Skip to main content
SpringerLink
Log in

Histological analysis of somatic embryogenesis in pineapple: AcSERK1 and its expression validation under stress conditions

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Somatic embryogenesis receptor-like kinase (SERK) is a small gene family found in plants. SERK is involved in somatic embryogenesis and can be found in various important signal transduction pathways. Research on SERK found in pineapple (AcSERK1 and AcSERK2) has indicated that these genes could be used as potential marker genes for monitoring the acquisition of embryogenic competence. This experiment was designed to study somatic embryogenesis in pineapple in detail using AcSERK1 as a marker gene. The results showed that somatic embryogenesis in pineapple callus originated from the surface, the inside, and the superficial layer of the callus. Very few parenchyma cells could be converted into competent cells under 2,4-D induction. The competent cells passed through the pro-embryo-protuberance, the pro-embryo, and the early stage globular embryo. The passage of competent cells through these channels formed the globular embryo. AcSERK1 expression was upregulated by jasmonic acid (JA), salicylic acid (SA), injury, and low temperature treatment. The His6-AcSERK1 protein had autophosphorylation activity. These results confirmed that AcSERK1 can be used as a marker gene for the study of embryogenesis and for expression of totipotency in pineapple. The results indicated that AcSERK1 may also play a role in pineapple stress-response signaling. For future studies, the prokaryotically-expressed His6-AcSERK1 protein can be used to examine the receptor-like kinases function of SERK proteins.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

2,4-D:

2,4-dichlorophenoxyacetic acid

BAK1:

BRI1-associated receptor kinase 1

CTAB:

Cetyl trimethyl ammonium bromide

FAA:

Formalin acetic acid

IPTG:

Isopropyl-β-D-thiogalactoside

JA:

Jasmonic acid

RLKs:

Receptor-like kinases

SA:

Salicylic acid

SDS-PAGE:

Sodium dodecyl sulfate polyacrylamide gel electrophoresis

SE:

Somatic embryogenesis

SERK:

Somatic embryogenesis receptor-like kinase

References

  • Baudino S, Hansen S, Brettschneider R, Hecht VFG, Dresselhaus T, Lorz H, Dumas C, Rogowsky PM (2001) Molecular characterisation of two novel maize LRR receptor-like kinases, which belong to the SERK gene family. Planta 213:1–10

    Article  PubMed  Google Scholar 

  • Chen K, Wu HJ, Chen JF, Cheng XF, Jing X, Wang XY (2012) Somatic embryogenesis and mass spectrometric identification of proteins related to somatic embryogenesis in Eruca sativa. Plant Biotechnol Rep 6:113–122

    Article  Google Scholar 

  • Chen XW, Zuo SM, Schwessinger B, Chen M, Canlas PE, Ruan DL, Zhou XG, Wang J, Daudi A, Petzold CJ, Christopher J, Heazlewood JL, Ronald PC (2014) An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol Plant 7:874–892

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, George F, Thomas B (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  PubMed  Google Scholar 

  • Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis Somatic Embryogenesis Receptor Kinases 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361

    Article  PubMed  PubMed Central  Google Scholar 

  • Collins JL (1968) The pineapple. Leonard Hill, London, p 295

    Google Scholar 

  • Fehér A, Pasternak TA, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228

    Article  Google Scholar 

  • Firoozabady E, Heckert M, Gutterson N (2006) Transformation and regeneration of pineapple. Plant Cell Tissue Organ Cult 84:1–16

    Article  Google Scholar 

  • Geldner N, Robatzek S (2008) Plant receptors go endosomal: a moving view on signal transduction. Plant Physiol 147:1565–1574

    Article  PubMed  PubMed Central  Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt EDL, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis Somatic Embryogenesis Receptor kinase 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816

    Article  PubMed  PubMed Central  Google Scholar 

  • Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Julian IS, Scott CP, Jhon PR (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci U S A 104:12217–12222

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu H, Xiong L, Ynag Y (2005) Rice SERK1 gene positively regulates somatic embryogenesis of cultured cell and host defense response against fungal infection. Planta 222:107–117

    Article  PubMed  Google Scholar 

  • Huang X, Lu XY, Zhao JT, Chen JK, Dai XM, Xiao W, Chen YP, Chen YF, Huang XL (2010) MaSERK1 gene expression associated with somatic embryogenic competence and disease resistance response in banana (Musa spp.). Plant Mol Biol Report 28:309–316

