The Maize Megagametophyte

  • Matthew M. S. Evans
  • Ueli Grossniklaus

Abstract

The life cycle of plants alternates between a diploid and a haploid generation. In flowering plants the haploid gametophytes are sexually dimorphic and produce the gametes, which fuse to produce the diploid sporophyte of the next generation. The megagametophyte of maize follows the Polygonum-type pattern of development: one of the four meiotic products, the functional megaspore, undergoes three free nuclear divisions to produce a polarized, eight-nucleate syncytium. Cellularization produces seven cells that differentiate into four cell types: two synergids, three antipodals, and the two female gametes, the egg cell and the central cell. The position of the nuclei in the syncytial phase and the position and differentiation of cell types after cellularization follow stereotypical patterns, suggesting a tight genetic regulation of the cellular processes involved. Recent genetic evidence demonstrates that many of these cellular processes are regulated by the activity of the haploid genome of the megagametophyte itself, rather than the parental diploid genome from which it originates. The functions performed by the megagametophyte includes both basic cellular functions and functions that unique to the megagametophyte, such as pollen tube guidance and reception, as well as processes associated with double fertilization and the maternal control over seed development. In this chapter we describe the development and functions of the megagametophyte, and what is known the regulation of the underlying processes.

References

  1. Acosta-Garcia G, and Vielle-Calzada JP (2004) A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16: 2614–2628.PubMedGoogle Scholar
  2. Antoine AF, Faure JE, Cordeiro S, Dumas C, Rougier M, and Feijó JA (2000) A calcium influx is triggered and propagates in the zygote as a wavefront during in vitro fertilization of flowering plants. PNAS USA 97:10643–10648.PubMedGoogle Scholar
  3. Antoine AF, Faure JE, Dumas C, and Feijó JA (2001) Differential contribution of cytoplasmic Ca 2+ and Ca2+influx to gamete fusion and egg activation in maize. Nat Cell Biol 3:1120–1123.PubMedGoogle Scholar
  4. Arthur KM, Vejlupkova Z, Meeley RB, and Fowler JE (2003) Maize ROP2 GTPase provides a competitive advantage to the male gametophyte. Genetics 165: 2137–2151.PubMedGoogle Scholar
  5. Auger DL, and Birchler JA (2002) Maize tertiary trisomic stocks derived from B-A translocations. J Hered 93: 42–47.PubMedGoogle Scholar
  6. Baroux C, Blanvillain R, and Gallois P (2001) Paternally inherited transgenes are down-regulated but retain low activity during early embryogenesis in Arabidopsis. FEBS Lett. 509: 11–16.PubMedGoogle Scholar
  7. Baroux C, Spillane C, and Grossniklaus U (2002) Genomic imprinting during seed development. Adv Genet Inc Mol Genet Med 46: 165–214.Google Scholar
  8. Barrell PJ, and Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis II. Plant J 43 : 309 – 320.PubMedGoogle Scholar
  9. Birchler JA (1993) Dosage analysis of maize endosperm development. Annu Rev Genet 2 7: 181–204.Google Scholar
  10. Bonhomme S, Horlow C, Vezon D, De Laissardiere S, Guyon A, (1998) T-DNA mediated disruption of essential gametophytic genes in Arabidopsis is unexpectedly rare and cannot be inferred from segregation distortion alone. Mol Gen Genet 260: 444–452.PubMedGoogle Scholar
  11. Brukhin V, Curtis MD, and Grossniklaus U (2005) The angiosperm female gametophyte: no longer the forgotten generation. Curr Sci 89: 1844–1852.Google Scholar
  12. Buckner B, and Reeves SL (1994) Viability of female gametophytes that possess deficiencies for the region of chromosome 6 containing the Y1 gene. Maydica 39: 247–254.Google Scholar
  13. Capron A, Serralbo O, Fulop K, Frugier F, Parmentier Y, (2003) The Arabidopsis anaphase-promoting complex or cyclosome: molecular and genetic characterization of the APC2 subunit. Plant Cell 15: 2370–2382.PubMedGoogle Scholar
  14. Chaudhury AM, Ming L, Miller C, Craig S, Dennis ES, (1997) Fertilization-independent seed development in Arabidopsis thaliana Proc Natl Acad Sci USA 94: 4223–4228.Google Scholar
