Skip to main content
Log in

Male gametogenesis and germline specification in flowering plants

  • Review
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

During angiosperm male gametophyte development, the male germline is segregated by an asymmetric cell division of the haploid microspore. This review encompasses recent advances in understanding the genetic and molecular mechanisms involved in generating the male germline from this pluripotent germline initial and in specifying the production of the twin sperm cells required for double fertilization. Genetic studies and access to the transcriptome of isolated gametes have enabled remarkable progress in understanding some of the key regulators that control and integrate germ cell cycle progression with germline specification, and an emerging regulatory model is presented. Rapid advances have also been made in understanding epigenetic regulation and small RNA pathways in the male gametophyte and germline that impact on genome integrity and gamete development, traits that are shared with animal germlines. The review concludes with a perspective of the outstanding issues and directions of future research that will further our understanding of germline specification and the gametophytic control of pollen development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

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 1:586–598

    Article  PubMed  CAS  Google Scholar 

  • Albert M, Peters AH (2009) Genetic and epigenetic control of early mouse development. Curr Opin Genet Dev 19:113–121

    Article  PubMed  CAS  Google Scholar 

  • Aw SJ, Hamamura Y, Chen Z, Schnittger A, Berger F (2010) Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development 137:2683–2690

    Article  PubMed  CAS  Google Scholar 

  • Baarends WM, Hoogerbrugge JW, Roest HP, Ooms M, Vreeburg J, Hoeijmakers JH, Grootegoed JA (1999) Histone ubiquitination and chromatin remodeling in mouse spermatogenesis. Dev Biol 207:322–333

    Article  PubMed  CAS  Google Scholar 

  • Berger F, Twell D (2011) Germline specification and function in plants. Annu Rev Plant Biol (in press)

  • Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181

    Article  PubMed  CAS  Google Scholar 

  • Brown RC, Lemmon BE (1991) Pollen development in orchids. 3. A novel generative pole microtubule system predicts unequal pollen mitosis. J Cell Sci 99:273–281

    Google Scholar 

  • Brown RC, Lemmon BE (1992) Pollen development in orchids. 4. Cytoskeleton and ultrastructure of the unequal pollen mitosis in Phalaenopsis. Protoplasma 167:183–192

    Article  Google Scholar 

  • Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009a) A plant germline-specific integrator of sperm specification and cell cycle progression. PLoS Genet 5:e1000430

    Article  PubMed  Google Scholar 

  • Brownfield L, Hafidh S, Durbarry A, Khatab H, Sidorova A, Doerner P, Twell D (2009b) Arabidopsis DUO POLLEN3 is a key regulator of male germline development and embryogenesis. Plant Cell 21:1940–1956

    Article  PubMed  CAS  Google Scholar 

  • Cartagena JA, Matsunaga S, Seki M, Kurihara D, Yokoyama M, Shinozaki K, Fujimoto S, Azumi Y, Uchiyama S, Fukui K (2008) The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315:355–368

    Article  PubMed  CAS  Google Scholar 

  • Chambers C, Shuai B (2009) Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol 9:87

    PubMed  Google Scholar 

  • Chen Z, Tan JLH, Ingouff M, Sundaresan V, Berger F (2008) Chromatin Assembly Factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana. Development 135:65–73

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Hafidh S, Poh SH, Twell D, Berger F (2009) Proliferation and cell fate establishment during Arabidopsis male gametogenesis depends on the retinoblastoma protein. Proc Natl Acad Sci USA 106:7257–7262

    Article  PubMed  CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    Article  PubMed  CAS  Google Scholar 

  • Corpet A, Almouzni G (2009) Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. Trends Cell Biol 19:29–41

    Article  PubMed  CAS  Google Scholar 

  • Dickinson HG, Grant-Downton R (2009) Bridging the generation gap: flowering plant gametophytes and animal germlines reveal unexpected similarities. Biol Rev Camb Philos Soc 84:589–615

    Article  PubMed  Google Scholar 

  • Doelling JH, Phillips AR, Soyler-Ogretim G, Wise J, Chandler J, Callis J, Otegui MS, Vierstra RD (2007) The ubiquitin-specific protease subfamily UBP3/UBP4 is essential for pollen development and transmission in Arabidopsis. Plant Physiol 145:801–813

    Article  PubMed  CAS  Google Scholar 

  • Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137:297–307

    Article  PubMed  CAS  Google Scholar 

  • Eady C, Lindsey K, Twell D (1995) The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7:65–74

    Article  PubMed  CAS  Google Scholar 

  • Engel ML, Chaboud A, Dumas C, McCormick S (2003) Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 34:697–707

