Genome-wide Analysis and Functional Identification of KCS Gene Family under Drought and Salt Stresses in Phaseolus vulgaris L

Year 2023, Volume: 4 Issue: 2, 138 - 151, 30.12.2023

Ceren Yılmaz Merve Yüce Ahmed Sidar Aygören Ayşe Gül Kasapoğlu Selman Muslu Murat Turan Emre İlhan Murat Aydın Ertan Yıldırım

https://doi.org/10.56430/japro.1371633

Abstract

β-ketoacyl-CoA synthase (KCS) is an important enzyme that catalyzes the biosynthesis of very-long-chain fatty acids (VLCFAs). In this study, the genome-wide analysis and functional characterization of the KCS gene family members in common bean (Phaseolus vulgaris L.) plants were conducted, and the response of the identified gene family to abiotic stresses was evaluated. In this study, 19 KCS genes were identified and characterized in the P. vulgaris genome. The molecular weights of these KCS proteins ranged from 49.14 kDa to 60.57 kDa, their amino acid lengths varied from 437 to 534, and their pI values ranged from 8.81 to 9.47, indicating a basic nature. Segmental and tandem duplications were observed in the Pvul-KCS gene family. Phylogenetic analysis revealed that Pvul-KCS proteins clustered into three main groups with Arabidopsis thaliana and Glycine max species. Comparative mapping analysis was also conducted with A. thaliana and G. max. Expression profile comparisons indicated that these genes had different expression levels in common bean varieties and played a role in the plant’s response to biotic and abiotic stresses. This study provides important insights into the biological functions of KCS genes in Phaseolus vulgaris and offers valuable information for improving drought and salt stress tolerance in common beans.

Keywords

Genome-wide analysis, KCS, Phaseolus vulgaris L, VLCFA

Thanks

This study was presented at the VI international symposium “Biodiversity in Eurasia - SEAB 2023” and published in the Abstract Book as an abstract.

