Comprehensive analysis of ERF transcription factor family and their expression in sesame under abiotic stresses

Document Type : Research Paper

Authors

1 Ph.D. Candidate, Department of Biotechnology and Plant Breeding, Sari Agricultural Sciences and Natural Resources University, Sari, Iran.

2 Associate Professor, Department of Biotechnology and Plant Breeding, Sari Agricultural Sciences and Natural Resources University, Sari, Iran.

3 Assistant Professor, Genetics and Agricultural Biotechnology Institute of Tabarestan (GABIT), Sari Agricultural Sciences and Natural Resources University, Sari, Iran.

4 Assistant Professor, Department of Basic Science, Sari Agricultural Sciences and Natural Resources University, Sari, Iran.

Abstract

Sesame (Sesamum indicum L.) is a nutritionally and medicinally important oilseed crop that environmental stresses limit its yield potential. Ethylene-responsive factor (ERF) is one of the largest transcription factor families that play key roles in regulating plant response to abiotic stress. In the current study, a total of 113 ERF genes were identified from the sesame genome and they were divided into two subfamilies including, 46 dehydration-responsive element-binding (DREB) members, and 67 ERF members. Phylogenetic relationships, physicochemical properties of proteins, structural properties of genes, and conserved amino acid motifs in the sesame ERF family were analyzed. Then, the expression profile of sesame ERF genes in various tissues as well as under environmental stresses was investigated. Overall, several genes of the ERF Family were expressed noticeably in different sesame tissues, especially in roots, capsules, and flowers. Expression profiles also showed that RAP2.2L, PTI6, ERF017L, and ERF096 genes were strongly induced by drought, osmotic, salinity, and waterlogging stresses, respectively. Moreover, the qPCR results showed that the relative expression of the ERF061L gene was higher in the sesame tolerant genotype compared to the susceptible one under drought conditions. This study provides important data for understanding the evolution and functions of the ERF family in sesame that can be used in future breeding programs for abiotic stresses tolerance.

