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Female gametophyte development and double fertilization in Balsas teosinte, Zea mays subsp. parviglumis (Poaceae)

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Abstract

Over the course of maize evolution, domestication played a major role in the structural transition of the vegetative and reproductive characteristics that distinguish it from its closest wild relative, Zea mays subsp. parviglumis (Balsas teosinte). Little is known, however, about impacts of the domestication process on the cellular features of the female gametophyte and the subsequent reproductive events after fertilization, even though they are essential components of plant sexual reproduction. In this study, we investigated the developmental and cellular features of the Balsas teosinte female gametophyte and early developing seed in order to unravel the key structural and evolutionary transitions of the reproductive process associated with the domestication of the ancestor of maize. Our results show that the female gametophyte of Balsas teosinte is a variation of the Polygonum type with proliferative antipodal cells and is similar to that of maize. The fertilization process of Balsas teosinte also is basically similar to domesticated maize. In contrast to maize, many events associated with the development of the embryo and endosperm appear to be initiated earlier in Balsas teosinte. Our study suggests that the pattern of female gametophyte development with antipodal proliferation is common among species and subspecies of Zea and evolved before maize domestication. In addition, we propose that the relatively longer duration of the free nuclear endosperm phase in maize is correlated with the development of a larger fruit (kernel or caryopsis) and with a bigger endosperm compared with Balsas teosinte.

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References

  • Adams JD, Mackay E (1953) Observing pollen tubes within the styles of Zea mays L. Biotech Histochem 28:295–298

    Article  CAS  Google Scholar 

  • Anton AM, Cocucci AE (1984) The grass megagametophyte and its possible phylogenetic implications. Pl Syst Evol 146:117–121

    Article  Google Scholar 

  • Bedinger P, Russell SD (1994) Gametogenesis in maize. In: Freeling M, Walbot V (eds) The maize handbook. Springer, New York, pp 48–64

    Google Scholar 

  • Benz BF, Iltis HH (1992) Evolution of female sexuality in the maize ear (Zea mays L. subsp. mays—Gramineae). Econ Bot 46:212–222

    Article  Google Scholar 

  • Bhanwra RK, Pathak P (1987) Embryology of Apluda mutica (Poaceae). Proc Indian Acad Sci (Plant Sci) 97:461–467

    Google Scholar 

  • Bortiri E, Chuck G, Vollbrecht E, Rocheford T, Martienssen R, Hake S (2006) Ramosa2 encodes a lateral organ boundary domain protein that determines the fate of stem cells in branch meristems of maize. Plant Cell 18:574–585

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Holtsford TP (1996) Zea systematics: ribosomal ITS evidence. Mol Biol Evol 13:612–622

    PubMed  CAS  Google Scholar 

  • Burson BL, Voigt PW, Sherman RA (1990) Apomixis and sexuality in Eastern Gamagrass. Crop Sci 30:86–89

    Article  Google Scholar 

  • Choda SP, Mitter H, Bhanwra RK (1982) Embryological studies in three species of Cymbopogon Spreng (Poaceae). Proc Indian Acad Sci (Plant Sci) 91:55–60

    Google Scholar 

  • Clore AM, Dannenhoffer JM, Larkins BA (1996) EF-1α is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells. Plant Cell 8:2003–2014

    Article  PubMed  CAS  Google Scholar 

  • Cooper DC (1937) Macrosporogenesis and embryo-sac development in Euchlaena mexicana and Zea mays. J Agric Res 55:539–551

    Google Scholar 

  • Cooper DC (1951) Caryopsis development following matings between diploid and tetraploid strains of Zea mays. Am J Bot 38:702–708

    Article  Google Scholar 

  • Dermastia M, Kladnik A, Dolenc Koce J, Chourey PS (2009) A cellular study of teosinte Zea mays subsp. parviglumis (Poaceae) caryopsis development showing several processes conserved in maize. Am J Bot 96:1798–1807

