Female Gametophyte Development in Higher Plants - Meiosis and Mitosis Break the Cellular Barrier

Abstract

Meiotic products in higher plants should undergo a determined number of mitotic cycles before differentiating gametes. This creates a unique meiosis-mitosis interface, traverse of which is an absolute requirement for gametophyte development. In the absence of cytokinesis during megasporogenesis - as seen in the bisporic and tetrasporic types - the haploid nuclei produced by meiosis are driven to undergo mitotic cycles within the same cell. Similarly, the last of the mitotic cycles leads to a unique type of cell wall formation resulting in cellularization of the coenocytic female gametophyte, creating a mitosis-cellularization interface. Cell cycle regulation in terms of the molecules that interface with these two key spatio-temporal developmental settings should be of interest to both cell and developmental biologists. High throughput techniques of functional genomics are required for both interpretation of female gametophyte evolution and success of the biotechnological initiatives of transferring apomixis-related genes to crop plants.

Angiosperm female gametophyte - cell and developmental biology interfaces - meiosis-mitosis interface - mitosis-cellularization interface - functional genomic perspectives

References

• 01 Arabidopsis Genome Initiative . (2000);  Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. .  Nature. 408 796-815
• 02 Asker,  J. E., and Jerling,  I.. (1992) Apomixis in plants. Boca Raton; CRC Press
• 03 Berger,  F.,, Haseloff,  J.,, Scheifelbein,  J.,, and Dolan,  L.. (1998 a);  Positional information in root epidermis is defined during embryogenesis and acts in domain with strict boundaries.  Current Biology. 8 421-430
• 04 Berger,  F.,, Linstead,  P.,, Dolan,  L.,, and Haseloff,  J.. (1998 b);  Stomata patterning on the hypocotyl of Arabidopsis thaliana is controlled by genes involved in the control of root epidermis patterning.  Developmental Biology. 194 225-234
• 05 Bhojwani,  S. S., and Bhatnagar,  S. P.. (1992) The embryology of angiosperms. New Delhi; Vikas Publishers
• 06 Brendel,  V.,, Kurtz,  S.,, and Walbot,  V.. (2002);  Comparative genomics of Arabidopsis and maize. Prospects and limitations.  Genome Biology. 3 (3): reviews 1005.1-1005.6
• 07 Bryant,  J. A.,, Moore,  K.,, and Aves,  S. J.. (2001);  Origins and complexes: the Initiation of DNA replication.  Journal of Experimental Botany. 52 193-202
• 08 Carroll,  S. B.. (1994);  Developmental regulatory mechanisms in the evolution of insect diversity.  Development. 21 S7-S23
• 09 Christensen,  C. A.,, Subramanian,  S.,, and Drews,  G. N.. (1998);  Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. .  Developmental Biology. 202 136-151
• 10 Cockcroft,  C. E.,, den Boer,  B. G. W.,, Healy,  J. M.,, and Murray,  J. A.. (2000);  Cyclin D control of growth rates in plants.  Nature. 405 575-579
• 11 Cronk,  Q. C. B.. (2001);  Plant evolution and development in a post genomic era.  Nature Reviews Genetics. 2 607-619
• 12 Davenport,  R. J.. (2001);  DNA: Once copied, thrice blocked.  Science. 292 241-242
• 13 den Boer,  B. G. W., and Murray,  J. A. H.. (2000);  Triggering the cell cycle in plants.  Trends in Cell Biology. 10 245-250
• 14 Dewas-Hoang,  R. E., and Weischaus,  E. F.. (2001);  Cell and developmental biology - A shared past, an intertwined future.  Developmental Cell. 1 27-36
• 15 Doebley,  J.,, Stec,  A.,, and Hubbard,  L.. (1997);  The evolution of apical dominance in maize.  Nature. 386 485-488
• 16 Doebley,  J., and Likens,  L.. (1998);  Transcriptional regulation and the evolution of plant form.  Plant Cell. 10 1075-1082
• 17 Drews,  G. N.,, Lee,  D.,, and Kranz,  E.. (1998);  Genetic analysis of female gametophyte development and function.  Plant Cell. 10 5-17
• 18 Durfee,  T.,, Feiler,  H. S.,, and Gruisse,  W.. (2000);  Retinoblastoma-related proteins in plants: homologues or orthologues?.  Plant Molecular Biology. 43 635-642
• 19 Elliott,  C. G.. (1994) Reproduction in Fungi - Genetical and Physiological aspects. NY, Madras; Chapman and Hall
• 20 Feldmann,  K. A., Coury,  D. A., and Christensen,  M. L.. (1997);  Exceptional segregation of a selective marker (KanR) in Arabidopsis identifies genes important for growth and development.  Genetics. 147 1411-1422
