Skip to main content

Advertisement

SpringerLink
Log in

Overexpression of coconut AINTEGUMENTA-like gene, CnANT, promotes in vitro regeneration in transgenic Arabidopsis

  • Original Paper
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Knowledge of the molecular biological changes underlying the process of embryogenesis is important for the improvement of somatic embryogenesis of coconut. Among the transcription factors that control the transition from vegetative to embryogenic growth, members of APETALA2/Ethylene-responsive element binding protein domain family play an important role in promoting embryo development. Significant insights into the role of AP2 genes have been obtained by the ectopic expression of AP2 sub family genes in transgenic Arabidopsis. A homolog of the AINTEGUMENTA-like gene that encodes the two AP2 domains and the linker region was identified in the coconut genome. Phylogenetic analysis showed that this gene, CnANT, encodes a protein that branched with BABY BOOM/PLETHORA clade in the AINTEGUMENTA-like major clade and was similar to the oil palm EgAP2-1 protein. According to real time RT-PCR results, higher expression of CnANT was observed in more mature zygotic embryos. Also, high CnANT expression was recorded in embryogenic callus compared to other stages of somatic embryogenesis. We examined the effect of ectopic CnANT expression on the development and regenerative capacity of transgenic Arabidopsis. Overexpression of CnANT in Arabidopsis induced hormone free regeneration of explants. Furthermore, ectopic expression of CnANT enhanced regeneration in vitro and suggested a role for this gene in cell proliferation during in vitro culture.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bandupriya HDD, Dunwell JM (2012) Overexpression of CnANT, coconut BABY BOOM homologue alters plant growth and morphology in transgenic Arabidopsis plants. Trop Agric Res 23:249–260

    Google Scholar 

  • Bandupriya HDD, Gibbings JG, Dunwell JM (2013) Isolation and characterization of an AINTEGUMENTA-like gene in different coconut (Cocos nucifera L.) varieties from Sri Lanka. Tree Genet Genomes 9:813–827

    Article  Google Scholar 

  • Banno H, Ikeda Y, Niu Q-W, Chua N-H (2001) Overespression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

    CAS  PubMed Central  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C-M, van Lammeren AAM, Miki BLA, Clusters JBM, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    CAS  PubMed Central  PubMed  Google Scholar 

  • Casson S, Spencer M, Walker K, Lindsey K (2005) Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. Plant J 42:111–123

    Article  CAS  PubMed  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNROSCHEN and DORNROSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 134:1653–1662

    Article  CAS  PubMed  Google Scholar 

  • Che P, Lall S, Nettleton D, Howell SH (2006) Gene expression programs during shoot, root and callus development in Arabidopsis tissue culture. Plant Physiol 141:620–637

    Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Drews GN, Bowman JL, Meyerowitz EM (1991) Negative regulation of the Arabidopsis homeotic gene AGAMOUS by the APETALA2 product. Cell 65:991–1002

    Article  CAS  PubMed  Google Scholar 

  • Eeuwens CJ (1976) Mineral requirements for growth and callus initiation of tissue explants excised from mature coconut (Cocos nucifera) and date (Phoenix dactylifera) palms cultured in vitro. Physiol Plant 36:23–28

    Article  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQJ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALAP-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harding EW, Tang W, Nichols KW, Fernandez DE, Perry SE (2003) Expression and maintenance of embryogenic potential is enhanced through constitutive expression of AGAMOUS-Like 15. Plant Physiol 133:653–663

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Irish VF, Sussex IM (1990) Function of the APETALA1 gene during Arabidopsis floral development. Plant Cell 2:741–753

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jofuku KD, den Boer BGW, van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci USA 102:3117–3122

    Article  CAS  PubMed  Google Scholar 

  • Karunaratne S, Periyapperuma K (1989) Culture of immature embryos of coconut (Cocos nucifera L.): callus proliferation and somatic embryogenesis. Plant Sci 62:247–253

    Article  Google Scholar 

  • Kim S, Soltis PM, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    Article  CAS  PubMed  Google Scholar 

  • Klucher KM (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153

    CAS  PubMed Central  PubMed  Google Scholar 

  • Krizek BA (2003) AINTEGUMENTA utilizes a mode of DNA recognition distinct from that used by proteins containing a single AP2 domain. Nucleic Acids Res 31:1859–1868

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lin R, Zhao W, Meng X, Peng Y-L (2007) Molecular cloning and characterization of rice gene encoding AP2/EREBP-type transcription factor and its expression in response to infection with blast fungus and abiotic stresses. Physiol Mol Plant Pathol 70:60–68

    Article  CAS  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  CAS  PubMed  Google Scholar 

  • Malik MR, Wang F, Dirpaul JM, Zhou N, Polowick PL, Ferrie AMR, Krochko JE (2007) Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol 144:134–154

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mine T, Hiyoshi T, Kasaoka K, Ohyama A (2003) CIP353 encodes an AP2/ERF-domain protein in potato (Solanum tuberosum L.) and responds slowly to cold stress. Plant Cell Physiol 44:10–15