  15. Chen YC, and McCormick S (1996) sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development 122: 3243–3253.PubMedGoogle Scholar
  16. Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, (2007) The central cell plays a critical role in pollen tube guidance in Arabidopsis. Plant Cell 19, 3563–3577.PubMedGoogle Scholar
  17. Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110: 33–42.PubMedGoogle Scholar
  18. Christensen CA, King EJ, Jordan JR, and Drews GN (1997) Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex Plant Reprod 10: 49–64.Google Scholar
  19. Christensen CA, Subramanian S, and Drews GN (1998) Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol 202: 136–151.PubMedGoogle Scholar
  20. Coe EH, Neuffer MG, and Hoisington DA (1988) The genetics of corn. In GF Sprague and WJ Dudley (eds.), Corn and Corn Improvement (pp. 81–258). Madison, Wisconsin: American Society for Agronomy.Google Scholar
  21. Cordts S, Bantin J, Wittich PE, Kranz E, Lorz H, (2001) ZmES genes encode peptides with structural homology to defensins and are specifically expressed in the female gametophyte of maize. Plant J 25: 103–114.PubMedGoogle Scholar
  22. Day RC, Grossniklaus U, and Macknight RC (2005) Be more specific! Laser-assisted microdissection of plant cells. Trends Plant Sci 10: 397–406.PubMedGoogle Scholar
  23. Diboll AG (1968) Fine structural development of the megagametophyte of Zea mays following fertilization. Am J Bot 55: 797–806.Google Scholar
  24. Diboll AG, and Larson DA (1966) An electron microscopic study of the mature megagametophyte in Zea mays Am J Bot 53: 391–402.Google Scholar
  25. Dilkes BP, and Comai L (2004) A differential dosage hypothesis for parental effects in seed development. Plant Cell 16: 3174–3180.PubMedGoogle Scholar
  26. Ebel C, Mariconti L, and Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429: 776–780.PubMedGoogle Scholar
  27. Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, (2007) The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science 317: 656–660.PubMedGoogle Scholar
  28. Evans MMS (2007) The Indeterminate gametophyte1 Gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 19: 46–62.PubMedGoogle Scholar
  29. Evans MMS, and Kermicle JL (2001) Interaction between maternal effect and zygotic effect mutations during maize seed development. Genetics 159: 303 – 315.PubMedGoogle Scholar
  30. Faure JE, Mogensen HL, Dumas C, Lorz H, and Kranz E (1993) Karyogamy after electrofusion of single egg and sperm cell protoplasts from maize: cytological evidence and time course. Plant Cell 5:747–755.PubMedGoogle Scholar
  31. Faure JE, Digonnet C, and Dumas C (1994) An in vitro system for adhesion and fusion of maize gametes. Science 263: 1598–1600.PubMedGoogle Scholar
  32. Faure JE, Rusche ML, Thomas A, Keim P, Dumas C, (2003) Double fertilization in maize: the two male gametes from a pollen grain have the ability to fuse with egg cells. Plant J 33: 1051–1062.PubMedGoogle Scholar
  33. Feldmann KA, Coury DA, and Christianson ML (1997) Exceptional segregation of a selectable marker (KanR) in Arabidopsis identifies genes important for gametophytic growth and development. Genetics 147: 1411–1422.PubMedGoogle Scholar
  34. Gavazzi G, Dolfini S, Allegra D, Castiglioni P, Todesco G, (1997) Dap ( Defective aleurone pigmentation) mutations affect maize aleurone development. Mol Gen Genet 256: 223–230.PubMedGoogle Scholar
  35. Golden TA, Schauer SE, Lang JD, Pien S, Mushegian AR, (2002) Short Integuments1/Suspensor1/ Carpel Factory, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiol 130: 808–822.PubMedGoogle Scholar
  36. Goubet F, Misrahi A, Park SK, Zhang Z, Twell D, (2003) AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol 131: 547–557.PubMedGoogle Scholar
  37. Gray-Mitsumune M, and Matton DP (2006) The Egg apparatus1 gene from maize is a member of a large gene family found in both monocots and dicots. Planta 223: 618–625.PubMedGoogle Scholar
