.04.269
- Xia, C., Tao, Y., Li, M. S., Che, T. J., & Qu, J. (2020). Protein acetylation and deacetylation: An important regulatory modification in gene transcription (review). Experimental and Therapeutic Medicine, 20, 2923–2940. https://doi.org/10.3892/etm.2020.9073
- Xia, Y., Jing, D. L., Kong, L. S., Zhan, J. W., OuYang, F. Q., Zhang, H. G., Wang, J. H., & Zhang, S. G. (2016). Global lysine acetylome analysis of desiccated somatic embryos of Picea asperata. Frontiers in Plant Science, 7, 1927. https://doi.org/10.3389/fpls.2016.01927
- Xing, S. F., & Poirier, Y. (2012). The protein acetylome and the regulation of metabolism. Trends in Plant Science, 17, 423–430. https://doi.org/10.1016/j.tplants.2012.03.008
- Xue, C., Liu, S., Chen, C., Zhu, J., Yang, X. B., Zhou, Y., Guo, R., Liu, X. Y., & Gong, Z. Y. (2018). Global proteome analysis links lysine acetylation to diverse functions in Oryza sativa. Proteomics, 18, 1700036. https://doi.org/10.1002/pmic.201700036
- Zhang, C. M., Chen, M. M., Zhou, N., & Qi, Y. H. (2020). Metformin prevents H₂O₂-induced senescence in human lens epithelial B3 cells. Medical Science Monitor Basic Research, 26, e923391. https://doi.org/10.12659/MSMBR.923391
- Zhang, J., Jiang, F. W., Yang, P., Li, J., Yan, G. J., & Hu, L. Y. (2015). Responses of canola (Brassica napus L.) cultivars under contrasting temperature regimes during early seedling growth stage as revealed by multiple physiological criteria. Acta Physiological Plant, 37, 7. https://doi.org/10.1007/s11738-014-1748-9
- Zhang, N., Zhang, L. R., Shi, C. N., Tian, Q. Z., Lv, G. G., Wang, Y., Cui, D. Q., & Chen, F. (2017). Comprehensive profiling of lysine ubiquitome reveals diverse functions of lysine ubiquitination in common wheat. Scientific Reports, 7, 13601. https://doi.org/10.1038/s41598-017-13992-y
- Zhang, S. B., Lv, Y. Y., Wang, Y. L., Jia, F., Wang, J. S., & Hu, Y. S. (2017). Physiochemical changes in wheat of different hardnesses during storage. Journal of Stored Products Research, 72, 161–165. https://doi.org/10.1016/j.jspr.2017.05.002
- Zhang, Y. K., Qu, Y. Y., Lin, Y., Wu, X. H., Chen, H. Z., Wang, X., Zhou, K. Q., Wei, Y., Guo, F. S., Yao, C. F., He, X. D., Liu, L. X., Yang, C., Guan, Z. Y., Wang, S. D., Zhao, J. Y., Liu, D. P., Zhao, S. M., & Xu, W. (2017). Enoyl-CoA hydratase-1 regulates mTOR signaling and apoptosis by sensing nutrients. Nature Communications, 8, 464. https://doi.org/10.1038/s41467-017-00489-5
- Zhang, Y. M., Song, L. M., Liang, W. X., Mu, P., Wang, S., & Lin, Q. (2016). Comprehensive profiling of lysine acetylproteome analysis reveals diverse functions of lysine acetylation in common wheat. PLoS ONE, 6, 21069. https://doi.org/10.1038/srep21069
- Zhen, S. M., Deng, X., Wang, J., Zhu, G. R., Cao, H., Yuan, L. L., & Yang, Y. M. (2016). First comprehensive proteome analyses of lysine acetylation and succinylation in seedling leaves of Brachypodium distachyon L. Scientific Reports, 6, 31574. https://doi.org/10.1038/srep3157
- Zhu, G. R., Xing, Y., Dong, Z., Xiong, D., Wu, J. S., Jian, X., & Yan, Y. M. (2018). Lysine acetylproteome profiling under water deficit reveals key acetylated proteins involved in wheat grain development and starch biosynthesis. Journal of Proteomics, 185, 8–24. https://doi.org/10.1016/j.jprot.2018.06.019