    Article  PubMed  CAS  Google Scholar 

  • Engel ML, Holmes-Davis R, McCormick S (2005) Green sperm. Identification of male gamete promoters in Arabidopsis. Plant Physiol 138:2124–2133

    Article  PubMed  CAS  Google Scholar 

  • FitzGerald J, Luo M, Chaudhury A, Berger F (2008) DNA methylation causes predominant maternal controls of plant embryo growth. PLoS One 3:e2298

    Article  PubMed  Google Scholar 

  • Friedman WE (1999) Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development 126:1065–1075

    PubMed  CAS  Google Scholar 

  • Friedman L, Santa Anna-Arriola S, Hodgkin J, Kimble J (2000) gon-4, a cell lineage regulator required for gonadogenesis in Caenorhabditis elegans. Dev Biol 228:350–362

    Article  PubMed  CAS  Google Scholar 

  • Gou X, Yuan T, Wei X, Russell SD (2009) Gene expression in the dimorphic sperm cells of Plumbago zeylanica: transcript profiling, diversity, and relationship to cell type. Plant J 60:33–47

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton R (2010) Through a generation darkly: small RNAs in the gametophyte. Biochem Soc Trans 38:617–621

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton R, Hafidh S, Twell D, Dickinson HG (2009a) Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2:500–512

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton R, Le Trionnaire G, Schmid R, Rodriguez-Enriquez J, Hafidh S, Mehdi S, Twell D, Dickinson H (2009b) MicroRNA and tasiRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10:643

    Article  PubMed  Google Scholar 

  • Gusti A, Baumberger N, Nowack M, Pusch S, Eisler H, Potuschak T, De Veylder L, Schnittger A, Genschik P (2009) The Arabidopsis thaliana F-box protein FBL17 is essential for progression through the second mitosis during pollen development. PLoS One 4:e4780

    Article  PubMed  Google Scholar 

  • Haerizadeh F, Singh MB, Bhalla PL (2006) Transcriptional repression distinguishes somatic from germ cell lineages in a plant. Science 313:496–499

    Article  PubMed  CAS  Google Scholar 

  • Hajkova P, Ancelin K, Waldmann T, Lacoste N, Lange UC, Cesari F, Lee C, Almouzni G, Schneider R, Surani MA (2008) Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452:877–881

    Article  PubMed  CAS  Google Scholar 

  • Hallmann A (2011) Evolution of the germline in volvocine algae. Sex Plant Reprod (in press)

  • Hause G, Hause B, van Lammeren AAM (1991) Microtubular and actin-filament configurations during microspore and pollen development in Brassica napus L. cv. Topas. Can J Bot 70:1369–1376

    Article  Google Scholar 

  • Hayashi K, Surani MA (2009) Resetting the epigenome beyond pluripotency in the germline. Cell Stem Cell 4:493–498

    Article  PubMed  CAS  Google Scholar 

  • Hemberger M, Dean W, Reik W (2009) Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington’s canal. Nat Rev Mol Cell Biol 10:526–537

    Article  PubMed  CAS  Google Scholar 

  • Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85

    Article  PubMed  Google Scholar 

  • Horvitz HR, Herskowitz I (1992) Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68:237–255

    Article  PubMed  CAS  Google Scholar 

  • Ingouff M, Berger F (2010) Histone3 variants in plants. Chromosoma 119:17–23

    Article  Google Scholar 

  • Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F (2007) Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol 17:1032–1037

    Article  PubMed  CAS  Google Scholar 

  • Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831

    Article  PubMed  CAS  Google Scholar 

  • Janousek B, Zluvova J, Vyscot B (2000) Histone H4 acetylation and DNA methylation dynamics during pollen development. Protoplasma 211:116–122

    Article  CAS  Google Scholar 

  • Johnston AJ, Matveeva E, Kirioukhova O, Grossniklaus U, Gruissem W (2008) A dynamic reciprocal RBR-PRC2 regulatory circuit controls Arabidopsis gametophyte development. Curr Biol 18:1680–1686

    Article  PubMed  CAS  Google Scholar 

  • Jullien PE, Berger F (2010) DNA methylation reprogramming during plant sexual reproduction? Trends Genet (in press)

  • Jullien PE, Kinoshita T, Ohad N, Berger F (2006) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18:1360–1372

    Article  PubMed  CAS  Google Scholar 

  • Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F (2008) Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6:e194

    Article  PubMed  Google Scholar 

  • Kim HJ, Oh SA, Brownfield L, Hong SH, Ryu H, Hwang I, Twell D, Nam HG (2008) Control of plant germline proliferation by SCFFBL17 degradation of cell cycle inhibitors. Nature 455:1134–1137

