In silico analysis of sirtuin-type histone deacetylase genes in sugar beet (Beta vulgaris L.)

Year 2024, Volume: 5 Issue: 1, 38 - 47, 30.04.2024

Seher Yolcu

https://doi.org/10.51753/flsrt.1412729

Abstract

Histone deacetylase (HDAC) enzymes catalyze the removal of an acetyl group from the lysine residues of histone N-terminal tails, and they repress gene transcription through condensation of chromatin. In plants, the sirtuins/silent information regulator 2 (SIR2) proteins which are NAD+-dependent deacetylases, have been identified in distinct plant species such as Arabidopsis, rice, tomato, soybean, maize, etc., but little is known about their functions in plants. They are mainly investigated in Arabidopsis and rice and found to be involved in H3K9 acetylation, metabolic pathways, repression of genes associated with stress response, and energy metabolism. A total of eight RPD3/HDA1 family HDAC genes have been recently identified in the sugar beet (Beta vulgaris L.) genome. However, B. vulgaris SIR2-type HDACs have not yet been identified and characterized. In this work, an in silico analysis of SIR2 family members was performed in sugar beet. Three SIR2 family HDACs were identified from the sugar beet genome, named BvSRT1, BvSRT2, and BvSRT3. The beet SIR2 gene family is found to be located on chromosomes 4, and 9. The phylogenetic tree building with B. vulgaris, Arabidopsis, tomato, soybean, Vitis vinifera, pepper, rice, maize, and Sorghum bicolor showed that 3 sugar beet SRTs were divided into two classes: Class II (BvSRT2) and IV (BvSRT1 and BvSRT3). SIR2 family proteins consisted of SIR2 domain (PF02146). The conserved motifs ranged from 6 to 50 amino acids, while the intron-exon numbers of genes ranged from 10 to 14. BvSRT1 and BvSRT3 exhibited similar motif distributions and exon/intron structures. Moreover, nuclear, and cytoplasmic localization of BvSRT1 and BvSRT3 has been predicted. BvSRT2 protein was located on the mitochondrion. Analysis of cis-elements revealed the involvement of BvSRT genes in hormone regulation, light response, abiotic stress response, and meristem expression. This study may shed light on the potential role of SIR2-type HDACs in beets.

Keywords

Beta vulgaris, histone deacetylase (HDAC), in silico analysis, sirtuins, SIR2, sugar beet