    Article  PubMed  Google Scholar 

  • Diboll AG (1968) Fine structural development of the megagametophyte of Zea mays following fertilization. Am J Bot 55:797–806

    Article  Google Scholar 

  • Diboll AG, Larson DA (1966) An electron microscopic study of the mature megagametophyte in Zea mays. Am J Bot 53:391–402

    Article  PubMed  CAS  Google Scholar 

  • Doebley JF (1990a) Molecular evidence and the evolution of maize. Econ Bot 44:6–27

    Article  CAS  Google Scholar 

  • Doebley JF (1990b) Molecular systematics of Zea (Gramineae). Maydica 35:143–150

    Google Scholar 

  • Doebley JF (2003) The taxonomy of Zea. http://teosinte.wisc.edu/taxonomy.html. Accessed 04 Nov 2010

  • Doebley JF (2004) The genetics of maize evolution. Annu Rev Genet 38:37–59

    Article  PubMed  CAS  Google Scholar 

  • Doebley JF, Iltis HH (1980) Taxonomy of Zea (Gramineae). I. A subgeneric classification with key to taxa. Am J Bot 67:982–993

    Article  Google Scholar 

  • Doebley JF, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    PubMed  CAS  Google Scholar 

  • Doebley JF, Stec A, Gustus C (1995) Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346

    PubMed  CAS  Google Scholar 

  • Doebley JF, Stec A, Hubbard L (1997) The evolution of apical dominance in maize. Nature 386:485–488

    Article  PubMed  CAS  Google Scholar 

  • Dorweiler JE, Doebley JF (1997) Developmental analysis of teosinte glume architecture1: a key locus in the evolution of maize (Poaceae). Am J Bot 84:1313–1322

    Article  PubMed  CAS  Google Scholar 

  • Dorweiler JE, Stec A, Kermicle J, Doebley JF (1993) Teosinte glume architecture1: a genetic locus controlling a key step in maize evolution. Science 262:233–235

    Article  PubMed  CAS  Google Scholar 

  • Doust A (2007) Architectural evolution and its implications for domestication in grasses. Ann Bot 100:941–950

    Article  PubMed  Google Scholar 

  • Evans MMS, Grossniklaus U (2009) The maize megagametophyte. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 79–104

    Chapter  Google Scholar 

  • Folsom MW, Peterson CM (1984) Ultrastructural aspects of the mature embryo sac of soybean. Glycine max (L.) Merr Bot Gaz 145:1–10

    Google Scholar 

  • Galinat WC (1985) The missing links between teosinte and maize: a review. Maydica 30:137–160

    Google Scholar 

  • Gallavotti A, Long JA, Stanfield S, Yang X, Jackson D, Vollbrecht E, Schmidt R (2010) The control of axillary meristem fate in the maize ramose pathway. Development 137:2849–2856

    Article  PubMed  CAS  Google Scholar 

  • Garcia D, Saingery V, Chambrier P, Mayer U, Jürgens G, Berger F (2003) Arabidopsis haiku mutants reveal new controls of seed size by endosperm. Plant Physiol 131:1661–1670

    Article  PubMed  CAS  Google Scholar 

  • Hector JM (1936) Introduction to the botany of field crops vol I—Cereals. Central News Agency Ltd., Johannesburg

    Google Scholar 

  • Heo K, Kimoto Y, Riveros M, Tobe H (2004) Embryology of Gomortegaceae (Laurales): characteristics and character evolution. J Plant Res 117:221–228

    Article  PubMed  Google Scholar 

  • Heslop-Harrison Y, Heslop-Harrison J, Reger BJ (1985) The pollen-stigma interaction in the grass. 7. Pollen-tube guidance and the regulation of pollen number in Zea mays L. Acta Bot Neerl 34:193–211

    Google Scholar 

  • Huang BQ, Sheridan WF (1994) Female gametophyte development in maize: microtubular organization and embryo sac polarity. Plant Cell 6:845–861

