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Control of Fertilization-Independent Endosperm Development by the MEDEA Polycomb Gene in Arabidopsis (Reproduction͞embryo͞seed͞apomixis)

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Control of Fertilization-Independent Endosperm Development by the MEDEA Polycomb Gene in Arabidopsis (Reproduction͞embryo͞seed͞apomixis) Proc. Natl. Acad. Sci. USA Vol. 96, pp. 4186–4191, March 1999 Plant Biology Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis (reproductionyembryoyseedyapomixis) TOMOHIRO KIYOSUE*†,NIR OHAD†‡,RAMIN YADEGARI*, MIKE HANNON*, JOSE DINNENY*, DEREK WELLS*, i ANAT KATZ‡,LINDA MARGOSSIAN*, JOHN J. HARADA§,ROBERT B. GOLDBERG¶, AND ROBERT L. FISCHER* *Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720; ‡Department of Plant Sciences, Tel Aviv University, Tel Aviv 69978, Israel; §Section of Plant Biology, Division of Biological Sciences, University of California, Davis, CA 95616; and ¶Department of Molecular, Cell, and Developmental Biology, University of California, Los Angeles, CA 90024-1606 Communicated by Brian A. Larkins, University of Arizona, Tuscon, AZ, January 25, 1999 (received for review November 24, 1998) ABSTRACT Higher plant reproduction is unique because These nuclei migrate within an expanding central cell (2), after two cells are fertilized in the haploid female gametophyte. Egg which cytokinesis occurs, and endosperm nuclei and cytoplasm and sperm nuclei fuse to form the embryo. A second sperm are partitioned into cells. The endosperm (Fig. 2H) produces nucleus fuses with the central cell nucleus that replicates to storage proteins, starch, and lipids, all of which are taken up generate the endosperm, a tissue that supports embryo de- by the developing embryo (1). velopment. To understand mechanisms that initiate repro- We and others isolated Arabidopsis mutants, fertilization- duction, we isolated a mutation in Arabidopsis, f644, that independent endosperm (fie) (3) and fertilization-independent allows for replication of the central cell and subsequent seed (fis) (4), that act in the female gametophyte and allow for endosperm development without fertilization. When mutant aspects of reproductive development to occur without fertili- f644 egg and central cells are fertilized by wild-type sperm, zation. When fertilization is prevented by the removal of embryo development is inhibited, and endosperm is overpro- pollen-producing anthers, the mutant central cell replicates to duced. By using a map-based strategy, we cloned and se- form a diploid endosperm, and the maternal ovary and ovule quenced the F644 gene and showed that it encodes a SET- domain polycomb protein. Subsequently, we found that F644 integuments generate the fruit and seed coat, respectively (3, is identical to MEDEA (MEA), a gene whose maternal-derived 4). Recently, the FIE gene has been shown to encode a allele is required for embryogenesis [Grossniklaus, U., Vielle- polycomb protein with WD repeats (5). Therefore, this class of Calzada, J.-P., Hoeppner, M. A. & Gagliano, W. B. (1998) polycomb protein functions to suppress central-cell nuclear Science 280, 446–450]. Together, these results reveal functions replication and endosperm development in the female gameto- for plant polycomb proteins in the suppression of central cell phyte until fertilization occurs. proliferation and endosperm development. We discuss models Inheritance of the mutant fie or fis allele by a female to explain how polycomb proteins function to suppress en- gametophyte is deleterious for embryo development even dosperm and promote embryo development. when the pollen bears the wild-type allele (3, 4). In Arabidopsis, two other mutations have been identified based on a similar How fertilization activates reproductive development is a maternal ‘‘parent-of-origin’’ effect on embryogenesis, embryo- fundamental problem in biology. In higher plants, the ovule defective173 (emb173) (6) and medea (mea) (7). produces a female gametophyte that is composed of egg, To understand how fertilization initiates reproductive de- central, synergid, and antipodal cells (Fig. 1 A and C). All are velopment, we have isolated the mutation f644. Central-cell haploid, except the central cell, which contains two daughter nuclei with the f644 mutant allele replicate and initiate en- nuclei that fuse before fertilization to form a diploid central dosperm development without fertilization. When the f644 cell nucleus. Surrounding and protecting the female gameto- mutant egg and central cells are fertilized with mutant or phyte are maternal cell layers, integuments (Fig. 1C). Egg and wild-type male gametes, the embryo aborts, and endosperm sperm fuse to generate the embryo (Fig. 1I). Fusion of the accumulates to a higher than normal level. By using a map- adjacent central cell with a second sperm cell generates the based strategy, we cloned the F644 gene and showed that it is primary triploid endosperm nucleus that replicates to form the related to the family of SET-domain polycomb proteins (8). endosperm (Fig. 1I), a tissue that supports the development of Subsequently, we became aware that the F644 gene was the embryo (1). Fertilization also activates maternal tissue identical to the