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Endosperm triploidy has a selective advantage during ongoing parental conflict by imprinting.

ABSTRACT: The endosperm of the flowering plant mediates the supply of maternal resources for embryogenesis. An endosperm formed in sexual reproduction between diploid parents is typically triploid, with a 2 : 1 ratio of maternal genetic material (denoted as 2m : 1p). Variation from this ratio affects endosperm size, indicating parent-specific expression of genes involved in endosperm growth and development. The presence of paternally or maternally imprinted genes can be explained by parental conflict over the transfer of nutrients from maternal to offspring tissue. Genomic imprinting can, for example, provide the male parent of an embryo in a mixed-paternity seed pod, with an opportunity for expressing its preference for a disproportionate allocation of resources to its embryo. It has been argued that a diploid 1m : 1p endosperm was ancestral and the 2m : 1p endosperm evolved after parental conflict, to improve maternal control over seed provisioning. We present a population genetic model, which instead places the origin of triploidy early in the parental conflict over resource allocation. We find that there is an advantage to having a triploid endosperm as the parental conflict continues. This advantage can help to explain why the 2m : 1p endosperm prevails among flowering plants.

SUBMITTER: Stewart-Cox JA

PROVIDER: S-EPMC1691787 | biostudies-literature | 2004 Aug

REPOSITORIES: biostudies-literature

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Endosperm triploidy has a selective advantage during ongoing parental conflict by imprinting.

Stewart-Cox J A JA Britton N F NF Mogie M M

Proceedings. Biological sciences 20040801 1549

The endosperm of the flowering plant mediates the supply of maternal resources for embryogenesis. An endosperm formed in sexual reproduction between diploid parents is typically triploid, with a 2 : 1 ratio of maternal genetic material (denoted as 2m : 1p). Variation from this ratio affects endosperm size, indicating parent-specific expression of genes involved in endosperm growth and development. The presence of paternally or maternally imprinted genes can be explained by parental conflict over ...[more]

PMID: 15306295

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Project description:In mammals, imprinted gene expression results from the sex-specific methylation of imprinted control regions (ICRs) in the parental germlines. Imprinting is linked to therian reproduction, that is, the placenta and imprinting emerged at roughly the same time and potentially co-evolved. We assessed the transcriptome-wide and ontology effect of maternally versus paternally methylated ICRs at the developmental stage of setting of the chorioallantoic placenta in the mouse (8.5dpc), using two models of imprinting deficiency including completely imprint-free embryos. Paternal and maternal imprints have a similar quantitative impact on the embryonic transcriptome. However, transcriptional effects of maternal ICRs are qualitatively focused on the fetal-maternal interface, while paternal ICRs weakly affect non-convergent biological processes, with little consequence for viability at 8.5dpc. Moreover, genes regulated by maternal ICRs indirectly influence genes regulated by paternal ICRs, while the reverse is not observed. The functional dominance of maternal imprints over early embryonic development is potentially linked to selection pressures favoring methylation-dependent control of maternal over paternal ICRs. We previously hypothesized that the different methylation histories of ICRs in the maternal versus the paternal germlines may have put paternal ICRs under higher mutational pressure to lose CpGs by deamination. Using comparative genomics of 17 extant mammalian species, we show here that, while ICRs in general have been constrained to maintain more CpGs than non-imprinted sequences, the rate of CpG loss at paternal ICRs has indeed been higher than at maternal ICRs during evolution. In fact, maternal ICRs, which have the characteristics of CpG-rich promoters, have gained CpGs compared to non-imprinted CpG-rich promoters. Thus, the numerical and, during early embryonic development, functional dominance of maternal ICRs can be explained as the consequence of two orthogonal evolutionary forces: pressure to tightly regulate genes affecting the fetal-maternal interface and pressure to avoid the mutagenic environment of the paternal germline.

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Endosperm triploidy has a selective advantage during ongoing parental conflict by imprinting.

Publications

Endosperm triploidy has a selective advantage during ongoing parental conflict by imprinting.

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