References

• Aquea, F., Timmermann, T., & Arce-Johnson, P. (2010). Analysis of histone acetyltransferase and deacetylase families of Vitis vinifera. Plant Physiology and Biochemistry, 48, 194-199.
• Bailey, T. L., & Elkan, C. (1994). Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Second International Conference on Intelligent Systems for Molecular Biology, California, USA. 28-36.
• Biłas, R., Szafran, K., Hnatuszko-Konka, K., & Kononowicz, A. K. (2016). Cis-regulatory elements used to control gene expression in plants. Plant Cell, Tissue and Organ Culture (PCTOC), 127, 269-287.
• Bolser, D. M., Staines, D. M., Perry, E., & Kersey, P. J. (2017). Ensembl plants: integrating tools for visualizing, mining, and analyzing plant genomic data. Methods in Molecular Biology, 1-31.
• Bruscalupi, G., Di Micco, P., Failla, C. M., Pascarella, G., Morea, V., Saliola, M., ... & Mauro, M. L. (2023). Arabidopsis thaliana sirtuins control proliferation and glutamate dehydrogenase activity. Plant Physiology and Biochemistry, 194, 236-245.
• Busconi, M., Reggi, S., Fogher, C., & Bavaresco, L. (2009). Evidence of a sirtuin gene family in grapevine (Vitis vinifera L.). Plant Physiology and Biochemistry, 47, 650-652.
• Cai, Y., Xu, M., Liu, J., Zeng, H., Song, J., Sun, B., ... & Zhu, Z. (2022). Genome-wide analysis of histone acetyltransferase and histone deacetylase families and their expression in fruit development and ripening stage of pepper (Capsicum annuum). Frontiers in Plant Science, 13, 971230.
• Carafa, V., Rotili, D., Forgione, M., Cuomo, F., Serretiello, E., Hailu, G. S., ... & Altucci, L. (2016). Sirtuin functions and modulation: from chemistry to the clinic. Clinical Epigenetics, 8, 1-21.
• Chao, J., Li, Z., Sun, Y., Aluko, O. O., Wu, X., Wang, Q., & Liu, G. (2021). MG2C: A user-friendly online tool for drawing genetic maps. Molecular Horticulture, 1, 1-4.
• Chen, B., Zang, W., Wang, J., Huang, Y., He, Y., Yan, L., ... & Zheng, W. (2015). The chemical biology of sirtuins. Chemical Society Reviews, 44(15), 5246-5264.
• Chen, C., Chen, H., Zhang, Y., Thomas, H. R., Frank, M. H., He, Y., & Xia, R. (2020). TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13(8), 1194-1202.
• Chunzheng, W., Feng, G., Jianguo, W., Jianli, D., Chunhong, W., & Yi, L. (2010). Arabidopsis putative deacetylase AtSRT2 regulates basal defense by suppressing PAD4, EDS5 and SID2 expression. Plant and Cell Physiology, 51, 1291-1299.
• Darzentas, N. (2010). Circoletto: visualizing sequence similarity with Circos. Bioinformatics, 26, 2620-2621. Dohm, J. C., Minoche, A. E., Holtgräwe, D., Capella-Gutiérrez, S., Zakrzewski, F., Tafer, H., ... & Himmelbauer, H. (2014). The genome of the recently domesticated crop plant sugar beet (Beta vulgaris). Nature, 505(7484), 546-549.
• Du, J., Zhou, Y., Su, X., Yu, J. J., Khan, S., Jiang, H., ... & Lin, H. (2011). Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science, 334(6057), 806-809.
• Du, Q., Fang, Y., Jiang, J., Chen, M., Fu, X., Yang, Z., ... & Xie, X. (2022). Characterization of histone deacetylases and their roles in response to abiotic and PAMPs stresses in Sorghum bicolor. BMC genomics, 23(1), 28.
• Ensembl, (2017). Ensembl Plants, https://plants.ensembl.org/, Last accessed on December 25, 2023. Fang, C., Zhang, H., Wan, J., Wu, Y., Li, K., Jin, C., ... & Luo, J. (2016). Control of leaf senescence by an MeOH-jasmonates cascade that is epigenetically regulated by OsSRT1 in rice. Molecular Plant, 9(10), 1366-1378.
• Fotouhi, K., Heravan, E. S., Rajabi, A., & Azizinejad, R. (2017). Screening sugar beet genotypes in drought stress condition using tolerance indices. Agri Forest, 63, 105-109.
