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American Society of Plant Biologists
Demeter: On Seeds and GoddessesCommonwealth Scientific and Industrial Research Organization Division of Plant Industry P.O. Box 1600, Canberra, ACT 2601, Australia abdul.chaudhury{at}csiro.au
The genetic and developmental processes that control grain and seed development have become a fertile area of research in recent years. Insights have been obtained on how two haploid genomes come together to form the diploid zygote and triploid endosperm inside the maternal organs that sustain them (Chaudhury et al., 2001
Three FIS genes (MEA/FIS1, FIS2, and FIE/FIS3) were identified in a genetic screen designed to isolate mutants that showed autonomous seed development and thus decouple seed development from fertilization (Peacock et al., 1995  ; Ohad et al., 1996; Chaudhury et al., 1997). Apart from their autonomous phenotype, these gametophytic mutants showed a parent-of-origin effect. When the mutation was carried by the male parent, the developing seeds were normal, but when the mutation was carried by the female parent, seed development was abnormal even with a wild-type pollen parent (Ohad et al., 1996; Chaudhury et al., 1997). In an independent screen, a tagged mutant with a phenotype similar to that of the fis mutants was found and named after the goddess Medea (Grossniklaus et al., 1998). MEA is identical to FIS1 and was shown to be an imprinted gene. At the molecular level, the paternally derived gene was not transcribed in the developing endosperm, whereas the maternally derived gene was expressed (Grossniklaus et al., 1998; Kinoshita et al., 1999). The FIS2 gene also was shown to be imprinted using a reporter gene to analyze expression (Luo et al., 2000).
Interest in the relationships between seed development and parent-of-origin effects has been stimulated with the characterization of DME, which has been shown to be a direct regulator of MEA (Choi et al., 2002
Using promoter fusions to reporter genes, Choi et al. (2002)
When RNA levels of MEA, FIS2, or FIE were examined in the presence of dme-1, only MEA expression was disrupted, suggesting that the expression of MEA is dependent on DME function. Before fertilization, MEA is expressed in the two polar nuclei before their fusion to form the double-haploid nucleus of the central cell in the embryo sac. MEA continues to be expressed after fertilization in the endosperm nuclei formed by the division of the now triploid central cell nucleus. It also was shown that the expression of MEA is dependent on the presence of a functional copy of DME in the female gametophyte. In ovules that inherited both the dme-1 mutation and a MEA reporter construct, there was no expression of the MEA reporter. From these and other results, Choi et al. (2002)
Choi et al. (2002)
The deduced amino acid sequence suggests that DME is a large, monofunctional DNA glycosylase domain protein of 1729 amino acids. DNA glycosylases are DNA repair proteins that excise mismatched, modified, or damaged bases by cleaving the N-glycosidic bond between the base and the sugar-phosphate backbone of the DNA. Base excision results in an abasic site that is mutagenic and must be repaired. Repair is initiated with strand cleavage 5' to the abasic site to produce a 3' hydroxyl that is recognized by a specialized DNA repair polymerase. Unlike bifunctional DNA glycosylases, monofunc-tional DNA glycosylases such as DME do not have DNA-nicking activity. Strand cleavage is performed by an apurinic or apyrimidinic endonuclease, which creates a single-strand nick at abasic sites. Repair is completed by sealing the nick with a DNA ligase. Choi et al. (2002)
The authors also present evidence to support the hypothesis that DME activity leads to a single-strand nick in the vicinity of the MEA promoter. Using a sensitive PCR-based assay for nicks produced in vivo, it was shown that nicking occurs in the sense strand within 2 kb of the start of MEA transcription, but only if the CaMV: DME transgene also is present in the genome. There was no detectable nicking within 14 kb of the sense strand of MEA in the absence of the CaMV:DME transgene. The bands produced by the nicking assay were of different sizes, suggesting that DME produces nicks in the MEA promoter at many different locations (Choi et al., 2002
In the absence of pollination, the endosperm develops autonomously in all alleles of the three FIS genes that have been examined, although the penetrance is variable (Ohad et al., 1996
It remains to be determined what role, if any, DME plays in seed development other than controlling MEA expression. The floral and vegetative pleiotropic phenotypes observed in dme-1 homozygous mutants, and the presence of DME RNA in stems, suggest that DME functions more broadly in plant development. But as shown by Choi et al. (2002)
In both the fis1 and fis2 mutants, the maternal defect can be rescued by pollen that carries a nonfunctional fis1 or fis2 allele, provided that the DNA of the pollen donor also is hypomethylated (Luo et al., 2000 The characterization of DME has initiated a new area of investigation by linking a presumptive DNA metabolism enzyme to a mechanism of imprinting. Future work may elucidate the mechanism by which FIS2, FIE, and other genes are imprinted. Under the gaze of many goddesses, this fertile area of investigation surely will bring many new surprises. Acknowledgments We thank Jean Broadhvest for helpful comments. References Baroux, C., Spillane, C., and Grossniklaus, U. (2002). Genomic imprinting during seed development. Adv. Genet. 46, 65–214. Chaudhury, A.M., Koltunow, A., Payne, T., Luo, M., Tucker, M.R., Dennis, E.S., and Peacock, W.J. (2001). Control of early seed development. Annu. Rev. Cell Dev. Biol. 17, 677–699.[CrossRef][Web of Science][Medline]
Chaudhury, A.M., Ming, L., Craig, S., Dennis, E.S., and Peacock, W.J. (1997). Fertilization independent seed development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 94, 4223–4228. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J.J., Goldberg, R.B., Jacobsen, S.E., and Fischer, R.L. (2002). DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42.[CrossRef][Web of Science][Medline] Grossniklaus, U., Spillane, C., Page, D.R., and Koehler, C. (2001). Genomic imprinting and seed development: Endosperm formation with and without sex. Curr. Opin. Plant Biol. 4, 21–27.[CrossRef][Web of Science][Medline]
Grossniklaus, U., Vielle-Calzada, J.P., Hoepner, M.A., and Gagliano, W.B. (1998). Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280, 446–450.
Kinoshita, T., Yadegari, R., Harada, J.H., Goldberg, R.B., and Fisher, R.L. (1999). Imprint-ing of the MEDEA Polycomb gene in the Arabidopsis endosperm. Plant Cell 11, 1945–1952.
Luo, M., Bilodeau, P., Dennis, E., Peacock, W.J., and Chaudhury, A.M. (2000). Expression and parent of origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 97, 10637–10642.
Ohad, N., Margossian, L., Hsu, Y.-C., Williams, C., Repetti, P., and Fischer, R.L. (1996). A mutation that allows endosperm development without fertilization. Proc. Natl. Acad. Sci. USA 93, 5319–5324. Peacock, W.J., Ming, L., Craig, S., Dennis, E., and Chaudhury, A. (1995). A mutagenesis programme for apomixis genes in Arabidopsis. In Induced Mutations and Molecular Techniques for Crop Improvement. (Vienna: Food and Agricultural Organization of the United Nations/International Atomic Energy Agency), pp. 117–125.
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