    Article  Google Scholar 

  • Ito Y, Takaya K, Kurata N (2005) Expression of SERK family receptor-like protein kinase genes in rice. Biochim Biophys Acta 1730:253–258

    Article  PubMed  Google Scholar 

  • Karlova R, Boeren S, van Dongen W, Kwaaitaal M, Aker J, Vervoort J, de Vries S (2009) Identification of in vitro phosphorylation sites in the Arabidopsis thaliana somatic embryogenesis receptor-like kinases. Proteomics 9:368–379

    Article  PubMed  Google Scholar 

  • Komamine A, Murata N, Nomura K (2005) Mechanisms of somatic embryogenesis in carrot suspension cultures- morphology, physiology, biochemistry, and molecular biology. In Vitro Cell Dev Biol Plant 41:6–10

    Article  Google Scholar 

  • Lan JB, Yu RC, Yu YY, Fan YP (2013) Molecular cloning and expression of Hedychium coronarium farnesyl pyrophosphate synthase gene and its possible involvement in the biosynthesis of floral and wounding/herbivory induced leaf volatile sesquiterpenoids. Gene 518:360–367

    Article  PubMed  Google Scholar 

  • Li HL, Wang Y, Guo D, Tian WM, Peng SQ (2011) Three MADS-box genes of Heveabrasiliensis expressed during somatic embryogenesis and in the laticifer cells. Mol Biol Rep 38:4045–4052

    Article  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△Ct method. Methods 25:402–408

    Article  PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MAL, Lo RK, Wong RW, Yamaqishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis Leafy cotyledon 1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  PubMed  Google Scholar 

  • Ma J, He YH, Wu CH, Liu HP, Hu ZY, Shun GM (2012) Cloning and molecular characterization of a SERK gene transcriptionally induced during somatic embryogenesis in Ananas comosus. cv. Shenwan. Plant Mol Biol 30:195–203

    Article  Google Scholar 

  • Ma J, He YH, Hu ZY, Xu WT, Guo CH, Wu CH, Lin SQ, Chen CJ, Zhang JL (2014) Characterization of the third SERK gene in pineapple (Ananas comosus) and analysis of its expression and autophosphorylation activity in vitro. Genet Mol Biol 37(4):530–539

    Article  PubMed  PubMed Central  Google Scholar 

  • Nolan KE, Irwanto RR, Rose RJ (2003) Auxin up-regulates MtSERK1 expression in both Medicago truncatula root-forming and embryogenic cultures. Plant Physiol 133:218–230

    Article  PubMed  PubMed Central  Google Scholar 

  • Nühse TS, Stensballe A, Jensen ON, Peck SC (2004) Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell 16:2394–2405

    Article  PubMed  PubMed Central  Google Scholar 

  • Pérez-Núñez MT, Souza R, Sáenz L, Chan JL, Zúñiga-Aguilar JJ, Oropeza C (2009) Detection of a SERK-like gene in cocnut and analysis of its expression during the formation of embryogenic callus and somatic embryos. Plant Cell Rep 28:11–19

    Article  PubMed  Google Scholar 

  • Podio M, Felitti SA, Siena LA, Delgado L, Mancini M, Seijo JG, González AM, Pessino SC, Ortiz JPA (2014) Characterization and expression anlysis of SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) genes in sexual and apomictic Paspalum notatum. Plant Mol Biol 84:479–495

  • Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Gene Dev 16:1139–1149

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanjeev KS, Steve M, Ingo H, Glenn JB (2008) Cloning and molecular characterisation of a potato SERK gene transcriptionally induced during initiation of somatic embryogenesis. Planta 228:319–330

    Article  Google Scholar 

  • Santos MO, Romano E, Vieira LS, Baldoni AB, Aragao FJL (2009) Suppression of SERK gene expression affects fungus tolerance and somatic embryogenesis in transgenic lettuce. Plant Biol 11:83–89

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Schmidt EDL, Guzzo F, Toonen MAJ, de Vries SC (1997) A leucine rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062

    PubMed  Google Scholar 

  • Shah K, Vervoort J, de Vries SC (2001) Role of threonines in Arabidopsis thaliana somatic embryogenesis receptor kinase 1 activation loop in phopsphorylation. J Biol Chem 276:41263–41269