  38. Grimanelli D, Perotti E, Ramirez J, and Leblanc O (2005) Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell 17: 1061–1072.PubMedGoogle Scholar
  39. Grini PE, Jurgens G, and Hulskamp M (2002) Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis. Genetics 162: 1911–1925.PubMedGoogle Scholar
  40. Gross-Hardt R, Kagi C, Baumann N, Moore JM, Baskar R, (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5: e47.Google Scholar
  41. Grossniklaus U (2005) Genomic imprinting in plants: a predominantly maternal affair. In P. Meyer (ed.) Annual Plant Reviews: Plant Epigenetics(pp. 174–200). Blackwell, Sheffield, UK.Google Scholar
  42. Grossniklaus U, and Schneitz K (1998) Genetic and molecular control of ovule development and megagametogenesis. Semin Cell Dev Biol 9: 227–238.PubMedGoogle Scholar
  43. Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, and Gagliano WB (1998) Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280: 446–450.PubMedGoogle Scholar
  44. Guignard L (1899) Sur les antherozoides et la double copulation sexuelle chez les végétaux angiospermes. Compt Rend Acad Sci Paris 128: 864–871.Google Scholar
  45. Guitton AE, Page DR, Chambrier P, Lionnet C, Faure JE, (2004) Identification of new members of FERTILIZATION INDEPENDENT SEED Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana Development 131: 2971–2981.Google Scholar
  46. Guo F, Huang B-Q, Han Y, and Zee SY (2004) Fertilization in maize indeterminate gametophyte1 mutant. Protoplasma 223: 111–120.PubMedGoogle Scholar
  47. Gupta R, Ting JT, Sokolov LN, Johnson SA, and Luan S (2002) A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell 14: 2495–2507.PubMedGoogle Scholar
  48. Gutierrez-Marcos JF, Costa LM, and Evans MMS (2006) Maternal gametophytic baseless1 is required for development of the central cell and early endosperm patterning in maize ( Zea mays). Genetics 174: 317–329.Google Scholar
  49. Hejatko J, Pernisova M, Eneva T, Palme K, and Brzobohaty B (2003) The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. Mol Genet Genomics 269: 443–453.PubMedGoogle Scholar
  50. Higashiyama T, Kuroiwa H, Kawano S, and Kuroiwa T (1997) Kinetics of double fertilization in Torenia fournieri based on direct observations of the naked embryo sac. Planta 203: 101–110.Google Scholar
  51. Higashiyama T, Kuroiwa H, Kawano S, and Kuroiwa T (1998) Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 10: 2019–2031.PubMedGoogle Scholar
  52. Higashiyama T, Kuroiwa H, Kawano S, and Kuroiwa T (2000) Explosive discharge of pollen tube contents in Torenia fournieri Plant Physiol 122:11–14.Google Scholar
  53. Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, (2001) Pollen tube attraction by the synergid cell. Science 293: 1480–1483.PubMedGoogle Scholar
  54. Higashiyama T, Inatsugi R, Sakamoto S, Sasaki N, Mori T, (2006) Species preferentiality of the pollen tube attractant derived from the synergid cell of Torenia fournieri Plant Physiol 142:481–491.Google Scholar
  55. Holt BF 3rd, Boyes DC, Ellerstrom M, Siefers N, Wiig A, (2002) An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development. Dev Cell 2: 807–817.PubMedGoogle Scholar
  56. Hoshina Y, Scholten S, von Wiegen P, Lorz H, and Kranz E (2004) Fertilization-induced changes in the microtubular architecture of the maize egg cell and zygote – an immunocytochemical approach adapted to single cells. Sex Plant Reprod 17: 89–95.Google Scholar
  57. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, (1998) Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149: 621–631.PubMedGoogle Scholar
  58. Huanca-Mamani W, Garcia-Aguilar M , Leon-Martinez G , Grossniklaus U , and Vielle-Calzada JP (2005) CHR11, a chromatin-remodeling factor essential for nuclear proliferation during female gametogenesis in Arabidopsis thaliana Proc Natl Acad Sci USA 102: 17231–17236.Google Scholar
  59. Huang BQ, and Russell SD (1994) Fertilization in Nicotiana tabacum – cytoskeletal modifications in the embryo sac during synergid degeneration – a hypothesis for short-distance transport of sperm cells prior to gamete fusion. Planta 194: 200–214.Google Scholar