References

• Araus, J. L., Slafer, G. A., Royo, C., & Serret, M. D. (2008). Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Science, 27(6), 377-412. https://doi.org/10.1080/07352680802467736
• Assefa, T., Mahama, A. A., Brown, A. V., Cannon, E. K., Rubyogo, J. C., Rao, I. M., & Cannon, S. B. (2019). A review of breeding objectives, genomic resources, and marker-assisted methods in common bean (Phaseolus vulgaris L.). Molecular Breeding, 39(2), 20. https://doi.org/10.1007/s11032-018-0920-0
• Aygören, A. S., Güneş, E., Muslu, S., Kasapoğlu, A. G., Yiğider, E., Aydın, M., & İlhan, E. (2023). Genome-wide analysis and characterization of SABATH gene family in Phaseolus vulgaris genotypes subject to melatonin under drought and salinity stresses. Plant Molecular Biology Reporter, 41(2), 242-259. https://doi.org/10.1007/s11105-022-01363-5
• Bailey, T. L., Williams, N., Misleh, C., & Li, W. W. (2006). MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research, 34(suppl_2), W369-W373. https://doi.org/10.1093/nar/gkl198
• Bernard, A., & Joubès, J. (2013). Arabidopsis cuticular waxes: Advances in synthesis, export and regulation. Progress in Lipid Research, 52(1), 110-129. https://doi.org/10.1016/j.plipres.2012.10.002
• Blair, M. W. (2013). Mineral biofortification strategies for food staples: The example of common bean. Journal of Agricultural and Food Chemistry, 61(35), 8287-8294. https://doi.org/10.1021/jf400774y
• Broughton, W. J., Hernández, G., Blair, M., Beebe, S., Gepts, P., & Vanderleyden, J. (2003). Beans (Phaseolus spp.)–model food legumes. Plant and Soil, 252, 55-128. https://doi.org/10.1023/A:1024146710611
• Buruchara, R., Chirwa, R., Sperling, L., Mukankusi, C., Rubyogo, J. C., Mutonhi, R., & Abang, M. M. (2011). Development and delivery of bean varieties in Africa: The pan-Africa bean research alliance (PABRA) model. African Crop Science Journal, 19(4), 227-245.
• 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. https://doi.org/10.1016/j.molp.2020.06.009
• Dai, H., Zhang, Y., Jin, P., Song, F., Xu, W., Liu, A., Meng, Z., & Yang, T. (2021). Identification of KCS gene family and functional analysis of FAE-like genes from Malania oleifera. Oil Crop Science, 6(1), 35-40. https://doi.org/10.1016/j.ocsci.2021.03.003
• Ekinci, M., Ors, S., Yildirim, E., Dursun, A., Turan, M., Sahin, U., & Kul, R. (2020). Monitoring some antioxidant enzymes and physiological indices of chard exposed to nitric oxide under drought stress. The Russian Journal of Plant Physiology, 67(4), 740-749.
• Ghanevati, M., & Jaworski, J. G. (2001). Active-site residues of a plant membrane-bound fatty acid elongase β-ketoacyl-CoA synthase, FAE1 KCS. Biochimica et Biophysica Acta (BBA)-Molecular and Cell Biology of Lipids, 1530(1), 77-85. https://doi.org/10.1016/S1388-1981(00)00168-2
• Gilbert, W. (1987). The exon theory of genes. Cold Spring Harbor Symposia on Quantitative Biology, 52(0), 901-905. https://doi.org/10.1101/sqb.1987.052.01.098
• Glick, B. R. (2012). Plant growth-promoting bacteria: Mechanisms and applications. Scientifica, 2012, 1-15. https://doi.org/10.6064/2012/963401
• Gregorio Jorge, J., Villalobos-López, M. A., Chavarría-Alvarado, K. L., Ríos-Meléndez, S., López-Meyer, M., & Arroyo-Becerra, A. (2020). Genome-wide transcriptional changes triggered by water deficit on a drought-tolerant common bean cultivar. BMC Plant Biology, 20, 525. https://doi.org/10.1186/s12870-020-02664-1
• Hiz, M. C., Canher, B., Niron, H., & Turet, M. (2014). Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PloS One, 9(3), e92598. https://doi.org/10.1371/journal.pone.0092598
• Horton, P., Park, K. J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C. J., & Nakai, K. (2007). WoLF PSORT: Protein localization predictor. Nucleic Acids Research, 35(suppl_2), W585-W587. https://doi.org/10.1093/nar/gkm259
• 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. https://doi.org/10.1093/bioinformatics/btu817
• İlhan, E. (2018). Eucalyptus grandis YABBY transkripsiyon faktörlerinin genom bazında analizi. Türkiye Tarımsal Araștırmalar Dergisi, 5(2), 158-166. https://doi.org/10.19159/tutad.408654 (In Turkish)
• İlhan, E., Kasapoğlu, A. G., Muslu, S., Aygören, A. S., & Aydin, M. (2023). Genome-wide analysis and characterization of Eucalyptus grandis TCP transcription factors. Journal of Agricultural Sciences, 29(2), 413-426. https://doi.org/10.15832/ankutbd.1104949
• Juretic, N., Hoen, D. R., Huynh, M. L., Harrison, P. M., & Bureau, T. E. (2005). The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Research, 15(9), 1292-1297. https://doi.org/10.1101/gr.4064205
