Gametogenesis

Abstract

Gametogenesis is the process of gamete formation, which includes micro‐ and megagametogenesis. Gametogenesis initiates after specialized cells in the sporophyte undergo meiosis, and subsequent mitotic divisions yield the gametophytic phase of the plant life cycle. In higher plants, microgametogenesis occurs in the anther, producing tricellular pollen with two sperm cells within a vegetative cell. Megagametogenesis occurs in the ovule, producing an embryo sac. The male gametes, the two sperm cells, and the female gametes, the egg and central cell, fuse to yield the zygote and the endosperm, respectively. Both micro‐ and megagametogenesis are under strict genetic control. Studies of gametophytic mutants have identified genes important for gametogenesis. Furthermore, high‐throughput expression profiling techniques have helped identify gene regulatory networks that operate during gametogenesis.

Key concepts:

  • Plant life cycles alternate between sporophyte and gametophyte generations.

  • Meiosis produces spores which then undergo gametogenesis.

  • Higher plants produce two types of gametes, sperm cells in microgametophytes and egg cell and central cell in megagametophytes.

  • The male and female gametes fuse and give rise to the zygote and to the endosperm.

  • Identification of gametophytic mutants showed that gametogenesis is under strict genetic control.

  • Expression profiling studies provided further insight into the gene regulation of gametogenesis and identified new gametophytic genes.

Keywords: pollen; embryo sac; egg; sperm; central cell

Figure 1.

Schematic representation of the events during micro‐ and megagametogenesis. (a) In male gametogenesis (microgametogenesis), the microspore mother cell undergoes meiosis to give rise to a tetrad with four haploid microspores. Uninucleate microspores are released when callaseβ1,3‐glucanase, is secreted from the surrounding tapetal cells. Each uninucleate microspore enlarges and undergoes an asymmetric division to yield a bicellular pollen grain. The generative cell in the bicellular pollen grain undergoes mitosis to yield two sperm cells. (b) Female gametogenesis (megagametogenesis) starts with two meiotic divisions of a diploid megasporocyte, which gives rise to four megaspores. Only one of the four megaspores survives and continues gametogenesis with three mitotic divisions. The megagametophyte, now with eight nuclei, undergoes cellularization, cell differentiation and nuclear fusion to give rise to the seven‐celled embryo sac. AP, antipodal cells; EC, egg cell; GC, generative cells; PN, polar nuclei; SY, synergids and VC, vegetative cell.

Figure 2.

Mature pollen grains (male gametophytes). The DNA in the nuclei of the cells is stained with a fluorescent dye. (a) Pine pollen grain has air bladders on either side that facilitate its dispersal by wind, whereas the central chamber contains two cells; the body cell will form the pollen tube and the generative cell will divide into two nonmotile sperm cells. (b) Brassica pollen grain, with two intensely stained sperm cell nuclei and a more diffusely stained vegetative nucleus. (c) Wheat pollen grain, with two elongated sperm cells and a more diffusely stained vegetative nucleus. (d) Tomato pollen grain, with a diffusely stained vegetative nucleus and a more intensely stained generative cell nucleus. The generative cell will divide into two sperm cells during pollen tube growth.

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References

Agashe B, Prasad CK and Siddiqi I (2002) Identification and analysis of DYAD: a gene required for meiotic chromosome organisation and female meiotic progression in Arabidopsis. Development 129: 3935–3943.

Alandete‐Saez M, Ron M and 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. Molecular Plant 1: 586–598.

Armstrong SJ, Caryl AP, Jones GH and Franklin FC (2002) Asy1, a protein required for meiotic chromosome synapsis, localizes to axis‐associated chromatin in Arabidopsis and Brassica. Journal of Cell Science 115: 3645–3655.

Berger F, Grini PE and Schnittger A (2006) Endosperm: an integrator of seed growth and development. Current Opinion in Plant Biology 9: 664–670.

Berger F, Hamamura Y, Ingouff M and Higashiyama T (2008) Double fertilization‐caught in the act. Trends in Plant Science 13: 437–443.

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.

Boavida LC, Shuai B, Yu H‐J et al. (2009) A collection of Ds insertions associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 181: 1369–1385.

Borg M, Brownfield L and Twell D (2009) Male gametophyte development: a molecular perspective. Journal of Experimental Botany 60: 1465–1478.

Borges F, Gomes G, Gardner R et al. (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiology 148: 1168–1181.

Canales C, Bhatt AM, Scott R and Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Current Biology 12: 1718–1727.

Chen C, Marcus A, Li W et al. (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129: 2401–2409.

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.

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

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

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

Escobar‐Restrepo JM, Huck N, Kessler S et al. (2007) The FERONIA receptor‐like kinase mediates male‐female interactions during pollen tube reception. Science 317: 656–660.

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.

