journal article May 15, 2003

The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception

Development Vol. 130 No. 10 pp. 2149-2159 · The Company of Biologists
View at Publisher Save 10.1242/dev.00458
Abstract
Reproduction in angiosperms depends on communication processes of the male gametophyte (pollen) with the female floral organs (pistil, transmitting tissue) and the female gametophyte (embryo sac). Pollen-pistil interactions control pollen hydration, germination and growth through the stylar tissue. The female gametophyte is involved in guiding the growing pollen tube towards the micropyle and embryo sac. One of the two synergids flanking the egg cell starts to degenerate and becomes receptive for pollen tube entry. Pollen tube growth arrests and the tip of the pollen tube ruptures to release the sperm cells. Failures in the mutual interaction between the synergid and the pollen tube necessarily impair fertility. But the control of pollen tube reception is not understood. We isolated a semisterile, female gametophytic mutant from Arabidopsis thaliana, named feronia after the Etruscan goddess of fertility, which impairs this process. In the feroniamutant, embryo sac development and pollen tube guidance were unaffected in all ovules, although one half of the ovules bore mutant female gametophytes. However, when the pollen tube entered the receptive synergid of a feronia mutant female gametophyte, it continued to grow, failed to rupture and release the sperm cells, and invaded the embryo sac. Thus, the feronia mutation disrupts the interaction between the male and female gametophyte required to elicit these processes. Frequently, mutant embryo sacs received supernumerary pollen tubes. We analysed feronia with synergid-specific GUS marker lines, which demonstrated that the specification and differentiation of the synergids was normal. However, GUS expression in mutant gametophytes persisted after pollen tube entry, in contrast to wild-type embryo sacs where it rapidly decreased. Apparently, the failure in pollen tube reception results in the continued expression of synergid-specific genes, probably leading to an extended expression of a potential pollen tube attractant.
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References
47
[1]
Christensen, C. A., Gorsich, S. W., Brown, R. H., Jones, L. G.,Brown, J., Shaw, J. M. and Drews, G. N. (2002). Mitochondrial GFA2 is required for synergid cell death in Arabidopsis.Plant Cell14,2215-2232. 10.1105/tpc.002170
[2]
Christensen, C. A., King, E. J., Jordan, J. R. and Drews, G. N. (1997). Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Repod.10, 49-64. 10.1007/s004970050067
[3]
Christensen, C. A., Subramanian, S. and Drews, G. N.(1998). Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis.Dev. Biol.202,136-151. 10.1006/dbio.1998.8980
[4]
Drews, G. N. and Yadegari, R. (2002). Development and function of the angiosperm female gametophyte. Annu. Rev. Genet.36,99-124. 10.1146/annurev.genet.36.040102.131941
[5]
Faure, J. E., Rotman, N., Fortune, P. and Dumas, C.(2002). Fertilization in Arabidopsis thaliana wild type:developmental stages and time course. Plant J.30,481-488. 10.1046/j.1365-313x.2002.01305.x
[6]
Franklin-Tong, V. E. (1999). Signaling and the modulation of pollen tube growth. Plant Cell11,727-738. 10.1105/tpc.11.4.727
[7]
The molecular and genetic basis of ovule and megagametophyte development

