Maternal Epigenetic Pathways Control Parental Contributions to Arabidopsis Early Embryogenesis

Diversité, Adaptation et Développement des Plantes, Institut de Recherche pour le Développement, Université de Montpellier, UMR 232, Montpellier 34394, France.
Cell (Impact Factor: 32.24). 05/2011; 145(5):707-19. DOI: 10.1016/j.cell.2011.04.014
Source: PubMed


Defining the contributions and interactions of paternal and maternal genomes during embryo development is critical to understand the fundamental processes involved in hybrid vigor, hybrid sterility, and reproductive isolation. To determine the parental contributions and their regulation during Arabidopsis embryogenesis, we combined deep-sequencing-based RNA profiling and genetic analyses. At the 2-4 cell stage there is a strong, genome-wide dominance of maternal transcripts, although transcripts are contributed by both parental genomes. At the globular stage the relative paternal contribution is higher, largely due to a gradual activation of the paternal genome. We identified two antagonistic maternal pathways that control these parental contributions. Paternal alleles are initially downregulated by the chromatin siRNA pathway, linked to DNA and histone methylation, whereas transcriptional activation requires maternal activity of the histone chaperone complex CAF1. Our results define maternal epigenetic pathways controlling the parental contributions in plant embryos, which are distinct from those regulating genomic imprinting.

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Available from: Thomas Lenormand
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    • "It has been shown that early embryo development in A. thaliana could be supported by the stored regulatory molecules until the preglobular stage consisting of 16–32 cells, while the endosperm strictly requires de novo transcription (Pillot et al. 2010). A globally delayed activation of gene expression in the early Arabidopsis embryo is controlled by the chromatin regulatory pathways (Autran et al. 2011), so the regulation of zygote silencing and rapid activation of the fertilized central cell is linked to specific global chromatin states inherited from each of the female gametes (Pillot et al. 2010). Chromatin structure and its transcriptional competence are determined by a combination of histone tail modifications and DNA methylation patterns (Vaillant and Paszkowski 2007). "
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    ABSTRACT: In many vascular plants, zygotic reproduction regularly alternates with different types of asexual reproduction, so embryos can develop not only from fertilized egg cells, but also from induced somatic cells through the process of somatic embryogenesis. Although somatic and zygotic embryogenesis are not directly correlated, their common features are presented, demonstrating that the origin and development of the somatic embryo morphologically and physiologically resemble zygotic embryogenesis at certain points. To initiate embryogenesis, both competent egg and somatic cells require activation either by fertilization or specific environmental signals, respectively. During induction of somatic and zygotic embryogenesis, modulation of DNA methylation, activation of particular hormonal and stress-related mechanisms and changes in cell wall properties are triggered. Here, we give an overview and discuss the most recent research in the field of plant somatic and zygotic embryogenesis, with special attention given to the onset of embryogenesis and early embryo development as well as to embryogenesis-related interconnections between plant hormones, stress responses, DNA methylation and regulatory gene expression.
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    • "Peng et al. (2013) in rice and Zhao et al. (2008) in maize also found that hybrid levels of cytosine methylation were closer to the maternal parent. Furthermore, Autran et al. (2011) found that during early embryogenesis in Arabidopsis, gene transcription is controlled by maternal epigenetic regulatory pathways, leading to a clear dominance of the transcripts from the maternal allele. Methylation polymorphism (or alterations) was found in 2927 sites (7.04%), indicating that methylation changes between parents and offspring (Table 5, Classes D1–D12) present a smaller percentage than the values reported by Peng et al. (2013) in rice (20.95%). "
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    ABSTRACT: Genetic inheritance and epigenetic inheritance are significant determinants of plant evolution, adaptation and plasticity. We studied inheritance of restriction site polymorphisms by the f-AFLP method and epigenetic DNA cytosine methylation inheritance by the f-MSAP technique. The study involved parents and 190 progeny of a Cupressus sempervirens L. full-sib family. Results from AFLP genetic data revealed that 71.8% of the fragments studied are under Mendelian genetic control, whereas faithful Mendelian inheritance for the MSAP fragments was low (4.29%). Further, MSAP fragment analysis showed that total methylation presented a mean of 28.2%, which was higher than the midparent value, while maternal inheritance was higher (5.65%) than paternal (3.01%). Interestingly de novo methylation in the progeny was high (19.65%) compared to parental methylation. Genetic and epigenetic distances for parents and offspring were not correlated (R 2 = 0.0005). Furthermore, we studied correlation of total relative methylation and CG methylation with growth (height, diameter). We found CG/CNG methylation (N: A, C, T) to be positively correlated with height and diameter, while total relative meth-ylation and CG methylation were positively correlated with height. Results are discussed in light of further research needed and of their potential application in breeding.
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    • "Hence, enzymatic or mechanical disruption is extremely challenging. Several studies have used microdissection to isolate entire embryos of defined stages to determine their transcriptome, and these have helped to provide a global view of the complexity of and changes in transcription in time (Autran et al., 2011; Xiang et al., 2011; Nodine and Bartel, 2012). However, the absence of tissue specificity is a major limitation, especially for genes expressed in only a few cells or at low levels. "

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