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Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes

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Key message

The PsASGR - BBML transgene, derived from a wild apomictic grass species, can induce parthenogenesis, embryo formation without fertilization, in rice and maize, leading to the formation of haploid plants.

Abstract

The ability to engineer apomictic crop plants using genes identified from naturally occurring apomicts will depend on the ability of those genes to function in crop plants. The PsASGR-BBML transgene, derived from the apomictic species Pennisetum squamulatum, promotes parthenogenesis in sexual pearl millet, a member of the same genus, leading to the formation of haploid embryos. This study determined that the PsASGR-BBML transgene can induce haploid embryo development in two major monocot crops, maize and rice. Transgene variations tested included two different promoters and the use of both genomic and cDNA PsASGR-BBML-derived sequences. Haploid plants were recovered from mature caryopses (seed) of rice and maize lines at variable rates. The PsASGR-BBML transgenes failed to induce measurable haploid seed development in the model genetic plant system Arabidopsis thaliana. Complexity of embryo development, as documented in transgenic rice lines, identifies the need for further characterization of the PsASGR-BBML gene.

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References

  • Albertsen MC, Chamberlin MA, Fox TW, Lawit SJ, Loveland BR (2013) Compositions and methods for the expression of a sequence in a reproductive tissue of a plant. Publication No. US 2013/0180009 A1

  • Bent A (2006) Arabidopsis thaliana floral dip transformation method. In: Wang K (ed) Agrobacterium protocols, 2nd edn. Humana Press, Totowa, pp 87–103

    Chapter  Google Scholar 

  • Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478

    Article  CAS  PubMed  Google Scholar 

  • Boutilier K et al (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method forAgrobacterium-mediated transformation ofArabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Conner JA, Mookkan M, Huo H, Chae K, Ozias-Akins P (2015) A parthenogenesis gene of apomict origin elicits embryo formation from unfertilized eggs in a sexual plant. Proc Natl Acad Sci 112:11205–11210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durantini D, Giulini A, Malgioglio A, Pilu R, Tuberosa R, Sanguineti C, Gavazzi G (2008) Vivipary as a tool to analyze late embryogenic events in maize. Heredity 101:465–470

    Article  CAS  PubMed  Google Scholar 

  • Eder J, Chalyk S (2002) In vivo haploid induction in maize. Theor Appl Genet 104:703–708

    Article  CAS  PubMed  Google Scholar 

  • El Ouakfaoui S et al (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74:313–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Eyster WH (1931) Vivipary in maize. Genetics 16:574

    CAS  PubMed  PubMed Central  Google Scholar 

  • Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol 15:1

    Article  Google Scholar 

  • Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  CAS  PubMed  Google Scholar 

  • Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25:989–994

    Article  CAS  PubMed  Google Scholar 

  • Hand ML, Koltunow AM (2014) The genetic control of apomixis: asexual seed formation. Genetics 197:441–450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hara T et al (2015) Rice SNF2 family helicase ENL1 is essential for syncytial endosperm development. Plant J 81:1–12

    Article  CAS  PubMed  Google Scholar 

  • Heidmann I, De Lange B, Lambalk J, Angenent GC, Boutilier K (2011) Efficient sweet pepper transformation mediated by the BABY BOOM transcription factor. Plant Cell Rep 30:1107–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horstman A, Willemsen V, Boutilier K, Heidstra R (2014) AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks. Trends Plant Sci 19:146–157

    Article  CAS  PubMed  Google Scholar 

  • Horstman A et al (2015) AIL and HDG proteins act antagonistically to control cell proliferation. Development 142:454–464

    Article  CAS  PubMed  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry: principles and practice. Freeman, San Francisco

  • Joshi PK, Gupta D, Nandal UK, Khan Y, Mukherjee SK, Sanan-Mishra N (2012) Identification of mirtrons in rice using MirtronPred: a tool for predicting plant mirtrons. Genomics 99:370–375

    Article  CAS  PubMed  Google Scholar 

  • Kageyama Y, Fukuoka H, Yamamoto K, Takeda G (1991) The rice plant bearing endospermless grains: a novel mutant induced by gamma-irradiation of tetraploid rice (Oryza sativa L.). Jpn J Breed 41:341–345. doi:10.1270/jsbbs1951.41.341