  60. Huang BQ, and Sheridan WF (1994) Female gametophyte development in maize: microtubular organization and embryo sac polarity. Plant Cell 6: 845–861.PubMedGoogle Scholar
  61. Huang BQ, and Sheridan WF (1996) Embryo sac development in the maize indeterminate gametophyte1 mutant: abnormal nuclear behavior and defective microtubule organization. Plant Cell 8: 1391–1407.PubMedGoogle Scholar
  62. Huang BQ, Pierson ES, Russell SD, Tiezzi A, and Cresti M (1993) Cytoskeletal organisation and modification during pollen tube arrival, gamete delivery and fertilisation in Plumbago zeylanica Zygote 1:143–154.Google Scholar
  63. Huck N, Moore JM, Federer M, and Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130: 2149–2159.PubMedGoogle Scholar
  64. Hülskamp M, Schneitz K, and Pruitt RE (1995) Genetic evidence for a long-range activity that directs pollen-tube guidance in Arabidopsis. Plant Cell 7: 57–64.PubMedGoogle Scholar
  65. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17: 584–596.PubMedGoogle Scholar
  66. Johnston AJ, Meier P, Gheyselinck J, Wuest SE, Federer M, (2007) Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol 8: R204.PubMedGoogle Scholar
  67. Jones-Rhoades MW, Borevitz JO, and Preuss D (2007) Genome-wide expression profiling of the Arabidopsis female gametophyte identifies families of small, secreted proteins. PLoS Genet 3: 1848–1861.PubMedGoogle Scholar
  68. Kasahara RD, Portereiko MF, Sandaklie-Nikolova L, Rabiger DS, and Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17: 2981–2992.PubMedGoogle Scholar
  69. Kerk NM, Ceserani T, Tausta SL, Sussex IM, and Nelson TM (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol 132: 27–35.PubMedGoogle Scholar
  70. Kermicle JL (1970) Somatic and meiotic instability of R-strippled, an aleurone spotting factor in maize. Genetics 64: 247.PubMedGoogle Scholar
  71. Kermicle JL (1971) Pleiotropic effects on seed development of the indeterminate gametophyte gene in maize. Am J Bot 58: 1–7.Google Scholar
  72. Kiesselbach TA (1949) The structure and reproduction of corn. Univ Nebraska Coll Agric, Agric Exp Stn Res Bull 161: 1–96.Google Scholar
  73. Kim HU, Li Y, and Huang AH (2005) Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 17: 1073–1089.PubMedGoogle Scholar
  74. Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, (2003) Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22: 4804–4814.PubMedGoogle Scholar
  75. Kranz E, and Lörz H (1994) In vitro fertilisation of maize by single egg and sperm cell protoplast fusion mediated by high calcium and high pH. Zygote 2: 125–128.PubMedGoogle Scholar
  76. Kranz E, Bautor J, and Lorz H (1991) Electrofusion-mediated transmission of cytoplasmic organelles through the in vitro fertilization process, fusion of sperm cells with synergids and central cells, and cell reconstitution in maize. Sex Plant Reprod 4: 17–21.Google Scholar
  77. Kranz E, von Wiegen P, Quader H, and Lorz H (1998) Endosperm development after fusion of isolated, single maize sperm and central cells in vitro Plant Cell 10:511–524.Google Scholar
  78. Kwee HS, and Sundaresan V (2003) The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the anaphase promoting complex in arabidopsis. Plant J 36: 853–866.PubMedGoogle Scholar
  79. Le Q, Gutierrez-Marcos JF, Costa LM, Meyer S, Dickinson HG, (2005) Construction and screening of subtracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene expression between maize egg cells and central cells. Plant J 4 4 : 167–178.PubMedGoogle Scholar
  80. Lin B-Y (1978) Structural modifications of the female gametophyte associated with the indeterminate gametophyte ( ig) mutant in maize. Can J Genet Cytol 20: 249–257.Google Scholar
  81. Lin B-Y (1981) Megagametogenetic alterations associated with the indeterminate gametophyte ( ig) mutation in maize. Rev Bras Biol 41: 557–563.Google Scholar
  82. Luo M, Bilodeau P, Koltunow A, Dennis ES, Peacock WJ, (1999) Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 96: 296–301.PubMedGoogle Scholar
  83. Luo M, Bilodeau P, Dennis ES, Peacock WJ, and Chaudhury A (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. PNAS USA 97: 10637–10642.PubMedGoogle Scholar
