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Female gametophyte development

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Abstract

Great attention has been drawn toward research on female gametophyte (FG) development, and many mutants have been identified with abnormal formation. Although studies are being conducted on the function and expression of individual regulatory genes, only a few projects have focused on gene regulatory networks. Here, we briefly reviewed the molecular mechanisms and factors that affect FG development and discuss our ongoing investigations with gymnosperms. The progress that has already been reported in this field serves as a strong foundation for future examinations of those gene networks that control steps in plant reproduction.

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References

  • Alandete-Saez M, Ron M, McCormick S (2008) GEX3, expressed in the male gametophyte and in the egg cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early embryogenesis. Mol Plant 4:586–598

    Google Scholar 

  • Alvarez J, Smyth DR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 11:2377–2386

    Google Scholar 

  • Andersen SU, Algreen-Petersen RG, Hoedl M, Jurkiewicz A, Cvitanich C, Braunschweig U, Schauser L, Oh SA, Twell D, Jensen EØ (2007) The conserved cysteine-rich domain of a tesmin/TSO1-like protein binds zinc in vitro and TSO1 is required for both male and female fertility in Arabidopsis thaliana. J Exp Bot 13:3657–3670

    Google Scholar 

  • Angenent GC, Franken J, Busscher M, van Dijken A, van Went JL, Dons HJ, van Tunen AJ (1995) A novel class of MADS box genes is involved in ovule development in Petunia. Plant Cell 10:1569–1582

    Google Scholar 

  • Awasthi A, Paul P, Kumar S, Verma SK, Prasad R, Dhaliwal HS (2012) Abnormal endosperm development causes female sterility in rice insertional mutant OsAPC6. Plant Sci 183:167–174

    PubMed  CAS  Google Scholar 

  • Azhakanandam S, Nole-Wilson S, Bao F, Franks RG (2008) SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development. Plant Physiol 3:1165–1181

    Google Scholar 

  • Bai X, Peirson BN, Dong F, Xue C, Makaroff CA (1999) Isolation and characterization of SYN1, a RAD21-like gene essential for meiosis in Arabidopsis. Plant Cell 3:417–430

    Google Scholar 

  • Balasubramanian S, Schneitz K (2002) NOZZLE links proximal-distal and adaxial-abaxial pattern formation during ovule development in Arabidopsis thaliana. Development 18:4291–4300

    Google Scholar 

  • Barrell PJ, Grossniklaus U (2005) Confocal microscopy of whole ovules for analysis of reproductive development: the elongate1 mutant affects meiosis II. Plant J 2:309–320

    Google Scholar 

  • Becker A, Bey M, Bürglin TR, Saedler H, Theissen G (2002) Ancestry and diversity of BEL1-like homeobox genes revealed by gymnosperm (Gnetum gnemon) homologs. Dev Genes Evol 9:452–457

    Google Scholar 

  • Bencivenga S, Simonini S, Benková E, Colombo L (2012) The transcription factors BEL1 and SPL required for cytokinin and auxin signaling during ovule development in Arabidopsis. Plant Cell 7:2886–2897

    Google Scholar 

  • Bereterbide A, Hernould M, Castera S, Mouras A (2001) Inhibition of cell proliferation, cell expansion and differentiation by the Arabidopsis SUPERMAN gene in transgenic tobacco plants. Planta 1:22–29

    Google Scholar 

  • Blanvillain R, Boavida LC, McCormick S, Ow DW (2008) Exportin 1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. Genetics 3:1493–1500

    Google Scholar 

  • Blázquez MA, Ferrándiz C, Madueño F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 6:855–870

    Google Scholar 

  • Bleuyard JY, Gallego ME, White CI (2004) Meiotic defects in the Arabidopsis rad50 mutant point to conservation of the MRX complex function in early stages of meiotic recombination. Chromosoma 4:197–203

    Google Scholar 

  • Boateng KA, Yang X, Dong F, Owen HA, Makaroff CA (2008) SWI1 is required for meiotic chromosome remodeling events. Mol Plant 4:620–633

    Google Scholar 

  • Boavida LC, Becker JD, Feijó JA (2005) The making of gametes in higher plants. Int J Dev Biol 56:595–614

    Google Scholar 

  • Bowman JL, Baum SF, Eshed Y, Putterill J, Alvarez J (1999) Molecular genetics of gynoecium development in Arabidopsis. Curr Top Dev Biol 45:155–205

    PubMed  CAS  Google Scholar 

  • Brambilla V, Kater M, Colombo L (2008) Ovule integument identity determination in Arabidopsis. Plant Signal Behav 4:246–247

