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Role of Plant Somatic Embryogenesis Receptor Kinases (SERKs) in Cell-to-Embryo Transitional Activity: Key at Novel Assorted Structural Subunits

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DOI: 10.4236/ajps.2014.521334    4,010 Downloads   4,916 Views   Citations


Somatic Embryogenesis Receptor Kinase (SERK) family of receptor kinases is functionally diverse, involved in cell-to-embryo transition and controlling a number of other fundamental aspects of plant development. The morphological transformation of somatic to embryonic cells has drawn scientific attention utmost due to remarkable genetic-switch system evolved across species. Receptor kinases having direct role in somatic embryogenesis (SE) and involved in other functions are designated as “SERK” and “SERK-like” genes, respectively. We aim for phylogenetic reconstruction to reveal major SERK groups across plant species (angiosperm to gymnosperm) for their functional diversification. Data indicate that the development of SERK proteins occurred prior to the divergence of monocots and eudicots. Also, the SERK orthology is not directly proportional to their functions. Structure prediction results identified novel transmembrane topologies, short linear motifs and O-glycosylation sites exclusively in SERK proteins than SERK-like proteins. Comparative temporal expression analyses of SERK and SERK-like genes provided significant accordance with their physiological function. The identification of intrinsic disordered regions (IDRs) exclusively in SERK proteins was assumed to perceive external stress-induced signals that may lead to rapid protein folding. In a result it switches-on the precise cellular signals essential for the acquisition of SE. Moreover, the regulatory sequences of SERK genes are evolved with unique cellular fate deciding AP2-like ethylene responsive transcription factor AINTEGUMENTA binding sites for their spatial expression in SE. Based on these analyses we suggest future avenues of research that may be imperative for elucidating the importance of SERK gene evolution in SE.

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Pandey, D. and Chaudhary, B. (2014) Role of Plant Somatic Embryogenesis Receptor Kinases (SERKs) in Cell-to-Embryo Transitional Activity: Key at Novel Assorted Structural Subunits. American Journal of Plant Sciences, 5, 3177-3193. doi: 10.4236/ajps.2014.521334.


[1] Gray, D., Compton, M., Harrell, R. and Cantliffe, D. (1995) Somatic Embryogenesis and the Technology of Synthetic Seed. In: Bajaj, Y., Ed., Somatic Embryogenesis and Synthetic Seed I. Biotechnology in Agriculture and Forestry, Vol. 30, Springer-Verlag, Berlin, 126-151.
[2] Toonen, M. and De Vries, S. (1996) Initiation of Somatic Embryos from Single Cells. In: Wang T. and Cuming, A., Eds., Embryogenesis: The Generation of a Plant, Bios Scientific Publishers, Oxford, 173-189.
[3] Kawahara, R. and Komamine, A. (1995) Molecular Basis of Somatic Embryogenesis. In: Bajaj, Y., Ed., Biotechnology in Agriculture and Forestry, Somatic Embryogenesis and Synthetic Seed, Vol. 30, Springer-Verlag, Berlin, 30-40.
[4] Arnold, S., Sabala, I., Bozhkov, P., Dyachok, J. and Filonova, L. (2002) Developmental Pathways of Somatic Embryogenesis. Plant Cell, Tissue and Organ Culture, 69, 233-249.
[5] Jimenez, V. (2001) Regulation of in Vitro Somatic Embryogenesis with Emphasis on to the Role of Endogenous Hormones. Revista Brasileira De Fisiologia Vegetal, 13, 196-223.
[6] Chugh, A. and Khurana, P. (2002) Gene Expression during Somatic Embryogenesis—Recent Advances. Current Science, 86, 715-730.
[7] Zavattieri, M., Frederico, A., Lima, M., Sabino, R. and Arnholdt-Schmitt, B. (2010) Induction of Somatic Embryogenesis as an Example of Stress-Related Plant Reactions. Electronic Journal of Biotechnology, 13.
[8] Dudits, D., Bogre, L. and Gyorgyey, J. (1991) Molecular and Cellular Approaches to the Analysis of Plant Embryo Development from Somatic Cells in Vitro. Journal of Cell Science, 99, 473-482.
[9] Dudits, D., Györgyey, J., Bögre, L. and Bakó, L. (1995) Molecular Biology of Somatic Embryogenesis. In: Thorpe, T., Ed., In Vitro Embryogenesis in Plants, Kluwer Academic Publishers, Dordrecht, 267-308.