  84. Marton ML, Cordts S, Broadhvest J, and Dresselhaus T (2005) Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307: 573–576.PubMedGoogle Scholar
  85. Meyer S, and Scholten S (2007) Equivalent parental contribution to early plant zygotic development. Curr Biol 17: 1686–1691.PubMedGoogle Scholar
  86. Meyer RC, Torjek O, Becher M, and Altmann T (2004) Heterosis of Biomass production in Arabidopsis. Establishment during early development. Plant Physiol 134: 1813–1823.PubMedGoogle Scholar
  87. Miyazaki S, and Ito M (2006) Calcium signals for egg activation in mammals. J Pharmacol Sci 100: 545–552 (Sp. Iss).PubMedGoogle Scholar
  88. Mogensen HL (1982) Double fertilization in barley and the cytological explanation for haploid embryo formation, embryoless caryopses, and ovule abortion. Carlsberg Res Commun 47: 313–354.Google Scholar
  89. Mol R, Matthys-Rochon E, and Dumas C (1994) The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5: 197–206.Google Scholar
  90. Mol R, Idzikowska K, Dumas C, and Matthys-Rochon E (2000) Late steps of egg cell differentiation are accelerated by pollination in Zea mays L. Planta 210: 749–757.Google Scholar
  91. Moll C, van Lyncker L, Zimmermann S, Kägi C, Baumann N, Twell D, Grossniklaus U, and Groß-Hardt R (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J., in press.Google Scholar
  92. Moore JM (2002) Isolation and characterization of gametophytic mutants in Arabidopsis thaliana. State University of New York at Stony Brook. Ph.D. Thesis.Google Scholar
  93. Moore JM, Calzada JP, Gagliano W, and Grossniklaus U (1997) Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 62: 35–47.PubMedGoogle Scholar
  94. Mori T, Kuroiwa H, Higashiyama T, and Kuroiwa T (2006) GENERATIVE CELL SPECIFIC1 is essential for angiosperm fertilization. Nat Cell Biol 8: 64–71.PubMedGoogle Scholar
  95. Mouline K, Very AA, Gaymard F, Boucherez J, Pilot G, (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. Genes Dev 16: 339–350.PubMedGoogle Scholar
  96. Murgia M, Huang B-Q, Tucker SC, and Musgrave ME (1993) Embryo sac lacking antipodal cells in Arabidopsis thaliana ( Brassicaceae). Am J Bot 80: 824–838.Google Scholar
  97. Nawaschin SG (1898) Resultate einer Revision der Befruchtungsvorgänge bei Lilium martagon und Fritillaria tenella. Bul Acad Imp des Sci St. Petersburg 9: 377–382.Google Scholar
  98. Nelson OM, and Clary GB (1952) Genic control of semi-sterility in maize. J Hered 43: 205–210.Google Scholar
  99. Ngo QA, Moore JM, Baskar R, Grossniklaus U, and Sundaresan V (2007) Arabidopsis GLAUCE promotes fertilization-independent endosperm development and expression of paternally inherited alleles. Development 134: 4107–4117.PubMedGoogle Scholar
  100. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17: 760–775.PubMedGoogle Scholar
  101. Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38: 63–67.PubMedGoogle Scholar
  102. Ohad N, Yadegari R, Margossian L, Hannon M, Michaeli D, Harada JJ, Goldberg RB, and Fischer RL (1999) Mutations in FIE, a WD Polycomb group gene, allow endosperm development without fertilization. Plant Cell 11: 407–416.PubMedGoogle Scholar
  103. Ohad N, Margossian L, Hsu YC, Williams C, Repetti P, (1996) A mutation that allows endosperm development without fertilization. Proc Natl Acad Sci USA 93: 5319–5324.PubMedGoogle Scholar
  104. Page DR, and Grossniklaus U (2002) The art and design of genetic screens: Arabidopsis thaliana. Nat Rev Genet 3: 124–136.PubMedGoogle Scholar
  105. Pagnussat GC, Yu HJ, Ngo QA, Rajani S, Mayalagu S, (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132:603–614.PubMedGoogle Scholar
  106. Pagnussat GC, Yu HJ, and Sundaresan V (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL1-like homeodomain gene BLH1. Plant Cell 19: 3578–3592.PubMedGoogle Scholar
  107. Palanivelu R, and Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6: 7.PubMedGoogle Scholar
  108. Palanivelu R, Brass L, Edlund AF, and Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114: 47–59.PubMedGoogle Scholar