    Google Scholar 

  • Broadhvest J, Baker SC, Gasser CS (2000) SHORT INTEGUMENTS 2 promotes growth during Arabidopsis reproductive development. Genetics 2:899–907

    Google Scholar 

  • Cairney J, Pullman GS (2007) The cellular and molecular biology of conifer embryogenesis. New Phytol 3:511–536

    Google Scholar 

  • Capomaccio S, Barone P, Reale L, Veronesi F, Rosellini D (2009) Isolation of genes from female sterile flowers in Medicago sativa. Sex Plant Reprod 2:97–107

    Google Scholar 

  • Cheng CY, Kieber JJ (2013) The role of cytokinin in ovule development in Arabidopsis. Plant Signal Behav 8(3). pii: e23393. [Epub ahead of print]

    PubMed  Google Scholar 

  • Chevalier E, Loubert-Hudon A, Matton DP (2013) ScRALF3, a secreted RALF-like peptide involved in cell-cell communication between the sporophyte and the female gametophyte in a solanaceous species. Plant J 6:1019–1033

    Google Scholar 

  • Christensen CA, Subramanian S, Drews GN (1998) Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol 1:136–151

    Google Scholar 

  • Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J, Shaw JM, Drews GN (2002) Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 9:2215–2232

    Google Scholar 

  • Clark SE, Running MP, Meyerowitz EM (1993) CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 2:397–418

    Google Scholar 

  • Clark SE, Williams RW, Meyerowitz EM (1997) The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 4:575–585

    Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 6339:31–37

    Google Scholar 

  • Coimbra S, Almeida J, Junqueira V, Costa ML, Pereira LG (2007) Arabinogalactan proteins as molecular markers in Arabidopsis thaliana sexual reproduction. J Exp Bot 15–16: 4027–4035

    Google Scholar 

  • Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ (1995) The Petunia MADS box gene FBP11 determines ovule identity. Plant Cell 11:1859–1868

    Google Scholar 

  • Colombo M, Masiero S, Vanzulli S, Lardelli P, Kater MM, Colombo L (2008) AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis. Plant J 6:1037–1048

    Google Scholar 

  • Colombo M, Brambilla V, Marcheselli R, Caporali E, Kater MM, Colombo L (2010) A new role for the SHATTERPROOF genes during Arabidopsis gynoecium development. Dev Biol 2:294–302

    Google Scholar 

  • Davidson EH (2007) The regulatory genome: gene regulatory networks in development and evolution. www.sciencep.com

    Google Scholar 

  • Deng Y, Dong H, Mu J, Ren B, Zheng B, Ji Z, Yang WC, Liang Y, Zuo J (2010) Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 4:1232–1248

    Google Scholar 

  • Dettmer J, Friml J (2011) Cell polarity in plants: when two do the same, it is not the same…. Curr Opin Cell Biol 6:686–696

    Google Scholar 

  • Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 21:1935–1940

    Google Scholar 

  • Drews GN, Koltunow AM (2011) The female gametophyte. Arabidopsis Book 9:e0155

    PubMed  Google Scholar 

  • Drews GN, Yadegari R (2002) Development and function of the angiosperm female gametophyte. Annu Rev Genet 36:99–124

    PubMed  CAS  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 2:155–168

    Google Scholar 

  • Evans MM (2007) The indeterminate gametophyte1 gene of maize encodes a LOB domain protein required for embryo sac and leaf development. Plant Cell 1:46–62

    Google Scholar 

  • Favaro R, Pinyopich A, Battaqlia R, Kooiker M, Borqhi L, Ditta G, Yanofsky MF, Kater MM, Colombo L (2003) MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell 11:2603–2611

    Google Scholar 

  • Flanagan CA, Hu Y, Ma H (1996) Specific expression of the AGL1 MADS-box gene suggests regulatory functions in Arabidopsis gynoecium and ovule development. Plant J 2:343–353

    Google Scholar 

  • Galla G, Zenoni S, Marconi G, Marino G, Botton A, Pinosa F, Citterio S, Ruperti B, Palme K, Albertini E, Pezzotti M, Mau M, Sharbel TF, De Storme N, Geelen D, Barcaccia G (2011) Sporophytic and gametophytic functions of the cell cycle-associated Mob1 gene in Arabidopsis thaliana L. Gene 1–2:1–12

    Google Scholar 

  • Gallagher TL, Gasser CS (2008) Independence and interaction of regions of the INNER OUTER protein in growth control during ovule development. Plant Physiol 1:306–315