• 21 Forsburg,  S. L.. (2001);  The art and design of genetic screens: Yeast.  Nature Reviews Genetics. 2 (9) 659-668
• 22 Gasser,  C. S.,, Broadhvest,  J.,, and Hauser,  B. A.. (1998);  Genetic analysis of ovule development.  Annual Review of Plant Physiology. 49 1-24
• 23 Gerlt,  J. A., and Babbitt,  P. C.. (2000);  Can sequence determine function?.  Genome Biology. 5, reviews 0005.1-0005.10
• 24 Gershon,  D.. (2002);  Microarray technology: An array of opportunities.  Nature. 416 885-891
• 25 Grafi,  G.. (1998);  Cell cycle regulation of DNA replication: the endoreduplication perspective.  Experimental Cell Research. 244 372-378
• 26 Grossniklaus,  U.. (2001) From sexuality to apomixis: molecular and genetic approaches. Advances in apomixis research. Savidan, Y., Carman, J., Dresslhauas, T., eds. Texcoco, Mexico; CYMMITT Press
• 27 Grossniklaus,  U., and Schneitz,  K.. (1998);  Genetic and molecular control of ovule development.  Seminars in Cell and Developmental Biology. 9 227-238
• 28 Grossniklaus,  U.,, Moore,  J. M.,, and Gagliono,  W. B.. (1998) Molecular and genetic approaches to understanding and engineering apomixis: Arabidopsis as a powerful tool. Advances in hybrid Rice technology. Proc. 3rd Int. Symp. Hybrid Rice. Viramani, S. S., Siddiqui, E. A., Muralidharan, K., eds. Manila, Philippines; Int. Rice Res. Inst. pp. 187-211
• 29 Grossniklaus,  U.,, Nogler,  G. A.,, and Dijk,  P. J.. (2001);  How to avoid sex.  Plant Cell. 13 1491-1498
• 30 Grini,  P. E.,, Schnittger,  A.,, Schwartz,  H.,, Zimmermann,  J.,, Schwah,  B.,, Jurgens,  G.,, and Hulskamp,  M.. (1999);  Identification of ethylmethanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1.  Genetics. 151 849-863
• 31 Gustafsson,  A.. (1947 a);  Apomixis in angiosperms II.  Lunds. Univ. Arsskr. NI. 42 71-179
• 32 Gustafsson,  A.. (1947 b);  Apomixis in angiosperms III.  Lunds. Univ. Arsskr. NI. 43 183-370
• 33 Gygi,  S. P.,, Rochon,  Y.,, Franza,  B. R.,, and Abersold,  R.. (1999);  Correlation between protein and mRNA abundance in yeast.  Molecular Cell Biology. 19 1720-1730
• 34 Harmer,  S. L., and Kay,  S. A.. (2000);  Microarrays: Determining the balance of cellular transcription.  Plant Cell. 12 (5) 613-616
• 35 Howden,  R.,, Park,  S. K.,, Moore,  J. M.,, Orme,  J.,, Grossniklaus,  U.,, and Twell,  D.. (1998);  Selection of T-DNA tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. .  Genetics. 149 621-631
• 36 Huang,  B.-Q., and Russell,  S. D.. (1992);  Female germ unit: organization, isolation and function.  International Review of Cytology. 140 233-292
• 37 Huang,  B.-Q., and Sheridan,  W. F.. (1996);  Embryo sac development in the maize indeterminate gametophyte 1 mutant: Abnormal nuclear behaviour and defective microtubule organization.  Plant Cell. 8 1391-1407
• 38 Huntley,  R. P., and Murray,  J. A. H.. (1999);  The plant cell cycle.  Current Opinion in Plant Biology. 2 440-446
• 39 Inze,  D. (ed.). (2000) The plant cell cycle. Plant Molecular Biology (special issue), Vol. 43
• 40 Jensen,  S.,, Geymont,  M.,, and Johnston,  L. H.. (2002);  Mitotic exit: Delaying the end without FEAR.  Current Biology. 12 R221-R223
• 41 Johnston,  D.-St.. (2002);  The art and design of genetic screens: Drosophila melanogaster. .  Nature Reviews Genetics. 3 (3) 176-188
• 42 Jorgensen,  E. M., and Mango,  S. E.. (2002);  The art and design of genetic screens: Caenorhabditis elegans. .  Nature Reviews Genetics. 3 356-369
• 43 Kearsey,  S.. (2002);  Surveying genome replication.  Genome Biology. 3 (6) 1016.1-1016.4
• 44 Keegan,  L. P.,, Galio,  A.,, and O'Connell,  A.. (2001);  The many roles of an RNA editor.  Nature Reviews Genetics. 2 865-878
• 45 Koltunow,  A. M.. (1993);  Apomixis: Embryo sacs and embryos formed without meiosis or fertilization in ovules.  Plant Cell. 5 1425-1437
• 46 Kumar,  A., and Snyder,  M.. (2002);  Proteomics: Protein complexes take the bait.  Nature. 415 123-124
• 47 Larkins,  B. A.,, Dilkes,  B. P.,, Dante,  R. A.,, Coelho,  C. M.,, Woo,  Y.-M.,, and Liu,  Y.. (2001);  Investigating the hows and whys of DNA endoreduplication.  Journal of Expermental Botany. 52 183-192
• 48 Lengronne,  A., and Schwob,  E.. (2002);  The yeast CDK inhibitor Sic1 prevents Genomic instability by promoting replication origin licensing in late G1.  Molecular Cell. 9 1064-1078
• 49 Maheswari,  P.. (1950) Embryology of Angiosperms. NY; McGraw Hill Book Company Inc.
