Molecular insights into somatic embryogenesis in Agave angustifolia: characterization of the AaSERK gene
DOI:
https://doi.org/10.18387/polibotanica.58.14Palavras-chave:
Somatic embryogenesis; Somatic Embryogenesis Receptor-like Kinase gene; Agave angustifolia.Resumo
The Agave genus, with 204 species, including 163 natives to Mexico, is of paramount significance in ethnobotanical, ecological, and economic contexts. However, over-exploitation and uncontrolled harvesting of these plants endanger their survival due to the prevention of sexual reproduction. In response, in vitro techniques, such as somatic embryogenesis, have been developed for vegetative propagation and species conservation. Somatic embryogenesis transitions cells to totipotency, driven by specific gene expression, endogenous hormones, and responses to external regulators. This work explores the first molecular insights into somatic embryogenesis in the Agave genus through the isolation and characterization of the AaSERK gene. Receptor-Like Kinases (RLKs) with Leucine-Rich Repeats (LRRs) have crucial roles in cellular signaling across various aspects of plant development, including embryogenesis. The presence of a Serine-Proline-Proline motif (SPP) distinguishes SERK from other RLKs, and its expression signifies embryogenic competence. The results reveal that AaSERK encodes a typical SERK protein with conserved domains, indicating its role in plant development. Phylogenetic analysis suggests that AaSERK shares evolutionary ancestry with SERKs of closely related plant species. These findings shed light on somatic embryogenesis in Agave angustifolia and may enhance the regeneration and transformation processes for the conservation of these valuable plants. Understanding the genetic control of totipotency and the molecular regulation of somatic embryogenesis is vital for advancing plant biotechnology and plant physiology.
Referências
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Cueva, A., Concia, L., & Cella, R. (2012). Molecular characterization of a Cyrtochilum loxense Somatic Embryogenesis Receptor-like Kinase (SERK) gene expressed during somatic embryogenesis. Plant Cell Reports, 31(6), 1129–1139. https://doi.org/10.1007/s00299-012-1236-x
De Oliveira Santos, M., Romano, E., Yotoko, K. S. C., Tinoco, M. L. P., Dias, B. B. A., & Aragão, F. J. L. (2005). Characterisation of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Science, 168(3), 723–729. https://doi.org/10.1016/j.plantsci.2004.10.004
Fisher, K., & Turner, S. (2007). PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development. Current Biology, 17(12), 1061–1066. https://doi.org/10.1016/j.cub.2007.05.049
Guzzo, F., Baldan, B., Mariani, P., Schiavo, F. Lo, & Terzi, M. (1994). Studies on the origin of totipotent cells in explants of Daucus carota L. Journal of Experimental Botany, 45(10), 1427–1432. https://doi.org/10.1093/jxb/45.10.1427
Hecht, V., Vielle-Calzada, J. P., Hartog, M. V, Schmidt, E. D., Boutilier, K., Grossniklaus, U., & de Vries, S. C. (2001). The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology, 127(3), 803–816. http://www.ncbi.nlm.nih.gov/pubmed/11706164
Hu, H., Xiong, L., & Yang, Y. (2005). Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta, 222(1), 107–117. https://doi.org/10.1007/s00425-005-1534-4
Kobe, B., & Deisenhofer, J. (1994). The leucine-rich repeat: a versatile binding motif. Trends in Biochemical Sciences, 19(10), 415–421. https://doi.org/10.1016/0968-0004(94)90090-6
Koehler, A. D., Irsigler, A. S. T., Carneiro, V. T. C., Cabral, G. B., Rodrigues, J. C. M., Gomes, A. C. M. M., Togawa, R. C., Costa, M. M. C., Martinelli, A. P., & Dusi, D. M. D. A. (2020). SERK genes identification and expression analysis during somatic embryogenesis and sporogenesis of sexual and apomictic Brachiaria brizantha (Syn. Urochloa brizantha). Planta, 252(3), 39. https://doi.org/10.1007/s00425-020-03443-w
