Skip to main content
Log in

Characterization of leafy cotyledon1-like during embryogenesis in Theobroma cacao L.

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Theobroma cacao L., an economically important crop for developing countries, can be experimentally propagated by somatic embryogenesis. Because of their potential roles in embryogenesis, a gene candidate strategy was initiated to find gene homologues of the members of the leafy cotyledon family of transcription factors. A homologue of the leafy cotyledon1-like gene, that encodes the HAP 3 subunit of the CCAAT box-binding factor, was found in the cocoa genome (TcL1L). The translated peptide shared a high amino acid sequence identity with the homologous genes of Arabidopsis thaliana, Phaseolus coccineus and Helianthus annuus. TcL1L transcripts mainly accumulated in young and immature zygotic embryos, and, to a lesser extent, in young and immature somatic embryos. In situ hybridization specified the localization of the transcripts as being mainly in embryonic cells of young embryos, the meristematic cells of the shoot and root apex of immature embryos, and in the protoderm and epidermis of young and immature embryos, either zygotic or somatic. Non-embryogenic explants did not show TcL1L expression. Ectopic expression of the TcL1L gene could partially rescue the Arabidopsis lec1 mutant phenotype, suggesting a similarity of function in zygotic embryogenesis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

SERK :

Somatic embryogenesis receptor kinase

BBM :

Baby boom

LEC :

Leafy cotyledon

ABI3 :

Abscisic acid insensitive3

SSEE:

Secondary somatic embryogenic explants

VYSE:

Very young somatic embryos

YSE:

Young somatic embryos

NEE:

Non-embryogenic explants

RT:

Reverse transcriptase

PCR:

Polymerase chain reaction

References

  • Alemanno L, Berthouly M, Michaux-Ferrière N (1996) Histology of somatic embryogenesis from floral tissues in Theobroma cacao L. Plant Cell Tissue Organ Cult 46:187–194

    Article  Google Scholar 

  • Alemanno L, Berthouly M, Michaux-Ferrière N (1997) A comparison between Theobroma cacao L. zygotic and somatic embryogenesis from floral explants. In Vitro Cell Dev Biol Plant 33:163–172

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bennett AB (2003) Out of the Amazon: Theobroma cacao enters the genomic era. Trends Plant Sci 8:561–563

    Article  PubMed  CAS  Google Scholar 

  • Bolognese F, Imbriano C, Caretti G, Mantovani R (2000) Cloning and characterization of the histone-fold proteins YBL1 and YCL1. Nucleic Acids Res 28:3830–3838

    Article  PubMed  CAS  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C-M, van Lammeren AM, Miki BLA, Custers 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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Esan EB (1974) Development of adventive embryos from immature embryos of Theobroma cacao L. culture in vitro 10th annual conference of Agricultural Society Nigeria 43

  • Eskes B (2000) Introductary notes. International workshop on new technologies and cocoa breeding. Kota Kinabalu, Malaysia, pp 8–11

    Google Scholar 

  • Fambrini M, Durante C, Cionini G, Geri C, Giorgetti L, Michelotti V, Salvini M, Pugliesi C (2006) Characterization of LEAFY COTYLEDON1-LIKE gene in Helianthus annuus and its relationship with zygotic and somatic embryogenesis. Dev Genes Evol 216:253–264

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Figueira A, Alemanno L (2004) Theobroma cacao. In: Litz RE (ed) Biotechnology of fruit and nut crops 29:639–669

  • Finkelstein RR, Lynch TJ (2000) The Arabidopsis Abscisic Acid Response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–610

    Article  PubMed  CAS  Google Scholar 

  • Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis Abscisic Acid Response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 22:977–988

    Article  CAS  Google Scholar 

  • Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7:373–385

    Article  PubMed  CAS  Google Scholar 

  • Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261

    Article  PubMed  CAS  Google Scholar 

  • Harada JJ (2001) Role of Arabidopsis LEAFY COTYLEDON genes in seed development. J Plant Physiol 158:405–409

    Article  CAS  Google Scholar 

  • Hecht V, Vielle-Calzada J-P, Hartog MV, Schmidt DL, 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  CAS  Google Scholar 

  • Irizarry H, Rivera E (1998) Early yield of five cacao families at three locations in Puerto Rico. J Agric 82:163–171

    Google Scholar 

  • Jones PG, Allaway D, Gilmour MD, Harris C, Rankin D, Retzel ER, Jones CA (2002) Gene discovery and microarray analysis of cacao (Theobroma cacao L.) varieties. Planta 216:255–264