    Article  PubMed  Google Scholar 

  • Iltis HH (2000) Homeotic sexual translocations and the origin of maize (Zea mays, Poaceae): a new look at an old problem. Econ Bot 54:7–42

    Article  Google Scholar 

  • Iltis HH, Benz BF (2000) Zea nicaraguensis (Poaceae), a new teosinte from Pacific Coastal Nicaragua. Novon 10:382–390

    Article  Google Scholar 

  • Iltis HH, Doebley JF (1980) Taxonomy of Zea (Gramineae). II. Subspecific categories in the Zea mays complex and a generic synopsis. Am J Bot 67:994–1004

    Article  Google Scholar 

  • Jensen WA (1965) The ultrastructure and composition of the egg and central cell of cotton. Am J Bot 52:781–797

    Article  Google Scholar 

  • Johann H (1935) Histology of the caryopsis of yellow dent corn, with reference to resistance and susceptibility to kernel rots. J Agric Res 51:855–883

    Google Scholar 

  • Kato A (1990) Heterofertilization exhibited by using highly haploid inducing line “Stock 6” and supplementary cross. Maize Genet Coop Newsl 64:109–110

    Google Scholar 

  • Kato A (2001) Heterofertilization exhibited by trifluralin-induced bicellular pollen on diploid and tetraploid maize crosses. Genome 44:1114–1121

    Article  PubMed  CAS  Google Scholar 

  • Kiesselbach TA (1980) The structure and reproduction of corn. University of Nebraska, Lincoln

    Google Scholar 

  • Kimoto Y, Tobe H (2001) Embryology of Laurales: a review and perspectives. J Plant Res 114:247–267

    Article  Google Scholar 

  • Kimoto Y, Tobe H (2003) Embryology of Siparunaceae (Laurales): characteristics and character evolution. J Plant Res 116:281–294

    Article  PubMed  Google Scholar 

  • Kliwer I, Dresselhaus T (2010) Establishment of the male germline and sperm cell movement during pollen germination and tube growth in maize. Plant Signal Behav 5:885–889

    Article  PubMed  Google Scholar 

  • Knowles RV, Phillips RL (1988) Endosperm development in maize. Int Rev Cytol 112:97–136

    Article  Google Scholar 

  • Koul AD (1959) Antipodals during the development of caryopsis in Euchlaena mexicana. Agra Univ J Res 8:31–33

    Google Scholar 

  • Kraptchev B, Kruleva M, Dankov T (2003) Induced heterofertilization in maize (Zea mays L.). Maydica 48:271–274

    Google Scholar 

  • Lausser A, Kliwer I, Srilunchang KO, Dresselhaus T (2010) Sporophytic control of pollen tube growth and guidance in maize. J Exp Bot 61:673–682

    Article  PubMed  CAS  Google Scholar 

  • Leblanc O, Peel MD, Carman JG, Savidan Y (1995) Megasporogenesis and megagametogenesis in several Tripsacum species (Poaceae). Am J Bot 82:57–63

    Article  Google Scholar 

  • Lora J, Hormaza JI, Herrero M (2010) The progamic phase of an early-divergent angiosperm, Annona cherimola (Annonaceae). Ann Bot 105:221–231

    Article  PubMed  CAS  Google Scholar 

  • Lovisolo MR, Galati BG (2007) Ultrastructure and development of the megagametophyte in Eleusine tristachya (Lam.) Lam. (Poaceae). Flora 202:293–301

    Google Scholar 

  • Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci USA 102:17531–17536

    Article  PubMed  CAS  Google Scholar 

  • Martin JN (1914) Comparative morphology of some Leguminosae. Bot Gaz 58:154–167

    Article  Google Scholar 

  • Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez J, Buckler E, Doebley JF (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA 99:6080–6084