Liu, Z., Zhao, Y., Zeng, L., Zhang, Y., Wang, Y., & Hua, J. (2018). Characterization of GhSERK2 and its expression associated with somatic embryogenesis and hormones level in Upland cotton. Journal of Integrative Agriculture, 17(3), 517–529. https://doi.org/10.1016/S2095-3119(17)61726-X
Ma, Y., Qin, F., & Tran, L.-S. P. (2012). Contribution of Genomics to Gene Discovery in Plant Abiotic Stress Responses. Molecular Plant, 5(6), 1176–1178. https://doi.org/10.1093/mp/sss085
Maulidiya, A. U. K., Sugiharto, B., Dewanti, P., & Handoyo, T. (2020). Expression of somatic embryogenesis-related genes in sugarcane (Saccharum officinarum L.). Journal of Crop Science and Biotechnology, 23(3), 207–214. https://doi.org/10.1007/s12892-020-00024-x
Monja-Mio, K. M., Olvera-Casanova, D., Herrera-Alamillo, M. Á., Sánchez-Teyer, F. L., & Robert, M. L. (2021). Comparison of conventional and temporary immersion systems on micropropagation (multiplication phase) of Agave angustifolia Haw. ‘Bacanora.’ 3 Biotech, 11(2), 77. https://doi.org/10.1007/s13205-020-02604-8
Murashige, T., & Skoog, F. (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15(3), 473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nodine, M. D., Yadegari, R., & Tax, F. E. (2007). RPK1 and TOAD2 Are Two Receptor-like Kinases Redundantly Required for Arabidopsis Embryonic Pattern Formation. Developmental Cell, 12(6), 943–956. https://doi.org/10.1016/j.devcel.2007.04.003
Porras-Murillo, R., Andrade-Torres, A., & Solís-Ramos, L. Y. (2018). Expression analysis of two SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes during in vitro morphogenesis in Spanish cedar (Cedrela odorata L.). 3 Biotech, 8(11). https://doi.org/10.1007/s13205-018-1492-8
Ramasamy, G., Ramasamy, S., Ravi, N. S., Krishnan, R., Subramanian, R., Raman, R., Duraialaguraja, S., Muthurajan, R., & Vellaichamy, J. (2022). Haploid embryogenesis and molecular detection of somatic embryogenesis receptor-like kinase (TcSERK) genes in sliced ovary cultures of cocoa (Theobroma cacao L.). Plant Biotechnology Reports, 16(3), 283–297. https://doi.org/10.1007/s11816-022-00756-y
Reyes-Díaz, J. I., Arzate-Fernández, A. M., Piña-Escutia, J. L., & Vázquez-García, L. M. (2017). Media culture factors affecting somatic embryogenesis in Agave angustifolia Haw. Industrial Crops and Products, 108, 81–85. https://doi.org/10.1016/j.indcrop.2017.06.021
Salaj, J., Von Recklinghausen, I. R., Hecht, V., De Vries, S. C., Schel, J. H. N., & Van Lammeren, A. A. M. (2008). AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiology and Biochemistry, 46(7), 709–714. https://doi.org/10.1016/j.plaphy.2008.04.011
Santos, M. O., Romano, E., Vieira, L. S., Baldoni, A. B., & Aragão, F. J. L. (2009). Suppression of SERK gene expression affects fungus tolerance and somatic embryogenesis in transgenic lettuce. Plant Biology, 11(1), 83–89. https://doi.org/10.1111/j.1438-8677.2008.00103.x
Schmidt, E. D. L., Guzzo, F., Toonen, M. A. J., & Vries, S. C. De. (1997). A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development, 124(10), 2049–2062. https://doi.org/10.1242/dev.124.10.2049
Schwessinger, B., & Rathjen, J. P. (2015). Changing SERKs and priorities during plant life. Trends in Plant Science, 20(9), 531–533. https://doi.org/10.1016/j.tplants.2015.06.006
Shah, K., Gadella Jr, T. W. J., Van Erp, H., Hecht, V., & De Vries, S. C. (2001). Subcellular Localization and Oligomerization of the Arabidopsis thaliana Somatic Embryogenesis Receptor Kinase 1 Protein. Journal of Molecular Biology, 309(3), 641–655. https://doi.org/10.1006/jmbi.2001.4706
Vázquez-Delfin, P., Casas, A., & Vallejo, M. (2022). Adaptation and biocultural conservation of traditional agroforestry systems in the Tehuacán Valley: access to resources and livelihoods strategies. Heliyon, 8(7). https://doi.org/10.1016/j.heliyon.2022.e09805
