Gene duplication, silencing and expression alteration govern the molecular evolution of PRC2 genes in plants

Furihata, Hazuka Y.; Suenaga, Kazuya; Kawanabe, Takahiro; Yoshida, Takanori; Kawabe, Akira

doi:10.1266/ggs.15-00055

Cited by 8 publications

(9 citation statements)

References 62 publications

(76 reference statements)

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“…We constructed gene family phylogenies for genes that are known to be important regulators of epigenetic patterning during reproduction, with a particular focus on those involved in gene imprinting (CMT, MET, DME, and the PCR2 components MEA, FIS, FIE, and MSI). Many of the relationships between gene family members corroborates previous studies (Furihata 2016) (Bewick 2017).…”

Section: Activity Of Genes Associated With Imprinting Via Dna and Histone Methylationsupporting

confidence: 87%

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

2021

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Studies of gene expression during seed development have been performed for a growing collection of species from a phylogenetically broad sampling of flowering plants (angiosperms). However, attention has mostly been focused on crop species or a small number of model systems. Information on gene expression during seed development is minimal for those angiosperm lineages whose origins predate the divergence of monocots and eudicots. In order to provide a new perspective on the early evolution of seed development in flowering plants, we sequenced transcriptomes of whole ovules and seeds from three key stages of reproductive development in the waterlily Nymphaea thermarum, an experimentally-tractable member of the Nymphaeales. We first explore general patterns of gene expression, beginning with mature ovules and continuing through fertilization into early and mid seed development. We then examine the expression of genes associated with DNA and histone methylation, processes known to be essential for development in distantly-related and structurally-divergent monocots and eudicots. Around 60% of transcripts putatively homologous to DNA and histone methylation modifiers are differentially expressed during seed development in N. thermarum, suggesting that the importance of dynamic epigenetic patterning during seed development dates to the earliest phases of angiosperm evolution. However, genes involved in establishing, maintaining, and removing methylation marks associated with genetic imprinting show a mix of conserved and unique expression patterns between N. thermarum and other flowering plants. Our data suggests that the regulation of imprinting has likely changed throughout angiosperm evolution, and furthermore identifies genes that merit further characterization in any angiosperm system.

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Section: Activity Of Genes Associated With Imprinting Via Dna and Histone Methylationsupporting

confidence: 87%

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

2021

Preprint

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“…For animals, there are usually only one or two members of each of the PRC2 groups, p55, E(z), Su(z)12 and ESC. However, plants usually have multiples of each group (Furihata et al ., 2016). For example, most of the monocots we analyzed in the present study had two or more FIE genes (Figure S1b).…”

Section: Discussionmentioning

confidence: 99%

“…Evolutionary analysis revealed that MEA had undergone natural selection in the promoter region (Kawabe et al ., 2007; Spillane et al ., 2007; Miyake et al ., 2009). Currently, our understanding of how the PRC2 members evolved and how they contribute to adaptation in plants other than Arabidopsis is limited (Furihata et al ., 2016). Given the strong similarities between OsFIE1 and OsFIE2 , we believed that it would not be a good strategy to use RNAi lines for functional analysis, owing to the spatiotemporal overlaps of expression of the two genes in seeds (Li et al ., 2014).…”

Section: Introductionmentioning

confidence: 99%

Functional divergence of two duplicated Fertilization Independent Endosperm genes in rice with respect to seed development

et al. 2020

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Fertilization Independent Endosperm (FIE) is an essential member of Polycomb Repressive Complex 2 (PRC2) that plays important roles in the developmental regulation of plants. OsFIE1 and OsFIE2 are two FIE homologs in the rice genome. Here, we showed that OsFIE1 probably duplicated from OsFIE2 after the origin of the tribe Oryzeae, but has a specific expression pattern and methylation landscape. During evolution, OsFIE1 underwent a less intensive purifying selection than did OsFIE2. The mutant osfie1 produced smaller seeds and displayed reduced dormancy, indicating that OsFIE1 predominantly functions in late seed development. Ectopic expression of OsFIE1, but not OsFIE2, was deleterious to vegetative growth in a dose-dependent manner. The newly evolved N-terminal tail of OsFIE1 was probably not the cause of the adverse effects on vegetative growth. The CRISPR/Cas9-derived mutant osfie2 exhibited impaired cellularization of the endosperm, which suggested that OsFIE2 is indispensable for early seed development as a positive regulator of cellularization. Autonomous endosperm was observed in both OsFIE2 +À and osfie1/OsFIE2 +À but at a very low frequency. Although OsFIE1-PRC2 exhibited H3K27me3 methyltransferase ability in plants, OsFIE1-PRC2 is likely to be less important for development in rice than is OsFIE2-PRC2. Our findings revealed the functional divergence of OsFIE1 and OsFIE2 and shed light on their distinct evolution following duplication.

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“…For animals, there are usually only one or two members of each of the PRC2 groups p55, E(z), Su(z)12 and ESC. However, plants usually have multiples of each group (Furihata et al , 2016). For example, most of the monocots we analyzed in the present study had two or more FIE genes ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Functional divergence of two duplicatedFertilization Independent Endospermgenes in rice with respect to seed development

Pan

Cheng

Zhiguo

et al. 2019

Preprint

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Fertilization Independent Endosperm (FIE) is an essential member of Polycomb Repression Complex 2 (PRC2) that plays important roles in the developmental regulation of plants. OsFIE1 and OsFIE2 are two FIE homologs in the rice genome. Here, we showed that OsFIE1 probably duplicated from OsFIE2 after the origin of the tribe Oryzeae, but has a specific expression pattern and methylation landscape. During evolution, OsFIE1 underwent a less intensive purifying selection than did OsFIE2. The mutant osfie1 produced smaller seeds and displayed reduced dormancy, indicating that OsFIE1 predominantly functions in late seed development. Ectopic expression of OsFIE1, but not OsFIE2, was deleterious to vegetative growth in a dosage-dependent manner. The newly evolved N-terminal tail of OsFIE1 was probably not the cause of the adverse effects on vegetative growth. The CRISPR/Cas9-derived mutant osfie2 exhibited impaired cellularization of the endosperm, which suggested that OsFIE2 is indispensable for early seed development as a positive regulator of cellularization. Autonomous endosperm was observed in both OsFIE2+− and osfie1/OsFIE2+− but at a very low frequency. Although OsFIE1-PRC2 exhibited H3K27me3 methyltransferase ability in plants, OsFIE1-PRC2 is likely to be less important for development in rice than is OsFIE2-PRC2. Our findings revealed the functional divergence of OsFIE1 and OsFIE2 and shed light on their distinct evolution following duplication.

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Gene duplication, silencing and expression alteration govern the molecular evolution of PRC2 genes in plants

Cited by 8 publications

References 62 publications

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

Transcriptomes across fertilization and seed development in the water lily Nymphaea thermarum (Nymphaeales) reveal dynamic expression of DNA and histone methylation modifiers

Functional divergence of two duplicated Fertilization Independent Endosperm genes in rice with respect to seed development

Functional divergence of two duplicatedFertilization Independent Endospermgenes in rice with respect to seed development

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