    Article  CAS  PubMed  Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947

    Article  CAS  PubMed  Google Scholar 

  • Montero-Cortes M, Rodrıguez-Paredes F, Burgeff C, Perez-Nunez T, Cordova I, Oropeza C, Verdeil J-L, Saenz L (2010) Characterisation of a cyclin-dependent kinase (CDKA) gene expressed during somatic embryogenesis of coconut palm. Plant Cell Tissue Organ Cult 102:251–258

    Article  CAS  Google Scholar 

  • Morcillo F, Gallard A, Pillot M, Jouannic S, Aberlenc-Bertossi F, Collin M, Verdeil J-L, Tregear JW (2007) EgAP2-1, an AINTEGUMENTA-like (AIL) gene expressed in meristematic and proliferating tissues of embryos in oil palm. Planta 226:1353–1362

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nole-Wilson S, Tranby TL, Kreizek A (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628

    Article  CAS  PubMed  Google Scholar 

  • Ohto M, Fischer RL, Goldberg RB, Nakamura K, Harada JJ (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128

    Article  CAS  PubMed  Google Scholar 

  • Okamuro JK, Caster B, Villarroel R, VanMontagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081

    Article  CAS  PubMed  Google Scholar 

  • Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) BABY BOOM target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68:225–237

    Article  CAS  PubMed  Google Scholar 

  • Perez-Nunez MT, Souza R, Saenz L, Chan JL, Gonzalez T, Zuniga JJ, 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 Rep 28:11–19

    Article  CAS  PubMed  Google Scholar 

  • Rider SD, Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J (2003) Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 35:33–43

    Article  CAS  PubMed Central  Google Scholar 

  • Riechmann JL, Heard J, Martin G, Reuber L, Jiang C-Z, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G-L (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2109

    Article  CAS  PubMed  Google Scholar 

  • Shigyo M, Ito M (2004) Analysis of gymnosperm two-AP2-domain-containing genes. Dev Genes Evol 214:105–114

    Article  CAS  PubMed  Google Scholar 

  • Shigyo M, Hasebe M, Ito M (2006) Molecular evolution of the AP2 subfamily. Gene 366:256–265

    Article  CAS  PubMed  Google Scholar 

  • Shukla R, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from Chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Srinivasan C, Liu Z, Heidmann I, Supena EDJ (2007) Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 225:341–351

    Article  CAS  PubMed  Google Scholar 

  • Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, Fischer RL, Goldberg RB, Harada JJ (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci 98:11806–11811

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Current Protocols Bioinformatics Chapter 2: Unit 2.3

  • Tsuwamoto R, Yokoi S, Takahata Y (2010) Arabidopsis EMBRYOMAKER encoding an AP2 domain transcription factor plays a key role in developmental change from vegetative to embryonic phase. Plant Mol Biol 73:481–492

    Article  CAS  PubMed  Google Scholar 

  • Vergunst AC, de Waal EC, Hooykaas PJJ (1998) Root transformation by Agrobacterium tumefaciens. In: Martinez-Zapater JM, Salinas J (eds) Arabidopsis protocols. Humana Press, Totowa, pp 227–244

    Google Scholar 

  • Weerakoon LK (2008) Report of the tissue culture division. Coconut Research Institute, Sri Lanka, pp 173–183

    Google Scholar 

  • Western TL, Burn J, Tan WL, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol 127:998–1011

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang GY, Chen M, Chen XP, Xu ZS, Guan S, Li LC, Li AL, Guo JM, Mao L, Ma YZ (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Cao G, Qu L-J, Gu H (2009) Involvement of an R2R3-MYB transcription factor gene AtMYB118 in embryogenesis in Arabidopsis. Plant Cell Rep 28:336–347

    CAS  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

The authors are gratefully acknowledged the Tissue Culture Division of the Coconut Research Institute, Sri Lanka for the assistance in providing coconut samples. Authors wish to thank Mr. Prasad Sanjeewa for the extended assistance in improving the quality of the pictures. This project was supported by the Commonwealth Commission of the United Kingdom and the Association of Commonwealth Universities, through the British Council.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Reading, Reading, RG6 6AS, UK

    H. D. Dharshani Bandupriya

  2. Tissue Culture Division, Coconut Research Institute, Lunuwila, 61150, Sri Lanka

    H. D. Dharshani Bandupriya

  3. School of Agriculture, Policy and Development, University of Reading, Reading, RG6 6AR, UK

    J. George Gibbings & Jim M. Dunwell

Authors
  1. H. D. Dharshani Bandupriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. George Gibbings
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jim M. Dunwell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to H. D. Dharshani Bandupriya.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bandupriya, H.D.D., Gibbings, J.G. & Dunwell, J.M. Overexpression of coconut AINTEGUMENTA-like gene, CnANT, promotes in vitro regeneration in transgenic Arabidopsis . Plant Cell Tiss Organ Cult 116, 67–79 (2014). https://doi.org/10.1007/s11240-013-0383-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-013-0383-2

Keywords

Search

Navigation