    Article  PubMed  CAS  Google Scholar 

  • Le Trionnaire G, Twell D (2010) Small RNAs in angiosperm gametophytes: from epigenetics to gamete development. Genes Dev 24:1081–1085

    Article  PubMed  CAS  Google Scholar 

  • Lee YR, Li Y, Liu B (2007) Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19:2595–2605

    Article  PubMed  CAS  Google Scholar 

  • Li C, Potuschak T, Colon-Carmona A, Gutierrez RA, Doerner P (2005) Arabidopsis TCP20 links regulation of growth and cell division control pathways. Proc Natl Acad Sci USA 102:12978–12983

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Du L, Osato M, Teo EH, Qian F, Jin H, Zhen F, Xu J, Guo L, Huang H, Chen J, Geisler R, Jiang YJ, Peng J, Wen Z (2007) The zebrafish udu gene encodes a novel nuclear factor and is essential for primitive erythroid cell development. Blood 110:99–106

    Article  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 20:1538–1554

    Article  PubMed  CAS  Google Scholar 

  • Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2006) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64–71

    Article  PubMed  CAS  Google Scholar 

  • Mu RL, Cao YR, Liu YF, Lei G, Zou HF, Liao Y, Wang HW, Zhang WK, Ma B, Du JZ, Yuan M, Zhang JS, Chen SY (2009) An R2R3-type transcription factor gene AtMYB59 regulates root growth and cell cycle progression in Arabidopsis. Cell Res 19:1291–1304

    Article  PubMed  CAS  Google Scholar 

  • Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19:2583–2594

    Article  PubMed  CAS  Google Scholar 

  • Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell KA, Boeke JD (2007) Mighty Piwis defend the germline against genome intruders. Cell 129:37–44

    Article  PubMed  Google Scholar 

  • Oakeley EJ, Podesta A, Jost J-P (1997) Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc Natl Acad Sci USA 94:11721–11725

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Johnson A, Smertenko A, Rahman D, Park SK, Hussey PJ, Twell D (2005) A divergent cellular role for the FUSED kinase family in the plant-specific cytokinetic phragmoplast. Curr Biol 15:2107–2111

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Bourdon V, Das ‘Pal M, Dickinson H, Twell D (2008) Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol Plant 1:794–799

    Article  PubMed  CAS  Google Scholar 

  • Oh SA, Pal MD, Park SK, Johnson JA, Twell D (2010) The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J Exp Bot 61:969–981

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Endo M, Singh MB, Bhalla PL (2005) Analysis of the histone H3 gene family in Arabidopsis and identification of the male-gamete-specific variant AtMGH3. Plant J 44:557–568

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Bhalla PL, Singh MB (2006a) Expressed sequence tag analysis of Lilium longiflorum generative cells. Plant Cell Physiol 47:698–705

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Singh MB, Bhalla PL (2006b) Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol Biol 62:503–512

    Article  PubMed  CAS  Google Scholar 

  • Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M, Demesa-Arévalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–632

    Article  PubMed  CAS  Google Scholar 

  • Ooi SL, Henikoff S (2007) Germline histone dynamics and epigenetics. Curr Opin Cell Biol 19:257–265

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–1689

    Article  PubMed  CAS  Google Scholar 

  • Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799

    PubMed  CAS  Google Scholar 

  • Park SK, Rahman D, Oh SA, Twell D (2004) gemini pollen 2, a male and female gametophytic cytokinesis defective mutation. Sex Plant Reprod 17:63–70

    Article  PubMed  CAS  Google Scholar 

  • Pastuglia M, Azimzadeh J, Goussot M, Camilleri C, Belcram K, Evrard JL, Schmit AC, Guerche P, Bouchez D (2006) Gamma-tubulin is essential for microtubule organization and development in Arabidopsis. Plant Cell 18:1412–1425

    Article  PubMed  CAS  Google Scholar 

  • Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756

    Article  PubMed  CAS  Google Scholar 

  • Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5:e1000621

    Article  PubMed  Google Scholar 

  • Ron M, Saez MA, Williams LE, Fletcher JC, McCormick S (2010) Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24:1010–1021

    Article  PubMed  CAS  Google Scholar 

  • Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248

    Article  PubMed  CAS  Google Scholar 

  • Sakai N, Sawada MT, Sawada H (2004) Non-traditional roles of ubiquitin–proteasome system in fertilization and gametogenesis. Int J Biochem Cell Biol 36:776–784

    Article  PubMed  CAS  Google Scholar 

  • Sasaki H, Matsui Y (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9:129–140