  109. Park SK, Howden R, and Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125: 3789–3799.PubMedGoogle Scholar
  110. Park SK, Rahman D, Oh SA, and Twell D (2004) Gemini pollen2, a male and female gametophytic cytokinesis defective mutation. Sex Plant Reprod 17: 63–70.PubMedGoogle Scholar
  111. Patterson EB (1978) Properties and uses of duplicate-deficient chromosome complements in maize. In D. B. Walden (ed.), Maize Breeding and Genetics (pp. 693–710). John Wiley and Sons, New York.Google Scholar
  112. Pischke MS, Jones LG, Otsuga D, Fernandez DE, Drews GN, (2002) An Arabidopsis histidine kinase is essential for megagametogenesis. Proc Natl Acad Sci USA 99: 15800–15805.PubMedGoogle Scholar
  113. Procissi A, De Laissardiere S, Ferault M, Vezon D, Pelletier G, (2001) Five gametophytic mutations affecting pollen development and pollen tube growth in Arabidopsis thaliana. Genetics 158: 1773–1783.PubMedGoogle Scholar
  114. Procissi A, Guyon A, Pierson ES, Giritch A, Knuiman B, (2003) KINKY POLLEN encodes a SABRE-like protein required for tip growth in Arabidopsis and conserved among eukaryotes. Plant J 36: 894–904.PubMedGoogle Scholar
  115. Punwani JA, Rabiger DS, and Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus localized proteins. Plant Cell 19: 2557–2568.PubMedGoogle Scholar
  116. Randolph LF (1936) Developmental morphology of the caryopsis in maize. J Agr Res 53: 881–916.Google Scholar
  117. Ray SM, Park SS, and Ray A (1997) Pollen tube guidance by the female gametophyte. Development 124: 2489–2498.PubMedGoogle Scholar
  118. Redei GP (1965) Non-Mendelian megagametogenesis in Arabidopsis. Genetics 51: 857–872.PubMedGoogle Scholar
  119. Rhoades MM, and Dempsey E (1966) Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics 54: 505–522.PubMedGoogle Scholar
  120. Roman H (1947) Mitotic nondisjunction in the case of interchanges involving the B-type chromosome in maize. Genetics 32: 391–409.Google Scholar
  121. Roman H (1948) Selective fertilization in maize. Genetics 33: 122–122.PubMedGoogle Scholar
  122. Rotman N, Rozier F, Boavida L, Dumas C, Berger F, (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13: 432–436.PubMedGoogle Scholar
  123. Russell SD (1979) Fine structure of megagametophyte development in Zea mays. Can J Bot 57: 1093–1110.Google Scholar
  124. Russell SD (1984) Ultrastructure of the sperm of Plumbago zeylanica. 2. Quantitative cytology and 3-dimensional organization. Planta 162: 385–391.Google Scholar
  125. Russell SD (1985) Preferential fertilization in Plumbago – ultrastructural evidence for gametelevel recognition in an angiosperm. PNAS USA 82: 6129–6132.PubMedGoogle Scholar
  126. Russell SD (1996) Attraction and transport of male gametes for fertilization. Sex Plant Reprod 9: 337–342.Google Scholar
  127. Sari-Gorla M, Ferrario S, Villa M, and Pe ME (1996) gaMS-1: a gametophytic male sterile mutant in maize. Sex Plant Reprod 9: 216–220.Google Scholar
  128. Sari-Gorla M, Gotti E, Villa M, and Pe ME (1997) A multi-nucleate male-sterile mutant of maize with gametophytic expression. Sex Plant Reprod 10: 22–26.Google Scholar
  129. Sheridan WF, and Huang BQ (1997) Nuclear behavior is defective in the maize ( Zea mays L.) lethal ovule2 female gametophyte. Plant J 11: 1029–1041.Google Scholar
  130. Sheridan WF, Avalkina NA, Shamrov II, Batygina TB, and Golubovskaya IN (1996) The Mac1 gene: controlling the commitment to the meiotic pathway in maize. Genetics 142: 1009–1020.PubMedGoogle Scholar
  131. Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17: 2340–2354.PubMedGoogle Scholar
  132. Shimizu KK, and Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127: 4511–4518.PubMedGoogle Scholar
  133. Singleton WR, and Mangelsdorf PC (1940) Gametic lethals on the fourth chromosome of maize. Genetics 25: 366–390.PubMedGoogle Scholar
  134. Sorensen MB, Chaudhury AM, Robert H, Bancharel E, and Berger F (2001) Polycomb group genes control pattern formation in plant seed. Curr Biol 11: 277–281.PubMedGoogle Scholar
  135. Sprague GF (1932) The nature and extent of hetero-fertilization in maize. Genetics 1 7: 0358–0368.Google Scholar