    Google Scholar 

  • Gremski K, Ditta G, Yanofsky MF (2007) The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 20:3593–3601

    Google Scholar 

  • Gross-Hardt R, Lenhard M, Laux T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes Dev 16:1129–1138

    PubMed  CAS  Google Scholar 

  • Gussakovskaya MA, Blintsov AN (2001) Changes in cytokinin distribution in the ovule and ovary of Taraxacum officinale Web. in early stages of embryogenesis. Biochemistry (Mosc) 3:305–311

    Google Scholar 

  • Heisler MG, Atkinson A, Bylstra YH, Walsh R, Smyth DR (2001) SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. Development 7:1089–1098

    Google Scholar 

  • Hejátko J, Pernisová M, Eneva T, Palme K, Brzobohatý B (2003) The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. Mol Genet Genomics 4:443–453

    Google Scholar 

  • Hennig L, Taranto P, Walser M, Schönrock N, Gruissem W (2003) Arabidopsis MSI1 is required for epigenetic maintenance of reproductive development. Development 12:2555–2565

    Google Scholar 

  • Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 5534:1480–1483

    Google Scholar 

  • Huang HY, Jiang WB, Hu YW, Wu P, Zhu JY, Liang WQ, Wang ZY, Lin WH (2013) BR signal influences Arabidopsis ovule and seed number through regulating related genes expression by BZR1. Mol Plant 2:456–469

    Google Scholar 

  • Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 10:2149–2159

    Google Scholar 

  • Immink RG, Posé D, Ferrario S, Ott F, Kaufmann K, Valentim FL, de Folter S, van der Wal F, van Dijk AD, Schmid M, Angenent GC (2012) Characterization of SOC1’s central role in flowering by the identification of its upstream and downstream regulators. Plant Physiol 1:433–449

    Google Scholar 

  • Irish VF, Sussex IM (1990) Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell 8:741–753

    Google Scholar 

  • Ishida T, Aida M, Takada S, Tasaka M (2000) Involvement of CUPSHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol 1:60–67

    Google Scholar 

  • Jack T (2001) Plant development going MADS. Plant Mol Biol 5:515–520

    Google Scholar 

  • Jiang H, Wang FF, Wu YT, Zhou X, Huang XY, Zhu J, Gao JF, Dong RB, Cao KM, Yang ZN (2009) MULTIPOLAR SPINDLE 1 (MPS1), a novel coiled-coil protein of Arabidopsis thaliana, is required for meiotic spindle organization. Plant J 6:1001–1010

    Google Scholar 

  • Johnston AJ, Meier P, Gheyselinck J, Wuest SE, Federer M, Schlagenhauf E, Becker JD, Grossniklaus U (2007) Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte. Genome Biol 10:R204

    Google Scholar 

  • Kater MM, Franken J, van Aelst A, Angenent GC (2000) Suppression of cell expansion by ectopic expression of the Arabidopsis SUPERMAN gene in transgenic Petunia and tobacco. Plant J 3:407–413

    Google Scholar 

  • Katoh N, Lörz H, Kranz E (1997) Isolation of viable egg cells of rape (Brassica napus L.). Zygote 1:31–33

    Google Scholar 

  • Kaufmann K, Muiño JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3:integration of developmental and hormonal pathways in the Arabidopsis flower. PLos Biol 4:e1000090. doi: 10.1371/journal.pbio.1000090

    Google Scholar 

  • Kelley DR, Skinner DJ, Gasser CS (2009) Roles of polarity determinants in ovule development. Plant J 6:10541064

    Google Scholar 

  • Kieffer M, Davies B (2001) Developmental programmes in floral organ formation. Semin Cell Dev Biol 5:373–380

    Google Scholar 

  • Kim HU, Li Y, Huang AH (2005) Ubiquitous and endoplasmic reticulum-located lysophosphatidyl acyltransferase, LPAT2, is essential for female but not male gametophyte development in Arabidopsis. Plant Cell 4:1073–1089

    Google Scholar 

  • Klintenäs M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O (2012) Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol 4:1260–1273

    Google Scholar 

  • Kobayashi K, Maekawa M, Miyao A, Hirochika H, Kyozuka J (2010) PANICLE PHYTOMER2 (PAP2), encoding a SEPALLATA subfamily MADS-box protein, positively controls spikelet meristem identity in rice. Plant Cell Physiol 1:47–57

    Google Scholar 

  • Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka J (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. Plant Cell 5:1848–1859

    Google Scholar 

  • Koltunow AM, Johnson SD, Lynch M, Yoshihara T, Costantino P (2001) Expression of rolB in apomictic Hieracium piloselloides Vill. causes ectopic meristems in planta and changes in ovule formation, where apomixis initiates at higher frequency. Planta 2:196–205

