Characterization of GhSERK2 and its expression associated with somatic embryogenesis and hormones level in Upland cotton

doi:10.1016/S2095-3119(17)61726-X

摘要/Abstract

Abstract: Somatic embryogenesis (SE) is one of the most important steps during regeneration of cotton, but the molecular mechanism of SE remains unclear. SOMATIC EMBRYOGENSIS RECEPTOR KINASE (SERK) gene is known to function in SE. A homolog GhSERK2 (accession number: JF430801) was cloned from Upland cotton and characterized for its functions in SE. GhSERK2 expressed in different tissues and showed higher expression level in floral organs than vegetative ones with the highest levels in ovule and anther. GhSERK2 expressed during SE with a high level at globular embryos stage. Upon treatment with indole-3-butytic acid (IBA), the transcription level of GhSERK2 was induced and promoted SE subsequently. A 2-day treatment of 2,4-dichlorophenoxyacetic acid (2,4-D) induced the expression of GhSERK2, but treatments of 2,4-D for longer periods sharply inhibited the GhSERK2 transcription level of embryogenic callus (EC). The levels of hormones, including 3-indoleacetic acid (IAA), abscisic acid (ABA), and brassinosteroid (BR), were increased in the initial calli induced from the over-expression of GhSERK2 cotton. Our results indicated that GhSERK2 expression was associated with induction of SE and closely related to hormone levels during tissue culture in Upland cotton, and the gene might play an important role in regeneration of cotton.

Key words: GhSERK2 , somatic embryogenesis , hormone level , expression pattern , Upland cotton (Gossypium hirsutum L.)

. [J]. Journal of Integrative Agriculture, 2018, 17(03): 517-529.

LIU Zheng-jie, ZHAO Yan-peng, ZENG Ling-he, ZHANG Yuan, WANG Yu-mei, HUA Jin-ping. Characterization of GhSERK2 and its expression associated with somatic embryogenesis and hormones level in Upland cotton[J]. Journal of Integrative Agriculture, 2018, 17(03): 517-529.

参考文献

Ahmadi B, Masoomi-Aladizgeh F, Shariatpanahi M E. 2016. Molecular characterization and expression analysis of SERK1 and SERK2 in Brassica napus L.: implication for microspore embryogenesis and plant regeneration. Plant Cell Reports, 35, 185–193.

Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S. 2005. The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. The Plant Cell, 17, 3337–3349.

Baudino S, Hansen S, Brettschneider R, Hecht V R G, Dresselhaus T, Lorz H, Dumas C, Rogowsky P M. 2001. Molecular characterization of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta, 213, 1–10.

Becraft P W. 2002. Receptor kinase signaling in plant development. Annual Review of Cell and Developmental Biology, 18, 163–192.

Bhumica S, Jitendra P K, Paramjit K. 2008. Characterization of three somatic embryogenesis receptor kinase genes from wheat, Triticum aestivum. Plant Cell Reports, 27, 833–843.

Boutilier K, Offringa R, Sharma V K, Kieft H, Ouellet T, Zhang L M, Hattori J, Liu C M, van Lammeren A A M, Miki B L A, Custers J B M, Campagne M M V. 2002. Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. The Plant Cell, 14, 1737–1749.

Che P, Love T M, Frame B R, Wang K, Carriquiry A L, Howell S H. 2006. Gene expression patterns during somatic embryo development and germination in maize Hi II callus cultures. Plant Molecular Biology, 62, 1–14.

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, 1129–1139.

Davidonis G H, Hamilton R H. 1983. Plant regeneration from callus tissue of Gossypium hirsutum L. Plant Science, 32, 89–93.

Deng A, Tan W, He S, Liu W, Nan T, Li Z, Wang B, Li Q X. 2008. Monoclonal antibody-based enzyme linked immunosorbent assay for the analysis of jasmonates in plants. Journal of Integrative Plant Biology, 50, 1046–1052.

Fraga H P, Vieira L D, Puttkammer C C, Dos Santos H P, Garighan J A, Guerra M P. 2016. Glutathione and abscisic acid supplementation influences somatic embryo maturation and hormone endogenous levels during somatic embryogenesis in Podocarpus lambertii Klotzsch ex Endl. Plant Science, 253, 98–106.

Hecht V, Vielle-Calzada J P, Hartog M V, Schmidt E D L, 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, 803–816.

Hedayat Z, Bjarne M S, Henrik L, Renate M. 2010. Isolation and characterization of four somatic embryogenesis receptor-like kinase (RhSERK) genes from miniature potted rose (Rosa hybrida cv. Linda). Plant Cell Tissue and Organ Culture, 101, 331–338.

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, 107–117.

Hu L S, Yang X Y, Yuan D J, Zeng F C, Zhang X L. 2011. GhHmgB3 deficiency deregulates proliferation and differentiation of cells during somatic embryogenesis in cotton. Plant Biotechnology Journal, 9, 1038–1048.

