Genomic imprinting in plants and mammals: how life history constrains convergence

In both flowering plants and mammals, DNA methylation is involved in silencing alleles of imprinted genes, but surprising differences in imprinting control are emerging between the two taxa which may be traced to differences in their life cycles. Imprinted gene expression in plants occurs in the endosperm, a separate fertilisation product which transmits nutrients to the embryo and does not contribute a genome to the next generation. Regulation of expression of the known imprinted genes in Arabidopsis involves a cascade of gene expression beginning in the gametophyte, a haploid life phase interposed between the meiotic products and the gametes, which evolved from free-living organisms that constitute the dominant life phase of lower plants. Although the gametophytes of flowering plants are highly reduced they still express large numbers of genes, perhaps reflecting their evolutionary legacy, and which may now be recruited for control of imprinting. Strikingly, the genes at the top of the expression cascade appear to be specifically activated by demethylation, rather than targeted for silencing. Unlike in mammals, there is no evidence for global resetting of methylation in plants, and although imprinting involves the activity of a maintenance methyltransferase, de novo methyltransferases do not appear to be required. Plants do not set aside a germline; instead the cells that undergo meiosis to produce gametophytes differentiate in the adult plant during flower development. Both the late differentiation of the lineage producing germ cells, and the extent of gene expression during the haploid phase, may be incompatible with global resetting of methylation. Resetting may be unnecessary in any case because the adult plant expresses imprinted loci either biallelically or not at all, suggesting there is no chromosomal memory of parent-of-origin in the lineage that produces the gametophytes. Thus several features of the plant life cycle may account for the different strategies used by plants and animals to regulate parent-specific gene expression.