    Google Scholar 

  • Kooiker M, Airoldi CA, Losa A, Manzotti PS, Finzi L, Kater MM, Colombo L (2005) BASIC PENTACYSTEINE1, a GA binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell 3:722–729

    Google Scholar 

  • Kou Y, Chang Y, Li X, Xiao J, Wang S (2012) The rice RAD51C gene is required for the meiosis of both female and male gametophytes and the DNA repair of somatic cells. J Exp Bot 14:5323–5335

    Google Scholar 

  • Kramer EM, Jaramillo MA, Di Stilio VS (2004) Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms. Genetics 2:1011–1023

    Google Scholar 

  • Krizek BA, Prost V, Macias A (2000) AINTEGUMENTA promotes petal identity and acts as a negative regulator AGAMOUS. Plant Cell 8:1357–1366

    Google Scholar 

  • Kubo T, Yoshimura A (2005) Epistasis underlying female sterility detected in hybrid breakdown in a Japonica-Indica cross of rice (Oryza sativa L). Theor Appl Genet 2:346–355

    Google Scholar 

  • Kwee HS, 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 6:853–866

    Google Scholar 

  • Lang JD, Ray S, Ray A (1994) sin 1, a mutation affecting female fertility in Arabidopsis, interacts with mod 1, its recessive modifier. Genetics 4:1101–1110

    Google Scholar 

  • Laudencia-Chingcuanco D, Hake S (2002) The indeterminate floral apex1 gene regulates meristem determinacy and identity in the maize inflorescence. Development 11:2629–2638

    Google Scholar 

  • Lee DS, Chen LJ, Li CY, Liu Y, Tan XL, Lu BR, Li J, Gan SX, Kang SG, Suh HS, Zhu Y (2013) The Bsister MADS gene FST determines ovule patterning and development of the zygotic embryo and endosperm. PLoS One 3:e58748

    Google Scholar 

  • León G, Holuigue L, Jordana X (2007) Mitochondrial complex II Is essential for gametophyte development in Arabidopsis. Plant Physiol. 4:1534–1546

    Google Scholar 

  • Lermontova I, Fuchs J, Schubert I (2008) The Arabidopsis checkpoint protein Bub3.1 is essential for gametophyte development. Front Biosci 13:5202–5211

    PubMed  CAS  Google Scholar 

  • Liu J, Zhang Y, Qin G, Tsuge T, Sakaguchi N, Luo G, Sun K, Shi D, Aki S, Zheng N, Aoyama T, Oka A, Yang W, Umeda M, Xie Q, Gu H, Qu LJ (2008) Targeted degradation of the cyclin-dependent kinase inhibitor ICK4/KRP6 by RING-type E3 ligases is essential for mitotic cell cycle progression during Arabidopsis gametogenesis. Plant Cell 6:1538–1554

    Google Scholar 

  • Liu M, Yuan L, Liu NY, Shi DQ, Liu J, Yang WC (2009) GAMETOPHYTIC FACOR1, involved in pre-mRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J Integr Plant Biol 3:261–271

    Google Scholar 

  • Liu DD, Dong QL, Fang MJ, Chen KQ, Hao YJ (2012) Ectopic expression of an apple apomixis-related gene MhFIE induces cosuppression and results in abnormal vegetative and reproductive development in tomato. J Plant Physiol18:1866–1873

    Google Scholar 

  • Liu C, Teo ZW, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H (2013) A conserved genetic pathway determines inflorescence architecture in Arabidopsis and rice. Dev Cell 6:612–622

    Google Scholar 

  • Lo HC, Wang YF (2001) Development of ovulate cones from initiation of reproductive buds to fertilization in Cephalotaxus wilsoniana Hay. Proc Natl Sci Counc Repub China B 2:97–118

    Google Scholar 

  • Losa A, Colombo M, Brambilla V, Colombo L (2010) Genetic interaction between AINTEGUMENTA (ANT) and the ovule identity genes SEEDSTICK (STK), SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2). Sex Plant Reprod 2:115–121

    Google Scholar 

  • Makkena S, Lee E, Sack FD, Lamb RS (2012) The R2R3 MYB transcription factors FOUR LIPS and MYB88 regulate female reproductive development. J Exp Bot 15:5545–5558

    Google Scholar 

  • Márton ML, Dresselhaus T (2010) Female gametophyte-controlled pollen tube guidance. Biochem Soc Trans 2:627–630