    Article  PubMed  Google Scholar 

  • Shi YL, Guo SD, Zhang R, Meng ZG, Ren MZ (2014) The role of somatic embryogenesis receptor-like kinase 1 in controlling pollen production of the Gossypium anther. Mol Biol Rep 41:411–422

    Article  PubMed  Google Scholar 

  • Silva AT, Barduche D, do Livramento KG, Ligterink W, Paiva LV (2014) Characterization of a putative Serk-like ortholog in embryogenic cell suspension cultures of Coffea Arabica L. Plant Mol Biol Report 32:176–184

    Article  Google Scholar 

  • Singla B, Khurana JP, Khurana P (2008) Characterization of three somatic embryogenesis genes from wheat, triticumaestivum. Plant Cell Rep 27:833–843

    Article  PubMed  Google Scholar 

  • Song DH, Li GJ, Song FM, Zheng Z (2008) Molecular characterization and expression analysis of OsBISERK1, a gene encoding a leucine-rich repeat receptor-like kinase, during disease resistance responses in rice. Mol Biol Rep 35:275–283

    Article  PubMed  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) Leafy Cotyledon 2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci U S A 98:11806–11811

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun GM (2011) Pineapple production and research in China. Acta Horticult 902:79–85

    Article  Google Scholar 

  • Talapatra S, Ghoshal N, Raychaudhuri SS (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 Organ Cult 116:271–283

    Article  Google Scholar 

  • Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95:15107–15111

    Article  PubMed  PubMed Central  Google Scholar 

  • Toonen MAJ, Hendriks T, Schmidt EDL, Verhoeven HA, de Vries SC (1994) Description of somatic-embryo-forming single cells in carrot suspension cultures employing video cell tracking. Planta 194:565–572

    Article  Google Scholar 

  • Umehara M, Kamada H (2005) Development of the embryo proper and the suspensor during plant embryogenesis. Plant Biotechnol 22:253–260

    Article  Google Scholar 

  • Verdeil JL, Alemann L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:243–252

    Article  Google Scholar 

  • Wang X, Goshe MB, Soderblom EJ, Phinney BS, Kuchar JA, Li J, Asami T, Yoshida S, Huber SC, Clouse SD (2005) Identification and functional analysis of in vivo phosphorylation sites of the Arabidopsis Brassinosteroid-Insensitive 1 receptor kinase. Plant Cell 17:1685–1703

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Parniske M (2005) Regulation of plant symbiosis receptor kinase through serine and threonine phosphorylation. J Biol Chem 280:9203–9209

    Article  PubMed  Google Scholar 

  • Yue YC, Yu RC, Fan YP (2014) Characterization of two monoterpene synthases involved in floral scent formation in Hedychium coronarium. Planta 240:745–762

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Natural Science Foundation of China (30971984), Project 948 of Ministry of Agriculture (2010-G2-11), Commonweal Industry Scientific Research Project of Ministry of Agriculture (nyhyzx201203021), and Open Found Project of Key Laboratory of Utilization of Tropical Crop Germplasm Resources, Ministry of Agriculture (KFKT-2010-07).

Conflict of interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

Author information

Authors and Affiliations

  1. College of Landscape Architecture of Sichuan Agricultural University, Chengdu, Sichuan, 611100, China

    J. Ma & J. L. Zhang

  2. Horticultural Biotechnology College of South China Agricultural University, Guangzhou, Guangdong, 510642, China

    J. Ma, Y. H. He, Z. Y. Hu, W. T. Xu, J. X. Xia, C. H. Guo, S. Q. Lin, C. J. Chen & C. H. Wu

  3. Institute of Plant Protection, Agricultural Research Organization, The Volcani Center, Beit Dagan, 50250, Israel

    S. Kanakala

Authors
  1. J. Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Y. H. He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. Y. Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Kanakala
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. W. T. Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. X. Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. C. H. Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Q. Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. C. J. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. C. H. Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. J. L. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Y. H. He.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, J., He, Y.H., Hu, Z.Y. et al. Histological analysis of somatic embryogenesis in pineapple: AcSERK1 and its expression validation under stress conditions. J. Plant Biochem. Biotechnol. 25, 49–55 (2016). https://doi.org/10.1007/s13562-015-0308-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-015-0308-8

Keywords

Search

Navigation