  136. Springer PS, Mc Combie WR, Sundaresan V, and Martienssen RA (1995) Gene trap tagging of PROLIFERA, an essential MCM2–3–5-like gene in Arabidopsis. Science 268: 877–880.PubMedGoogle Scholar
  137. Springer PS, Holding DR, Groover A, Yordan C, and Martienssen RA (2000) The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127: 1815–1822.PubMedGoogle Scholar
  138. Sprunck S, Baumann U, Edwards K, Langridge P, and Dresselhaus T (2005) The transcript composition of egg cells changes significantly following fertilization in wheat ( Triticum aestivum L.). Plant J 41: 660–672.PubMedGoogle Scholar
  139. Stinard PS, and Robertson DS (1987) Dappled: a putative Mu-induced aleurone develomental mutant. Maize Genet Coop Newsl 61: 7–9.Google Scholar
  140. Sun M-X, Kranz E, Yang H-Y, Lorz H, Moscatelli A, (2002) Fluorophore-conjugated lectin labeling of the cell surface of isolated male and female gametes, central cells and synergids before and after fertilization in maize. Sex Plant Reprod 15: 159–166.Google Scholar
  141. Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, Dean C, Ma H, and Martienssen R (1995) Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797–1810.PubMedGoogle Scholar
  142. Tsaadon A, Eliyahu E, Shtraizent N, and Shalgi R (2006) When a sperm meets an egg: block to polyspermy. Mol Cell Endocrinol 252:107–114.PubMedGoogle Scholar
  143. Vielle-Calzada JP, Baskar R, and Grossniklaus U (2000) Delayed activation of the paternal genome during seed development. Nature 404: 91–94.PubMedGoogle Scholar
  144. Vielle-Calzada J-P, Moore JM, Gagliano WB, and Grossniklaus U (1998) Altering sexual development in Arabidopsis. J. Plant Biol. 41: 71–83.Google Scholar
  145. Vollbrecht E, and Hake S (1995) Deficiency analysis of female gametogenesis in maize. Dev Genet 16: 44–63.Google Scholar
  146. von Besser K, Frank AC, Johnson MA, and Preuss D (2006) Arabidopsis HAP2 ( GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133: 4761–4769.Google Scholar
  147. von Wangenheim KH, and Peterson HP (2004) Aberrant endosperm development in interploidy crosses reveals a timer of differentiation. Dev Biol 270: 277–289.Google Scholar
  148. Walbot V, and Evans MMS (2003) Unique features of the plant life cycle and their consequences. Nat Rev Genet 4: 369–379.PubMedGoogle Scholar
  149. Wang FH (1947) Embryological development of inbred and hybrid Zea mays I. Am J Bot 3 4 : 113–125.Google Scholar
  150. Weijers D, Franke-van Dijk M, Vencken RJ, Quint A, Hooykaas P, (2001) An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development 128: 4289–4299.PubMedGoogle Scholar
  151. Xu Z, and Dooner HK (2006) The maize Aberrant pollen transmission 1 gene is a SABRE/KIP homolog required for pollen tube growth. Genetics 172: 1251–1261.PubMedGoogle Scholar
  152. Yadegari R, Kinoshita T, Lotan O, Cohen G, Katz A, (2000) Mutations in the FIE and MEA genes that encode interacting Polycomb proteins cause parent-of-origin effects on seed development by distinct mechanisms. Plant Cell 12: 2367–2381.PubMedGoogle Scholar
  153. Yang H, Kaur N, Kiriakopolos S, and Mc Cormick S (2006) EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. Planta 224: 1004–1014.PubMedGoogle Scholar
  154. Yang W, Jefferson RA, Huttner E, Moore JM, Gagliano WB, (2005) An egg apparatus-specific enhancer of Arabidopsis, identified by enhancer detection. Plant Physiol 139: 1421–1432.PubMedGoogle Scholar
  155. Yu HJ, Hogan P, and Sundaresan V (2005) Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol 139: 1853–1869.PubMedGoogle Scholar
  156. Zhang Z, and Russell SD (1995) Sperm cell surface characteristics of flowering plants in relation to transport in the embryo sac (abstract). American Society for Cell Biology Annual Meeting (Suppl), p. 21.Google Scholar

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© Springer Science + Business Media, LLC 2009

Authors and Affiliations

  • Matthew M. S. Evans
  • Ueli Grossniklaus

There are no affiliations available

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