    Google Scholar 

  • Matias-Hernandez L, Battaglia R, Galbiati F, Rubes M, Eichenberger C, Grossniklaus U, Kater MM, Colombo L (2010) VERDANDI is a direct target of the MADS domain ovule identity complex and affects embryo sac differentiation in Arabidopsis. Plant Cell 6:1702–1715

    Google Scholar 

  • Meister RJ, Oldenhof H, Bowman JL, Gasser CS (2005) Multiple protein regions contribute to differential activities of YABBY proteins in reproductive development. Plant Physiol 2:651–662

    Google Scholar 

  • Meister RJ, Kotow LM, Gasser CS (2002) SUPERMAN attenuates INNER NO OUTER antoregulation to maintain polar development of Arabidopsis ovule outer integuments. Development 18:4281–4289

    Google Scholar 

  • Melzer R, Wang YQ, Theissen G (2010) The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower. Semin Cell Dev Biol 1:118–128

    Google Scholar 

  • Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 2:942–947

    Google Scholar 

  • Mizumoto K, Hatano H, Hirabayashi C, Murai K, Takumi S (2009) Altered expression of wheat AINTEGUMENTA homolog, WANT-1, in pistil and pistil-like transformed stamen of an alloplasmic line Aegilops crassa cytoplasm. Dev Genes Evol 4:175–187

    Google Scholar 

  • Mól R, Filek M, Machackova I, Matthys-Rochon E (2004) Ethylene synthesis and auxin augmentation in pistil tissues are important for egg cell differentiation after pollination in maize. Plant Cell Physiol 10:1396–1405

    Google Scholar 

  • Molinero-Rosales N, Latorre A, Jamilena M, Lozano R (2004) SINGLE FLOWER TRUSS regulates the transition and maintenance of flowering in tomato. Planta 3:427–434

    Google Scholar 

  • Moll C, von Lyncker L, Zimmermann S, Kägi C, Baumann N, Twell D, Grossniklaus U, Gross-Hardt R (2008) CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J 6:913–921

    Google Scholar 

  • Moody SA (2007) Principles of developmental genetics. www.sciencep.com

    Google Scholar 

  • Müller B, Sheen J (2007) Arabidopsis cytokinin signaling pathway. Sci STKE 407:cm5

    Google Scholar 

  • Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nuture 7367:119–122

    Google Scholar 

  • Nole-Wilson S, Rueschhoff EE, Bhatti H, Franks RG (2010) Synergistic disruptions in seuss cyp85A2 double mutants reveal a role for brassinolide synthesis during gynoecium and ovule development. BMC Plant Biol 10:198

    PubMed  Google Scholar 

  • Oh TJ, Wartell RM, Cairney J, Pullman GS (2008) Evidence for stage-specific modulation of specific microRNAs (miRNAs) and miRNA processing components in zygotic embryo and female gametophyte of loblolly pine (Pinus taeda). New Phytol 1:67–80

    Google Scholar 

  • Ohmori S, Kimizu M, Sugita M, Miyao A, Hirochika H, Uchida E, Nagato Y, Yoshida H (2009) MOSAIC FLORAL ORGANS1, an AGL6-like MADS box gene, regulates floral organ identity and meristem fate in rice. Plant Cell 10:3008–3025

    Google Scholar 

  • Ordidge M, Chiurugwi T, Tooke F, Battey NH (2005) LEAFY, TERMINAL FLOWER1 and AGAMOUS are functionally conserved but do not regulate terminal flowering and floral determinacy in Impatiens balsamina. Plant J 6:985–1000

    Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gemtophyte. Science 5935:1684–1689

    Google Scholar 

  • Pagnussat GC, Yu HJ, Sundaresan V (2007) Cell-fate switch of synergid to egg cell in Arabidopsis eostre mutant embryo sacs arises from misexpression of the BEL-like homeodomain gene BLH1. Plant Cell 11:3578–3592

    Google Scholar 

  • Palmer RG, Sandhu D, Curran K, Bhattacharyya MK (2008) Molecular mapping of 36 soybean male-sterile, female-sterile mutants. Theor Appl Genet 5:711–719

    Google Scholar 

  • Park SO, Zheng Z, Oppenheimer DG, Hauser BA (2005) The PRETTY FEW SEEDS2 gene encodes an Arabidopsis homedomain protein that regulates ovule development. Development 4:841–849

    Google Scholar 

  • Pereira T, Lersten N, Palmer R (1997) Genetic and cytological analyses of a partial-female-sterile mutant (PS-1) in soybean (Glycine Max; Leguminosae). Am J Bot 6:781–791