    Article  PubMed  CAS  Google Scholar 

  • Karimi M, Inzé D, Depicker A (2002) Gateway vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  PubMed  CAS  Google Scholar 

  • Karlova R, Boeren S, Russinova E, Aker J, Vervoort J, de Vries S (2006) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE1 protein complex includes BRASSINOSTEROID-INSENSITIVE1. Plant Cell 18:626–638

    Article  PubMed  CAS  Google Scholar 

  • Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, Hattori T (2005) LEAFY COTYLEDON1 controls Seed Storage Protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46:399–406

    Article  PubMed  CAS  Google Scholar 

  • Kuhn DN, Heath M, Wisser RJ, Meerow A, Brown JS, Lopes U, Schnell RJ (2003) Resistance gene homologues in Theobroma cacao as useful genetic markers. Theor Appl Genet 107:191–202

    Article  PubMed  CAS  Google Scholar 

  • Kwong RW, Bui AQ, Lee H, Kwong LW, Fischer RL, Goldberg RB, Harada JJ (2003) LEAFY COTYLEDON1-LIKE defines a class of regulators essential for embryo development. Plant Cell 15:5–18

    Article  PubMed  CAS  Google Scholar 

  • Lee H, Fischer RL, Goldberg RB, Harada JJ (2003) Arabidopsis LEAFY COTYLEDON1 represents a functionally specialized subunit of the CCAAT binding transcription factor. Proc Natl Acad Sci USA 100:2152–2156

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Traore A, Maximova S, Guiltinan M (1998) Somatic embryogenesis and plant regeneration from floral explants of cacao (Theobroma cacao L.) using thidiazuron. In Vitro Cell Dev Biol Plant 34:293–299

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maximova NS, Alemanno L, Young A, Ferrière N, Traore A, Guiltinan MJ (2002) Efficiency, genotypic variability and cellular origin of primary and secondary somatic embryogenesis of Theobroma cacao L. In Vitro Cell Dev Biol Plant 38:252–259

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Parcy F, Valon C, Kohara A, Misera S, Giraudat J (1997) The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 9:1265–1277

    Article  PubMed  CAS  Google Scholar 

  • Risterucci AM, Grivet L, N’Goran JKA, Pieretti I, Flament MH, Lanaud C (2000) A high density linkage map of Theobroma cacao L. Theor Appl Genet 101:948–955

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sinha S, Kim IS, Sohn KY, de Crombrugghe B, Maity SN (1996) Three classes of mutations in the A subunit of the CAAT-binding factor CBF delineate functional domains involved in the three-step assembly of the CBF-DNA complex. Mol Cell Biol 16:328–337

    PubMed  CAS  Google Scholar 

  • Somleva MN, Schmidt ED, de Vries SC (2000) Embryogenic cells in Dactylis glomerata L. (Poaceae) explants identified by cell-tracking and by SERK expression. Plant Cell Rep 19:718–726

    Article  CAS  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 USA 98:11806–11811

    Article  PubMed  CAS  Google Scholar 

  • To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18:1642–1651

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Xing Y, Fikes JD, Guarente L (1993) Mutations in yeast HAP2/HAP3 define a hybrid CCAAT box binding domain. EMBO J 12:4647–4655

    PubMed  CAS  Google Scholar 

  • Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding carrot leafy cotyledon1 and expression analysis during somatic and zygotic embryogenesis. Plant Physiol Biochem 42:215–223

    Article  PubMed  CAS  Google Scholar 

  • Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latche A, Pech J-C, Bouzayen M (1999) Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600

    Article  PubMed  CAS  Google Scholar 

  • Zemzoumi K, Frontini M, Bellorini M, Mantovani R (1999) NF-Y histone fold? 1 helices help impart CCAAT specificity. J Mol Biol 286:327–337

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Wong L, Meng L, Lemaux PG (2002) Similarity of expression patterns of Knotted1 and ZmLEC1 during somatic and zygotic embryogenesis in maize (Zea mays L.). Planta 215:191–194

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Peter Biggins for checking the English and Fabienne Lapeyre-Montes for technical help. Plant Gateway vectors were provided by the Functional Genomics Division of the Department of Plant Systems Biology (VIB-Ghent University).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pascal Montoro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alemanno, L., Devic, M., Niemenak, N. et al. Characterization of leafy cotyledon1-like during embryogenesis in Theobroma cacao L.. Planta 227, 853–866 (2008). https://doi.org/10.1007/s00425-007-0662-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-007-0662-4

Keywords

Navigation