Zhao, D.-Z., Wang, G.-F., Speal, B., & Ma, H. (2002). The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes & Development, 16(15), 2021–2031. https://doi.org/10.1101/gad.997902
Zhao, L., Zeng, X., Hu, X., Sheng, J., Zhu, F., Zhong, L., Zhou, F., Jin, S., Hu, Z., & Diao, Y. (2020). Molecular cloning and characterization of five genes from embryogenic callus in Miscanthus lutarioriparius. Acta Physiologiae Plantarum, 42(5), 89. https://doi.org/10.1007/s11738-020-03071-7
Baudino, S., Hansen, S., Brettschneider, R., Hecht, V. F. G., Dresselhaus, T., Lörz, H., Dumas, C., & Rogowsky, P. M. (2001). Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta, 213(1), 1–10. https://doi.org/10.1007/s004250000471
Becraft, P. W. (1998). Receptor kinases in plant development. Trends in Plant Science, 3(10), 384–388. https://doi.org/10.1016/S1360-1385(98)01301-6
Becraft, P. W. (2002). Receptor Kinase Signaling in Plant Development. Annual Review of Cell and Developmental Biology, 18(1), 163–192. https://doi.org/10.1146/annurev.cellbio.18.012502.083431
Cueva, A., Concia, L., & Cella, R. (2012). Molecular characterization of a Cyrtochilum loxense Somatic Embryogenesis Receptor-like Kinase (SERK) gene expressed during somatic embryogenesis. Plant Cell Reports, 31(6), 1129–1139. https://doi.org/10.1007/s00299-012-1236-x
De Oliveira Santos, M., Romano, E., Yotoko, K. S. C., Tinoco, M. L. P., Dias, B. B. A., & Aragão, F. J. L. (2005). Characterisation of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Science, 168(3), 723–729. https://doi.org/10.1016/j.plantsci.2004.10.004
Fisher, K., & Turner, S. (2007). PXY, a Receptor-like Kinase Essential for Maintaining Polarity during Plant Vascular-Tissue Development. Current Biology, 17(12), 1061–1066. https://doi.org/10.1016/j.cub.2007.05.049
Guzzo, F., Baldan, B., Mariani, P., Schiavo, F. Lo, & Terzi, M. (1994). Studies on the origin of totipotent cells in explants of Daucus carota L. Journal of Experimental Botany, 45(10), 1427–1432. https://doi.org/10.1093/jxb/45.10.1427
Hecht, V., Vielle-Calzada, J. P., Hartog, M. V, Schmidt, E. D., Boutilier, K., Grossniklaus, U., & de Vries, S. C. (2001). The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiology, 127(3), 803–816. http://www.ncbi.nlm.nih.gov/pubmed/11706164
Hu, H., Xiong, L., & Yang, Y. (2005). Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta, 222(1), 107–117. https://doi.org/10.1007/s00425-005-1534-4
Kobe, B., & Deisenhofer, J. (1994). The leucine-rich repeat: a versatile binding motif. Trends in Biochemical Sciences, 19(10), 415–421. https://doi.org/10.1016/0968-0004(94)90090-6
Koehler, A. D., Irsigler, A. S. T., Carneiro, V. T. C., Cabral, G. B., Rodrigues, J. C. M., Gomes, A. C. M. M., Togawa, R. C., Costa, M. M. C., Martinelli, A. P., & Dusi, D. M. D. A. (2020). SERK genes identification and expression analysis during somatic embryogenesis and sporogenesis of sexual and apomictic Brachiaria brizantha (Syn. Urochloa brizantha). Planta, 252(3), 39. https://doi.org/10.1007/s00425-020-03443-w
Liu, Z., Zhao, Y., Zeng, L., Zhang, Y., Wang, Y., & Hua, J. (2018). Characterization of GhSERK2 and its expression associated with somatic embryogenesis and hormones level in Upland cotton. Journal of Integrative Agriculture, 17(3), 517–529. https://doi.org/10.1016/S2095-3119(17)61726-X
Ma, Y., Qin, F., & Tran, L.-S. P. (2012). Contribution of Genomics to Gene Discovery in Plant Abiotic Stress Responses. Molecular Plant, 5(6), 1176–1178. https://doi.org/10.1093/mp/sss085
Maulidiya, A. U. K., Sugiharto, B., Dewanti, P., & Handoyo, T. (2020). Expression of somatic embryogenesis-related genes in sugarcane (Saccharum officinarum L.). Journal of Crop Science and Biotechnology, 23(3), 207–214. https://doi.org/10.1007/s12892-020-00024-x