    Google Scholar 

  • Pérez-España VH, Sánchez-León N, Vielle-Calzada JP (2011) CYP85A1 is required for the initial of female gametogenesis in Arabidopsis thaliana. Plant Signal Behav 3:321–326

    Google Scholar 

  • Pillitteri LJ, Bemis SM, Shpak ED, Torii KU (2007) Haploinsuficiency after successive loss of signaling a role for ERECTA-family genes in Arabidopsis ovule development. Development 17:3099–3109

    Google Scholar 

  • Pinyopich A, Ditta GS, Savidge B, Liljegren SJ, Baumann E, Wisman E, Yanofsky MF (2003) Assessing the redundancy of MADSbox genes during carpel and ovule development. Nature 6944: 85–88

    Google Scholar 

  • Pischke MS, Jones LG, Otsuga D, Fernandez DE, Drews GN, Sussman MR (2002) An Arabidopsis histidine kinase is essential for megagametogenesis. Proc Natl Acad Sci USA 24: 15800–15805

    Google Scholar 

  • Portereinko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18:1862–1872

    Google Scholar 

  • Punwani JA, Rabiger DS, Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed encoding filiform apparatus localized proteins. Plant Cell 8:2557–2568

    Google Scholar 

  • Punwani JA, Rabiger DS, Lloyd A, Drews GN (2008) The MYB98 subcircuit of the synergid gene regulatory network includes genes directly and indirectly regulated by MYB98. Plant J 3:406–414

    Google Scholar 

  • Quan L, Xiao R, Li W, Oh SA, Kong H, Ambrose JC, Malcos JL, Cyr R, Twell D, Ma H (2008) Functional divergence of the duplicated AtKIN14a and AtKIN14b genes: critical roles in Arabidopsis meiosis and gametophyte development. Plant J 6:1013–1026

    Google Scholar 

  • Raval J, Baumbach J, Ollhoff AR, Pudake RN, Palmer RG, Bhattacharyya MK, Sandhu D (2013) A candidate male-fertility female-fertility gene tagged by the soybean endogenous transposon, Tgm9. Funct Integr Genomics 1:67–73

    Google Scholar 

  • Ray S, Golden T, Ray A (1996) Maternal effects of the short integument mutation on embryo development in Arabidopsis. Dev Biol 1:365–369

    Google Scholar 

  • Ray A, Lang JD, Golden T, Ray S (1996) SHORT INTEGUMENT (SIN1), a gene required for ovule development in Arabidopsis, also controls flowering time. Development 9:2631–2638

    Google Scholar 

  • Ray A, Robinson-Beers K, Ray S, Baker SC, Lang JD, Preuss D, Milligan SB, Gasser CS (1994) Arabidopsis floral homeotic gene BELL (BEL1) controls ovule development through negative regulation of AGAMOUS gene (AG). Proc Natl Acad Sci USA 13:5761–5765

    Google Scholar 

  • Reiser L, Fischer RL (1993) The ovule and the embryo sac. Plant Cell 10:1291–1301

    Google Scholar 

  • Rieu I, Bots M, Mariani C, Weterings KA (2005) Isolation and expression analysis of a tobacco AINTEGUMENTA ortholog (NtANTL). Plant Cell Physiol 5:803–805

    Google Scholar 

  • Rijpkema AS, Zethof J, Gerats T, Vandenbussche M (2009) The Petunia AGL6 gene has a SEPALLATA-like function in floral patterning. Plant J 1:1–9

    Google Scholar 

  • Robinson-Beers K, Pruitt RE, Gasser CS (1992) Ovule development in wild-type Arabidopsis and two female-sterile mutants. Plant Cell 10:1237–1249

    Google Scholar 

  • Roe JL, Nemhauser JL, Zambryski PC (1997) TOUSLED participates in apical tissue formation during gynoecium development in Arabidopsis. Plant Cell 3:335–353

    Google Scholar 

  • Sakai S (2013) Evolutionarily stable size of a megagametophyte: evolution of tiny megagametophytes of angiosperms from large ones of gymnosperms. Evolution 2:539–547

    Google Scholar 

  • Schiefthaler U, Balasubramanian S, Sieber P, Chevalier D, Wisman E, Schneitz K (1999) Molecular analysis of NOZZLE, a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana. Proc Natl Acad Sci USA 20:11664–11669

    Google Scholar 

  • Schneitz K, Hülskamp M, Kopczak SD, Pruitt RE (1997) Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 7:1367–1376

    Google Scholar 

  • Scofield S, Dewitte W, Murray JA (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J 5:767–781

