Maternal components of <scp>RNA</scp>‐directed <scp>DNA</scp> methylation are required for seed development in <i>Brassica rapa</i>

Grover, Jeffrey W.; Kendall, Timmy; Baten, Abdul; Burgess, Diane; Freeling, Michael; King, Graham J.; Mosher, Rebecca A.

doi:10.1111/tpj.13910

Cited by 73 publications

(107 citation statements)

References 55 publications

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“…The AGO4-siRNA complex interacts with the Cterminal domain of RNA Pol V and either the Pol V transcript or DNA within the Pol V transcription bubble (El-shami et al, 2007;Lahmy et al, 2016;Li et al, 2006;Liu et al, 2018), leading to the recruitment of the DNA methyltransferase DRM2 and methylation of cytosines (Matzke and Mosher, 2014). RdDM activity is associated with transcriptional silencing of transposable elements in euchromatin (Stroud et al, 2013;Zemach et al, 2013), and can influence the expression of genes (Grover et al, 2018;Pontier et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Abundant expression of maternal siRNAs is a conserved feature of seed development

Grover

Burgess

Kendall

et al. 2019

Preprint

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Small RNAs are abundant in plant reproductive tissues, especially 24-nt short interfering (si)RNAs. Most 24-nt siRNAs are dependent on RNA Pol IV and RDR2, and establish DNA methylation at thousands of genomic loci in a process called RNA-directed DNA methylation (RdDM). In Brassica rapa, RdDM is required in the maternal sporophyte for successful seed development. Here we demonstrate that a small number of siRNA loci account for over 90% of siRNA expression during B. rapa seed development. These loci exhibit unique characteristics with regard to their copy number and association with genomic features, but they resemble canonical 24-nt siRNA loci in their dependence on RNA Pol IV/RDR2 and role in RdDM. These loci are expressed in ovules before fertilization and in the seed coat, embryo, and endosperm following fertilization. We observed a similar pattern of 24-nt siRNA expression in diverse angiosperms despite rapid sequence evolution at siren loci. In the endosperm, siren siRNAs show a marked maternal bias, and siren expression in maternal sporophytic tissues is required for siren siRNA accumulation. Together these results demonstrate that seed development occurs under the influence of abundant maternal siRNAs that might be transported to, and function in, filial tissues.

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Section: Introductionmentioning

confidence: 99%

Abundant expression of maternal siRNAs is a conserved feature of seed development

Grover

Burgess

Kendall

et al. 2019

Preprint

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“…Yet loss of function phenotypes of these pathways have only subtle phenotypes during embryogenesis (Pillot et al, 2010;Autran et al, 2011). By contrast, loss of the maternal RdDM pathway in the outcrossing species Brassica rapa causes severe phenotypes during reproduction (Grover et al, 2018), demonstrating the importance of maternal RdDM regulation of seed development in a close relative of Arabidopsis. A better understanding of the mechanisms that regulate maternal and paternal transcript ratios in the zygote and early embryo will reveal more about the biological role that maternal dominance plays in early embryogenesis in Arabidopsis thaliana, and will facilitate comparative studies of maternal and paternal regulation of embryogenesis in species of agronomic importance like rice and maize.…”

Section: Resultsmentioning

confidence: 99%

Maternal genome dominance in early plant embryogenesis

Alaniz-Fabián

Xiang

León

et al. 2020

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Previous studies have alternately supported and discounted the hypothesis that the maternal genome plays a predominant role in early embryogenesis in plants. We used 24 embryo defective (emb) mutants of Arabidopsis thaliana to test for maternal and paternal effects in early embryogenesis. 5 emb mutants had equal maternal and paternal effects, 5 showed maternal effects and weak paternal effects, and the remaining 14 emb mutants conditioned only maternal effects, demonstrating a more important role for the maternal allele for most of these EMB genes. To assess genome-wide maternal and paternal contributions to early embryos, we produced allele-specific transcriptomes from zygote to mature stage embryos derived from reciprocal crosses of Columbia-0 and Tsu-1, a hybrid combination we show to be a faithful proxy for isogenic Columbia-0. Parent-of-origin analysis of these transcriptomes revealed a reciprocal maternal bias in thousands of genes from the zygote to octant stage. This bias greatly diminished by the globular stage, and was absent at later stages. Comparison with egg cell transcriptomes revealed no correlation between transcript levels in the egg and maternal bias in pre-globular embryos, suggesting that the maternal bias observed in early embryos is due to preferential zygotic transcription of maternal alleles. Taken together, the functional and transcriptome data presented here support a predominant role for the maternal genome in early Arabidopsis embryogenesis. SignificanceIn both animals and plants, the zygote is produced by the union of the egg and sperm cells. In animals, it is well accepted that mRNAs and proteins from the egg direct the first steps of embryogenesis. Here we present genetic and genomic experiments that support a predominant role for the maternal genome in early embryogenesis of plants, as well. In contrast to animals, our data suggest that this maternal influence is primarily derived not from inheritance of egg transcripts, but from preferential transcription of maternal alleles in the zygote and early embryo. This transient maternal zygotic bias may reflect an ancestral condition to diminish paternal influence on early embryogenesis in outcrossing plants.

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“…Mutants with compromised RdDM have been found to affect multiple post-fertilization processes, such as zygotic genome activation (Autran et al 2011), genome dosage sensitivity in endosperm (Erdmann et al 2017;Borges et al 2018;Martinez et al 2018), imprinting [reviewed in (Anderson and Springer 2018)], and seed development (Grover et al 2018). There are currently no available small RNA transcriptomes from sperm cells other than Arabidopsis, and none from egg cells for any plant.…”

Section: Introductionmentioning

confidence: 99%

Reprogramming of 24nt siRNAs in rice gametes

Li¹,

Cao

et al. 2019

Preprint

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Gametes constitute a critical stage of the plant life cycle, during which the genome undergoes reprogramming in preparation for embryogenesis. Here we characterized the small RNA transcriptomes of egg cells and sperm cells from rice to elucidate genome-wide distributions of 24nt siRNAs, which are a hallmark of RNA-directed DNA methylation (RdDM) in plants and are typically concentrated at boundaries of heterochromatin. We found that 24nt siRNAs were depleted from heterochromatin boundaries in both gametes, reminiscent of siRNA patterns in DDM1-type nucleosome remodeler mutants. In sperm, 24nt siRNAs were spread across broad heterochromatic regions, while in eggs, 24nt siRNAs were concentrated at a smaller number of heterochromatic loci throughout the genome, which were shared with vegetative tissues and sperm. In both gametes, patterns of CHH methylation, typically a strong indicator of RdDM, were similar to vegetative tissues, although lower in magnitude. These findings indicate that the small RNA transcriptome undergoes large-scale re-programming in both male and female gametes, which is not correlated with recruitment of DNA methyltransferases in gametes and suggestive of unexplored regulatory activities of gamete small RNAs in seeds after fertilization.

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Maternal components of RNA‐directed DNA methylation are required for seed development in Brassica rapa

Cited by 73 publications

References 55 publications

Abundant expression of maternal siRNAs is a conserved feature of seed development

Abundant expression of maternal siRNAs is a conserved feature of seed development

Maternal genome dominance in early plant embryogenesis

Reprogramming of 24nt siRNAs in rice gametes

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