Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor

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Abstract

Background

Theobroma cacao, the chocolate tree, is an important economic crop in East Africa, South East Asia, and South and Central America. Propagation of elite varieties has been achieved through somatic embryogenesis (SE) but low efficiencies and genotype dependence still presents a significant limitation for its propagation at commercial scales. Manipulation of transcription factors has been used to enhance the formation of SEs in several other plant species. This work describes the use of the transcription factor Baby Boom ( BBM) to promote the transition of somatic cacao cells from the vegetative to embryonic state.

Results

An ortholog of the Arabidopsis thaliana BBM gene ( AtBBM) was characterized in T. cacao ( TcBBM). TcBBM expression was observed throughout embryo development and was expressed at higher levels during SE as compared to zygotic embryogenesis (ZE). TcBBM overexpression in A. thaliana and T. cacao led to phenotypes associated with SE that did not require exogenous hormones. While transient ectopic expression of TcBBM provided only moderate enhancements in embryogenic potential, constitutive overexpression dramatically increased SE proliferation but also appeared to inhibit subsequent development.

Conclusion

Our work provides validation that TcBBM is an ortholog to AtBBM and has a specific role in both somatic and zygotic embryogenesis. Furthermore, our studies revealed that TcBBM transcript levels could serve as a biomarker for embryogenesis in cacao tissue. Results from transient expression of TcBBM provide confirmation that transcription factors can be used to enhance SE without compromising plant development and avoiding GMO plant production. This strategy could compliment a hormone-based method of reprogramming somatic cells and lead to more precise manipulation of SE at the regulatory level of transcription factors. The technology would benefit the propagation of elite varieties with low regeneration potential as well as the production of transgenic plants, which similarly requires somatic cell reprogramming.

Electronic supplementary material

The online version of this article (doi:10.1186/s12870-015-0479-4) contains supplementary material, which is available to authorized users.

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Most cited references 28

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The genome of Theobroma cacao.

Xavier Argout, Jérôme Salse, Jean-Marc Aury … (2011)

We sequenced and assembled the draft genome of Theobroma cacao, an economically important tropical-fruit tree crop that is the source of chocolate. This assembly corresponds to 76% of the estimated genome size and contains almost all previously described genes, with 82% of these genes anchored on the 10 T. cacao chromosomes. Analysis of this sequence information highlighted specific expansion of some gene families during evolution, for example, flavonoid-related genes. It also provides a major source of candidate genes for T. cacao improvement. Based on the inferred paleohistory of the T. cacao genome, we propose an evolutionary scenario whereby the ten T. cacao chromosomes were shaped from an ancestor through eleven chromosome fusions.

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A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos.

E. Schmidt, F Guzzo, Hilde Toonen … (1997)

The first somatic single cells of carrot hypocotyl explants having the competence to form embryos in the presence of 2,4-dichlorophenoxyacetic acid (2,4-D) were identified using semi-automatic cell tracking. These competent cells are present as a small subpopulation of enlarged and vacuolated cells derived from cytoplasm-rich and rapidly proliferating non-embryogenic cells that originate from the provascular elements of the hypocotyl. A search for marker genes to monitor the transition of somatic into competent and embryogenic cells in established suspension cell cultures resulted in the identification of a gene transiently expressed in a small subpopulation of the same enlarged single cells that are formed during the initiation of the embryogenic cultures from hypocotyl explants. The predicted amino acid sequence and in vitro kinase assays show that this gene encodes a leucine-rich repeat containing receptor-like kinase protein, designated Somatic Embryogenesis Receptor-like Kinase (SERK). Somatic embryos formed from cells expressing a SERK promoter-luciferase reporter gene. During somatic embryogenesis, SERK expression ceased after the globular stage. In plants, SERK mRNA could only be detected transiently in the zygotic embryo up to the early globular stage but not in unpollinated flowers nor in any other plant tissue. These results suggest that somatic cells competent to form embryos and early globular somatic embryos share a highly specific signal transduction chain with the zygotic embryo from shortly after fertilization to the early globular embryo.