    Article  PubMed  CAS  Google Scholar 

  • Moco MCC, Mariath JEA (2004) Female gametophyte development in Adesmia latifolia (Spreng.) Vog. (Leguminosae-Papilionoideae). Rev Brasil Bot 27:241–248

    Article  Google Scholar 

  • Mol R, Matthys-Rochon E, Dumas C (1994) The kinetics of cytological events during double fertilization in Zea mays L. Plant J 5:197–206

    Article  Google Scholar 

  • Ohto M, Floyd SK, Fischer RL, Goldberg RB, Harada JJ (2009) Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis. Sex Plant Reprod 22:277–289

    Article  PubMed  Google Scholar 

  • Orr AR, Sundberg MD (1994) Inflorescence development in a perennial teosinte: Zea perennis (Poaceae). Am J Bot 81:598–608

    Article  Google Scholar 

  • Orr AR, Sundberg MD (2007) Inflorescence development in the teosinte Zea luxurians (Poaceae) and implication for the origin of maize inflorescences. Maydica 52:31–47

    Google Scholar 

  • Pennington PD, Costa LM, Gutierrez-Marcos JF, Greenland AJ, Dickinson HG (2008) When genomes collide: aberrant seed development following maize interploidy crosses. Ann Bot 101:833–843

    Article  PubMed  CAS  Google Scholar 

  • Phillips KA, Skirpan AL, Kaplinsky NJ, McSteen P (2009) Developmental disaster1: a novel mutation causing defects during vegetative and inflorescence development in maize (Zea mays, Poaceae). Am J Bot 96:420–430

    Article  PubMed  Google Scholar 

  • Randolph LF (1936) Developmental morphology of the caryopsis in maize. J Agric Res 53:881–916

    Google Scholar 

  • Reed EL (1924) Anatomy, embryology, and ecology of Arachis hypogea. Bot Gaz 78:289–310

    Article  Google Scholar 

  • Rotarenco V, Eder J (2003) Possible effects of heterofertilization on the induction of maternal haploids in maize. Maize Genet Coop Newsl 77:30

    Google Scholar 

  • Sajo MG, Longhi-Wagner HM (2008) Reproductive morphology of the early-divergent grass Streptochaeta and its bearing on the homologies of the grass spikelet. Plant Syst Evol 275:245–255

    Article  Google Scholar 

  • Sajo MG, Longhi-Wagner HM, Rudall PJ (2007) Floral development and embryology in the early-divergent grass Pharus. Int J Plant Sci 168:181–191

    Article  Google Scholar 

  • Satyamurty TVC (1984) Development of the caryopsis in Chionachne koenigii Linn. Plant Sci 93:567–570

    Google Scholar 

  • Schulz P, Jensen WA (1973) Capsella embryogenesis: the central cell. J Cell Sci 12:741–763

    PubMed  CAS  Google Scholar 

  • Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    PubMed  CAS  Google Scholar 

  • Sehgal CB, Gifford EM (1979) Developmental and histochemical studies of the ovules of Nicotiana rustica L. Bot Gaz 140:180–188

    Article  Google Scholar 

  • Sigmon B, Vollbrecht E (2010) Evidence of selection at the ramosa1 locus during maize domestication. Mol Ecol 19:1296–1311

    Article  PubMed  CAS  Google Scholar 

  • Smith BW (1956) Arachis hypogaea. Normal megasporogenesis and syngamy with occasional single fertilization. Am J Bot 43:81–89

    Article  Google Scholar 

  • Sprague GF (1929) Hetero-fertilization in maize. Science 69:526–527

    Article  PubMed  CAS  Google Scholar 

  • Sprague GF (1932) The nature and extent of hetero-fertilization in maize. Genetics 17:358–368

    PubMed  CAS  Google Scholar 

  • Stover EL (1937) The embryo sac of Eragrostis cilianensis (All.) Link. Ohio J Sci 37:172–184