• Kasapoğlu, A. G., Ilhan, E., Kizilkaya, D., Hossein-Pour, A., & Haliloğlu, K. (2020). Sorgum [Sorghum bicolor (L.) Moench] genomunda BES1 transkripsiyon faktör ailesinin genom çaplı analizi. Türkiye Tarımsal Araştırmalar Dergisi, 7(1), 85-95. https://doi.org/10.19159/tutad.671605 (In Turkish)
• 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. https://doi.org/10.1038/nprot.2015.053
• Kunst, L., Taylor, D. C., & Underhill, E. W. (1992). Fatty acid elongation in developing seeds of Arabidopsis thaliana. Plant Physiology and Biochemistry, 30(4), 425-434.
• Lamesch, P., Berardini, T. Z., Li, D., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D. L., Garcia-Hernandez, M., Karthikeyan, A. S., Lee, C. H., Nelson, W. D., Ploetz, L., Singh, S., Wensel, A., & Huala, E. (2012). The Arabidopsis information resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Research, 40(D1), D1202-D1210. https://doi.org/10.1093/nar/gkr1090
• Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P., & 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. https://doi.org/10.1093/nar/30.1.325
• Letunic, I., & Bork, P. (2011). Interactive tree of life v2: Online annotation and display of phylogenetic trees made easy. Nucleic Acids Research, 39(suppl_2), W475-W478. https://doi.org/10.1093/nar/gkr201
• Lian, X. Y., Wang, X., Gao, H. N., Jiang, H., Mao, K., You, C. X., & Hao, Y. J. (2020). Genome wide analysis and functional identification of MdKCS genes in apple. Plant Physiology and Biochemistry, 151, 299-312. https://doi.org/10.1016/j.plaphy.2020.03.034
• Liu, E. K., Mei, X. R., Yan, C. R., Gong, D. Z., & Zhang, Y. Q. (2016). Effects of water stress on photosynthetic characteristics, dry matter translocation and WUE in two winter wheat genotypes. Agricultural Water Management, 167, 75-85. https://doi.org/10.1016/j.agwat.2015.12.026
• Lynch, M., & Conery, J. S. (2003). The evolutionary demography of duplicate genes. Journal of Structural and Functional Genomics, 3, 35-44. https://doi.org/10.1023/A:1022696612931
• Maggio, A., De Pascale, S., Ruggiero, C., & Barbieri, G. (2005). Physiological response of field-grown cabbage to salinity and drought stress. European Journal of Agronomy, 23(1), 57-67. https://doi.org/10.1016/j.eja.2004.09.004
• Muslu, S., Kasapoğlu, A. G., Güneş, E., Aygören, A. S., Yiğider, E., İlhan, E., & Aydın, M. (2023). Genome-wide analysis of glutathione S-transferase gene family in P. vulgaris under drought and salinity stress. Plant Molecular Biology Reporter. https://doi.org/10.1007/s11105-023-01400-x
• Oner, B. M., Ilhan, E., Kasapoglu, A. G., Muslu, S., Aygoren, A. S., Ucar, S., & Aydin, M. (2022). Genome wide analysis and characterization of NPR-like gene family of Phaseolus vulgaris L. Natural Products and Biotechnology, 2(1), 23-41.
• Ors, S., Ekinci, M., Yildirim, E., & Sahin, U. (2016). Changes in gas exchange capacity and selected physiological properties of squash seedlings (Cucurbita pepo L.) under well-watered and drought stress conditions. Archives of Agronomy and Soil Science, 62(12), 1700-1710. https://doi.org/10.1080/03650340.2016.1168517
• Patthy, L. (1987). Intron-dependent evolution: Preferred types of exons and introns. FEBS Letters, 214(1), 1-7. https://doi.org/10.1016/0014-5793(87)80002-9
• Piya, S., Shrestha, S. K., Binder, B., Stewart Jr, C. N., & Hewezi, T. (2014). Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science, 5, 744. https://doi.org/10.3389/fpls.2014.00744
• Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., & Lopez, R. (2005). InterProScan: Protein domains identifier. Nucleic Acids Research, 33(suppl_2), W116-W120. https://doi.org/10.1093/nar/gki442
• Rakhimzhanova, A., Kasapoğlu, A. G., Sapakova, A., İlhan, E., Zharmukhametova, R., Turan, M., Zekenova, L., Muslu, S., Kazhygeldiyeva, L., Aydın, M., & Çiltaş, A. (2023). Expression analysis and characterization of the CPP gene family of melatonin-treated common bean cultivars under different abiotic stresses. South African Journal of Botany, 160, 282-294. https://doi.org/10.1016/j.sajb.2023.07.013
• Rizwan, H. M., Shaozhong, F., Li, X., Bilal Arshad, M., Yousef, A. F., Chenglong, Y., & Chen, F. (2022). Genome-wide identification and expression profiling of KCS gene family in passion fruit (Passiflora edulis) under Fusarium kyushuense and drought stress conditions. Frontiers in Plant Science, 13, 872263. https://doi.org/10.3389/fpls.2022.872263