    Article  Google Scholar 

  • Krizek BA (2015) Intronic sequences are required for AINTEGUMENTA-LIKE6 expression in Arabidopsis flowers. BMC Res Notes 8:1

    Article  Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation—a novel source of variability from cell cultures for plant improvement. Theor Appl Genet 60:197–214

    Article  CAS  PubMed  Google Scholar 

  • Lawit SJ, Chamberlin MA, Agee A, Caswell ES, Albertsen MC (2013) Transgenic manipulation of plant embryo sacs tracked through cell-type-specific fluorescent markers: cell labeling, cell ablation, and adventitious embryos Plant. Reproduction 26:125–137

    Google Scholar 

  • Le BH et al (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci 107:8063–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luehrsen KR, Walbot V (1991) Intron enhancement of gene expression and the splicing efficiency of introns in maize cells. Mol Gen Genet MGG 225:81–93

    Article  CAS  PubMed  Google Scholar 

  • McGinnis K et al (2005) Transgene-induced RNA interference as a tool for plant functional genomics. Methods Enzymol 392:1–24

    Article  CAS  PubMed  Google Scholar 

  • Nanda D, Chase S (1996) An embryo marker for detecting monoploids of maize. Crop Sci 6:213–215

    Article  Google Scholar 

  • Neelakandan AK, Wang K (2012) Recent progress in the understanding of tissue culture-induced genome level changes in plants and potential applications. Plant Cell Rep 31:597–620

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi Y, Hoshino R, Okamoto T (2014) Dynamics of male and female chromatin during karyogamy in rice zygotes. Plant Physiol 165:1533–1543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ozias-Akins P, Roche D, Hanna WW (1998) Tight clustering and hemizygosity of apomixis-linked molecular markers in Pennisetum squamulatum implies genetic control of apospory by a divergent locus that may have no allelic form in sexual genotypes. Proc Natl Acad Sci 95:5127–5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Passarinho P et al (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 

  • Porcar M, Ramos S, Latorre A (2007) A simple DNA extraction method suitable for PCR detection of genetically modified maize. J Sci Food Agric 87:2728–2731

    Article  CAS  PubMed  Google Scholar 

  • Rober F, Gordillo G, Geiger H (2005) In vivo haploid induction in maize-performance of new inducers and significance of doubled haploid lines in hybrid breeding. Maydica 50:275

    Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srinivasan C et al (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 

  • Steffen JG, Kang IH, Macfarlane J, Drews GN (2007) Identification of genes expressed in the Arabidopsis female gametophyte. Plant J 51:281–292

    Article  CAS  PubMed  Google Scholar 

  • Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16:S133–S141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Q-H, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell C (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 18:1456–1465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We are grateful to Rebecca Grantham, Yinping Guo and Greg Thomas for providing technical assistance, especially with genotyping and flow cytometry, and to Tracey Vellidis for figure preparation. This research was funded by a Grant from the National Institute of Food and Agriculture (AFRI Award No. 2015-67030-23494) to JAC and POA and funding through the University of Georgia. MP was supported by a sub-award from the CSIRO under the Capturing Heterosis for Smallholder Farmers grant from the Bill and Melinda Gates Foundation.

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Authors and Affiliations

  1. Department of Horticulture, University of Georgia, Tifton Campus, Tifton, GA, 31793, USA

    Joann A. Conner, Maricel Podio & Peggy Ozias-Akins

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  1. Joann A. Conner
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  2. Maricel Podio
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  3. Peggy Ozias-Akins
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Correspondence to Joann A. Conner.

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Communicated by Thomas Dresselhaus.

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Conner, J.A., Podio, M. & Ozias-Akins, P. Haploid embryo production in rice and maize induced by PsASGR-BBML transgenes. Plant Reprod 30, 41–52 (2017). https://doi.org/10.1007/s00497-017-0298-x

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  • DOI: https://doi.org/10.1007/s00497-017-0298-x

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