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Beyond promiscuity: From sexuality to apomixis in flowering plants

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Summary

Little is known about the genetic basis and molecular mechanisms regulating female gametogenesis in flowering plants. In many species sexuality is replaced by apomixis, a method of asexual reproduction that circumvents female meiosis and fertilization, and culminates in the formation of clonal seeds. Using a new generation of transposon based insertional mutagenesis strategies and their resulting molecular tools, we are investigating how female meiotically derived cells (megaspores) acquire their identity. We are also determining their function and interactions, and attempting the induction of apomixis initiation in the ovule of Arabidopsis. This basic knowledge will contribute to establish the transfer of apomixis into sexual crops, a major challenge faced by plant biotechnology. The introduction of apomixis as a reproductive alternative could represent a unique opportunity to simplify breeding schemes and genetically perpetuate any desired heterozygous genotype, including hybrids.

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References

  • Asker, S. E.; Jerling, L. Apomixis in plants. Boca Raton, FL: CRC Press; 1992.

    Google Scholar 

  • Beadle, G. W.; McClintock, B.. A genetic disturbance of meiosis in Zea mays. Science 68:433: 1928.

    Article  PubMed  CAS  Google Scholar 

  • Bell, P. R. Incompatibility in flowering plants: adaptation of an ancient response. Plant Cell 7:5–16; 1995.

    Article  PubMed  CAS  Google Scholar 

  • Bellen, H. J.; O'Kane, C. J.; Wilson, C.; Grossniklaus, U.; Pearson, R. K.; Gehring, W. J.; P-element mediated enhancer detection: a versatile method to study development in Drosophila. Genes Dev. 3:1288–1300; 1989.

    PubMed  CAS  Google Scholar 

  • Bicknell, R. A. Isolation of a diploid, apomictic plant of Hieracium aurantiacum. Sex. Plant Reprod. 10:168–172; 1997.

    Article  Google Scholar 

  • Bretagnolle, F.; Thompson, J. D. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129:1–22; 1995.

    Article  Google Scholar 

  • Carman, J. G. Asynchronous expression of duplicate genes in angiosperms may cause apomixes, bispory, tetraspory and polyembryony. J. Linnean Soc. 61:51–94; 1997.

    Article  Google Scholar 

  • Carman, J. G.; Crane, C. F.; Rieralizarazu O. Comparative histology of cell walls during meiotic and apomeiotic megasporogenesis in two hexaploid Australasian Elymus species. Crop. Sci. 31(6):1527–1532; 1991.

    Article  Google Scholar 

  • Conteau, F.; Belzile, F.; Horlow, C.; Grandjean, O.; Vezon, D.; Doutriaux, M. P. Random chromosome segregation without meiotic arrest in both male and female meiocytes of a dmel mutant of Arabidopsis. Plant Cell 11(9):1623–1634; 1999.

    Article  Google Scholar 

  • D'Amato, F. Polyploidy in cell differentiation. Caryologis 42:183–211; 1989.

    Google Scholar 

  • De Haan, A.; Maceira, N. O.; Lumaret, R.; Delay, J. Production of 2n gametes in diploid subspecies of Dactylis glomerata L. 2. Occurrence and frequency of 2n eggs. Ann. Bot. 69:345–350; 1992.

    Google Scholar 

  • Golubovkaya, I. N. Effect of several meiotic mutants on female meiosis in maize. Dev. Genet. 13:411–424; 1992.

    Article  Google Scholar 

  • Golubovskaya, I. N.; Avalkin, N. A.; Sheridan, W. F. New insights into the role of the maize ameiotic 1 locus. Genetics 147:1339–1350; 1997.

    PubMed  CAS  Google Scholar 

  • Golubovskaya, I. N.; Grebennikova, Z. K.; Avalkina, N. A.; Sheridan, W. F. The role of the ameiotic 1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135:1115–1166; 1993.

    Google Scholar 

  • Golubovskaya, I. N.; Sitnikova, D. V. Three meiotic mutations disturbing chromosome segregation at the first meiotic division in corn. Genetica 16:656–666; 1980.

    Google Scholar 

  • Grimanelli D.; Leblane, O.; Espinosa, E.; Perotti, R.; De Leon D. G.; Savidan, Y. Mapping diplosporous apomixes in tetrapoid Tripsacum, one gene or several genes. Heredity 80:40–47; 1998.