[10] Faure, O., Dewitte, W., Nougarède, A. and Van Onckelen, H. (1998) Precociously Germinating Somatic Embryos of Vitis vinifera Have Lower ABA and IAA Levels than Their Germinating Zygotic Counterparts. Physiologia Plantarum, 102, 591-595.
[11] Ikeda-Iwai, M., Umehara, M., Satoh, S. and Kamada, H. (2003) Stress-Induced Somatic Embryogenesis in Vegetative Tissues of Arabidopsis thaliana. The Plant Journal, 34, 107-114.
[12] Kamada, H., Kobayashi, K., Kiyosue, T. and Harada, H. (1989) Stress Induced Somatic Embryogenesis in Carrot and Its Application to Synthetic Seed Production. In Vitro Cellular & Developmental Biology, 25, 1163-1166.
[13] Davletova, S., Meszaros, T., Mészáros, P., Oberschal, A., Török, K., Magyar, Z., Dudits, D. and Deák, M. (2001) Auxin and Heat Shock Activation of a Novel Member of the Calmodulin Like Domain Protein Kinase Gene Family in Cultured Alfalfa Cells. Journal of Experimental Botany, 52, 215-221.
[14] Györgyey, J., Gartner, A., Magyar, Z., Hirt, H., Heberle-Bors, E. and Dudits, D. (1991) Alfalfa Heat Shock Genes Are Differentially Expressed during Somatic Embryogenesis. Plant Molecular Biology, 16, 999-1007.
[15] Pandey, D.K., Singh, A. and Chaudhary, B. (2012) Boron-Mediated Plant Somatic Embryogenesis: A Provocative Model. Journal of Botany, 2012, Article ID: 375829.
[16] Fujimura, T. and Komamine, A. (1980) Mode of Action of 2,4-D and Zeatin on Somatic Embryogenesis in a Carrot Cell Suspension Culture. Zeitschrift für Pflanzenphysiologie, 99, 1-8.
[17] Saze, H., Scheid, O. and Paszkowski, J. (2003) Maintenance of CpG Methylation Is Essential for Epigenetic Inheritance during Plant Gametogenesis. Nature Genetics, 34, 65-69.
[18] Schmidt, E., Guzzo, F., Toonen, M. and de Vries, S. (1997) A Leucine-Rich Repeat Containing Receptor-Like Kinase marks Somatic Plant Cells Competent to Form Embryos. Development, 124, 2049-2062.
[19] Hecht, V., Vielle-Calzada, J., Hartog, M., Schmidt, E., Boutilier, K., Grossniklaus, U. and de Vries, S. (2001) The Arabidopsis Somatic Embryogenesis Receptor Kinase1 Gene Is Expressed in Developing Ovules and Embryos and Enhances Embryogenic Competence in Culture. Plant Physiology, 127, 803-816.
[20] Baudino, S., Brettschneider, R., Hecht, V., Dresselhaus, T., Lörz, H., Dumas, C. and Rogowsky, P. (2001) Molecular Characterization of Novel Maize LRR Receptor-Like Kinases, Which Belong to the SERK Family. Planta, 213, 1-10.
[21] Pérez-Núñez, M., Souza, R., Sáenz, L., Chan, J., Zúñiga-Aguilar, J. and Oropeza, C. (2009) Detection of a SERK-Like Gene in Coconut in Vitro Cultures and Analysis of Its Expression during the Formation of Embryogenic Callus and Somatic Embryos. Plant Cell Reports, 28, 11-19.
[22] Shimada, T., Hirabayashi, T., Fujii, H., Kita, M. and Omura, M. (2005) Isolation and Characterization of the Somatic Embryogenesis Receptor-Like Kinase Gene Homologue (CitSERK) from Cirus unshiu. Marc. Scientia Horticulturae, 103, 233-238.
[23] Somleva, M., Schmidt, E. and de Vries, S. (2000) Embryogenic Cells in Dactylis glomerata L. (Poaceae) Explants Identified by Cell Tracking and by SERK Expression. Plant Cell Reports, 19, 718-726.
[24] Thomas, C., Meyer, D., Himber, C. and Steinmetz, A. (2004) Spatial Expression of a Sunflower SERK Gene during Induction of Somatic Embryogenesis and Shoot Organogenesis. Plant Physiology and Biochemistry, 42, 35-42.
[25] Nolan, K., Irwanto, R.R. and Rose, R.J. (2003) Auxin Up-Regulates MtSERK1 Expression in Both Medicago truncatula Root-Forming and Embryogenic Cultures. Plant Physiology, 133, 218-230.
[26] Hu, H., Xiong, L. and Yang, Y. (2005) Rice SERK1 Gene Positively Regulates Somatic Embryogenesis of Cultured Cell and Host Defense Response against Fungal Infection. Planta, 222, 107-117.