• Fu, W., Wu, K., & Duan, J. (2007). Sequence and expression analysis of histone deacetylases in rice. Biochemical and Biophysical Research Communications, 356(4), 843-850.
• Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S. E., Wilkins, M. R., Appel, R. D., & Bairoch, A. (2005). Protein Identification and Analysis Tools on the ExPASy Server (pp. 571-607). Humana Press.
• Goodstein, D. M., Shu, S., Howson, R., Neupane, R., Hayes, R. D., Fazo, J., ... & Rokhsar, D. S. (2012). Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research, 40(D1), D1178-D1186.
• Greiss, S., & Gartner, A. (2009). Sirtuin/Sir2 phylogeny, evolutionary considerations and structural conservation. Molecules and Cells 28, 407-415.
• Hoffmann, C. M. (2010). Sucrose accumulation in sugar beet under drought stress. Journal of Agronomy and Crop Science, 196(4), 243-252.
• Houtkooper, R. H., Pirinen, E., & Auwerx, J. (2012). Sirtuins as regulators of metabolism and healthspan. Nature reviews Molecular cell biology, 13(4), 225-238.
• Hu, B., Jin, J., Guo, A. Y., Zhang, H., Luo, J., & Gao, G. (2015). GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 31(8), 1296-1297.
• Huang, L., Sun, Q., Qin, F., Li, C., Zhao, Y., & Zhou, D. X. (2007). Down-regulation of a SILENT INFORMATION REGULATOR2-related histone deacetylase gene, OsSRT1, induces DNA fragmentation and cell death in rice. Plant Physiology, 144, 1508-1519.
• Imai, S., Armstrong, C. M., Kaeberlein, M., & Guarente, L. (2000). Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800.
• Jeong, S. M., Xiao, C., Finley, L. W., Lahusen, T., Souza, A. L., Pierce, K., ... & Haigis, M. C. (2013). SIRT4 has tumor-suppressive activity and regulates the cellular metabolic response to DNA damage by inhibiting mitochondrial glutamine metabolism. Cancer Cell, 23(4), 450-463.
• Jiangtao, C., Yingzhen, K., Qian, W., Yuhe, S., Daping, G., Jing, L., & Guanshan, L. (2015). Mapgene2chrom, a tool to draw gene physical map based on perl and svg languages. Yi Chuan, 37, 91-97.
• Kaur, A., Pati, P. K., Pati, A. M., & Nagpal, A. K. (2017). In-silico analysis of cis-acting regulatory elements of pathogenesis-related proteins of Arabidopsis thaliana and Oryza sativa. PLoS One, 12(9), e0184523.
• Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845-858.
• König, A. C., Hartl, M., Pham, P. A., Laxa, M., Boersema, P. J., Orwat, A., ... & Finkemeier, I. (2014). The Arabidopsis class II sirtuin is a lysine deacetylase and interacts with mitochondrial energy metabolism. Plant Physiology, 164(3), 1401-1414.
• Kouzarides, T. (2007). Chromatin modifications and their function. Cell 128, 693-705.
• Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., ... & Marra, M. A. (2009). Circos: an information aesthetic for comparative genomics. Genome Research, 19(9), 1639-1645.
• Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., ... & Rombauts, S. (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30(1), 325-327.
• Letunic, I., and Bork, P. (2020). SMART, http://smart.emblheidelberg.de/, Last accessed on December 25, 2023. Letunic, I., Doerks, T., & Bork, P. (2012). SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Research, 40, 302-305.
• Marand, A. P., Eveland, A. L., Kaufmann, K., & Springer, N. M. (2023). cis-Regulatory elements in plant development, adaptation, and evolution. Annual Review of Plant Biology, 74, 111-137.
• Martínez-Redondo, P., & Vaquero, A. (2013). The diversity of histone versus nonhistone sirtuin substrates. Genes & Cancer, 4(3-4), 148-163.