    Article  PubMed  Google Scholar 

  • Grossniklaus, U.; Bellen, H. J.; Wilson, C.; Gehring, W. J. P-element mediated enhancer detection applied to the study of oogenesis in Drosophila. Development 107:189–200; 1989.

    PubMed  CAS  Google Scholar 

  • Grossniklaus, U.; Pearson, R. K.; Gehring, W. J. The Drosophila sloppy paired locus encodes two proteins involved in segmentation that show homology to mammalian transcription factors. Genes Dev. 6:1030–1051; 1992.

    PubMed  CAS  Google Scholar 

  • Grossniklaus, U.; Schneitz, K. The molecular and genetic basis of ovule and megagametophyte development. Sem. Cell Dev. Biol. 9:227–238; 1998.

    Article  CAS  Google Scholar 

  • Gustafsson, Å. Apomixis in angiosperms II. Lunds Univ. Årsskr N F II 43:71–179; 1947.

    Google Scholar 

  • Harlau, J. R.; de Wet, J. M. J. Pathways of genetic transfer from Tripsacum to Zea mays. Proc. Natl Acad. Sci. USA 74:3494–3497; 1977

    Article  Google Scholar 

  • Hermsen, J. G. T. Mechanisms and genetic implications of 2n-gamete formation Iowa State. J. Res. 58:421–434; 1984.

    Google Scholar 

  • Jongedijk, E. Desynapsis and FDR 2N-megaspore formation in diploid potato: potentials and limitations for breeding and for the induction of diplosporic apomixis. PhD Dissertation, University of Wageningen; 1991:111 pp.

  • Kimber, G.; Riley, H. Haploid angiosperms. Bot. Rev. 29:480–531; 1963.

    Google Scholar 

  • Knox, R. B. Apomixis: seasonal and population differences in a grass. Science 157:325–326; 1967.

    Article  PubMed  CAS  Google Scholar 

  • Koltunow, A. M. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5:1425–1437; 1993.

    Article  PubMed  Google Scholar 

  • Koltunow, A. M.; Soltys, N.; Nobumasa, N.; McClure, S. Anther, ovule, and nucellar embryo development in Citrus sinensis cv Valencia. Can. J. Bot. 73:1567–1582; 1995.

    Google Scholar 

  • Leblanc, O.; Mazzucato, A. Screening procedures to identify and quantify apomixis. In: Savidan, Y.; Carman, J. G.; Dresselhaus, T., eds., The flowering apomixis: from mechanisms to genetic engineering. Mexico, D.F.: CIMMYT, IRD, European Commission DG VI (FAIR); 2001:121–136.

    Google Scholar 

  • Leblane, O.; Peel, M. D.; Carman, J. G.; Savidan, Y. Megasporogenesis and megagametogenesis in several Tripsacum species (Poaceae). Am. J. Bot. 82:57–63; 1995.

    Article  Google Scholar 

  • Ligrone, R.; Duckett, J. G.; Renzaglia, K. S. The gametophytic-sporophytic junction in land plants. Adv. Bot. Res. 19:231–317; 1993.

    Article  Google Scholar 

  • Lin, Y.-G.; Mitzukawa, N.; Oosumi, T.; Whittier, R. F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 8:457–463; 1995.

    Article  Google Scholar 

  • Maheswari, P. An introduction to the embryology of angiosperms. New York: McGraw-Hill Book Co., Inc.: 1950:453 pp.

    Google Scholar 

  • Maizonnier, D. Production de tetraploïdes et de trisomiques naturels chez le Pétunia. Ann. d'Amel. Plantes 26:305–318; 1976.

    Google Scholar 

  • Miller, O. L. Cytological studies of asynaptic maize. Genetics 48:1445–1466; 1963.

    PubMed  CAS  Google Scholar 

  • Naumova, T. N.; Willemse, M. T. M. Ultrastructural characterization of apospory in Panicum maximum. Sex. Plant Reprod. 8:197–204; 1995.

    Article  Google Scholar 

  • Nogler, G. A. Gametophytic apomixis. In: Johri, B. M., ed. Embryology of angiosperms. New York: Springer Verlag: 1984:475–518.

    Google Scholar 

  • O'Kane, C. J.; Gehring, W. J. Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl Acad. Sci USA 85:9123–9127; 1987.

    Article  Google Scholar 

  • Parrott, W. A.; Smith, R. R. Production of 2n pollen in red clover. Crop Sci. 24:469–472; 1986.