MEA gene that had been reported to control differentiation. The seed coat (Fig. 1I) is generated from the embryonic cell proliferation during the middle and late stages ovule integuments. To support the development of the rapidly of embryogenesis (7). The phenotypes associated with the f644 growing seeds, the ovary differentiates and elongates to form mutation revealed functions for the MEAyF644 gene in the the fruit, or silique, in Arabidopsis (Fig. 2A). suppression of central cell proliferation and endosperm de- Embryo and endosperm follow distinct patterns of devel- velopment. opment. In Arabidopsis, the embryo passes through a series of stages that have been defined morphologically as preglobular (Fig. 1I), globular, heart, cotyledon (Fig. 2H), and maturation METHODS (Fig. 2F). During these stages, an axis of polarity is fixed, shoot and root meristems are formed, and storage organs are Plant Material. Siliques, seed-like structures, and seeds generated. In contrast, the primary endosperm nucleus mitot- were prepared and photographed as described (3). Approxi- ically divides and produces a syncytium of nuclei (Fig. 1I). mate seed volume was calculated by using the equation The publication costs of this article were defrayed in part by page charge Abbreviation: DAP, days after pollination. †T.K. and N.O. contributed equally to this work. payment. This article must therefore be hereby marked ‘‘advertisement’’ in i To whom reprint requests should be addressed at: 111 Koshland Hall, accordance with 18 U.S.C. §1734 solely to indicate this fact. University of California, Berkeley, CA 94720-3102. e-mail: rfischer@ PNAS is available online at www.pnas.org. uclink4.berkeley.edu. 4186 Downloaded by guest on October 1, 2021 Plant Biology: Kiyosue et al. Proc. Natl. Acad. Sci. USA 96 (1999) 4187 FIG. 2. Seed development in wild-type and mutant Arabidopsis plants. Siliques and seeds shown in panels A–G were harvested 9 days after self-pollination. Those in panels H–I were harvested 5 days after self-pollination. Seeds in F–I were cleared and photographed by using Nomarski optics as described in Methods.(A) Portion of a wild-type silique. (B) Portion of an f644 heterozygous silique. (C) Portion of an f644 homozygous silique. (D and F) Seeds with wild-type phenotype from f644 heterozygous silique in B.(E and G) Seeds with mutant FIG. 1. Endosperm and seed coat development in mutant Arabi- phenotype from f644 heterozygous silique in B. Arrows in Inset point dopsis plants when fertilization is prevented. (A) Wild-type silique. (B) to nuclei. (H) Wild-type seed. (I) Homozygous f644 seed. AE, f644 homozygous silique. (C) Wild-type ovule. (D–H) f644 homozy- abnormal embryo; EM, embryo; EN, endosperm; m, seed with a gous seed-like structures. (I) Wild-type seed with globular embryo 2 mutant phenotype; wt, seed with a wild-type phenotype; SC, seed coat. days after self-pollination. Siliques, ovules and seed-like structures in [Bar 5 0.5 mm (A–C), 0.1 mm (D–I), and 0.04 mm (Inset in G).] A–H were harvested 6 days after removal of anthers. CCN, central cell nucleus; ECN, egg cell nucleus; EM, embryo, EN, endosperm; ENN, one of the endosperm nuclei in the endosperm; FG, female gameto- We also selected plants bearing recombinant chromosomes phyte; I, integument; OV, ovule; SC, seed coat; SLS, seed-like with breakpoints between f644 and the upstream morpholog- structure. Unlabeled arrows indicate nuclei derived from the unfer- ical marker, emb60 (10). Twenty-six recombinant F2 plants tilized central cell. [Bar 5 0.5 mm (A–B) and 0.1 mm (C–I).] were identified and used to map the f644 mutation relative to closely linked upstream RFLP markers. 4y3pa2b, where a is the minor axis and b is the major axis of Complementation. Agrobacterium-mediated transformation the ellipsoid-shaped seed. of f644 heterozygous plants was performed as described (11). Mapping the f644 Mutation. The F644 mutation was For cosmid 6–22, 10 transgenic T1 lines were obtained that mapped to position 3.0 on chromosome 1 between restriction displayed 25% seed abortion (e.g., 81 normal:22 aborted, 3:1, fragment length polymorphism (RFLP) markers nga59 and x2 5 0.02, P . 0.9) in self-pollinated siliques, suggesting that 0846A by using procedures described previously (3). For fine an unlinked wild-type F644 allele on cosmid 6-22 comple- structure mapping, we selected plants bearing recombinant mented the mutant f644 allele. Lines homozygous for both the chromosomes with breakpoints between f644 and the down- mutant f644 allele and the transgenic wild-type F644 allele stream morphological marker, axr3 (9). Eighty-one F2 recom- displayed no seed abortion in self-pollinated siliques. After binant plants were identified and used to map the f644 fertilization was prevented by the removal of anthers, all ovules mutation relative to closely linked downstream RFLP markers. (n 5 177) displayed a central cell with a single nucleus. Downloaded by guest on October 1, 2021 4188 Plant Biology: Kiyosue et al. Proc. Natl. Acad. Sci. USA 96 (1999) DNA Sequencing. Cosmid 6-22 DNA sequence was deter- Table 1. Penetrance of the fertilization-independent endosperm mined by LARK Sequencing Technologies (Houston).
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