Ueli Grossniklaus, Kay Schneitz

Seminars in Cell & Developmental Biology 10.1006/scdb.1997.0214
[8]
Grossniklaus, U., Vielle-Calzada, J. P., Hoeppner, M. A. and Gagliano, W. B. (1998). Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science280,446-450. 10.1126/science.280.5362.446
[9]
Hepler, P. K., Vidali, L. and Cheung, A. Y.(2001). Polarized cell growth in higher plants. Annu. Rev. Cell Dev. Biol.17,159-187. 10.1146/annurev.cellbio.17.1.159
[10]
Higashiyama, T., Kuroiwa, H., Kawano, S. and Kuroiwa, T.(1998). Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri.Plant Cell10,2019-2032. 10.1105/tpc.10.12.2019
[11]
Higashiyama, T., Yabe, S., Sasaki, N., Nishimura, Y.,Miyagishima, S., Kuroiwa, H. and Kuroiwa, T. (2001). Pollen tube attraction by the synergid cell. Science293,1480-1483. 10.1126/science.1062429
[12]
Hogenboom, N. G. (1984). Incongruity:non-function of intercellular and intracellular partner relationships through non-matching information. In Cellular Interactions,vol. 17 (ed. H. F. Linskens and J. Heslop-Harrison),pp. 640-654. Berlin: Springer-Verlag.
[13]
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. Genetics149,621-631. 10.1093/genetics/149.2.621
[14]
Huang, B. Q., Pierson, E. S., Russell, S. D., Tiezzi, A. and Cresti, M. (1993). Cytoskeletal organisation and modification during pollen tube arrival, gamete delivery and fertilisation in Plumbago zeylanica. Zygote1,143-154. 10.1017/s0967199400001404
[15]
Huang, B. Q. and Sheridan, W. F. (1998). Actin coronas in normal and indeterminate gamtophyte 1 embryo sacs of maize. Sex. Plant Repod.11,257-264. 10.1007/s004970050151
[16]
Hülskamp, M., Kopczak, S. D., Horejsi, T. F., Kihl, B. K. and Pruitt, R. E. (1995a). Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana.Plant J.8,703-714. 10.1046/j.1365-313x.1995.08050703.x
[17]
Hülskamp, M., Schneitz, K. and Pruitt, R. E.(1995b). Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis.Plant Cell7, 57-64. 10.1105/tpc.7.1.57
[18]
Jander, G., Norris, S. R., Rounsley, S. D., Bush, D. F., Levin,I. M. and Last, R. L. (2002). Arabidopsis map-based cloning in the post-genome era. Plant Physiol.129,440-450. 10.1104/pp.003533
[19]
Jefferson, R. A., Kavanagh, T. A. and Bevan, M. W.(1987). GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J.6,3901-3907. 10.1002/j.1460-2075.1987.tb02730.x
[20]
Jensen, W. A. and Fisher, D. B. (1968). Cotton embryogenesis: the entrance and discharge of the pollen tube in the embryo sac. Planta78,158-183.
[21]
Johnson, M. A. and Preuss, D. (2002). Plotting a course: multiple signals guide pollen tubes to their targets. Dev. Cell2,273-281. 10.1016/s1534-5807(02)00130-2
[22]
Kapil, R. N. and Bhatnagar, A. K. (1975). A fresh look at the process of double fertilization in angiosperms. Phytomorphology25,334-368.
[23]
Kaul, V., Rouse, J. L. and Williams, E. G.(1986). Early events in the embryo sac after intraspecific and interspecific pollinations in Rhododendron kawakamii and R. retsum.Can. J. Bot.64,282-291. 10.1139/b86-042
[25]
Lush, W. M. (1999). Whither chemotropism and pollen tube guidance? Trends Plant Sci.4, 413-418.
[26]
Mansfield, S. G. and Briarty, L. G. (1991). Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot.69,461-476.
[27]
Matzk, F., Meister, A. and Schubert, I. (2000). An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J.21,97-108. 10.1046/j.1365-313x.2000.00647.x
[28]
Moore, J. M., Vielle-Calzada, J. P., Gagliano, W. B. and Grossniklaus, U. (1997). Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana.Cold Spring Harbor Symp. Quant. Biol.62, 35-47.
[29]
Murgia, M., Huang, B. Q., Tucker, S. C. and Musgrave, M. E.(1993). Embryo sac lacking antipodal cells in Arabidopsis thaliana (Brassicaceae). Amer. J. Bot.80,824-838. 10.1002/j.1537-2197.1993.tb15298.x
[30]
Page, D. R. and Grossniklaus, U. (2002). The art and design of genetic screens: Arabidopsis thaliana.Nat. Rev. Genet.3,124-136. 10.1038/nrg730
[31]
Pruitt, R. E. (1999). Complex sexual signals for the male gametophyte. Curr. Opin. Plant Biol.2, 419-422. 10.1016/s1369-5266(99)00015-1
[32]
Raghavan, V. (1997). Molecular Embryology of Flowering Plants. Cambridge, UK: Cambridge University Press. 10.1017/cbo9780511574528
[33]
Raven, P. H., Evert, R. F. and Eichhorn, S. E.(1999). Biology of Plants. New York: W. H. Freeman and Company/Worth Publishers.
[34]
Ray, S. M., Park, S. S. and Ray, A. (1997). Pollen tube guidance by the female gametophyte. Development124,2489-2498. 10.1242/dev.124.12.2489
[35]
Female Control of Male Gamete Delivery during Fertilization in Arabidopsis thaliana

Nicolas Rotman, Frédérique Rozier, Leonor Boavida et al.

Current Biology 10.1016/s0960-9822(03)00093-9
[36]
Russell, S. D. (1992). Double fertilization. Int. Rev. Cytol.140,357-388. 10.1016/s0074-7696(08)61102-x
[37]
Attraction and transport of male gametes for fertilization

Scott D. Russell

Sexual Plant Reproduction 10.1007/bf02441952
[38]
Wild‐type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole‐mount tissue

Kay Schneitz, Martin Hülskamp, Robert E. Pruitt

The Plant Journal 10.1046/j.1365-313x.1995.07050731.x
[39]
Shimizu, K. K. and Okada, K. (2000). Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development127,4511-4518. 10.1242/dev.127.20.4511
[40]
Smyth, D. R. (1997). Attractive ovules. Curr. Biol.7,R64-66. 10.1016/s0960-9822(06)00037-6
[41]
Sundaresan, V., Springer, P., Volpe, T., Haward, S., Jones, J. D., Dean, C., Ma, H. and Martienssen, R. (1995). Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev.9,1797-1810. 10.1101/gad.9.14.1797
[42]
van Went, J. L. and Willemse, M. T. M. (1984). Fertilization. In Embryology of Angiosperms (ed. B. M. Johri), pp. 273-317. Berlin:Springer-Verlag. 10.1007/978-3-642-69302-1_6
[43]
Vielle-Calzada, J. P., Baskar, R. and Grossniklaus, U.(2000). Delayed activation of the paternal genome during seed development. Nature404,91-94. 10.1038/35003595
[44]
Wilhelmi, L. K. and Preuss, D. (1999). The mating game: pollination and fertilization in flowering plants. Curr. Opin. Plant Biol.2, 18-22. 10.1016/s1369-5266(99)80004-1
[45]
Williams, E. G., Kaul, V., Rouse, J. L. and Palser, B. F.(1986). Overgrowth of pollen tubes in embryo sacs of Rhododendron following interspecific pollinations. Aust. J. Bot.34,413-423. 10.1071/bt9860413
[46]
Wilms, H. J. (1981). Pollen tube penetration and fertilization in spinach. Acta Bot. Neerl.30,101-122. 10.1111/j.1438-8677.1981.tb00390.x
[47]
Yadegari, R., Paiva, G., Laux, T., Koltunow, A. M., Apuya, N.,Zimmerman, J. L., Fischer, R. L., Harada, J. J. and Goldberg, R. B.(1994). Cell differentiation and morphogenesis are uncoupled in Arabidopsis raspberry embryos. Plant Cell6,1713-1729.
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