Huang X, Lu X Y, Zhao J T, Chen J K, Dai X M, Xiao W, Chen Y P, Chen Y F, Huang X L. 2010. MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Molecular Biology Reporter, 28, 309–316.

Jiménez V M, Guevara E, Herrera J, Bangerth F. 2005. Evolution of endogenous hormone concentration in embryogenic cultures of carrot during early expression of somatic embryogenesis. Plant Cell Reports, 23, 567–572.

Kumria R, Sunnichan V G, Das D K, Gupta S K, Reddy V S, Bhatnagar R K, Leelavathi S. 2003. High frequency somatic embryo production and maturation into normal plants in cotton (Gossypium hirsutum) though metabolic stress. Plant Cell Reports, 21, 635–639.

Li J, Wen J, Lease K A, Doke J T, Tax F E, Walker J C. 2002. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell, 110, 213–222.

Li Z Y, Wang Y, Huang J, Ahsan N, Biener G, Paprocki J, Thelen J J, Raicu V, Zhao D Z. 2016. Two SERK receptor-like kinases interact with EMS1 to control anther cell fate determination. Plant Physiology, 173, 326–337.

Liu Z J, Zhang Y, Wang Y X, Li P B, Su Y, Zhang X, Wang Y M, Hua J P. 2011. Construction of seed specific expression vectors and genetic transformation for genes of heteromeric ACCase in Upland cotton. Molecular Plant Breeding, 9, 270–277. (in Chinese)

Lotan T, Ohto M, Yee K M, West M A L, Lo R, Kwong R W, Yamagishi K, Fischer R L, Goldberg R B, Harada J J. 1998. Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell, 93, 1195–1205.

Ma J, He Y H, Hu Z Y, Kanakala S, Xu W T, Xia J X, Guo C H, Lin S Q, Chen C J, Wu C H, Zhang J L. 2016. Histological analysis of somatic embryogenesis in pineapple: AcSERK1 and its expression validation under stress conditions. Journal of Plant Biochemistry and Biotechnology, 25, 49–55.

Ma J, He Y H, Hu Z Y, Xu W T, Xia J X, Guo C H, Lin S Q, Cao L, Chen C J, Wu C H, Zhang J L. 2012a. Characterization and expression analysis of AcSERK2, a somatic embryogenesis and stress resistance related gene in pineapple. Gene, 500, 115–123.

Ma J, He Y H, Wu C G, Liu H P, Hu Z Y, Sun G M. 2012b. Cloning and molecular characterization of a SERK gene transcriptionally induced during somatic embryogenesis in Ananas comosus cv. Shenwan. Plant Molecular Biology Reporter, 30, 195–203.

Mahdavi-Darvari F, Noor N M, Ismanizan I. 2015. Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tissue and Organ Culture, 120, 407–422.

Nolan K E, Kurdyukov S, 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.

Nolan K E, Kurdyukov S, Rose R J. 2011. Characterisation of the legume SERK-NIK gene superfamily including splice variants: implications for development and defence. BMC Plant Biology, 11, 44–60.

Pandey D K, 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.

Paterson A H, Brubaker C L, Wendel J F. 1993. A rapid method for extraction of cotton (Gossypium spp.) genomic DNA suitable for RFLP or PCR analysis. Plant Molecular Biology Reporter, 11, 122–127.

Pérez-Núñez M T, Souza R, Sáenz L. 2009. Detection of a SERK-like gene in coconut and analysis of its expression during the formation of embryogenic callus and somatic embryos. Plant Cell Reports, 28, 11–19.

Qi J N, Yu S C, Zhang F L, Shen X Q, Zhao X Y, Yu Y J, Zhang D S. 2010. Reference gene selection for real-time quantitative polymerase chain reaction of mRNA transcript levels in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Molecular Biology Reporter, 28, 597–604.

Rajesh M K, Fayas T P, Naganeeswaran S, Rachana K E, Bhavyashree U, Sajini K K, Karun A. 2016. De novo assembly and characterization of global transcriptome of coconut palm (Cocos nucifera L.) embryogenic calli using Illumina paired-end sequencing. Protoplasma, 253, 913–928.

Rocha D I, Monte-Bello C C, Aizza L C B, Dornelas M C. 2016. A passion fruit putative ortholog of the SOMATIC EMBRYOGENESIS RECEPTOR KINASE1 gene is expressed throughout the in vitro de novo shoot organogenesis developmental program. Plant Cell Tissue and Organ Culture, 125, 107–117.

Sakhanokho H F, Zipf A, Rajasekaran K, Sukumar S, Govind C S. 2001. Induction of highly embryogenic calluses and plant regeneration in Upland (Gossypium hirsutum L.) and pima (Gossypium barbadense L.) cottons. Crop Science, 41, 1235–1240.

Santa-Catarina C, Hanai L R, Dornelas M C, Viana A M, Floh E I S. 2004. SERK gene homolog expression, polyamines and amino acids associated with somatic embryogenic competence of Ocotea catharinensis Mez. (Lauraceae). Plant Cell Tissue and Organ Culture, 79, 53–61.