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LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis

Barbara Wójcikowska, Karolina Jaskóła, Przemysław Gąsiorek … (2013)

The LEAFY COTYLEDON2 (LEC2) transcription factor with a plant-specific B3 domain plays a central role in zygotic and somatic embryogenesis (SE). LEC2 overexpression induced in planta leads to spontaneous somatic embryo formation, but impairs the embryogenic response of explants cultured in vitro under auxin treatment. The auxin-related functions of LEC2 appear during SE induction, and the aim of the present study was to gain further insights into this phenomenon. To this end, the effect of LEC2 overexpression on the morphogenic responses of Arabidopsis explants cultured in vitro under different auxin treatments was evaluated. The expression profiles of the auxin biosynthesis genes were analysed in embryogenic cultures with respect to LEC2 activity. The results showed that LEC2 overexpression severely modifies the requirement of cultured explants for an exogenous auxin concentration at a level that is effective in SE induction and suggested an increase in the auxin content in 35S::LEC2-GR transgenic explants. The assumption of an LEC2 promoted increase in endogenous auxin in cultured explants was further supported by the expression profiling of the genes involved in auxin biosynthesis. The analysis indicated that YUCCAs and TAA1, working in the IPA-YUC auxin biosynthesis pathway, are associated with SE induction, and that the expression of three YUCCA genes (YUC1, YUC4 and YUC10) is associated with LEC2 activity. The results also suggest that the IAOx-mediated auxin biosynthesis pathway involving ATR1/MYB34 and CYP79B2 does not seem to be involved in SE induction. We conclude that de novo auxin production via the tryptophan-dependent IPA-YUC auxin biosynthesis pathway is implicated in SE induction, and that LEC2 plays a key role in this mechanism. Electronic supplementary material The online version of this article (doi:10.1007/s00425-013-1892-2) contains supplementary material, which is available to authorized users.

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Author and article information

Contributors

Sergio L Florez: Sergio.florez@curtislab.org

Rachel L Erwin: Rachel.erwin@curtislab.org

Siela N Maximova: snm104@psu.edu

Mark J Guiltinan: mjg9@psu.edu

Wayne R Curtis: wrc2@psu.edu

Journal

Journal ID (nlm-ta): BMC Plant Biol

Journal ID (iso-abbrev): BMC Plant Biol

Title: BMC Plant Biology

Publisher: BioMed Central (London )

ISSN (Electronic): 1471-2229

Publication date (Electronic): 16 May 2015

Publication date PMC-release: 16 May 2015

Publication date Collection: 2015

Volume: 15

Electronic Location Identifier: 121

Affiliations

[ ]Department of Chemical Engineering, The Pennsylvania State University, University Park, PA 16802 USA

[ ]Department of Plant Science and Huck Institute of Life Sciences, The Pennsylvania State University, University Park, PA 16802 USA

Article

Publisher ID: 479

DOI: 10.1186/s12870-015-0479-4

PMC ID: 4449528

PubMed ID: 25976599

SO-VID: f9b65325-eba4-4237-9dbc-7a183db67852

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

History

Date received : 10 October 2014

Date accepted : 23 March 2015

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ScienceOpen disciplines: Plant science & Botany

Keywords: baby boom,somatic embryogenesis,theobroma cacao,cell reprogramming,plant propagation,transient gene expression

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ScienceOpen disciplines: Plant science & Botany

Keywords: baby boom, somatic embryogenesis, theobroma cacao, cell reprogramming, plant propagation, transient gene expression

Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor

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Plant MYBs

Most cited references 28

The genome of Theobroma cacao.

A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos.

LEAFY COTYLEDON2 (LEC2) promotes embryogenic induction in somatic tissues of Arabidopsis, via YUCCA-mediated auxin biosynthesis

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