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Main Subjects


Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., ... & Noble, W.S. (2009). MEME SUITE: tools for motif discovery and searching. Nucleic acids research 37(suppl_2): W202-W208. Banno, H., Ikeda, Y., Niu, Q.W., & Chua, N.H. (2001). Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. The Plant Cell, 13(12), 2609-2618. Bedigian, D. (2010). Introduction History of the Cultivationand Use of Sesame. In Sesame (pp. 25-56). CRC Press. Charfeddine, M., Saïdi, MN., Charfeddine, S., Hammami, A., & Gargouri Bouzid, R. (2015). Genome-wide analysis and expression profiling of the ERF transcription factor family in potato (Solanum tuberosum L.). Molecular biotechnology, 57(4), 348-358. Dong, C. J., & Liu, J. Y. (2010). The Arabidopsis EAR-motif-containing protein RAP2. 1 function as an active transcriptional repressor to keep stress responses under tight control. BMC plant biology, 10(1), 1-15. Dossa, K., Mmadi, M.A., Zhou, R., Zhang, T., Su, R., Zhang, Y.,...& Zhang, X. (2019). Depicting the core transcriptome modulating multiple abiotic stresses responses in sesame (Sesamum indicum L.). International Journal of Molecular Sciences, 20(16), 3930. Dossa, K., Wei, X., Li, D., Fonceka, D., Zhang, Y., Wang, L., ... & Zhang, X. (2016). Insight into the AP2/ERF transcription factor superfamily in sesame and expression profiling of DREB subfamily under drought stress. BMC plant biology, 16(1), 1-16. Dossa, K., You, J., Wang, L., Zhang, Y., Li, D., Zhou, R., ... & Zhang, X. (2019). Transcriptomic profiling of sesame during waterlogging and recovery. Scientific data, 6(1), 1-5. Du, X., Li, W., Sheng, L., Deng, Y., Wang, Y., Zhang, W., ... & Chen, S. (2018). Over-expression of chrysanthemum CmDREB6 enhanced tolerance of chrysanthemum to heat stress. BMC plant biology, 18(1), 1-10. Duvaud, S., Gabella, C., Lisacek, F., Stockinger, H., Ioannidis, V., & Durinx, C. (2021). Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Research, 49(W1), W216-W227. Eddy, S. R. (2011). Accelerated profile HMM searches. PLoS computational biology, 7(10), e1002195. El-Gebali, S., Mistry, J., Bateman, A., Eddy, S. R., Luciani, A., Potter, S. C., ... & Finn, R. D. (2019). The Pfam protein families database in 2019. Nucleic acids research, 47(D1), D427-D432. Guo, M., Yin, Y. X., Ji, J. J., Ma, B. P., Lu, M. H., & Gong, Z. H. (2014). Cloning and expression analysis of heat-shock transcription factor gene CaHsfA2 from pepper (Capsicum annuum L.). Genet. Mol. Res, 13, 1865-1875. Hong, J. C. (2016). General aspects of plant transcription factor families. In Plant transcription factors (pp. 35-56). Academic Press. 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. Islam, F., Gill, R.A., Ali, B., Farooq, M.A., Xu, L., Najeeb, U., Zhou, W. (2016). Sesame. In: Gupta SK (ed) Breeding Oilseed Crops for Sustainable Production, Academic Press, Cambridge, pp 135-147. Islam, M. S., & Wang, M. H. (2009). Expression of dehydration responsive element-binding protein-3 (DREB3) under different abiotic stresses in tomato. BMB reports, 42(9), 611-616. Jeffares, D. C., Penkett, C. J., & Bähler, J. (2008). Rapidly regulated genes are intron poor. Trends in genetics, 24(8), 375-378. Jin, J., Tian, F., Yang, D. C., Meng, Y. Q., Kong, L., Luo, J., & Gao, G. (2016). PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic acids research, gkw982. Jing, H., Li, C., Ma, F., Ma, J. H., Khan, A., Wang, X., ... & Chen, R. G. (2016). Genome-wide identification, expression diversication of dehydrin gene family and characterization of CaDHN3 in pepper (Capsicum annuum L.). PloS one, 11(8), e0161073. Kabir, S. M. T., Hossain, M. S., Bashar, K. K., Honi, U., Ahmed, B., Emdad, E. M., ... & Islam, M. S. (2021). Genome-wide identification and expression profiling of AP2/ERF superfamily genes under stress conditions in dark jute (Corchorus olitorius L.). Industrial Crops and Products, 166, 113469. Kudo, M., Kidokoro, S., Yoshida, T., Mizoi, J., Todaka, D., Fernie, A. R., ... & Yamaguchi‐Shinozaki, K. (2017). Double overexpression of DREB and PIF transcription factors improves drought stress tolerance and cell elongation in transgenic plants. Plant biotechnology journal, 15(4), 458-471. Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular biology and evolution, 35(6), 1547. León, J., Costa-Broseta, Á., & Castillo, M. C. (2020). RAP2. 3 negatively regulates nitric oxide biosynthesis and related responses through a rheostat-like mechanism in Arabidopsis. Journal of experimental botany, 71(10), 3157-3171. Letunic, I., & Bork, P. (2021). Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic acids research, 49(W1), W293-W296. Li, Z. H. A. N. G., Qiaoying, L. I., Jie, S. H. E. N., Jinai, X. U. E., & Yuanhuai, H.A.N. (2012). Transcriptional regulatory networks in response to salt and drought stress in Arabidopsis thaliana. Journal of Medicinal Plants Research, 6(6), 950-958. Lin, R. C., Park, H. J., & Wang, H. Y. (2008). Role of Arabidopsis RAP2. 4 in regulating light-and ethylene-mediated developmental processes and drought stress tolerance. Molecular plant, 1(1), 42-57. Luan, H., Guo, B., Shen, H., Pan, Y., Hong, Y., Lv, C., & Xu, R. (2020). Overexpression of barley transcription factor HvERF2. 11 in Arabidopsis enhances plant waterlogging tolerance. International journal of molecular sciences, 21(6), 1982. Marchler-Bauer, A., & Bryant, S. H. (2004). CD-Search: protein domain annotations on the fly. Nucleic acids research, 32(suppl_2), W327-W331. Mizoi, J., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2012). AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms, 1819(2),86-96. Morris, J.B. (2002). Food, industrial, nutraceutical, and pharmaceutical uses of sesame genetic resources. Trends in new crops and new uses, 1(1),153-156. Nakano, T., Suzuki, K., Fujimura, T., & Shinshi, H. (2006). Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant physiology, 140(2), 411-432. Osorio, D., Rondón-Villarreal, P., & Torres, R. (2015). Peptides: a package for data mining of antimicrobial peptides. Small, 12, 44-444. Pandey, G. K., Grant, J. J., Cheong, Y. H., Kim, B. G., Li, L., & Luan, S. (2005). ABR1, an APETALA2-domain transcription factor that functions as a repressor of ABA response in Arabidopsis. Plant Physiology, 139(3), 1185-1193. Patro, R., Duggal, G., Love, M. I., Irizarry, R. A., & Kingsford, C. (2017). Salmon provides fast and bias-aware quantification of transcript expression. Nature methods, 14(4), 417-419. Rae, L., Lao, N. T., & Kavanagh, T.A. (2011). Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta, 234(3), 429-444. Rao, G., Sui, J., Zeng, Y., He, C., & Zhang, J. (2015). Genome-wide analysis of the AP2/ERF gene family in Salix arbutifolia. FEBS Open Bio, 5, 132-137. Robinson, M. D., McCarthy, D. J., & Smyth, G.K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. Rudnik, R., Bulcha, J. T., Reifschneider, E., Ellersiek, U., & Baier, M. (2017). Specificity versus redundancy in the RAP2. 4 transcription factor family of Arabidopsis thaliana: transcriptional regulation of genes for chloroplast peroxidases. BMC plant biology, 17(1), 1-17. Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., & Yamaguchi-Shinozaki, K. (2002). DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochemical and biophysical research communications, 290(3), 998-1009. Sharma, M.K., Kumar, R., Solanke, A.U., Sharma, R., Tyagi, A.K., & Sharma, A.K. (2010). Identification, phylogeny, and transcript profiling of ERF family genes during development and abiotic stress treatments in tomato. olecular Genetics and Genomics, 284(6),455-475. Shkolnik-Inbar, D., & Bar-Zvi, D. (2011). Expression of abscisic acid insensitive 4 (ABI4) in developing Arabidopsis seedlings. Plant Signaling & Behavior, 6(5), 694-696. Shu, K., Zhang, H., Wang, S., Chen, M., Wu, Y., Tang, S., ... & Xie, Q. (2013). ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PloS genetics, 9(6), e1003577. Soneson, C., Love, M. I., & Robinson, M. D. (2015). Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences. F1000Research, 4. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B. C., Remm, M., & Rozen, S. G. (2012). Primer3-new capabilities and interfaces. Nucleic acids research, 40(15), e115-e115. Van der Graaff, E., Dulk-Ras, A. D., Hooykaas, P. J., & Keller, B. (2000). Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development, 127(22), 4971-4980. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome biology, 3(7), 1-12. Voorrips, R. (2002). MapChart: software for the graphical presentation of linkage maps and QTLs. Journal of heredity, 93(1), 77-78. Wang, W., Vinocur, B., & Altman, A. (2003). Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 218(1), 1-14. Wei, L., Miao, H., Zhao, R., Han, X., Zhang, T., & Zhang, H. (2013). Identification and testing of reference genes for Sesame gene expression analysis by quantitative real-time PCR. Planta, 237(3), 873-889. Weirauch, M. T., Yang, A., Albu, M., Cote, A. G., Montenegro-Montero, A., Drewe, P., ... & Hughes, T. R. (2014). Determination and inference of eukaryotic transcription factor sequence specificity. Cell, 158(6), 1431-1443. Wessler, S. R. (2005). Homing into the origin of the AP2 DNA binding domain. Trends in plant science, 10(2), 54-56. Wuddineh, W. A., Mazarei, M., Turner, G. B., Sykes, R. W., Decker, S. R., Davis, M. F., & Stewart Jr, C. N. (2015). Identification and molecular characterization of the switchgrass AP2/ERF transcription factor superfamily, and overexpression of PvERF001 for improvement of biomass characteristics for biofuel. Frontiers in bioengineering and biotechnology, 3, 101. Xu, W., Li, F., Ling, L., & Liu, A. (2013). Genome-wide survey and expression profiles of the AP2/ERF family in castor bean (Ricinus communis L.). BMC genomics, 14(1), 1-15. Xu, Z. S., Xia, L. Q., Chen, M., Cheng, X. G., Zhang, R. Y., Li, L. C., ... & Ma, Y.Z. (2007). Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant molecular biology, 65(6),719-732. Yamaguchi-Shinozaki, K., & Shinozaki, K. (2006). Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu. Rev. Plant Biol., 57, 781-803. Yang, S. U., Kim, H., Kim, R. J., Kim, J., & Suh, M. C. (2020). AP2/DREB transcription factor RAP2. 4 activates cuticular wax biosynthesis in Arabidopsis leaves under drought. Frontiers in plant science, 895. You, J., Zhang, Y., Liu, A., Li, D., Wang, X., Dossa, K., ... & Zhang, X. (2019). Transcriptomic and metabolomic profiling of drought-tolerant and susceptible sesame genotypes in response to drought stress. BMC plant biology, 19(1), 1-16. Zhang, J. Y., Broeckling, C. D., Blancaflor, E. B., Sledge, M. K., Sumner, L. W., & Wang, Z. Y. (2005). Overexpression of WXP1, a putative Medicago truncatula AP2 domain‐containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). The Plant Journal, 42(5), 689-707. Zhang, X., Liu, X., Zhang, D., Tang, H., Sun, B., Li, C., ... & Li, Y. (2017). Genome-wide identification of gene expression in contrasting maize inbred lines under field drought conditions reveals the significance of transcription factors in drought tolerance. PLoS One, 12(7), e0179477. Zhang, Y., Li, D., Zhou, R., Wang, X., Dossa, K., Wang, L., ... & You, J. (2019). Transcriptome and metabolome analyses of two contrasting sesame genotypes reveal the crucial biological pathways involved in rapid adaptive response to salt stress. BMC plant biology, 19(1), 1-14. Zhou, Y., Zhou, W., Liu, H., Liu, P., & Li, Z. (2020). Genome‐wide analysis of the soybean DREB gene family: Identification, genomic organization and expression profiles in response to drought stress. Plant Breeding, 139(6), 1158-1167.