• Meng, J., Wen, Z., Li, M., Cheng, T., Zhang, Q., & Sun, L. (2022). HDACs gene family analysis of eight Rosaceae genomes reveals the genomic marker of cold stress in Prunus mume. International Journal of Molecular Sciences, 23(11), 5957.
• Nakai, K., & Horton, P. (1999). PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends in Biochemical Sciences, 24(1), 34-35.
• Narusaka, Y., Nakashima, K., Shinwari, Z. K., Sakuma, Y., Furihata, T., Abe, H., ... & Yamaguchi‐Shinozaki, K. (2003). Interaction between two cis‐acting elements, ABRE and DRE, in ABA‐dependent expression of Arabidopsis rd29A gene in response to dehydration and high‐salinity stresses. The Plant Journal, 34(2), 137-148.
• Pandey, R., MuÈller, A., Napoli, C. A., Selinger, D. A., Pikaard, C. S., Richards, E. J., ... & Jorgensen, R. A. (2002). Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Research, 30(23), 5036-5055.
• Peng, M., Ying, P., Liu, X., Li, C., Xia, R., Li, J., & Zhao, M. (2017). Genome-wide identification of histone modifiers and their expression patterns during fruit abscission in litchi. Frontiers in Plant Science, 8, 639.
• Perrella, G., Fasano, C., Donald, N. A., Daddiego, L., Fang, W., Martignago, D., Carr, C., Conti, L., Herzyk, P., & Amtmann, A. (2024). Histone Deacetylase Complex 1 and histone 1 epigenetically moderate stress responsiveness of Arabidopsis thaliana seedlings. New Phytologist, 241, 166-179.
• Reiser, L., Bakker, E., Subramaniam, S., Chen, X., Sawant, S., Khosa, K., ... & Berardini, T. Z. (2024). The Arabidopsis information resource in 2024. Genetics, iyae027.
• Salgotra, R. K., & Gupta, M. (2019). Exploring the role of epigenetics in cereal and leguminous crops exposed to abiotic stress. In: Alvarez-Venegas R., De-la-Peña C., Casas-Mollano J. (eds) Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications: Transcriptional Regulation and Chromatin Remodelling in Plants (pp. 149-170). Springer, Cham.
• Shu, B., Xie, Y., Zhang, F., Zhang, D., Liu, C., Wu, Q., & Luo, C. (2021). Genome-wide identification of citrus histone acetyltransferase and deacetylase families and their expression in response to arbuscular mycorrhizal fungi and drought. Journal of Plant Interactions, 16, 367-376.
• Skorupa, M., Szczepanek, J., Mazur, J., Domagalski, K., Tretyn, A., & Tyburski, J. (2021). Salt stress and salt shock differently affect DNA methylation in salt-responsive genes in sugar beet and its wild, halophytic ancestor. PLoS One, 16, e0251675.
• Song, H., Ding, G., Zhao, C., & Li, Y. (2023). Genome-wide identification of b-box gene family and expression analysis suggest its roles in responses to cercospora leaf spot in sugar beet (Beta Vulgaris L.). Genes, 14(6), 1248.
• Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38, 3022-3027.
• Wang, J., Chitsaz, F., Derbyshire, M. K., Gonzales, N. R., Gwadz, M., Lu, S., Marchler, G. H., … & Marchler-Bauer, A. (2022). Conserved Domain Database, https://www.ncbi.nlm.nih.gov/cdd/, Last accessed on December 25, 2023.
• Wang, W., Sun, Y. Q., Li, G. L., & Zhang, S. Y. (2019). Genome-wide identification, characterization, and expression patterns of the BZR transcription factor family in sugar beet (Beta vulgaris L.). BMC Plant Biology, 19, 1-12.
• Wedeking, R., Mahlein, A. K., Steiner, U., Oerke, E. C., Goldbach, H. E., & Wimmer, M. A. (2016). Osmotic adjustment of young sugar beets (Beta vulgaris) under progressive drought stress and subsequent rewatering assessed by metabolite analysis and infrared thermography. Functional Plant Biology, 44, 119-133.
• Yan, H., Chen, H., Liao, Q., Xia, M., Yao, T., Peng, L., Zou, L., Zhao, G., Zhao, J., & Wu, D. T. (2023). Genome-wide identification of histone deacetylases and their roles related with light response in tartary buckwheat (Fagopyrum tataricum). International Journal of Molecular Sciences, 24, 8090.