• Rui, C., Chen, X., Xu, N., Wang, J., Zhang, H., Li, S., & Ye, W. (2022). Identification and structure analysis of KCS family genes suggest their reponding to regulate fiber development in long-staple cotton under salt-alkaline stress. Frontiers in Genetics, 13, 812449. https://doi.org/10.3389%2Ffgene.2022.812449
• Sahin, U., Ekinci, M., Ors, S., Turan, M., Yildiz, S., & Yildirim, E. (2018). Effects of individual and combined effects of salinity and drought on physiological, nutritional and biochemical properties of cabbage (Brassica oleracea var. capitata). Scientia Horticulturae, 240, 196-204. https://doi.org/10.1016/j.scienta.2018.06.016
• Schmutz, J., McClean, P. E., Mamidi, S., Wu, G. A., Cannon, S. B., Grimwood, J., ... & Jackson, S. A. (2014). A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics, 46(7), 707-713. https://doi.org/10.1038/ng.3008
• Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10), 2731-2739. https://doi.org/10.1093/molbev/msr121
• Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25(24), 4876-4882. https://doi.org/10.1093/nar/25.24.4876
• Tong, T., Fang, Y. X., Zhang, Z., Zheng, J., Zhang, X., Li, J., & Zhang, X. (2021). Genome-wide identification and expression pattern analysis of the KCS gene family in barley. Plant Growth Regulation, 93, 89-103. https://doi.org/10.1007/s10725-020-00668-3
• Valliyodan, B., Cannon, S. B., Bayer, P. E., Shu, S., Brown, A. V., Ren, L., ... & Nguyen, H. T. (2019). Construction and comparison of three reference‐quality genome assemblies for soybean. The Plant Journal, 100(5), 1066-1082. https://doi.org/10.1111/tpj.14500
• Verslues, P. E., Agarwal, M., Katiyar‐Agarwal, S., Zhu, J., & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal, 45(4), 523-539. https://doi.org/10.1111/j.1365-313X.2005.02593.x
• Voorrips, R. (2002). MapChart: Software for the graphical presentation of linkage maps and QTLs. Journal of Heredity, 93(1), 77-78. https://doi.org/10.1093/jhered/93.1.77
• Wang, Y., Tang, H., DeBarry, J. D., Tan, X., Li, J., Wang, X., Lee, T., Jin, H., Marler, B., Guo, H., Kissinger, J. C., & Paterson, A. H. (2012). MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40(7), e49-e49. https://doi.org/10.1093/nar/gkr1293
• Wang, X., Guan, Y., Zhang, D., Dong, X., Tian, L., & Qu, L. Q. (2017). A β-ketoacyl-CoA synthase is involved in rice leaf cuticular wax synthesis and requires a CER2-LIKE protein as a cofactor. Plant Physiology, 173(2), 944-955. https://doi.org/10.1104/pp.16.01527
• Weinstein, J. N., Myers, T. G., O’Connor, P. M., Friend, S. H., Fornace Jr, A. J., Kohn, K. W., & Paull, K. D. (1997). An information-intensive approach to the molecular pharmacology of cancer. Science, 275(5298), 343-349. https://doi.org/10.1126/science.275.5298.343
• Xiao, G. H., Wang, K., Huang, G., & Zhu, Y. X. (2016). Genome‐scale analysis of the cotton KCS gene family revealed a binary mode of action for gibberellin A regulated fiber growth. Journal of Integrative Plant Biology, 58(6), 577-589. https://doi.org/10.1111/jipb.12429
• Xue, Y., Jiang, J., Yang, X., Jiang, H., Du, Y., Liu, X., Xie, R., & Chai, Y. (2020). Genome-wide mining and comparative analysis of fatty acid elongase gene family in Brassica napus and its progenitors. Gene, 747, 144674. https://doi.org/10.1016/j.gene.2020.144674
• Yang, Z., & Nielsen, R. (2000). Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Eevolution, 17(1), 32-43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
• Yang, H., Mei, W., Wan, H., Xu, R., & Cheng, Y. (2021). Comprehensive analysis of KCS gene family in Citrinae reveals the involvement of CsKCS2 and CsKCS11 in fruit cuticular wax synthesis at ripening. Plant Science, 310, 110972. https://doi.org/10.1016/j.plantsci.2021.110972
• You, F. M., Li, P., Kumar, S., Ragupathy, R., Li, Z., Fu, Y. B., & Cloutier, S. (2014). Genome-wide identification and characterization of the gene families controlling fatty acid biosynthesis in flax (Linum usitatissimum L). Journal of Proteomics & Bioinformatics, 7(10), 310-326. https://doi.org/10.4172/jpb.1000334
• Zhang, A., Xu, J., Xu, X., Wu, J., Li, P., Wang, B., & Fang, H. (2022). Genome-wide identification and characterization of the KCS gene family in sorghum (Sorghum bicolor (L.) Moench). PeerJ, 10, e14156. https://doi.org/10.7717/peerj.14156
• Zheng, H., Liang, Y., Hong, B., Xu, Y., Ren, M., Wang, Y., & Tao, J. (2023). Genome-scale analysis of the grapevine KCS genes reveals its potential role in male sterility. International Journal of Molecular Sciences, 24(7), 6510. https://doi.org/10.3390/ijms24076510