A Brief History of Seed Size Whether the Egg Cell Is Capable of Zmea1 Angela T

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A Brief History of Seed Size Whether the Egg Cell Is Capable of Zmea1 Angela T R EPORTS the nucellus cells. We are currently trying to References and Notes 16. M. L. Ma´rton, S. Cordts, J. Broadhvest, T. Dresselhaus, identify the mature ZmEA1 protein, which 1. K. Weterings, S. D. Russell, Plant Cell 16, S107 (2004). unpublished observations. 2. T. Higashiyama, H. Kuroiwa, T. Kuroiwa, Curr. Opin. 17. We thank S. Sprunck for providing cDNA from maize will then be used to study in vitro pollen tube Plant Biol. 6, 36 (2003). zygotes and R. Brettschneider for the maize OsACTp:: guidance in maize. Nevertheless, our results 3. R. Palanivelu, L. Brass, A. F. Edlund, D. Preuss, Cell GUS line. J. Bantin, E. Kranz, S. Scholten, and P. von bring potentially new insights into the 114, 47 (2003). Wiegen are acknowledged for providing cells of the 4. H. M. Wu, E. Wong, J. Ogdahl, A. Y. Cheung, Plant J. female gametophyte, in vitro zygotes, and pro- fertilization process. It had been suggested 22, 165 (2000). embryos for single-cell RT-PCR analyses. We are in 1918 (11) that the filiform apparatus is 5. S. Kim et al., Proc. Natl. Acad. Sci. U.S.A. 100, 16125 grateful to L. Viau for EST clustering and R. Reimer for required for pollen tube attraction, and in (2003). support with the CLSM. The nucleotide sequence data 6. A. M. Sanchez et al., Plant Cell 16, S98 (2004). reported is available in the European Molecular 1964, the existence of chemotropic sub- 7. T. Higashiyama et al., Science 293, 1480 (2001). Biology Laboratory, GenBank, and DNA Databank stances, which are produced by the syner- 8. T. Dresselhaus, H. Lo¨rz, E. Kranz, Plant J. 5, 605 of Japan Nucleotide Sequence Databases under the gids, was postulated (12). Also, numerous (1994). accession no. AY733074 (ZmEA1 gene). secretory vesicles have been observed at the 9. R. Mo´l, K. Idzikowska, C. Dumas, E. Matthys-Rochon, Planta 210, 749 (2000). Supporting Online Material micropylar region of maize synergids but not 10. R. Brettschneider, D. Becker, H. Lo¨rz, Theor. Appl. www.sciencemag.org/cgi/content/full/307/5709/573/ the egg cell (13). Loss of pollen tube Genet. 94, 737 (1997). DC1 guidance via synergid ablation was recently 11. M. Ishikawa, Ann. Bot. (London) 32, 279 (1918). Materials and Methods 12. J. E. van der Pluijm, in Pollen Physiology and Fertiliza- Figs. S1 to S5 substantiated in Torenia fournieri (7). Our tion, H. F. Linskens, Ed. (North Holland, Amsterdam, Table S1 data suggest that, at least in maize, not 1964), pp. 8–16. References and Notes only the synergids but the whole egg ap- 13. A. G. Diboll, Am. J. Bot. 55, 797 (1968). 14. H. C. Sharma, Euphytica 82, 43 (1995). 7 September 2004; accepted 19 November 2004 paratus could be involved in micropylar 15. K. K. Shimizu, K. Okada, Development 127, 4511 (2000). 10.1126/science.1104954 pollen tube guidance. Whether the egg cell is also involved in synthesizing a ZmEA1 precursor that is transported toward the synergids via the endoplasmic reticulum or A Brief History of Seed Size whether the egg cell is capable of ZmEA1 Angela T. Moles,1,2* David D. Ackerly,3. Campbell O. Webb,4 secretion itself is a matter of further ex- John C. Tweddle,5,6 John B. Dickie,6 Mark Westoby2 perimentation. Rapid down-regulation of the pollen tube guidance signal(s) is a major Improved phylogenies and the accumulation of broad comparative data sets prerequisite to preventing polyspermy, and have opened the way for phylogenetic analyses to trace trait evolution in fertilization is first sensed by the synergids major groups of organisms. We arrayed seed mass data for 12,987 species on and egg cell, features of ZmEA1 gene activ- the seed plant phylogeny and show the history of seed size from the ity and protein. emergence of the angiosperms through to the present day. The largest single The occurrence of ZmEA1-related genes contributor to the present-day spread of seed mass was the divergence in cereals, but not in dicotyledonous species, between angiosperms and gymnosperms, whereas the widest divergence was might be one explanation; wide crosses between Celastraceae and Parnassiaceae. Wide divergences in seed size were involving successful pollen tube guidance more often associated with divergences in growth form than with divergences and fertilization are possible within genera in dispersal syndrome or latitude. Cross-species studies and evolutionary of the Gramineae but not between species theory are consistent with this evidence that growth form and seed size spanning wider taxonomic boundaries (14). evolve in a coordinated manner. In Torenia fournieri, pollen tubes of related species do not respond to the synergids Seed mass affects many aspects of plant seed bank (7–13). Present-day species have attraction signal, which suggests species- ecology. Small-seeded species are able to seed masses ranging over 11.5 