    Google Scholar 

  • Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell. 9:877–892

    Google Scholar 

  • Shi DQ, Yang WC (2011) Ovule development in Arabidopsis: progress and challenge. Curr Opin Plant Biol 1:74–18

    Google Scholar 

  • Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 7:1491–1501

    Google Scholar 

  • Sicard A, Hernould M, Chevalier C (2008) The INHIBITOR OF MERISTEM ACTIVITY (IMA) protein: the nexus between cell division, differentiation and hormonal control of development. Plant Signal Behav 10:908–910

    Google Scholar 

  • Sicard A, Petit J, Mouras A, Chevalier C, Hernould M (2008) Meristem activity during flower and ovule development in tomato is controlled by the mini zinc finger gene INHIBITOR OF MERISTEM ACTIVITY. Plant J 3: 415–427

    Google Scholar 

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

    Google Scholar 

  • Sieber P, Petrascheck M, Barberis A, Schneitz K (2004) Organ polarity in Arabidopsis. NOZZLE physically interacts with members of the YABBY family. Plant Physiol 4:2172–2185

    Google Scholar 

  • Skinner DJ, Baker SC, Meister RJ, Broadhvest J, Schneitz K, Gasser CS (2001) The Arabidopsis HUELLENLOS gene, which is essential for normal ovule development, encodes a mitochondrial ribosomal protein. Plant Cell 12:3719–2730

    Google Scholar 

  • Skinner DJ, Hill TA, Gasser CS (2004) Regulation of ovule development. Plant Cell 16: S32–S45

    PubMed  CAS  Google Scholar 

  • Skinner DJ, Gasser CS (2009) Expression-based discovery of candidate ovule development regulators through transcriptional profiling of ovule mutants. BMC Plant Biol 9:29

    PubMed  Google Scholar 

  • Sprunck S, Gross-Hardt R (2011) Nuclear behavior, cell polarity, and cell specification in the female gametophyte. Sex Plant Reprod 2:123–136

    Google Scholar 

  • Steffen JG, Kang IH, Macfarlane J, Drews GN (2007) Identification of genes expressed in the Arabidopsis female gametophyte. Plant 2:281–292

    Google Scholar 

  • Steffen JG, Kang IH, Portereiko MF, Lloyd A, Drews GN (2008) AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol 1:259–268

    Google Scholar 

  • Stevens R, Grelon M, Vezon D, Oh J, Meyer P, Perennes C, Domenichini S, Bergounioux C (2004) A CDC45 homolog in Arabidopsis is essential for meiosis, as shown by RNA interference-induced gene silencing. Plant Cell 1:99–113

    Google Scholar 

  • Stone JM, Trotochaud AE, Walker JC, Clark SE (1998) Control of meristem development by CLAVATA1 receptor kinase and kinaseassociated protein phosphatase interactions. Plant Physiol 4:1217–1225

    Google Scholar 

  • Sun K, Cui Y, Hauser BA (2005) Environmental stress alters genes expression and induces ovule abortion: reactive oxygen species appear as ovules commit to abort. Planta 4: 632–642

    Google Scholar 

  • Sundaresan V, Alandete-Saez M (2010) Pattern formation in miniature: the female gametophyte of flowering plants. Development 2:179–189

    Google Scholar 

  • Tavares A, Goncalves J, Florindo C, Tavares AA, Soares H (2012) Mob1: defining cell polarity for proper cell division. J Cell Sci 125(Pt2):516–527

    PubMed  CAS  Google Scholar 

  • Teeri TH, Uimari A, Kotilainen M, Laitinen R, Help H, Elomaa P, Albert VA (2006) Reproductive meristem fates in Gerbera. J Exp Bot 13:3445–3455

    Google Scholar 

  • Tooke F, Ordidge M, Chiurugwi T, Battey N (2005) Mechanisms and function of flower and inflorescence reversion. J Exp Bot 420:2587–2599

    Google Scholar 

  • Tsai WC, Lee PF, Chen HI, Hsiao YY, Wei WJ, Pan ZJ, Chuang MH, Kuoh CS, Chen WH, Chen HH (2005) PeMADS, a GLOBOSA/PISTILLATA-like gene in Phalaenopsis equestris involved in petaloid formation, and correlated with flower longevity and ovary development. Plant Cell Physiol 7:1125–1139

    Google Scholar 

  • Urbanus SL, Folter S, Shchennikova AV, Kaufmann K, Immink RG, Angenent GC (2009) In planta localization patterns of MADS domain proteins during floral development in Arabidopsis thaliana. BMC Plant Biology 9:5

