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Review
. 2024 Sep 27:15:1455685.
doi: 10.3389/fpls.2024.1455685. eCollection 2024.

Unveiling the imprinted dance: how parental genomes orchestrate seed development and hybrid success

Affiliations
Review

Unveiling the imprinted dance: how parental genomes orchestrate seed development and hybrid success

Muthusamy Muthusamy et al. Front Plant Sci. .

Abstract

Parental epigenetic asymmetries, which contribute to the monoallelic expression of genes known as imprints, play a critical role in seed development in flowering plants. Primarily, differential DNA methylation patterns and histone modifications on parental alleles form the molecular basis of gene imprinting. Plants predominantly exhibit this non-Mendelian inheritance phenomenon in the endosperm and the early embryo of developing seeds. Imprinting is crucial for regulating nutrient allocation, maintaining seed development, resolving parental conflict, and facilitating evolutionary adaptation. Disruptions in imprinted gene expression, mediated by epigenetic regulators and parental ploidy levels, can lead to endosperm-based hybridization barriers and hybrid dysfunction, ultimately reducing genetic diversity in plant populations. Conversely, imprinting helps maintain genetic stability within plant populations. Imprinted genes likely influence seed development in various ways, including ensuring proper endosperm development, influencing seed dormancy, and regulating seed size. However, the functions of most imprinted genes, the evolutionary significance of imprinting, and the long-term consequences of imprinting disruptions on plant development and adaptation need further exploration. Thus, it is clear that research on imprinting has immense potential for improving our understanding of plant development and ultimately enhancing key agronomic traits. This review decodes the possible genetic and epigenetic regulatory factors underpinning genomic imprinting and their positive and negative consequences on seed development. This study also forecasts the potential implications of exploiting gene imprinting for crop improvement programs.

Keywords: RNA-directed DNA methylation; epigenetic regulators; hybrid vigor; hybridization barriers; imprints; parent-of-origin effect; ploidy dosage; seed size.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Schematic representation of inheritance pattern of parental imprints and their parent of origin-effect on endosperm development in the developing seed of Arabidopsis. EN, endosperm; MEN, micropylar endosperm; CEN, chalazal endosperm; EM, embryo; EBN, endosperm balance number; New hybridization possibilities P1 and P2, predominantly leading to abnormal EBN in some of the interspecific crosses or individual with different ploidy levels. Parental imprints set during gametogenesis and imprint maintenance after fertilization determines the endosperm development and early embryogenesis as part of seed development. Double fertilization involves two fertilization events within the ovule of a flower, leading to the formation of both the endosperm (sperm cell fused with central cell in the ratio of 2 maternal: 1 paternal genome composition) and embryo (sperm cell fused with egg cell in the ratio of 1 maternal and 1 paternal genome contribution), as part of coordinated seed development in flowering plants including Arabidopsis. EBN 2:1 ensures proper endosperm development while abnormal EBN can cause defective endosperm and ultimately affect the size and viability of the developing seed.

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Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This work was supported by a grant from the New Breeding Technologies Development Program (Grant No. RS-2024-00419763), Rural Development Administration, Republic of Korea.

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