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Altering sexual development inArabidopsis

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Abstract

The reproductive system determines the way in which gametes develop and interact to form a new organism. Therefore, it exerts the primary level of control of genotypic frequencies in plant populations, and plays a fundamental role in plant breeding. A basic understanding of plant reproductive development will completely transform current breeding strategies used for seed production. Apomixis is an asexual form of reproduction in which embryogenesis occurs in a cell lineage lacking both meiosis and fertilization, and that culminates in the formation of viable progeny genetically identical to the mother plant. The transfer of apomixis into sexual crops will allow the production of self-perpetuating improved hybrids, and the fixation of any desired heterozygous genotype. The initiation of apomictic development invariably takes place at early stages of ovule ontogeny, before the establishment of the megagametophytic phase. The developmental versatility associated with megagametophyte formation suggests that the genetic and molecular regulation of apomixis is intimately related to the regulation of sexuality. Differences between the initiation of sexual and apomictic development may be determined by regulatory genes that act during megasporogenesis, and that control events leading to the formation of unreduced female gametophytes. To test this hypothesis, we are isolating and characterizing genes that act during megasporogenesis inArabidopsis thaliana and investigating their potential role in the induction of apomixis. We are using a recently established transposon-based enhancer detection and gene trap insertional mutagenesis system that allows the identification of genes based on their expression patterns. An initial screen of transposants has yielded over 20 lines conferring restricted GUS expression during early ovule development. We have obtained the sequence of genomic fragments flanking the transposon insertion. Several have homology to genes playing important roles in plant and animal development. They include cell cycle regulators, enzymes involved in callose hydrolysis, leucine-rich repeat protein kinase receptors, and expressed sequence tags (ESTs) of unknown function. Independently, a genetic screen allows the identification of female sterile mutants defective in megasporogenesis. Results from these experiments will improve our basic understanding of reproductive development in plants, and will set the basis for a sustained effort in plant germ line biotechnology, a first step toward a flexible transfer of apomixis into a large variety of sexual crops.

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Literature Cited

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

    Google Scholar 

  • Baker, U.S., A.T.C. Cartpenter, M.S. Esposito, R.E. Esposito and E. Sandler. 1976. The genetic control of meiosis.Ann. Rev. den.10: 53–134.

    Article  CAS  Google Scholar 

  • Bell, P.R. 1992. Aposporv and apogamy: implications for understanding the plant life cyclc.Int. J. Plant Sci.153: 123–136.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bier, E., H. Vaessin, S. Shepherd, K. Fee, K. McCall, S. Barbel, L. Ackerman, R. Carretto, T. Uemura, E. Grell, L.Y. Jan and V.N. Jan. 1989. Searching for pattern and mutation in theDrosophila genome with P-lacZ vector,Genes and Dev.3. 1273–1287.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bouchard, R.A. 1990. Characterisation of expressed inactive transcript clones of Lilium, relatedness, and affinity to small heal shock proteins,Genome33: 68–76.

    PubMed  CAS  Google Scholar 

  • Bretagnolle, F. and J.D. Thompson. 1995. Gametes with the somatic chromosome number: mechanisms of then formation and role in the evolution of autopoly-ploid plants.New Phviol.129: 1–22.

    Article  Google Scholar 

  • Burton, G.W. 1992. Manipulating apomixis inPaspatum. In Proceedings of the Apomixis Workshop. USDA-ARS. Atlanta, pp 16–14.

  • Cass, D.D. and W.A. Jensen. 1970. Fertilization in barky.Amer. J. Hot.57: 62–70.

    Article  Google Scholar 

  • Chaudhry, A.M., L. Ming, C. Miller, S. Craig, E.S. Dennis and W.J. Peacock. 1997. Fertilization-independent seed development inArabidopsis thaliana.Proc. Nat. Acad. Sci. USA15: 4223–4228.

    Article  Google Scholar 

  • Christensen, C.A., E.J. King, J.R. Jordan and G.N. Drews. 1667. Megagametogenesis in Arabidopsis wild type and Gf mutant.Sex. Plant Reprod.10: 46–64.

    Google Scholar 

  • Coen, E.S. and E. Meverowilz 1661. The war of the whorls.Nature353: 31–37

    Article  Google Scholar 

  • Curie, C. and S. McCormick. 1997. A strong inhibitor of gene expression in the 5’ untranslated region of the pollen-specific LAT59 gene totomato.The Plant Cell9: 2025–2036.

    Article  PubMed  CAS  Google Scholar 

  • D’Amatom, F. 1989. Polyploidy in cell differentiation.Carvologis42: 183–211.