• 50 Martienssen,  R. A.. (1998);  Functional genomics: Probing plant gene function and expression with transposons.  Proceedings of National Academy of Science USA. 95 2021-2026
• 51 Meijer,  M., and Murray,  A. J. H.. (2001);  Cell cycle controls and the development of plant form.  Current Opinion in Plant Biology. 4 44-49
• 52 Meinke,  D., and Tanksley,  S.. (2000);  Genome studies and molecular genetics. The maturization and specialization of plant genomics.  Current Opinion in Plant Biology. 3 95-96
• 53 Mering,  C. V.,, Krause,  R.,, Snel,  B.,, Cornell,  M.,, Oliver,  S. G.,, Fields,  S.,, and Bork,  P.. (2002) Comparative assessment of large scale data sets of protein-protein interactions. Nature AGP. Published online. 8th May 2002; doi 10.1038/Nature 750
• 54 Meyerowitz,  E. M.. (2002);  Plants compared to animals: The broadest comparative study of development.  Science. 245 1482-1485
• 55 Montomayor,  J. C.,, Vezon,  D.,, Bazon,  C.,, Sauvanet,  A.,, Grandjeon,  O.,, Marchand,  M.,, Bechtold,  M. G.,, Pelletier,  G.,, and Horlow,  C.. (2000);  Switch1 (swi1), an Arabidopsis mutant affected in the female meiotic switch.  Sexual Plant Reproduction. 12 209-218
• 56 Moore,  J. M.,, Vielle Calzada,  J.-P.,, Gagliana,  W.,, and Grossniklaus,  U.. (1997);  Genetic characterization of hadad, a mutant disrupting female gametophyte in Arabidopsis thaliana. .  Cold Spring Harbor Symposium Quantenery Biology. 62 35-47
• 57 Morgan,  D. O.. (1997);  Cyclin dependent kinases: Engines, clocks and microprocessors.  Annual Review of Cell and Developmental Biology. 18 261-284
• 58 Nacry,  P.,, Mayer,  U.,, and Jurgens,  G.. (2000);  Genetic dissection of cytokinesis.  Plant Molecular Biology. 43 719-723
• 59 Nigg,  E. A.. (2001);  Mitotic kinases as regulators of cell division and its checkpoints.  Nature Reviews Molecular Cell Biology. 2 21-32
• 60 Otegui,  M., and Staehelin,  L. A.. (2000);  Cytokinesis in flowering plants: More than one way to divide a cell.  Current Opinion in Plant Biology. 3 493-502
• 61 Page,  D. R., and Grossniklaus,  U.. (2002);  The art and design of genetic screens in Arabidopsis thaliana. .  Nature Reviews Genetics. 3 124-136
• 62 Patton,  E. E., and Zon,  L. I.. (2001);  The art and design of genetic screens: zebrafish.  Nature Reviews Genetics. 2 956-966
• 63 Richmond,  T., and Somerville,  S.. (2000);  Chasing the dream: Plant EST microarrays.  Current Opinion in Plant Biology. 3 108-116
• 64 Riou-Khamlichi,  C.,, Hyntley,  R.,, Jacqmard,  A.,, and Murray,  J. A. H.. (1999);  Cytokinin activation of Arabidopsis cell division through a D type cyclin.  Science. 283 1541-1544
• 65 Russell,  S. D.. (2001) Female gametogenesis: Ontogenesis of the embryo sac and female gametes. Current Trends in the Embryology of the Angiosperms. Bhojwani, S., Soh, W. Y., eds. Dordrecht, The Netherlands; Kluwer Academic Publishers pp. 65-88
• 66 Savidan,  Y.. (2000);  Apomixis: Genetics and breeding.  Plant Breed Review. 18 13-86
• 67 Schneitz,  K.,, Balasubramanian,  S.,, and Schciefthaler,  U.. (1998);  Organogenesis in plants: The molecular and genetic control of ovule development.  Trends in Plant Science. 3 468-472
• 68 Sheridan,  W. F., and Huang,  B.-Q.. (1997);  Nuclear behaviour is defective in the maize (Zea mays L.) lethal ovule2 (lo2) female gametophyte.  Plant Journal. 11 1029-1041
• 69 Smith,  L. G.. (2001);  Plant cell division: building walls in the right places.  Nature Reviews Molecular Cell Biology. 2 33-39