• Yang, C., Shen, W., Chen, H., Chu, L., Xu, Y., Zhou, X., ... & Luo, M. (2018). Characterization and subcellular localization of histone deacetylases and their roles in response to abiotic stresses in soybean. BMC Plant Biology, 18, 1-13.
• Yang, X., Wu, G., Wei, M., & Wang, B. (2022). Genome-wide identification of BvHAK gene family in sugar beet (Beta vulgaris) and their expression analysis under salt treatments. Sheng Wu Gong Cheng Xue Bao, 38, 3773-3789.
• Yolcu, S., Alavilli, H., Ganesh, P., Asif, M., Kumar, M., and Song, K. (2022). An insight into the abiotic stress responses of cultivated beets (Beta vulgaris L.). Plants, 11, 12.
• Yolcu, S., Ozdemir, F., Guler, A., & Bor, M. (2016). Histone acetylation influences the transcriptional activation of POX in Beta vulgaris L. and Beta maritima L. under salt stress. Plant Physiology and Biochemistry, 100, 37-46.
• Yolcu, S., Skorupa, M., Uras, M. E., Mazur, J., & Ozyigit, I. I. (2024). Genome-wide identification, phylogenetic classification of histone acetyltransferase genes, and their expression analysis in sugar beet (Beta vulgaris L.) under salt stress. Planta, 259(4), 85.
• Yu, B., Chen, M., Grin, I., & Ma, C. (2020). Mechanisms of sugar beet response to biotic and abiotic stresses. Advances in Experimental Medicine and Biology, 1241, 167-194.
• Yu, C. S., Chen, Y. C., Lu, C. H., & Hwang, J. K. (2006). Prediction of protein subcellular localization. Proteins, 64, 643-651.
• Yu, Q., Guo, Q., Li, B., Tan, X., Wang, L., Li, S., & Pi, Z. (2023). Identification of RPD3/HDA1 family genes in sugar beet and response to abiotic stresses. Sugar Technology, 25(4), 834-845.
• Yuan, L., Dai, H., Zheng, S., Huang, R., & Tong, H. (2020). Genome-wide identification of the HDAC family proteins and functional characterization of CsHD2C, a HD2-type histone deacetylase gene in tea plant (Camellia sinensis L. O. Kuntze). Plant Physiology and Biochemistry,155, 898-913.
• Yuan, L., Liu, X., Luo, M., Yang, S., & Wu, K. (2013). Involvement of histone modifications in plant abiotic stress responses. Journal of Integrative Plant Biology, 55(10), 892-901.
• Zhang, H., Lu, Y., Zhao, Y., & Zhou, D. X. (2016). OsSRT1 is involved in rice seed development through regulation of starch metabolism gene expression. Plant Science, 248, 28-36.
• Zhang, H., Zhao, Y., & Zhou, D. X. (2017). Rice NAD+-dependent histone deacetylase OsSRT1 represses glycolysis and regulates the moonlighting function of GAPDH as a transcriptional activator of glycolytic genes. Nucleic Acids Research, 45, 12241-12255.
• Zhang, K., Yu, L., Pang, X., Cao, H., Si, H., Zang, J., Xing, J., & Dong, J. (2020). In silico analysis of maize HDACs with an emphasis on their response to biotic and abiotic stresses. PeerJ, 8, e8539.
• Zhang, P., Liu, L., Wang, X., Wang, Z., Zhang, H., Chen, J., ... & Li, C. (2021). Beneficial effects of exogenous melatonin on overcoming salt stress in sugar beets (Beta vulgaris L.). Plants, 10(5), 886.
• Zhao, L., Lu, J., Zhang, J., Wu, P. Y., Yang, S., & Wu, K. (2014). Identification and characterization of histone deacetylases in tomato (Solanum lycopersicum). Frontiers in Plant Science, 5, 760.
• Zhao, S., Zhang, X., & Li, H. (2018). Beyond histone acetylation-writing and erasing histone acylations. Current Opinion in Structural Biology, 53, 169-177.
• Zheng, W. (2020). Review: The plant sirtuins. Plant Science, 293, 110434.
• Ziętara, P., Dziewięcka, M., & Augustyniak, M. (2023). Why is longevity still a scientific mystery? Sirtuins-past, present and future. International Journal of Molecular Sciences, 24, 728.