Polycomb group-dependent imprinting of the actin regulator<i>AtFH5</i>regulates morphogenesis in<i>Arabidopsis thaliana</i>

Gerald, Jonathan N. Fitz; Hui, Poh Shi; Berger, Frédéric

doi:10.1242/dev.036921

Cited by 64 publications

(55 citation statements)

References 41 publications

(49 reference statements)

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“…Previous analysis of imprinted genes that do not exhibit activation of the paternal allele in endosperm fertilized with met1 pollen (FH5 and MEA) revealed that the maternally expressed PRC2 complex silences the paternal allele (10,11). In accordance with this idea, we identified 20 genes that exhibited activation of the paternal allele caused by a maternally inherited fie mutation (Fig.…”

Section: Effects Of Paternal Met1 and Maternal Dme And Fie Mutations Onsupporting

confidence: 75%

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Regulation of imprinted gene expression in Arabidopsis endosperm

Hsieh

Shin²,

Uzawa³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

305

551

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Imprinted genes are expressed primarily or exclusively from either the maternal or paternal allele, a phenomenon that occurs in flowering plants and mammals. Flowering plant imprinted gene expression has been described primarily in endosperm, a terminal nutritive tissue consumed by the embryo during seed development or after germination. Imprinted expression in Arabidopsis thaliana endosperm is orchestrated by differences in cytosine DNA methylation between the paternal and maternal genomes as well as by Polycomb group proteins. Currently, only 11 imprinted A. thaliana genes are known. Here, we use extensive sequencing of cDNA libraries to identify 9 paternally expressed and 34 maternally expressed imprinted genes in A. thaliana endosperm that are regulated by the DNA-demethylating glycosylase DEMETER, the DNA methyltransferase MET1, and/or the core Polycomb group protein FIE. These genes encode transcription factors, proteins involved in hormone signaling, components of the ubiquitin protein degradation pathway, regulators of histone and DNA methylation, and small RNA pathway proteins. We also identify maternally expressed genes that may be regulated by unknown mechanisms or deposited from maternal tissues. We did not detect any imprinted genes in the embryo. Our results show that imprinted gene expression is an extensive mechanistically complex phenomenon that likely affects multiple aspects of seed development.

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Section: Effects Of Paternal Met1 and Maternal Dme And Fie Mutations Onsupporting

confidence: 75%

“…The MEA gene is selfimprinted, with maternal MEA protein activity required to silence the paternal allele after fertilization (10). Maternal PRC2 proteins also silence the paternal allele of the actin regulator, ARABIDOPSIS FORMIN HOMOLOG 5 (FH5) (11).…”

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confidence: 99%

Regulation of imprinted gene expression in Arabidopsis endosperm

Hsieh

Shin²,

Uzawa³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

305

551

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“…Alternatively, the delay of early embryogenesis could be due to an indirect effect of loss of LRE in the endosperm. Nevertheless, our study adds LRE to a growing list of MEGs whose loss negatively impacts seed development, including ZIX, FH5, and NUWA in Arabidopsis (Ingouff et al, 2005;Fitz Gerald et al, 2009;Ngo et al, 2012;He et al, 2017) and MEG1 in maize (Gutiérrez-Marcos et al, 2004;Costa et al, 2012). Additionally, mutations in MEGs like FWA and AGL36 do not result in endosperm phenotypes (Kinoshita et al, 2004;Shirzadi et al, 2011).…”

Section: Silencing Of the Paternal Allele Of Lre May Be Controlled Bymentioning

confidence: 79%

Arabidopsis LORELEI, a Maternally Expressed Imprinted Gene, Promotes Early Seed Development

et al. 2017

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In flowering plants, the female gametophyte controls pollen tube reception immediately before fertilization and regulates seed development immediately after fertilization, although the controlling mechanisms remain poorly understood. Previously, we showed that LORELEI (LRE), which encodes a putative glycosylphosphatidylinositol-anchored membrane protein, is critical for pollen tube reception by the female gametophyte before fertilization and the initiation of seed development after fertilization. Here, we show that LRE is expressed in the synergid, egg, and central cells of the female gametophyte and in the zygote and proliferating endosperm of the Arabidopsis (Arabidopsis thaliana) seed. Interestingly, LRE expression in the developing seeds was primarily from the matrigenic LRE allele, indicating that LRE expression is imprinted. However, LRE was biallelically expressed in 8-d-old seedlings, indicating that the patrigenic allele does not remain silenced throughout the sporophytic generation. Regulation of imprinted LRE expression is likely novel, as LRE was not expressed in pollen or pollen tubes of mutants defective for MET1, DDM1, RNA-dependent DNA methylation, or MSI-dependent histone methylation. Additionally, the patrigenic LRE allele inherited from these mutants was not expressed in seeds. Surprisingly, and contrary to the predictions of the parental conflict hypothesis, LRE promotes growth in seeds, as loss of the matrigenic but not the patrigenic LRE allele caused delayed initiation of seed development. Our results showed that LRE is a rare imprinted gene that functions immediately after double fertilization and supported the model that a passage through the female gametophyte establishes monoalleleic expression of LRE in seeds and controls early seed development.

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“…Imprinting (de novo monoallelic expression after fertilization) but also cytoplasmic inheritance of maternal or paternal transcripts can explain these observations Vielle-Calzada et al, 2000;Bayer et al, 2009). Thus, an analysis of steady state levels of parental transcripts is only sufficient to demonstrate imprinting if the candidate gene is not expressed prior to fertilization in the gametes, as is the case for the Arabidopsis genes PHERES1 (PHE1) and FORMIN HOMOLOG5 (FH5) and, in the embryo, for the maize gene Maternally expressed in embryo1 (Mee1) (Kö hler et al, 2005;Fitz Gerald et al, 2009;Jahnke and Scholten, 2009;Wuest et al, 2010). Alternatively, parent-of-origin-specific expression that increases after fertilization provides evidence for genomic imprinting in addition to parental transcripts potentially inherited from the gametes, whose abundance cannot increase.…”

Section: Defining Imprinted Loci: Meeting the Standardsmentioning

confidence: 99%

Regulation and Flexibility of Genomic Imprinting during Seed Development

2011

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Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner. It is achieved by the differential epigenetic marking of parental alleles. Over the past decade, studies in the model systems Arabidopsis thaliana and maize (Zea mays) have shown a strong correlation between silent or active states with epigenetic marks, such as DNA methylation and histone modifications, but the nature of the primary imprint has not been clearly established for all imprinted genes. Phenotypes and expression patterns of imprinted genes have fueled the perception that genomic imprinting is specific to the endosperm, a seed tissue that does not contribute to the next generation. However, several lines of evidence suggest a potential role for imprinting in the embryo, raising questions as to how imprints are erased and reset from one generation to the next. Imprinting regulation in flowering plants shows striking similarities, but also some important differences, compared with the mechanisms of imprinting described in mammals. For example, some imprinted genes are involved in seed growth and viability in plants, which is similar in mammals, where imprinted gene regulation is essential for embryonic development. However, it seems to be more flexible in plants, as imprinting requirements can be bypassed to allow the development of clonal offspring in apomicts.

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Polycomb group-dependent imprinting of the actin regulatorAtFH5regulates morphogenesis inArabidopsis thaliana

Cited by 64 publications

References 41 publications

Regulation of imprinted gene expression in Arabidopsis endosperm

Regulation of imprinted gene expression in Arabidopsis endosperm

Arabidopsis LORELEI, a Maternally Expressed Imprinted Gene, Promotes Early Seed Development

Regulation and Flexibility of Genomic Imprinting during Seed Development

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