    Google Scholar 

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

    Google Scholar 

  • Dickinson, H.G. 1995. The regulation of the alternation of generations in flowering plants.Biol. Rev.69: 419–442.

    Article  Google Scholar 

  • Drews, G.N., D. Lee and C.A. Christensen. 1998 Genetic analysis of female gametophyte development and function.Plant Cell10: 5–17.

    Article  PubMed  CAS  Google Scholar 

  • Fobert, P.R., B.L. Miki and V.N. Iyer, 1981 Detection of gene regulatory signals in plants revealed by T-DNA-mediated fusions.Plant Mal. Biol.17. 837–851.

    Article  Google Scholar 

  • Greyson, R.I. 1994. The Development of Flowers. New York: Oxford University Press.

    Google Scholar 

  • Grossniklaus, U., H.J. Bellen, C. Wilson and W.J. Gehring. 1989. P-element mediated enhnacer detection applied to the study of oogenesis inDrosophila.Development107: 189–200.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Grossniklaus, F. and K. Schneitz. 1998a. The molecular and genetic basis of ovule and megagametopln ie development.Sem in Cell and Dev. Biol.9: 227–238.

    Article  CAS  Google Scholar 

  • Grossniklaus, U., J.M. Moore and W. Gagliano. 1998b. Molecular and genetic approaches to understanding and egineering apomixis: Arabidopsis as a powerful tool. In Hybrid Rice, B. Hardy (ed.) IRRI. Manila. Philippines (in press).

    Google Scholar 

  • Grossniklaus, U., J-Ph., Vielle-Calzada, M.A. Hoeppner and W.B. Gagliano. 1998c. Maternal control of em-bryogenesis byMEDEA. aPolycomb-group gene inArabidopsis. Science280: 446–450.

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson, A. 1947. Apomixis in angiosperms II. Funds Univ. Arsskr NF II43: 71–179.

    Google Scholar 

  • Hermsen, J.G.T. 1984. Mechanisms and genetic implications of 2n-gamele formation lowa StateJ. of Res.58: 421–434.

    Google Scholar 

  • Huang, B.Q. and S.D. Russell. 1992. The female germ unit. In Sexual reproduction in flowering plants. S.D. Russell and C. Dumas (guest eds.).Int. Rev. Cytol.140: 233–293.

    Article  Google Scholar 

  • Huang, B.Q. and W.F. Sheridan. 1996. Fmbryo sac development in the maizeindeterminate gametophytel mutant: abnormal nuclear behavior and defective microtubule organization.Plant Cell8: 1391–1407.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, R.C. and J. Casey. 1980. Cytogenetics of polyploids. In Polyploidy, biological relevance. W.H. Lewis (ed.) Plenum Press. New York pp. 17–44.

    Google Scholar 

  • Jurgens, G., M. Grebe and T. Steinman. 1997. Establishment of cell polarity during early plant development.Curr. Opin. Cell. Biol.9: 849–852.

    Article  PubMed  CAS  Google Scholar 

  • Kaul, M.L.H. and T.G.K. Murthy. 1985. Mutant genes affecting higher plant meiosis.Theor. Appl. Genet.70: 449–466.

    Article  Google Scholar 

  • Kertbundit, S., H. de Greve, F. Deboeck, M. van Montagu and J.-P. Hernalsteens. 1991.ln-vivo random β-glucuronidase gene fusions inArabidopsis thaliana.Proc. Nat. Acad. Sci. USA88: 5212–5216.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Knox, R.B. 1967. Apomixis: seasonal and population differences in a grass.Science157: 325–326.

    Article  PubMed  CAS  Google Scholar 

  • Koduru, P.R.K. and M.K. Rao. 1981. Cytogenetics of synaptic mutants.Theor, Appl. Cenet.59: 197–214.

    Google Scholar 

  • Kojima, A. and Y. Nagato. 1997. Discovery of highly apomictic and highly amphimictic dihaploids inAllium tuberosum.Sex. Pl. Reprod.10: 8–12.

    Article  Google Scholar 

  • Koltunow, A.M. 1993 Apomixis: embryo sacs and embryos lormed without meiosis or fertilization in ovules.Plant Cell5: 1425–1437.

    Article  PubMed  Google Scholar 

  • Koltunow, A.M., K. Soltys, N. Nito and S. McClure. 1995. Anther, ovule, seed and micellar embryo development inCitrus sinensis cv. Valencia.Can. J. Bat.73: 1567–1582.