    Article  Google Scholar 

  • Peel, M. D.; Carman, J. G.; Leblane, O. Megasporocyte callose in apomictic buffelgrass Kentucky bluegrass, Pennisetum squamulatum Fresen, Tripsacum L., and weeping lovegrass. Crop Sci. 37:717–723; 1997.

    Article  Google Scholar 

  • Rhoades, M. M. Genic control of chromosomal behavior. Maize Genet. Cooperative Newsletter 30:38–42; 1956.

    Google Scholar 

  • Rhoades, M. M.; Dempsey, E. Induction of chromosome doubling by the elongate gene in maize. Genetics 54:505–522; 1966.

    PubMed  CAS  Google Scholar 

  • Savidan, Y. Apomixis: genetic and breeding. Plant Breed. Rev. 18:13–86; 2000.

    CAS  Google Scholar 

  • Sheridan, W. F.; Avalkina, N. A.; Shamrov, I.-I.; Batygina T. B.; Golubovskaya, I. N. The macl gene: Controlling the commitment to the meiotic pathway in maize. Genetics 142(3):1009–1020; 1996.

    PubMed  CAS  Google Scholar 

  • Sheridan, W. F.; Golubeva, E. A.; Abrhamova, L. I.; Golubovskaya, I. The Macl mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–941; 1999.

    PubMed  CAS  Google Scholar 

  • Siddiqui, I.; Ganesh, G.; Grossniklaus U.; Subbiah, V. The dyad gene is required for progression througth female meiosis in Arabidopsis. Development 127(1):197–207; 2000.

    Google Scholar 

  • Skarnes, W. C. Entrapment vectors: a new tool for mammalian genetics. Bio/Technology 8:827–831; 1990.

    Article  PubMed  CAS  Google Scholar 

  • Staiger, C. J.; Cande, W. Z. Cytoskeletal analysis of maize meiotic mutants. In: Ormrod, J. C.; Francis, D., eds., Molecular and cell biology of the plant cell cycle. Dordrecht: Kluwer Academic Publishers; 1993: 157–171.

    Google Scholar 

  • Sumner, M. J.; van Cascele, L. Ovule development in Brassica campestris. A light microscope study. Can. J. Bot. 66:473–476; 1988.

    Article  Google Scholar 

  • Sundaresan, V.; Springer, P.; Volpe, T.; Haward, S.; Jones, J. D. G.; Dean, C. Ma, H.; Martienssen, R. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9:1797–1810; 1995.

    PubMed  CAS  Google Scholar 

  • Veilleux, R. Diploid and polyploid gametes in crop plants: mechanisms of formation and utilization in plant breeding. Plant Breed. Rev. 3:252–288; 1985.

    Google Scholar 

  • Veronesi, F.; Mariani, A.; Bingham, E. T. Unreduced gametes in diploid Medicago and their importance in alfalfa breeding. Theor. Appl. Genet. 72:37–41; 1986.

    Article  Google Scholar 

  • Vielle-Calzada, J.-Ph.; Baskar, R.; Grossniklaus, U. Delayed activation of the paternal genome during seed development. Nature 404:91–94; 2000.

    Article  PubMed  CAS  Google Scholar 

  • Vielle-Calzada, J.-Ph.; Crane, C. F.; Stelly, D. M. Apomixis: the asexual revolution. Science 274:1322–1323; 1996.

    Article  Google Scholar 

  • Werner, J. E.; Peloquin, S. J. Frequency and mechanisms of 2n egg formation in haploid tuberosum-wild species F1 hybrids. Am. Potato J. 64:641–654; 1987.

    Google Scholar 

  • Willemse, M. T. M.; Van Went, J. L. The female gametophyte. In: Johri, B. M., ed. Embryology of angiosperms. New York: Springer Verlag; 1984;159–196.

    Google Scholar 

  • Willson, C.; Pearson, R. K.; Bellen, H. J.; O'Kane, C. J.; Grossniklaus, U.; Gehring, W. J. P-element mediated enhancer detection: an efficient method for isolating and characterizing developmentally regulated genes. Genes Dev. 3:1301–1313; 1989.

    Google Scholar 

  • Yang, W. C.; Sundaresan, V. Genetics and gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. 3:53–57; 2000.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Ph. Vielle-Calzada.

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Estrada-Luna, A.A., Huanca-Mamani, W., Acosta-García, G. et al. Beyond promiscuity: From sexuality to apomixis in flowering plants. In Vitro Cell.Dev.Biol.-Plant 38, 146–151 (2002). https://doi.org/10.1079/IVP2001278

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  • DOI: https://doi.org/10.1079/IVP2001278

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