Santos M O, Romano E, Vieira L S, Baldoni A B, Aragao F G L. 2009. Suppression of SERK gene expression affects fungus tolerance and somatic embryogenesis in transgenic lettuce. Plant Biology, 11, 83–89.

Santos M O, Romano E, Yotoko K S C, Tinoco M L P, Dias B B A, Aragao F J L. 2005. Characterisation of the cacao somatic embryogenesis receptor-like kinase (SERK) gene expressed during somatic embryogenesis. Plant Science, 168, 723–729.

Schellenbaum P, Jacques A, Maillot P, Bertsch C, Mazet F, Farine S, Walter B. 2008. Characterization of VvSERK1, VvSERK2, VvSERK3, and VvL1L genes and their expression during somatic embryogenesis of grapevine (Vitis vinifera L.). Plant Cell Reports, 27, 1799–1809.

Schmidt E D L, Guzzo F, Toonen M A J, deVries S C. 1997. A leucine rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development, 124, 2049–2062.

Sharma S K, Millam S, Hein I, Bryan G J. 2008. Cloning and molecular characterization of a potato SERK gene transcriptionally induced during initiation of somatic embryogenesis. Planta, 228, 319–330.

Shi Y L, Guo S D, Zhang R, Meng Z G, Ren M Z. 2014. The role of Somatic Embryogenesis Receptor-like Kinase 1 in controlling pollen production of the Gossypium anther. Molecular Biology Reports, 41, 411–422.

Shi Y L, Zhang R, Wu X P, Meng Z G, Guo S D. 2012. Cloning and characterization of a Somatic Embryogenesis Receptor-like Kinase gene in cotton (Gossypium hirsutum). Journal of Integrative Agriculture, 11, 898–909.

Somleva M N, Schmidt E D L, de Vries S C. 2000. Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell tracking and by SERK expression. Plant Cell Reports, 19, 718–726.

Srinivas L, Ganapathi T R, Suprasanna P, Bapat V A. 2006. Desiccation and ABA treatment improves conversion of somatic embryos to plantlets in banana (Musa spp.) cv. Rasthali (AAB). Indian Journal of Biotechnology, 5, 521–526.

Steiner N, Santa-Catarina C, Guerra M P, Cutri L, Dornelas M C, 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.

Steward F C, Mapes M O, Mears K. 1958. Growth and organized development of cultured cells: II. Organization in cultures grown from freely suspended cells. American Journal of Botany, 45, 705–708.

Stone J M, Trotochaud A E, Walker J C, Clark S E. 1998. Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interaction. Plant Physiology, 117, 1217–1225.

Stone S L, Kwong L W, Yee K M, Pelletier J, Lepiniec L, Fischer R L, Goldberg R B, Harada J J. 2001. LEAFY COTYLEDON2 encodes B3 domain transcription factor that induces embryo development. Proceedings of the National Academy of Sciences of the United States of America, 98, 11806–11811.

Talapatra S, Ghoshal N, 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.

Thomas C, Meyer D, Himber C, 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.

Walker J C. 1994. Structure and function of the receptor-like protein kinases of higher plants. Plant Molecular Biology, 26, 1599–1609.

Wu X M, Li F G, Zhang C J, Liu C L, Zhang X Y. 2009. Differential gene expression of cotton cultivar CCRI24 during somatic embryogenesis. Journal of Plant Physiology, 166, 1275–1283.

Wu Y, Dor E, Hershenhorn J. 2017. Strigolactones affect tomato hormone profile and somatic embryogenesis. Planta, 245, 583–594.

Yang C, Zhao T J, Yu D Y, Gai J Y. 2011. Isolation and functional characterization of a SERK gene from soybean (Glycine max (L.) Merr.). Plant Molecular Biology Reporter, 29, 334–344.

Yang X Y, Zhang X L. 2010. Regulation of somatic embryogenesis in higher plants. Critical Reviews in Plant Science, 29, 36–57.

Zeng F C, Zhang X L, Zhu L F, Tu L L, Guo X P, Nie Y C. 2006. Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Molecular Biology, 60, 167–183.

Zhang N, Bryant S. 2009. CDD: Specific functional annotation with the Conserved Domain Database. Nucleic Acids Research, 37, 205–210.

Zhang S Z, Liu X, Lin Y, Xie G, Fu F, Liu H, Wang J, Gao S, Lan H, Rong T. 2011. Characterization of a ZmSERK gene and its relationship to somatic embryogenesis in a maize culture. Plant Cell Tissue and Organ Culture, 105, 29–37.

Zhang X, Zhen J B, Li Z H, Kang D M, Yang Y M, Kong J, Hua J P. 2011. Expression profile of early responsive genes under salt stress in upland cotton (Gossypium hirsutum L.). Plant Molecular Biology Reporter, 29, 626–637.

Zuo J, Niu Q W, Frugis G, Chua N H. 2002. The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. The Plant Journal, 30, 349–359.