    Article  Google Scholar 

  • Ltblanc, O., M.D. Peel, J.G. Carman and Y. Savidan. 1995 Megasporogenesis and megagametogenesis in severalTripsacum species (Poaceae)Am. J. Hot.82: 57–63.

    Article  Google Scholar 

  • Liu, Y.-G., N. Misukawa, T. Oosumi and R.F. Whittier. 1995. Effcient isolation and mapping ofArabidopsis thaliana T-DNA insert junctions by thermal asym-mertric interlaced PCR.Plant J.8: 457–463.

    Article  PubMed  CAS  Google Scholar 

  • Maizonnier, D. 1976. Production de tetraploides et de tri-somiques naturels chez le Petunia.Annates d’Amel. des Piantes26: 305–318.

    Google Scholar 

  • Mascarenhas, J.P. 1992. Pollen gene expression: molecular evidence Pages 3–18 m Sexual Reproduction in flowering Plants. S.D. Russell and C. Dumas eds. International Review of Cvtologv. Vol. 140. Academic Press. New York.

    Google Scholar 

  • McCormick, S. 1993. Male gametophyte development.Plant Cell5: 1265–1275.

    Article  PubMed  Google Scholar 

  • Mogensen, H.L. 1982. Double fertilization in barley and the evtological explanation lor haploid embryo formation. embrvoless caryopses. and ovule abortion.Carlsberg Res. Comm.47: 313–354.

    Article  Google Scholar 

  • Mogensen, H.L. 1988. Exclusion of male mitochondria and plastids during svngamy in barley as a basis for maternal inheritance.Proc Narl. Acad. Sci. USA85: 2594–2597.

    Article  CAS  Google Scholar 

  • Moore, J.M., J-Ph. Vielle-Calzada, W. Gagliano and U. Grossniklaus. 1997. Genetic characterization of hadad. a mutant disrupting female gametogenesis inArabidopsis tlialiana.Cold Spring Harbor Symp. Quam. Biol.62: 35–47.

    CAS  Google Scholar 

  • Nadeau, J.A., X.S. Zhang, J. Li and S.D. O’Neill. 1996. Ovule development: identification of stage specific and tissue specific cDNAs.Plant Cell8: 213–239.

    Article  PubMed  CAS  Google Scholar 

  • Naumova T.N. and M.T.M. Willemse. 1995 Ultra-structural characterization of apospory inPanicum maximum.Sex. Plant Reprod.8: 197–204.

    Article  Google Scholar 

  • Naumova T.N. and J-Ph. Vielle-Calzada. 1998. Ultr-structural analysis of apomictic development. In Apo-mixis: Techniques and Trends. Y. Savidan and J. Carman (eds.). FAO Publications (in press).

  • Nogler, G.A. 1984a. Gamctophytic apomixis. InEmbryology of angiosperms B.M. Johri (ed.). Springer Verlag. New York, pp. 475–518.

    Google Scholar 

  • Nogler, G.A. 1984b. Genetics of apospory in apomicticRanvnculus auricomus. V. Conclusion.Bot. Helvet.94: 411–422.

    Google Scholar 

  • Ohad N., L. Margossian, Y-C. Hsyu, C. Williams, P. Repetti and R.L. Fischer. 1996. A mutation that allows endosperm development without fertilization.Proc. Natl. Acad. Sci. USA93: 5319–5324.

    Article  PubMed  CAS  Google Scholar 

  • O’Kane, C.J. and W.J. Gehring. 1987. Detection in situ of genomic regulatory elements inDrosophila.Proc. Natl. Acad. Sci. USA85: 9123–9127.

    Article  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Pruitt, R.E., M. Hulskamp, D. Kopczak and K. Schneitz 1994. Genetic analysis of reproductive interactions inArabidopsis. In Pollen-Pistil Interactions and Pollen Tube Growth. A.G. Stephenson and T.H. Kao (eds.)Proc. Ninth Annual Perm State Syrup. Plant Physiol.12: 94–102.

    Google Scholar 

  • Porter, E.K., D. Parry, J. Bird and H.G. Dickinson. 1984. Nucleic acid metabolism in the nucleus and cytoplasm of angiosperm meiocytes. In Controlling Events in Meiosis. C. Evans and H.G. Dickinson (eds.) Company of Biologists, Cambridge, pp. 363–369.

    Google Scholar 

  • Ramanna, M.S. 1992. The use of 2n-gametes in breeding polysomic polyploid species; some achievements and perspectives. In Gametes with somatic chromosome number in the evolution and breeding of polyploid polysomic species: achievements and perspectives. A. Mariani and S. Tavoletti (eds.) Perugia, Italy, pp. 91–99.