• 70 Smith,  L. G.. (2002);  Plant cytokinesis: Motoring to the finish.  Current Biology. 12 206-208
• 71 Spillane,  C.,, Vielle-Calzada,  J.-P.,, and Grossniklaus,  U.. (2001);  APO 2001. A sexy apomixier in como.  Plant Cell. 13 1480-1491
• 72 Springer,  P. S.. (2000);  Gene traps: Tools for plant development and genomics.  Plant Cell. 12 1007-1020
• 73 Springer,  P. S.,, McCombie,  R.,, Sundaresan,  V.,, and Martienssen,  R. A.. (1995);  Gene trap tagging of PROLIFERA. An essential MCM2, -3, -5 like gene in Arabidopsis. .  Science. 268 877-880
• 74 Sundaresan,  V.,, Springer,  P.,, Volpe,  T.,, Haward,  S.,, Jones,  J. D. G.,, Dean,  C.,, Ma,  H.,, and Martienssen,  R. A.. (1995);  Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements.  Genes and Development. 9 1793-1810
• 75 Sylvester,  A. W.. (2000);  Division decisions and the spatial regulation of cytokinesis.  Current Opinion in Plant Biology. 3 58-68
• 76 Szymanski,  M., and Barciszewski,  J.. (2002);  Beyond the proteome: non-coding Regulatory RNAs.  Genome Biology. 3 (5), reviews 0005.1-0005.8
• 77 Tabata,  S., and Caboche,  M.. (2001);  Genome studies and molecular studies: We know the sequence, how do we identify the function?.  Current opinion in Plant Biology. 4 103-104
• 78 Topping,  J. F.,, Agyeman,  F.,, Herricot,  B.,, and Linsey,  K.. (1994);  Identification of molecular markers of embryogenesis in Arabidopsis thaliana by promoter trapping.  Plant Journal. 5 895-903
• 79 van Dijke,  P., and van Damme,  J.. (2000);  Apomixis technology and the paradox of sex.  Trends in Plant Science. 5 81-84
• 80 Vidwans,  S. J., and Su,  T. T.. (2001);  Cycling through development of Drosophila and other metazoa.  Nature Cell Biology. 3 E35-E39
• 81 Vielle-Calzada,  J.-P.,, Crane,  C. F.,, and Stelly,  D. M.. (1996);  Apomixis: The asexual revolution.  Science. 274 1322-1323
• 82 Vielle-Calzada,  J.-P.,, Moore,  J. M.,, Gagliano,  W. B.,, and Grossniklaus,  U.. (1998);  Altering sexual development in Arabidopsis. .  Journal of Plant Biology. 41 71-83
• 83 Volbrecht,  E., and Hake,  S.. (1995);  Deficiency analysis of female gametogenesis in maize.  Developmental Genetics. 16 44-63
• 84 Wang,  R.-L.,, Stec,  A.,, Hey,  J.,, Lukens,  L.,, and Doebley,  J.. (1999);  The limits of selection during maize domestication.  Nature. 398 236-239
• 85 Williams,  J. H., and Friedman,  W. E.. (2002);  Identification of diploid endosperm in an early angiosperm lineage.  Nature. 415 522-526
• 86 Willemsen,  V.,, Wolkenfelt,  H.,, de Vrieze,  G.,, Weisbeck,  P.,, and Scheres,  B.. (1998);  The HOBBIT gene is required for formation of root meristem in the Arabidopsis embryo.  Development. 125 521-531
• 87 Yang,  W.-C., and Sundaresan,  V.. (2000);  Genetics of gametophyte biogenesis in Arabidopsis. .  Current Opinion in Plant Biology. 3 53-57
• 88 Zhou,  H.,, Ray,  S.,, Schulman,  H.,, and Natan,  M. J.. (2001);  Solution and chip arrays in protein profiling.  Trends in Biotechnology. 19 534-539
• 89 Zhu,  H., et al.. (2001);  Global analysis of protein activities using proteome chips.  Science. 293 2101-2105
• 90 Zong,  Q.,, Schummer,  M.,, Hood,  L.,, and Morris,  D. R.. (1999);  Messenger RNA translation state: The second dimension of high throughput expression screening.  Proceedings of National Academy of Sciences USA. 96 10632-10636

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