A Small RNA Pathway Mediates Allelic Dosage in Endosperm

Erdmann, Robert M.; Satyaki, P. R. V.; Klosinska, Maja; Gehring, Mary

doi:10.1016/j.celrep.2017.11.078

Cited by 76 publications

(147 citation statements)

References 36 publications

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“…In accordance with Erdmann et al, although not addressing the regulation of the silenced allele, we do observe derepression of maternal mRNA from MEGs in crosses with paternal as well as maternal depletion of RdDM components. The observed effect is in line with previous observations (Erdmann et al, 2017), however limited compared to the effect observed for met1 and mea-9.…”

Section: Rddm Alone Is Not Required For Establishment Of Imprintingsupporting

confidence: 93%

Regulation of Parent-of-Origin Allelic Expression inArabidopsis thalianaendosperm

Miller

Grini

2019

Preprint

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Genomic imprinting is an epigenetic phenomenon set in the gametes prior to fertilization that causes differential expression of parental alleles mainly in the endosperm of flowering plants. The overlap between previously identified panels of imprinted genes is limited. In order to achieve high resolution sequencing data we have used sequence capture technology to investigate imprinting. Here, we present a bioinformatics pipeline to assay parent-of-origin allele specific expression and report more than 300 loci with parental expression bias. We find that the level of expression from maternal and paternal alleles in most cases is not binary, instead favouring a differential dosage hypothesis for the evolution of imprinting in plants. To address imprinting regulation, we systematically employed mutations in regulative epigenetic pathways suggested to be major players in the process. We establish the mechanistic mode of imprinting for more than 50 loci regulated by DNA methylation and Polycombdependent histone methylation. However, the imprinting patterns of the majority of genes were not affected by these mechanisms. To this end we also demonstrate that the RNA-directed DNA methylation pathway alone does not influence imprinting patterns in a substantial manner, suggesting more complex epigenetic regulation pathways for the majority of identified imprinted genes. Author summaryExpression of gene copies only from the mother or the father´s genome, also termed imprinting, is a specialized epigenetic phenomenon that is found to be enriched at some genes expressed in the mammalian placenta and in the endosperm of the plant seed. Although several studies have reported on imprinted genes in plants, the identified loci are at large non-overlapping between reports. This motivated us to investigate in detail the expression pattern of imprinted genes in the endosperm and to determine how imprinting patterns are established at various imprinted loci. Although several underlying epigenetic regulation mechanisms have been demonstrated to establish imprinting patterns at certain genes, the majority of imprinted genes have not been linked to such mechanisms. In the present study we systematically investigated the mechanisms that are involved in establishing imprinting, by employing mutants of epigenetic regulators and high-throughput sequencing. In our high resolution study, we report more than 300 imprinted genes and demonstrate that the biological phenomenon imprinting involves gradual expression of parental gene copies rather than switching gene copies on or off. Notably, for the majority of imprinted genes, the mechanisms previously believed to be major to establish their imprinting patterns, are not responsible for mediating imprinting.

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Section: Rddm Alone Is Not Required For Establishment Of Imprintingsupporting

confidence: 93%

Regulation of Parent-of-Origin Allelic Expression inArabidopsis thalianaendosperm

Miller

Grini

2019

Preprint

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“…Loss of RdDM could negatively affect seed development in several possible ways. Massive deregulation of transposons would explain the asynchronous and nearly complete seed abortion we observed, and is consistent with reports of transposon deregulation linked to seed abortion during the triploid block (Erdmann et al ., ; Borges et al ., ; Martínez et al ., ). It is also possible that mobile maternal p4‐siRNAs are required for correct expression of specific transposon‐associated genes, such as AGAMOUS‐like transcription factors, which are upregulated in Arabidopsis seeds lacking maternal NRPD1 (Lu et al ., ).…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2018

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Small RNAs trigger repressive DNA methylation at thousands of transposable elements in a process called RNA-directed DNA methylation (RdDM). The molecular mechanism of RdDM is well characterized in Arabidopsis, yet the biological function remains unclear, as loss of RdDM in Arabidopsis causes no overt defects, even after generations of inbreeding. It is known that 24 nucleotide Pol IV-dependent siRNAs, the hallmark of RdDM, are abundant in flowers and developing seeds, indicating that RdDM might be important during reproduction. Here we show that, unlike Arabidopsis, mutations in the Pol IV-dependent small RNA pathway cause severe and specific reproductive defects in Brassica rapa. High rates of abortion occur when seeds have RdDM mutant mothers, but not when they have mutant fathers. Although abortion occurs after fertilization, RdDM function is required in maternal somatic tissue, not in the female gametophyte or the developing zygote, suggesting that siRNAs from the maternal soma might function in filial tissues. We propose that recently outbreeding species such as B. rapa are key to understanding the role of RdDM during plant reproduction.

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“…Total gene expression levels are derived from the contribution of maternally and 491 paternally inherited alleles. Based on the effect of nrpd1 mutations on allele-specific 492 expression in balanced endosperm, we previously proposed that 4N nrpd1 might 493 suppress paternal excess lethality by increasing transcriptional dosage from maternal 494 alleles for many genes (Erdmann et al, 2017). To test this hypothesis, we evaluated 495 allele-specific expression in balanced, lethal, and viable paternal excess endosperm for 496 genes with at least 50 allele-specific reads in both balanced and paternal excess 497 crosses ( Figure 7) (Supplemental Dataset 9).…”

Section: Paternal Excess Differentially Affects the Expression Of Matmentioning

confidence: 99%

Paternally-acting canonical RNA-directed DNA methylation pathway genes sensitize Arabidopsis endosperm to paternal genome dosage

Satyaki

Gehring

2019

Preprint

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22Seed development is sensitive to parental dosage, with excess maternal or paternal 23 genomes creating reciprocal phenotypes. Paternal genomic excess results in extensive 24 endosperm proliferation without cellularization and eventual seed abortion. We 25 previously showed that loss of the RNA POL IV gene nrpd1 in tetraploid fathers 26 represses seed abortion in paternal excess crosses. Here we show genetically that 27 RNA-directed DNA methylation (RdDM) pathway activity in the paternal parent is 28 sufficient to determine the viability of paternal excess seeds. The status of the RdDM 29 pathway in paternal excess endosperm does not impact seed viability. Comparison of 30 endosperm transcriptomes, DNA methylation, and small RNAs from balanced and 31 paternal excess endosperm demonstrates that paternal excess seed abortion is unlikely 32 to be dependent on either transposable element or imprinted gene mis-regulation. We 33 suggest instead that loss of paternal RdDM modulates expression at a small subset of 34 genes and desensitizes endosperm to paternal excess. Finally, using allele-specific 35 transcription data, we present evidence of a transcriptional buffering system that up-36

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A Small RNA Pathway Mediates Allelic Dosage in Endosperm

Cited by 76 publications

References 36 publications

Regulation of Parent-of-Origin Allelic Expression inArabidopsis thalianaendosperm

Regulation of Parent-of-Origin Allelic Expression inArabidopsis thalianaendosperm

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

Paternally-acting canonical RNA-directed DNA methylation pathway genes sensitize Arabidopsis endosperm to paternal genome dosage

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