    Google Scholar 

  • Rhoades, M.M. and E. Dempsey. 1966. Induction of chromosome doubling by the elongate gene in maize.Genetics54: 505–522.

    PubMed  CAS  Google Scholar 

  • Russell S.D. 1985. Preferential fertilization inPlumbago: Ultrastructural evidence for gamete-level recognition in an angiosperm.Proc Natl. Acad. Sci. USA82: 6129–6132.

    Article  PubMed  CAS  Google Scholar 

  • Savidan, Y.H. 1980. Chromosomal and embryological analyses in sexual and apomicitc hybrids ofPanicum maximum Jacq.Theor. Appl. Genet.57: 153–156.

    Article  Google Scholar 

  • Savidan Y.H. 1992. Progress in research on apomixis and its transfer to major grain crops. InReproductive Biology and Plant Breeding. Y. Dattée and C. Dumas (eds.). Springer-Verlag. Berlin.

    Google Scholar 

  • Sherwood, R.T., C.C. Berg and B.A. Young. 1994 Inheritance of apospory in buffelgrass.Crop Sci.34: 1490–1494.

    Article  Google Scholar 

  • Skarnes, W.C. 1990. Entrapment vectors: a new tool for mamalian genetics.Biotechnology8: 827–831.

    Article  PubMed  CAS  Google Scholar 

  • Smith, D.L., andN.V. Fedoroff. 1995. LRP1. a gene expressed in lateral and adventitious root primordia ofArabidopsis.Plant Cell7, 735–745.

    Article  PubMed  CAS  Google Scholar 

  • Springer, P.S., W.R. McCombie, V. Sundaresan and R. A. Martienssen. 1995. Gene trap tagging ofprolifera. an essential MCM2-3-5-like gene inArabidopsis.Science268: 877–880.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Toppingz, J.F., W. Wei and K. Lindsey, 1991 Func tional tagging of regulatory elements in the plant genome.Development112, 1009–1019.

    Google Scholar 

  • Twell, D. 1994. The diversity and regulation of gene expression in the pathway of male gametophyte development. In Molecular and Cellular Aspects of Plant reproduction. R. I Scott and A.D. Stead (eds.). Cambridge University Press, Cambridge, pp. 83–136.

    Google Scholar 

  • Twell D. and R. Howden 1998. Mechanisms of assymetric division and cell fate detrmination in developing pollen. In Haploidy: A critical review. M. Caboche (ed.) Springer Verlag. Berlin, Germany (in press). Veilleux, R. 1985. Diploid and polyploid gametes in crop plants: mechanisms of formation and utilization in plant breeding.Plant Breed. Rev.3: 252–288.

    Google Scholar 

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

    Article  Google Scholar 

  • Vielle-Calzada, J-Ph., B.L. Burson, E.C. Bashaw and M.A Hussey. 1995. Early fertilization events in the sexual and aposporous egg apparatus ofPennisetum eiliare (L.) Link.Plant J.8: 309–316.

    Article  Google Scholar 

  • Vielle-Calzada, J-Ph., C.F. Crane and D.M. Stelly. 1996a. Apomixis: the asexual revolution.Science274: 1322–1323.

    Article  Google Scholar 

  • Vielle-Calzada, J-Ph., M. Nuccio, M.A. Budiman, T.L. Thomas, B.L. Burson, M.A. Hussey and R.A. Wing. 1996b. Comparative gene expression in sexual and apomictic ovaries ofPennisetum eiliare.Plant Mol. Biol.32: 1085–1092.

    Article  PubMed  CAS  Google Scholar 

  • Vollbrecht, E. and S. Hake. 1995. Deficiency analysis of female gametogenesis in maize.Dev. Genet.16: 44–63.

    Article  Google Scholar 

  • Watanabe, K. and S.J. Peloquin. 1989. Occurrence of on pollen and ps gene frequencies in cultivated groups and their related wild species in tuber-bearingSolanums.Theor. Appl. Genet.78: 329–336.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Willemse, M.T.M. and J.L. Van Went. 1984. The female gametophytc. In Embryology of angiosperms B.M Johri (ed.). Springer Verlag, New York. pp. 159–196.

    Google Scholar 

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

    Article  CAS  Google Scholar 

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Vielle-Calzada, JP., Moore, J.M., Gagliano, W.B. et al. Altering sexual development inArabidopsis . J. Plant Biol. 41, 73–81 (1998). https://doi.org/10.1007/BF03030391

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