[27] Sharma, S., Millam, S., Hein, I. and Bryan, G. (2008) Cloning and Molecular Characterisation of a Potato SERK Gene Transcriptionally Induced during Initiation of Somatic Embryogenesis. Planta, 228, 319-330.
[28] Santos, M., Romano, E., Yotoko, K., Tinoco, M., Dias, B. and Argao, F. (2005) Characterisation of the Cacao Somatic Embryogenesis Receptor-Like Kinase (SERK) Gene Expressed during Somatic Embryogenesis. Plant Science, 168, 723-729.
[29] Singla, B., Khurana, J. and Khurana, P. (2008) Charecterization of Three Somatic Embryogenesis Receptor Kinase Genes from Wheat, Triticum aestivum. Plant Cell Reports, 27, 833-843.
[30] Maillot, P., Lebel, S., Schellenbaum, P., Jacques, A. and Walter, B. (2009) Differential Regulation of SERK, LEC1-Like and Pathogenesis-Related Genes during Indirect Secondary Somatic Embryogenesis in Grapevine. Plant Physiology and Biochemistry, 47, 743-752.
[31] Albrecht, C., Russinova, E., Kemmerling, B., Kwaaitaal, M. and de Vries, S. (2008) Arabidopsis Somatic Embryogenesis Receptor Kinase Protein Serves Brassinosteroid-Dependent and Independent Signalling Pathway. Plant Physiology, 148, 611-619.
[32] Braybrook, S., Stone, S., Park, S., Bui, A., Le, B., Fischer, R., Goldberg, R. and Harada, J. (2006) Genes Directly Regulated by LEAFY COTYLEDON2 Provide Insight into the Control of Embryo Maturation and Somatic Embryogenesis. Proceedings of the National Academy of Sciences of the United States of America, 103, 3468-3473.
[33] Casson, S., Spencer, M., Walker, K. and Lindsey, K. (2005) Laser Capture Microdissection for the Analysis of Gene Expression during Embryogenesis of Arabidopsis. The Plant Journal, 42, 111-123.
[34] Heidmann, I., Lambalk, J., Joosen, R., Angenent, G., Custers, J. and Boutilier, K. (2006) Expression of BABY BOOM Induces Somatic Embryogenesis in Tobacco. International Conference “Haploids in Higher Plants III”, Vienna, 52, 12-15.
[35] Ikeda, M., Umehara, M. and Kamada, H. (2006) Embryogenesis-Related Genes; Its Expression and Roles during Somatic and Zygotic Embryogenesis in Carrot and Arabidopsis. Plant Biotechnology, 23, 153-161.
[36] Nolan, K.E., Kurdyukov, S. and Rose, R.J. (2009) Expression of the SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 (SERK1) Gene Is Associated with Developmental Change in the Life Cycle of the Model Legume Medicago truncatula. Journal of Experimental Botany, 60, 1759-1771.
[37] Passarinho, P., Ketelaar, T., Xing, M., Van Arkel, J., Maliepaard, C., Hendriks, M., Joosen, R., Lammers, M., Herdies, L., Boer, B., Van Der Geest, L. and Boutilier, K. (2008) BABY BOOM Target Genes Provide Diverse Entry Points into Cell Proliferation and Cell Growth Pathways. Plant Molecular Biology, 68, 225-237.
[38] Zhenga, Y., Renb, N., Wanga, H., Strombergb, A.J. and Perrya, S.E. (2009) Global Identification of Targets of the Arabidopsis MADS Domain Protein AGAMOUS-Like15. The Plant Cell, 21, 2563-2577.
[39] Shi, Y.L., Zhang, R., Wu, X.P., Meng, Z.G. and Guo, S. (2012) Cloning and Characterization of a Somatic Embryogenesis Receptor-Like Kinase Gene in Cotton (Gossypium hirsutum). Journal of Integrative Agriculture, 11, 898-909.
[40] Käll, L., Krogh, A. and Sonnhammer, E. (2004) A Combined Transmembrane Topology and Signal Peptide Prediction Method. Journal of Integrative Agriculture, 338, 1027-1036.
[41] Dinkel, H., Michael, S., Weatheritt, R.J., Davey, N.E., Van Roey, K., Altenberg, B., et al. (2012) ELM—The Database of Eukaryotic Linear Motifs. Nucleic Acids Research, 40, D242-D251.
[42] Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J., Guindon, S., Lefort, V., Lescot, M., Claverie, J. and Gascuel, O. (2008) Robust Phylogenetic Analysis for the Non-Specialist. Nucleic Acids Research, 36, W465-W469.