Monja-Mio, K. M., Olvera-Casanova, D., Herrera-Alamillo, M. Á., Sánchez-Teyer, F. L., & Robert, M. L. (2021). Comparison of conventional and temporary immersion systems on micropropagation (multiplication phase) of Agave angustifolia Haw. ‘Bacanora.’ 3 Biotech, 11(2), 77. https://doi.org/10.1007/s13205-020-02604-8
Murashige, T., & Skoog, F. (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum, 15(3), 473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Nodine, M. D., Yadegari, R., & Tax, F. E. (2007). RPK1 and TOAD2 Are Two Receptor-like Kinases Redundantly Required for Arabidopsis Embryonic Pattern Formation. Developmental Cell, 12(6), 943–956. https://doi.org/10.1016/j.devcel.2007.04.003
Porras-Murillo, R., Andrade-Torres, A., & Solís-Ramos, L. Y. (2018). Expression analysis of two SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes during in vitro morphogenesis in Spanish cedar (Cedrela odorata L.). 3 Biotech, 8(11). https://doi.org/10.1007/s13205-018-1492-8
Ramasamy, G., Ramasamy, S., Ravi, N. S., Krishnan, R., Subramanian, R., Raman, R., Duraialaguraja, S., Muthurajan, R., & Vellaichamy, J. (2022). Haploid embryogenesis and molecular detection of somatic embryogenesis receptor-like kinase (TcSERK) genes in sliced ovary cultures of cocoa (Theobroma cacao L.). Plant Biotechnology Reports, 16(3), 283–297. https://doi.org/10.1007/s11816-022-00756-y
Reyes-Díaz, J. I., Arzate-Fernández, A. M., Piña-Escutia, J. L., & Vázquez-García, L. M. (2017). Media culture factors affecting somatic embryogenesis in Agave angustifolia Haw. Industrial Crops and Products, 108, 81–85. https://doi.org/10.1016/j.indcrop.2017.06.021
Salaj, J., Von Recklinghausen, I. R., Hecht, V., De Vries, S. C., Schel, J. H. N., & Van Lammeren, A. A. M. (2008). AtSERK1 expression precedes and coincides with early somatic embryogenesis in Arabidopsis thaliana. Plant Physiology and Biochemistry, 46(7), 709–714. https://doi.org/10.1016/j.plaphy.2008.04.011
Santos, M. O., Romano, E., Vieira, L. S., Baldoni, A. B., & Aragão, F. J. L. (2009). Suppression of SERK gene expression affects fungus tolerance and somatic embryogenesis in transgenic lettuce. Plant Biology, 11(1), 83–89. https://doi.org/10.1111/j.1438-8677.2008.00103.x
Schmidt, E. D. L., Guzzo, F., Toonen, M. A. J., & Vries, S. C. De. (1997). A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development, 124(10), 2049–2062. https://doi.org/10.1242/dev.124.10.2049
Schwessinger, B., & Rathjen, J. P. (2015). Changing SERKs and priorities during plant life. Trends in Plant Science, 20(9), 531–533. https://doi.org/10.1016/j.tplants.2015.06.006
Shah, K., Gadella Jr, T. W. J., Van Erp, H., Hecht, V., & De Vries, S. C. (2001). Subcellular Localization and Oligomerization of the Arabidopsis thaliana Somatic Embryogenesis Receptor Kinase 1 Protein. Journal of Molecular Biology, 309(3), 641–655. https://doi.org/10.1006/jmbi.2001.4706
Vázquez-Delfin, P., Casas, A., & Vallejo, M. (2022). Adaptation and biocultural conservation of traditional agroforestry systems in the Tehuacán Valley: access to resources and livelihoods strategies. Heliyon, 8(7). https://doi.org/10.1016/j.heliyon.2022.e09805
Zhao, D.-Z., Wang, G.-F., Speal, B., & Ma, H. (2002). The EXCESS MICROSPOROCYTES1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes & Development, 16(15), 2021–2031. https://doi.org/10.1101/gad.997902
Zhao, L., Zeng, X., Hu, X., Sheng, J., Zhu, F., Zhong, L., Zhou, F., Jin, S., Hu, Z., & Diao, Y. (2020). Molecular cloning and characterization of five genes from embryogenic callus in Miscanthus lutarioriparius. Acta Physiologiae Plantarum, 42(5), 89. https://doi.org/10.1007/s11738-020-03071-7
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2024-06-21
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Molecular insights into somatic embryogenesis in Agave angustifolia: characterization of the AaSERK gene. (2024). POLIBOTÁNICA, 58. https://doi.org/10.18387/polibotanica.58.14