Golubovskaya I, Grebennikova ZK, Avalkina NA and Sheridan WF (1993) The role of the ameiotic1 gene in the initiation of meiosis and in subsequent meiotic events in maize. Genetics 135: 1151–1166.

Gusti A, Baumberger N, Nowack M et al. (2009) The Arabidopsis thaliana F‐box protein FBL17 is essential for progression through the second mitosis during pollen development. PLoS ONE 4: e4780.

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

Howden R, Park SK, Moore JM et al. (1998) Selection of T‐DNA‐tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149: 621–631.

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.

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

Johnson‐Brousseau SA and McCormick S (2004) A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically expressed genes. Plant Journal 39: 761–775.

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 Genetics 3: 1848–1861.

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.

Kim HJ, Oh SA, Brownfield L et al. (2008) Control of plant germline proliferation by SCF(FBL17) degradation of cell cycle inhibitors. Nature 455: 1134–1137.

Liu Y, Tewari R, Ning J et al. (2008) The conserved plant sterility gene HAP2 functions after attachment of fusogenic membranes in Chlamydomonas and Plasmodium gametes. Genes & Development 22: 1051–1068.

Moore G and Shaw P (2009) Improving the chances of finding the right partner. Current Opinion in Genetics & Development 19: 99–104.

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

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

Otto SP and Gerstein AC (2008) The evolution of haploidy and diploidy. Current Biology 18: R1121–R1124.

Pagnussat GC, Yu HJ, Ngo QA et al. (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development 132: 603–614.

Pawlowski WP, Wang CJ, Golubovskaya IN et al. (2009) Maize AMEIOTIC1 is essential for multiple early meiotic processes and likely required for the initiation of meiosis. Proceedings of the National Academy of Sciences of the USA 106: 3603–3608.

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.

Russell SD (1985) Preferential fertilization in Plumbago: ultrastructural evidence for gamete‐level recognition in an angiosperm. Proceedings of the National Academy of Sciences of the USA 82: 6129–6132.

Rotman N, Durbarry A, Wardle A et al. (2005) A novel class of MYB factors controls sperm‐cell formation in plants. Current Biology 15: 244–248.

Singh MB, Bhalla PL and Russell SD (2008) Molecular repertoire of flowering plant male germ cells. Sexual Plant Reproduction 21: 27–36.

Spielman M, Preuss D, Li FL et al. (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124: 2645–2657.

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 Journal 41: 660–672.

Staiger CJ and Cande WZ (1992) Ameiotic, a gene that controls meiotic chromosome and cytoskeletal behavior in maize. Developmental Biology 154: 226–230.

Steffen JG, Kang IH, Macfarlane J and Drews GN (2007) Identification of genes expressed in the Arabidopsis female gametophyte. Plant Journal 51: 281–292.

Wassarman PM, Jovine L and Litscher ES (2001) A profile of fertilization in mammals. Nature Cell Biology 3: E59–64.

Yang CY, Spielman M, Coles JP et al. (2003a) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant Journal 34: 229–240.

Yang H, Kaur N, Kiriakopolos S and McCormick S (2006) EST generation and analyses towards identifying female gametophyte‐specific genes in Zea mays L. Planta 224: 1004–1014.

Yang WC, Ye D, Xu J and Sundaresan V (1999) The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein. Genes & Development 13: 2108–2117.

Yang X, Makaroff CA and Ma H (2003b) The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD‐finger protein that is required for male meiosis. Plant Cell 15: 1281–1295.

Zhang ZB, Zhu J, Gao JF et al. (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant Journal 52: 528–538.

Zhao DZ, Wang GF, Speal B and Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine‐rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes & Development 16: 2021–2031.

Further Reading

Hamant O, Ma H and Cande ZW (2006) Genetics of meiotic prophase I in plants. Annual Review of Plant Biology 57: 267–302.

McCormick S (1993) Male gametophyte development. Plant Cell 5: 1265–1275.

McCormick S (1993) Male gametophyte development. Annual Review of Plant Biology 56: 393–434.

McCormick S (2004) Control of male gametophyte development. Plant Cell 16(suppl.): S142–S153.

Olsen O‐A (2001) ENDOSPERM DEVELOPMENT: Cellularization and cell fate specification. Annual Review of Plant Physiology and Plant Molecular Biology 52: 233–267.

Wilson ZA and Yang C (2004) Plant gametogenesis: conservation and contrasts in development. Reproduction 128: 483–492.

Wilson ZA and Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. Journal of Experimental Botany 60: 1479–1492.

Yadegari R and Drews GN (2004) Female gametophyte development. Plant Cell 16(suppl.): S133–141.

Yang WC and Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Current Opinion in Plant Biology 3: 53–57.

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Guan, Yuefeng, Boavida, Leonor, and McCormick, Sheila(Jan 2010) Gametogenesis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002037.pub2]