[43] Kumar, S., Sharma, P. and Pental, D. (1998) A Genetic Approach to in Vitro Regeneration of Non-Regenerating Cotton (Gossypium hirsutum L.) Cultivars. Plant Cell Reports, 18, 59-63.
[44] Hemphill, J., Maier, C. and Chapman, K. (1998) Rapid in-Vitro Plant Regeneration of Cotton (Gossypium hirsutum L.). Plant Cell Reports, 17, 273-278.
[45] Dosztányi, Z., Csizmók, V., Tompa, P. and Simon, I. (2005) IUPred: Web Server for the Prediction of Intrinsically Unstructured Regions of Proteins Based on Estimated Energy Content. Bioinformatics, 21, 3433-3434.
[46] Dosztányi, Z., Csizmók, V., Tompa, P. and Simon, I. (2005) The Pairwise Energy Content Estimated from Amino Acid Composition Discriminates between Folded and Intrinsically Unstructured Proteins. Journal of Molecular Biology, 347, 827-839.
[47] Albrecht, C., Russinova, E., Hecht, V., Baaijens, E. and de Vries, S. (2005) The Arabidopsis thaliana Somatic Embryogenesis Receptor-Like Kinase1 and 2 Control Male Sporogenesis. The Plant Cell, 17, 3337-3349.
[48] Diella, F., Haslam, N., Chica, C., Budd, A., Michael, S., Brown, N., Trave, G. and Gibson, T. (2008) Understanding Eukaryotic Linear Motifs and Their Role in Cell Signaling and Regulation. Frontiers in Bioscience, 13, 6580-6603.
[49] Gibson, T. (2009) Cell Regulation: Determined to Signal Discrete Cooperation. Trends in Biochemical Sciences, 34, 471-482.
[50] Davey, N., Van Roey, K., Weatheritt, R., Toedt, G., Uyar, B., Altenberg, B., Budd, A., Diella, F., Dinkel, H. and Gibson, T. (2011) Attributes of Short Linear Motifs. Molecular BioSystems, 8, 268-281.
[51] Bennett, E., Mandel, U., Clausen, H., Gerken, T., Fritz, T. and Tabak, L. (2011) Control of Mucin-Type O-Glycosylation: A Classification of the Polypeptide GalNAc-Transferase Gene Family. Glycobiology, 22, 736-756.
[52] Poon, S., Heath, R. and Clarke, A.E. (2012) A Chimeric Arabinogalactan Protein Promotes Somatic Embryogenesis in Cotton Cell Culture. Plant Physiology, 160, 684-695.
[53] Pandey, D.K. and Chaudhary, B. (2014) Oxidative Stress Responsive SERK1 Gene Directs the Progression of Somatic Embryogenesis in Cotton (Gossypium hirsutum L. cv. Coker 310). American Journal of Plant Sciences, 5, 80-102.
[54] Sickmeier, M., Hamilton, J., LeGall, T., Vacic, V., Cortese, M., Tantos, A., Szabo, B., Tompa, P., Chen, J., Uversky, V., Obradovic, Z. and Dunker, A. (2007) DisProt: The Database of Disordered Proteins. Nucleic Acids Research, 35, D786-D793.
[55] Tompa, P. (2002) Intrinsically Unstructured Proteins. Trends in Biochemical Sciences, 27, 527-533.
[56] Toorn, M., Huijbers, M., de Vries, S. and van Mierlo, C. (2012) The Arabidopsis thaliana SERK1 Kinase Domain Spontaneously Refolds to an Active State in Vitro. PLoS ONE, 7, e50907.
[57] Salaj, J., von Recklinghausen, I., Hecht, V., de Vries, S., Schel, J. and van Lammeren, A. (2008) AtSERK1 Expression Precedes and Coincides with Early Somatic Embryogenesis in Arabidopsis thaliana. Plant Physiology and Biochemistry, 46, 709-714.
[58] Azhakanandam, S., Nole-Wilson, S., Bao, F. and Franks, R. (2008) SEUSS and AINTEGUMENTA Mediate Patterning and Ovule Initiation during Gynoecium Medial Domain Development. Plant Physiology, 146, 1165-1181.
[59] Klucher, K., Chow, H., Reiser, L. and Fischer, R. (1996) The AINTEGUMENTA Gene of Arabidopsis Required for Ovule and Female Gametophyte Development Is Related to the Floral Homeotic Gene APETALA2. The Plant Cell, 8, 137-153.