orders of specific short-range attractants (2). A similar produce more seeds for a given amount of magnitude, from the dust-like seeds of observation was made conducting inter- energy than are large-seeded species (1, 2), orchids (some of which weigh just 0.0001 specific crosses using Arabidopsis and other whereas large-seeded species have seedlings mg) to the 20-kg seeds of the double coconut Brassicaceaes where pollen tubes grew nor- that are better able to tolerate many of the (Fig. 1A). Improving our knowledge of the mally through the transmitting tissue but stresses encountered during seedling estab- changes in seed mass that occurred as the rarely arrived at the funiculus and did not lishment (3). Seed mass is also correlated angiosperms radiated out of the tropics, enter the micropyle (15). Sequence identity with the environmental conditions under colonized a wide range of habitats, devel- between ZmEA1 from two maize inbred which species establish (4–6) and with traits oped a range of growth forms and dispersal lines (A188 and H99) is 91.5% (16) and less such as plant size, dispersal syndrome, plant strategies, and became the most abundant than 45 and 43% between the maize and the life-span, and the ability to form a persistent and diverse group of plants on earth (14–18) two rice homologs (Fig. 1A). The low will greatly enhance our understanding of the homology between EA1 proteins provides 1National Center for Ecological Analysis and Synthe- ecological history of plants. further support that specific short-range sis, 735 State Street, Santa Barbara, CA 93101–5304, Using newly developed software (19, 20), guidance signals may be involved in the USA. 2Department of Biological Sciences, Macquarie we integrated a large seed mass data set with 3 species-barrier concept. The identification of University, Sydney, NSW 2109, Australia. Depart- current best opinion for the phylogeny of ment of Biological Sciences, Stanford University, further molecules involved in female game- Stanford, CA 94305–5020, USA. 4Department of seed plants. Our seed mass data set included tophyte pollen tube guidance in maize and Ecology and Evolutionary Biology, Yale University, 12,669 angiosperms and 318 gymnosperms. other plant species should not only help New Haven, CT 06520–8106, USA. 5The Natural This is È5% of all extant angiosperm and History Museum, Cromwell Road, London, SW7 5BD, understanding of many outstanding issues 6 38% of all extant gymnosperm species. The in plant reproductive biology but may also UK. Royal Botanic Gardens (RBG), Kew, Wakehurst angiosperm species are from 3158 genera Place, Ardingly, West Sussex, RH17 6TN, UK. be used for future plant breeding to over- (22% of the global total) and 260 families come some of the current crossing barriers *To whom correspondence should be addressed. (57%) and include representatives from all ex- E-mail: [email protected] and to allow hybridization between plant .Present address: Department of Integrative Biology, tant orders. The gymnosperm species are from genera that cannot be crossed today. University of California, Berkeley, CA 94720, USA. 52 genera (63%) and 10 families (63%) (21). 576 28 JANUARY 2005 VOL 307 SCIENCE www.sciencemag.org R EPORTS The resulting phylogeny has 2223 nodes (un- ular evidence generally supports the view tainty around this node, it is clear that the certain regions of the phylogeny were repre- that the extant gymnosperms are mono- evolution of the angiosperms was associated sented by polytomies), which we analyzed for phyletic (23, 24), but there is still some with a major reduction in seed mass. The dif- divergences in seed size. The dense coverage doubt about this (25). Under the mono- ference in seed mass between gymnosperms of this data set allows us to locate and quan- phyletic gymnosperm hypothesis, there is a and angiosperms is also apparent in the fossil tify the major divergences in seed mass. 59-fold divergence in seed mass between record. The earliest angiosperms have much We identified the largest divergence events angiosperms (small-seeded) and gymno- smaller seeds (averaging È1mm3) than coeval and those that contributed most to the spread sperms (large-seeded), È325 million years gymnosperms (200 mm3)(17, 28, 29). of seed mass across present-day species by ago (Ma) (26) (Fig. 2, node A). This is the The lower costs of pollen capture, early using two indicators, width and contribution: 54th widest divergence in the data set and abortion, and reduced gametophyte size (1) Divergence width is a measure of the contributes six times more to present-day associated with the angiosperm reproductive absolute size of divergences. Width was variation in seed mass than the next highest system might have allowed angiosperms to 0 calculated as the standard deviation of log10 contributing divergence (contribution 0.43) produce smaller seeds than was economical- seed mass across the clades immediately (Fig.
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