    Google Scholar 

  • Streetman LJ (1963) Reproduction of the lovegrasses, the genus Eragrostis—I. E. chloromelas Steud., E. curvula (Schrad.) Nees, E. lehmanniana Nees, and E. superba Peyr. Wrightia 3:41–51

    Google Scholar 

  • Styles ED (1987) Pollen tube growth in maize. Maydica 32:139–150

    Google Scholar 

  • Suen DF, Huang AH (2007) Maize pollen coat xylanase facilitates pollen tube penetration into silk during sexual reproduction. J Biol Chem 282:625–636

    Article  PubMed  CAS  Google Scholar 

  • Sundberg MD, Orr AR (1990) Inflorescence development in two annual teosintes: Zea mays subsp. mexicana and Z. mays subsp. parviglumis. Am J Bot 77:141–152

    Article  Google Scholar 

  • Sundberg MD, LaFargue C, Orr AR (1995) Inflorescence development in the “standard exotic” maize, argentine popcorn (Poaceae). Am J Bot 82:64–74

    Article  Google Scholar 

  • Thompson BE, Bartling L, Whipple C, Hall DH, Sakai H, Schmidt R, Hake S (2009) Bearded-ear encodes a MADS box transcription factor critical for maize floral development. Plant Cell 21:2578–2590

    Article  PubMed  CAS  Google Scholar 

  • Torosian C (1972) Ultrastructural and histochemical studies of endosperm differentiation in Lobelia dunnii. Ph.D. Dissertation, University of California, Berkeley

  • USDA, ARS, National Genetic Resources Program (2010) Germplasm resources information network—(GRIN). [Online database] National germplasm resources laboratory, Beltsville, Maryland. http://www.ars-grin.gov/cgi-bin/npgs/acc/display.pl?1087195 Accessed 19 Dec 2010

  • Vollbrecht E, Springer PS, Goh L, Buckler ES, Martienssen R (2005) Architecture of floral branch systems in maize and related grasses. Nature 436:1119–1126

    Article  PubMed  CAS  Google Scholar 

  • Weber AL, Briggs WH, Rucker J, Baltazar BM, de Jesús Sánchez-Gonzalez J, Feng P, Buckler ES, Doebley JF (2008) The genetic architecture of complex traits in teosinte (Zea mays ssp. parviglumis): new evidence from association mapping. Genetics 180:1221–1232

    Article  PubMed  CAS  Google Scholar 

  • Whipple CJ, Schmidt RJ (2006) Genetics of grass flower development. Adv Bot Res 44:385–424

    Article  CAS  Google Scholar 

  • Williams JH (2008) Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proc Natl Acad Sci USA 105:11259–11263

    Article  PubMed  CAS  Google Scholar 

  • Yan H, Yang HY, Jensen WA (1991) Ultrastructure of the developing embryo sac of sunflower (Helianthus annuus) before and after fertilization. Can J Bot 69:191–202

    Article  Google Scholar 

  • You R, Jensen WA (1985) Ultrastructural observations of the mature megagametophyte and the fertilization in wheat (Triticum aestivum). Can J Bot 63:163–178

    Article  Google Scholar 

  • Zhou Y, Zhang X, Kang X, Zhao X, Zhang X, Ni M (2009) SHORT HYPOCOTYL UNDER BLUE1 associates with MINISEED3 and HAIKU2 promoters in vivo to regulate Arabidopsis seed development. Plant Cell 21:106–117

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Julien Bachelier for his helpful suggestions toward the improvement of the manuscript. This work was supported by grants from the Department of Ecology and Evolutionary Biology, University of Colorado.

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Correspondence to William E. Friedman.

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Communicated by Thomas Dresselhaus.

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Wu, CC., Diggle, P.K. & Friedman, W.E. Female gametophyte development and double fertilization in Balsas teosinte, Zea mays subsp. parviglumis (Poaceae). Sex Plant Reprod 24, 219–229 (2011). https://doi.org/10.1007/s00497-011-0164-1

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