[60] Mizukami, Y. and Fischer, R. (2000) Plant Organ Size Control: AINTEGUMENTA Regulates Growth and Cell Numbers during Organogenesis. Proceedings of the National Academy of Sciences of the United States of America, 97, 942-947.
[61] Nole-Wilson, S., Tranby, T. and Krizek, B. (2005) AINTEGUMENTA-Like (AIL) Genes Are Expressed in Young Tissues and May Specify Meristematic or Division-Competent States. Plant Molecular Biology, 57, 613-628.
[62] Nissen, P. (1994) Stimulation of Somatic Embryogenesis in Carrot by Ethylene: Effects of Modulators of Ethylene Biosynthesis and Action. Physiologia Plantarum, 92, 397-403.
[63] Reinhardt, D., Mandel, T. and Kuhlemeier, C. (2000) Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs. The Plant Cell, 12, 507-518.
[64] Vernoux, T., Kronenberger, J., Grandjean, O., Laufs, P. and Traas, J. (2000) PIN-FORMED 1 Regulates Cell Fate at the Periphery of the Shoot Apical Meristem. Development, 127, 5157-5165.
[65] Chaudhary, B., Kumar, S., Prasad, K.V.S.K., Oinam, G.S., Burma, P.K. and Pental, D. (2003) Slow Desiccation Leads to High-Frequency Shoot Recovery from Transformed Somatic Embryos of Cotton (Gossypium hirsutum L. cv. Coker 310 FR). Plant Cell Reports, 21, 955-960.
[66] Gou, X., Yin, H., He, K., Du, J., Yi, J., Xu, S., Lin, H., Clouse, S.D. and Li, J. (2012) Genetic Evidence for an Indispensable Role of Somatic Embryogenesis Receptor Kinases in Brassinosteroid Signaling. PLoS Genetics, 8, e1002452.
[67] He, K. (2008) Functional Analyses of Somatic Embryogenesis Receptor-Like Kinase Family in Multiple Signaling Pathways in Arabidopsis. Ph.D. Thesis, The University of Oklahoma, Norman, 143.
[68] Hu, H. and Brown, P.H. (1994) Localization of Boron in Cell Walls of Squash and Tobacco and Its Association with pectin. Plant Physiology, 105, 681-689.
[69] Nolan, K.E., Kurdyukov, S. and Rose, R.J. (2011) Characterisation of the Legume SERK-NIK Gene Superfamily Including Splice Variants: Implications for Development and Defence. BMC Plant Biology, 11, 44.
[70] Santa-Catarina, C., Hanai, L., Dornelas, M., Viana, A. and Floh, E.I.S. (2004) SERK Gene Homolog Expression, Polyamines and Amino Acids Associated with Somatic Embryogenic Competence of Ocotea catharinensis. Plant Cell, Tissue and Organ Culture, 79, 53-61.
[71] Albertini, E., Marconi, G., Reale, L., Barcaccia, G., Porceddu, A., Ferranti, F. and Falcinelli, M. (2005) SERK and APOSTART. Candidate Gene for Apomixis in Poa pratensis. Plant Physiology, 138, 2185-2199.
[72] Talapatra, S., Ghoshal, N. and Raychaudhuri, S.S. (2014) Molecular Characterization, Modeling and Expression Analysis of a Somatic Embryogenesis Receptor Kinase (SERK) Gene in Momordica charantia L. during Somatic Embryogenesis. Plant Cell, Tissue and Organ Culture, 116, 271-283.
[73] Ge, X.X., Fan, G.E., Chai, L.J. and Guo, W.W. (2010) Cloning, Molecular Characterization and Expression Analysis of a SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE Gene (CitSERK1-Like) in Valencia Sweet Orange. Acta Physiologiae Plantarum, 32, 1197-1207.
[74] Yang, C., Zhao, T., Yu, D. and Gai, J. (2011) Isolation and Functional Characterization of a SERK Gene from Soybean (Glycine max (L.) Merr.). Plant Molecular Biology Reporter, 29, 334-344.
[75] Steiner, N., Santa-Catarina, C., Guerra, M.P., Cutri, L., Dornelas, M.C. and Floh, E.I.S. (2012) A Gymnosperm Homolog of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE-1 (SERK1) Is Expressed during Somatic Embryogenesis. Plant Cell, Tissue and Organ Culture, 109, 41-50.
[76] Cueva, A., Concia, L. and Cella, R. (2012) Molecular Characterization of a Cyrtochilum loxense Somatic Embryogenesis Receptor-Like Kinase (SERK) Gene Expressed during Somatic Embryogenesis. Plant Cell Reports, 31, 1129-1139.

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