Development, Vol 126, Issue 5 1065-1075, Copyright © 1999 by Company of Biologists

JOURNAL ARTICLES

Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes

WE Friedman
Department of EPO Biology, University of Colorado, Boulder, CO 80309, USA.

The relationship between developmental events and the cell cycle was examined in sperm of Arabidopsis thaliana. Sperm of Arabidopsis rapidly enter the S (synthesis) phase of the cell cycle after inception from mitosis of the generative cell. Sperm in pollen grains within anthers continue to synthesize DNA, and at the time of pollination, contain approximately 1.5C DNA. Following pollination, sperm continue through the S phase of the cell cycle during pollen tube growth. By the time pollen tubes reach the ovary, sperm nuclei contain approximately 1.75C DNA. Just prior to double fertilization, sperm nuclei within embryo sacs contain the 2C quantity of DNA. These data indicate that molecular programs associated with the G1-S transition and the S phase of the cell cycle are expressed in sperm cells of developing pollen grains and pollen tubes in Arabidopsis. This pattern of prefertilization S phase activity in the sperm of a flowering plant stands in marked contrast to all other non-plant eukaryotes (from ciliates to yeast to sea urchins to mammals) where sperm remain in G1 during development, prior to the initiation of gametic fusion. In addition, when patterns of cell cycle activity in sperm of Arabidopsis and other flowering plants are compared, developmental analysis reveals that heterochronic alterations (changes in the relative timing of ontogenetic events) in cell cycle activity are a central cause of the diversification of patterns of gametogenesis in higher plants. Finally, comparative analysis of the patterns of cell cycle activity in Arabidopsis and other angiosperms may be used to predict which flowering plants will be amenable to development of successful in vitro fertilization techniques.
CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

This article has been cited by other articles:

				L. Brownfield, S. Hafidh, A. Durbarry, H. Khatab, A. Sidorova, P. Doerner, and D. Twell Arabidopsis DUO POLLEN3 Is a Key Regulator of Male Germline Development and Embryogenesis PLANT CELL, July 1, 2009; 21(7): 1940 - 1956. [Abstract] [Full Text] [PDF]

				J. Lora, M. Herrero, and J. I. Hormaza The coexistence of bicellular and tricellular pollen in Annona cherimola (Annonaceae): Implications for pollen evolution Am. J. Botany, April 1, 2009; 96(4): 802 - 808. [Abstract] [Full Text] [PDF]

				J. H. Williams Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase Am. J. Botany, January 1, 2009; 96(1): 144 - 165. [Abstract] [Full Text] [PDF]

				F. Borges, G. Gomes, R. Gardner, N. Moreno, S. McCormick, J. A. Feijo, and J. D. Becker Comparative Transcriptomics of Arabidopsis Sperm Cells Plant Physiology, October 1, 2008; 148(2): 1168 - 1181. [Abstract] [Full Text] [PDF]

				J. Liu, Y. Zhang, G. Qin, T. Tsuge, N. Sakaguchi, G. Luo, K. Sun, D. Shi, S. Aki, N. Zheng, et al. 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, June 1, 2008; 20(6): 1538 - 1554. [Abstract] [Full Text] [PDF]

				C. C. Sheldon, M. J. Hills, C. Lister, C. Dean, E. S. Dennis, and W. J. Peacock Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization PNAS, February 12, 2008; 105(6): 2214 - 2219. [Abstract] [Full Text] [PDF]

				Z. Chen, J. L. H. Tan, M. Ingouff, V. Sundaresan, and F. Berger Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana Development, January 1, 2008; 135(1): 65 - 73. [Abstract] [Full Text] [PDF]

				R. Wen, J. A. Torres-Acosta, L. Pastushok, X. Lai, L. Pelzer, H. Wang, and W. Xiao Arabidopsis UEV1D Promotes Lysine-63-Linked Polyubiquitination and Is Involved in DNA Damage Response PLANT CELL, January 1, 2008; 20(1): 213 - 227. [Abstract] [Full Text] [PDF]

				L. L. Ge, H. Q. Tian, and S. D. Russell Calcium function and distribution during fertilization in angiosperms Am. J. Botany, June 1, 2007; 94(6): 1046 - 1060. [Abstract] [Full Text] [PDF]

				C. Pina, F. Pinto, J. A. Feijo, and J. D. Becker Gene Family Analysis of the Arabidopsis Pollen Transcriptome Reveals Biological Implications for Cell Growth, Division Control, and Gene Expression Regulation Plant Physiology, June 1, 2005; 138(2): 744 - 756. [Abstract] [Full Text] [PDF]

				A. Durbarry, I. Vizir, and D. Twell Male Germ Line Development in Arabidopsis. duo pollen Mutants Reveal Gametophytic Regulators of Generative Cell Cycle Progression Plant Physiology, January 1, 2005; 137(1): 297 - 307. [Abstract] [Full Text] [PDF]

				W. E. Friedman and J. H. Williams Developmental Evolution of the Sexual Process in Ancient Flowering Plant Lineages PLANT CELL, June 1, 2004; 16(suppl_1): S119 - S132. [Full Text] [PDF]

				J. D. Becker, L. C. Boavida, J. Carneiro, M. Haury, and J. A. Feijo Transcriptional Profiling of Arabidopsis Tissues Reveals the Unique Characteristics of the Pollen Transcriptome Plant Physiology, October 1, 2003; 133(2): 713 - 725. [Abstract] [Full Text] [PDF]

				J.-L. Magnard, M. Yang, Y.-C. S. Chen, M. Leary, and S. McCormick The Arabidopsis Gene Tardy Asynchronous Meiosis Is Required for the Normal Pace and Synchrony of Cell Division during Male Meiosis Plant Physiology, November 1, 2001; 127(3): 1157 - 1166. [Abstract] [Full Text] [PDF]

				F. Corellou, C. Brownlee, L. Detivaud, B. Kloareg, and F.-Y. Bouget Cell Cycle in the Fucus Zygote Parallels a Somatic Cell Cycle but Displays a Unique Translational Regulation of Cyclin-Dependent Kinases PLANT CELL, March 1, 2001; 13(3): 585 - 598. [Abstract] [Full Text]

				J. H. Williams Jr., W. E. Friedman, and M. L. Arnold Developmental selection within the angiosperm style: Using gamete DNA to visualize interspecific pollen competition PNAS, August 3, 1999; 96(16): 9201 - 9206. [Abstract] [Full Text] [PDF]