    PubMed  Google Scholar 

  • Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T (2003) Toward the analysis of the Petunia MADS box gene family by reverse and forward transposon insertion mutagenesis Approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in Petunia. Plant Cell 11:2680–2693

    Google Scholar 

  • Vanneste S, Friml (2009) Auxin: A trigger for change in plant development. Cell 6:1005–1016

    Google Scholar 

  • Vielle-Calzada JP, Hernández-Lagana E, Rodríguez-Leal D, I Rodríguez-Arévalo, León-Martínez G, Abad-Vivero U, Demesa-Arévalo E, Armenta-Medina A, Alvarez-Mejía C (2012) Reproductive versatility and the epigenetic control of female gametogenesis. Cold Spring Harb Symp Quant Biol 77:17–21

    PubMed  Google Scholar 

  • Villanueva JM., Broadhvest J, Hauser BA, Meister RJ, Schneitz K, Gasser CS (1999) INNER NO OUTER regulates abaxial-adaxial patterning in Arabidopsis ovules. Genes Dev 23:3160–3169

    Google Scholar 

  • Wagner D, Meyerowitz EM (2002) SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr Biol 2:85–94

    Google Scholar 

  • Wang Y, Hou Y, Gu H, Kang D, Chen ZL, Liu J, Qu LJ (2013) The Arabidopsis anaphase-promoting complex/cyclosome subunit 1 is critical for both female gametogenesis and embryogenesis (F). J Integr Plant Biol 1:64–74

    Google Scholar 

  • Weigel D (1995) The genetics of flower development: from floral induction to ovule morphogenesis. Annu Rev Genet 29:19–39

    PubMed  CAS  Google Scholar 

  • Wu H, Cui DF, Hu ZH (2000) Initiation and development of the ovulate strobilus in Pinus tabulaeformis. Acta Botanica Sinica 4:353–357

    Google Scholar 

  • Wu MF, Tian Q, Reed JW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 21:4211–4218

    Google Scholar 

  • Xiang L, Li X, Qin D, Guo F, Wu C, Miao L, Sun C (2012) Functional analysis of FLOWERING LOCUS T orthologs from spring orchid (Cymbidium goeringii Rchb. f.) that regulates the vegetative to reproductive transition. Plant Physiol Biochem 58:98–105

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Yanagida M, Yamashita YM, Tatebe H, Ishii K, Kumada K, Nakaseko Y (1999) Control of metaphase-anaphase progression by proteolysis: cyclosome function regulated by the protein kinase A pathway, ubiquitination and localization. Philos Trans R Soc Lond B Biol Sci 1389:1559–1569

    Google Scholar 

  • Yang WC, Shi DQ (2007) Research advances in plant female gametogenesis. Chinese Bulletin of Botany 3:302–310

    Google Scholar 

  • Yu HJ, Hogan P, Sundaresan V (2005) Analysis of the female gametophyte transcriptome of Arabidopsis by comparative expression profiling. Plant Physiol 4:1853–1869

    Google Scholar 

  • Yu LX, Yao YL, Wu XL, Tang XQ, Yan B (2012) Alternative splicing of flowering regulatory gene LFY in Arabidopsis thaliana. Guihaia 3:371–376

    Google Scholar 

  • Yuan L, Yang X, Ellis JL, Fisher NM, Makaroff CA (2012) The Arabidopsis SYN3 cohensin protein is important for early meiotic events. Plant J 1:147–160

    Google Scholar 

  • Zhang HX, Li FL, Shen XH, Li GF, Yang XH (1997) Formation of male and female gametophytes and development of embryo in Pinus tabulaeformis Carr. Journal of Beijing Forestry University 3:1–7

    Google Scholar 

  • Zhang Z, Clayton SC, Cui K, Lee C (2013) Developmental synchronization of male and female gametophytes in Ginkgo biloba and its neck mother cell division prior to fertilization. Physiol Plant 4:541–552

    Google Scholar 

  • Zhao XY, Cheng ZJ, Zhang XS (2006) Overexpression of TaMADS1, a SEPALLATA-like gene in wheat, causes early flowering and the abnormal development of floral organs in Arabidopsis. Planta 4:698–707

    Google Scholar 

  • Zhou LH, Jiang CN, Zheng CX (2006) Determination of ovule development of Pinus tabulaeformis Beijing, China. Acta Botanica Boreali-Occidentalia Sinca 12:2583–2586

    Google Scholar 

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Guo, A., Zheng, C.X. Female gametophyte development. J. Plant Biol. 56, 345–356 (2013). https://doi.org/10.1007/s12374-013-0131-5

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