Imprinting--a Green Variation

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Science  23 Jan 2004:
Vol. 303, Issue 5657, pp. 483-485
DOI: 10.1126/science.1094375

The conquest of the terrestrial environment by plants and mammals is linked to the parallel evolution of a predominantly maternal control over embryogenesis. This evolution of maternal control spurred the development of an intriguing epigenetic mechanism, called imprinting, for controlling gene expression. Imprinted genes are those in which expression depends on their parental origin. For example, imprinted genes are expressed only from the maternal allele, the paternal allele having been silenced by methylation of cytosines in the gene sequence. On page 521 of this issue, Kinoshita and colleagues (1) propose a mechanism for establishing one-way control of imprinting in plants that is distinct from imprinting in mammals.

The nutrition and protection of the embryo by the mother requires the invention of a specific interface between the two. In mammals, this interface derives from extraembryonic tissues, which form the placenta. In plants, the embryo is connected to the maternal tissues by the endosperm, the product of a second fertilization event (see the figure). The plant endosperm and the mammalian placenta are both subjected to imprinting, resulting in the preferential expression of maternal copies of genes, most notably those involved in the control of growth (2, 3, 4). In the mouse, disruption of the imprinting of specific genes, such as Igfr2r, leads to aberrant development of the trophoblast (which contributes to the placenta) (5, 6). In plants, the polycomb-group gene MEDEA, a master regulator of endosperm development, is known to be imprinted in the endosperm but not in the embryo (7, 8). Kinoshita et al. now report that a second plant gene, FWA, which encodes a homeodomain transcription factor, is imprinted in the endosperm of the model plant Arabidopsis and is expressed only from the maternal allele (1). Expression of FWA in endosperm coincides with an overall reduction in the amount of methylated cytosine residues in the direct repeat sequences of the 5' region of this gene. The level of FWA methylation remains high in other tissues of the plant, preventing transcription of FWA in these tissues.

The control of imprinting.

Maternal imprints in the extraembryonic tissues of plants and mammals. (A) In plants, two identical male gametes are delivered by the pollen tube to two distinct female gametes, the egg cell and the central cell. A double fertilization process leads to the development of the embryo (yellow) surrounded by the nurturing endosperm (green). Genes specifically expressed in the endosperm, such as FWA, are subjected to release of constitutive repression (caused by methylation of cytosines) of the maternal but not the paternal allele (possibly through the action of DEMETER). Repression of FWA expression through DNA methylation of 5' repeats is maintained throughout the plant vegetative phase by the methyltransferase MET1. A more complex cycle of imprinting must exist for the MEDEA gene, which is expressed during vegetative development. (B) In mammals, maintenance of imprinting relies on the activity of the methyltransferase DNMT1 and is very complex. Imprinting is initially erased during global DNA demethylation in the germline; it is then reestablished during gametogenesis through unknown mechanisms. For example, in the case of the Igfr2r gene, the paternal allele is silenced by a mechanism involving DNA methylation, a noncoding RNA, and the PcG gene Eed. In female gametogenesis, methylation of the ICR of Igfr2r is prevented and expression of the maternal allele of Igfr2r is possible (19). After fertilization, methylation imprints in mammals are fully resistant to waves of DNA demethylation in both the extraembryonic and embryonic lineages. Expression of the imprints in the placenta requires a specific transcription mechanism, which is not active in the embryo.


The 5' direct repeats were originally identified in a study of epigenetic mutations in the FWA gene. The late flowering mutant fwa-1 of Arabidopsis is characterized by hypomethylation of the 5' direct repeats associated with ectopic expression of FWA in vegetative tissues (9). Kinoshita et al. investigated the origin of methylation of the 5' repeats in the Arabidopsis mutant. In plants, DNA methylation is maintained on cytosine residues by methyltransferase 1 (MET1), which is similar to mammalian DNMT1 (10), and by the plant-specific chromomethylase 3 (CMT3) (11). Domain-rearranged methyltransferases (DRMs) 1 and 2, with activities similar to the mammalian de novo methylase Dnmt3, are involved in reestablishing methylation patterns (12). MET1 targets CpG sites, whereas CMT3 and DRMs target other sites. The imprint of the FWA paternal allele is affected by reduced methylation induced by loss-of-function mutations in MET1, but not in CMT3 or in DRMs. This finding demonstrates that maintenance of the imprint relies on MET1 activity throughout the plant life cycle. Similarly, in mammals, DNMT1, which has strong homology to MET1, is involved in the maintenance of methylation linked to imprinted genes (13).

As the default status of FWA is to be silenced, differential expression of the maternal and paternal alleles (the basis of imprinting) relies on the release of maternal allele silencing. The DNA glycosylase DEMETER is specifically expressed in the central cell, the female gamete that gives rise to the endosperm (14). Loss of DEMETER activity results in the absence of FWA expression in endosperm (1). A similar result has been reported for the endosperm-specific expression of MEDEA (14). DEMETER activity may result in removal of methyl groups from cytosine residues in the 5' region of the maternal allele of MEDEA, and may have a similar effect on the maternal allele of FWA. A study reported in a recent issue of Developmental Cell (15) proposes that imprinting of MEDEA is controlled by antagonism between the two DNA-modifying enzymes, MET1 and DEMETER (15). Thus, imprinting of MEDEA and FWA in endosperm may rely on the same mechanism. Initially, both parental copies are silenced, then DEMETER removes methylation of FWA 5' repeats but only for the maternal allele of the central cell, triggering endosperm-specific expression of FWA. Unlike FWA, which is expressed only during formation of the female gametes, MEDEA is expressed during the vegetative phase of the plant life cycle (16). It is not yet clear when and how MEDEA expression is silenced before female gametogenesis begins. Mutation of MEDEA causes a marked phenotype in endosperm (17), but only when the mutation is maternally inherited. The maternal effect is currently presumed to rely on the imprinted, silenced status of the paternal allele. In contrast to MEDEA, the function of FWA in endosperm remains unknown (18).

Imprinting in Arabidopsis apparently relies on a different mechanism for controlling DNA methylation compared with imprinting in mammals. Imprinting in mammals is linked to DNA methylation of large (up to 100 kb) specific intergenic regions, called imprinting control centers (ICRs), that regulate the expression of a group of genes (19). Mammalian DNA methylation undergoes a cycle where it is removed globally in the germline. Imprints are erased in primordial germ cells and are then reestablished during gametogenesis. In plants, no such global demethylation has been detected during the plant life cycle (20). Imprinting results from the removal of the methylation mark from one of the parental alleles. Unlike the situation in mammals, the imprinted status of plants is not inherited and appears to be confined to the endosperm, which does not contribute to the next generation.


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