    Article  PubMed  CAS  Google Scholar 

  • Saze H (2008) Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 19:527–536

    Article  PubMed  Google Scholar 

  • Schoft VK, Chumak N, Mosiolek M, Slusarz L, Komnenovic V, Brownfield L, Twell D, Kakutani T, Tamaru H (2009) Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep 10:1015–1021

    Article  PubMed  CAS  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijó JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    Article  PubMed  CAS  Google Scholar 

  • Sprunck S, Groß-Hardt R (2011) Nuclear behavior, cell polarity and cell specification in the female gametophyte. Sex Plant Reprod 24 (this issue)

  • Strome S, Lehmann R (2007) Germ versus soma decisions: lessons from flies and worms. Science 316:392–393

    Article  PubMed  CAS  Google Scholar 

  • Tanaka I, Ito M (1980) Induction of typical cell division in isolated microspores of Lilium longiflorum and Tulipa gesneriana. Plant Sci Lett 17:279–285

    Article  Google Scholar 

  • Tanaka I, Ito M (1981) Control of division patterns in explanted microspores of Tulipa gesneriana. Protoplasma 108:329–340

    Article  Google Scholar 

  • Tanaka I, Ono K, Fukuda T (1998) The developmental fate of angiosperm pollen is associated with a preferential decrease in the level of histone H1 in the vegetative nucleus. Planta 206:561–569

    Article  CAS  Google Scholar 

  • Terasaka O, Niitsu T (1987) Unequal cell division and chromatin differentiation in pollen grain cells. I. Centrifugal, cold and caffeine treatments. Bot Mag Tokyo 100:205–216

    Article  Google Scholar 

  • Terasaka O, Niitsu T (1995) The mitotic apparatus during microspore division observed by a confocal laser scanning microscope. Protoplasma 189:187–193

    Article  Google Scholar 

  • Thomson T, Lin H (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 25:355–376

    Article  PubMed  CAS  Google Scholar 

  • Twell D, Park SK, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  • Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ (2002) MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 4:711–714

    Article  PubMed  CAS  Google Scholar 

  • Ueda K, Tanaka I (1995) The appearance of male gamete-specific histones gH2B and gH3 during pollen development in Lilium longiflorum. Dev Biol 169:210–217

    Article  PubMed  CAS  Google Scholar 

  • Ueda K, Kinoshita Y, Xu ZJ, Ide N, Ono M, Akahori Y, Tanaka I, Inoue M (2000) Unusual core histones specifically expressed in male gametic cells of Lilium longiflorum. Chromosoma 108:491–500

    Article  PubMed  CAS  Google Scholar 

  • von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133:4761–4769

    Article  Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed  CAS  Google Scholar 

  • Weterings K, Reijnen W, van Aarssen R, Kortstee A, Spijkers J, van Herpen M, Schrauwen J, Wullems G (1992) Characterization of a pollen-specific cDNA clone from Nicotiana tabacum expressed during microgametogenesis and germination. Plant Mol Biol 18:1101–1111

    Article  PubMed  CAS  Google Scholar 

  • Wuest SE, Vijverberg K, Schmidt A, Weiss M, Gheyselinck J, Lohr M, Wellmer F, Rahnenfuhrer J, von Mering C, Grossniklaus U (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20:506–512

    Article  PubMed  CAS  Google Scholar 

  • Xu H, Swoboda I, Bhalla PL, Singh MB (1999) Male gametic cell-specific expression of H2A and H3 histone genes. Plant Mol Biol 39:607–614

    Article  PubMed  CAS  Google Scholar 

  • Zaki MAM, Dickinson HG (1991) Microspore-derived embryos in Brassica: the significance of division asymmetry in pollen mitosis I to embryogenic development. Sex Plant Reprod 4:48–55

    Article  Google Scholar 

  • Zilberman D (2008) The evolving functions of DNA methylation. Curr Opin Plant Biol 11:554–559

    Article  PubMed  CAS  Google Scholar 

  • Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  PubMed  CAS  Google Scholar 

  • Zonia LTJ, Staiger CJ (1999) Unique actin and microtubule arrays co-ordinate the differentiation of microspores to mature pollen in Nicotiana tabacum. J Exp Bot 50:581–594

    Article  CAS  Google Scholar 

Download references

Acknowledgments

I thank Twell lab members and Fred Berger, Hugh Dickinson and Robert Grant-Downton for their support and valued discussions on the topics reviewed, and two anonymous reviewers for helpful suggestions. DT is funded by the UK Biotechnology and Biological Research Council.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to David Twell.

Additional information

Communicated by Thomas Dresselhaus.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Twell, D. Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24, 149–160 (2011). https://doi.org/10.1007/s00497-010-0157-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-010-0157-5

Keywords

Navigation