Functional characterization of <i>Nicotiana benthamiana</i> chromomethylase 3 in developmental programs by virus‐induced gene silencing

Hou, Pin-Quan; Lee, Yung-I; Hsu, Kuei-Ting; Lin, Yu-Ting; Wu, Wei; Lin, John-Yee; Trịnh, Ngọc Nam; Fu, Shih Feng

doi:10.1111/ppl.12071

Cited by 11 publications

(20 citation statements)

References 62 publications

(91 reference statements)

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“…A paralog of ZMET2, ZMET5, contributes to the maintenance of mCHG to a lesser degree in Z. mays [5, 7]. Homologous CMTs have been identified in other flowering plants (angiosperms) [16–19], early diverging land plants (Embryophyta) – the moss Physcomitrella patens and the lycophyte Selaginella moellendorffii – and the green algae (Chlorophyta) Chlorella sp. NC64A and Volvox carteri [20].…”

Section: Introductionmentioning

confidence: 99%

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

et al. 2017

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BackgroundThe evolution of gene body methylation (gbM), its origins, and its functional consequences are poorly understood. By pairing the largest collection of transcriptomes (>1000) and methylomes (77) across Viridiplantae, we provide novel insights into the evolution of gbM and its relationship to CHROMOMETHYLASE (CMT) proteins.ResultsCMTs are evolutionary conserved DNA methyltransferases in Viridiplantae. Duplication events gave rise to what are now referred to as CMT1, 2 and 3. Independent losses of CMT1, 2, and 3 in eudicots, CMT2 and ZMET in monocots and monocots/commelinids, variation in copy number, and non-neutral evolution suggests overlapping or fluid functional evolution of this gene family. DNA methylation within genes is widespread and is found in all major taxonomic groups of Viridiplantae investigated. Genes enriched with methylated CGs (mCG) were also identified in species sister to angiosperms. The proportion of genes and DNA methylation patterns associated with gbM are restricted to angiosperms with a functional CMT3 or ortholog. However, mCG-enriched genes in the gymnosperm Pinus taeda shared some similarities with gbM genes in Amborella trichopoda. Additionally, gymnosperms and ferns share a CMT homolog closely related to CMT2 and 3. Hence, the dependency of gbM on a CMT most likely extends to all angiosperms and possibly gymnosperms and ferns.ConclusionsThe resulting gene family phylogeny of CMT transcripts from the most diverse sampling of plants to date redefines our understanding of CMT evolution and its evolutionary consequences on DNA methylation. Future, functional tests of homologous and paralogous CMTs will uncover novel roles and consequences to the epigenome.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-017-1195-1) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

et al. 2017

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“…A paralog of ZMET2, ZMET5, contributes to the maintenance of mCHG to a lesser degree in Z. mays [5, 7]. Homologous CMTs have been identified in other flowering plants (angiosperms) [16, 17, 18, 19]: the moss Physcomitrella patens , the lycophyte Selaginella moellendorffii , and the green algae Chlorella sp. NC64A and Volvox carteri [20].…”

Section: Introductionmentioning

confidence: 99%

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

Bewick¹,

Niederhuth²,

Rohr³

et al. 2016

Preprint

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Background: The evolution of gene body methylation (gbM), its origins, and its functional consequences are poorly understood. By pairing the largest collection of transcriptomes (>1000) and methylomes (77) across Viridiplantae, we provide novel insights into the evolution of gbM and its relationship to CHROMOMETHYLASE (CMT) proteins. Results: CMTs are evolutionary conserved DNA methyltransferases in Viridiplantae. Duplication events gave rise to what are now referred to as CMT1, 2 and 3. Independent losses of CMT1, 2, and 3 in eudicots, CMT2 and ZMET in monocots and monocots/commelinids, variation in copy number, and non-neutral evolution suggests overlapping or fluid functional evolution of this gene family. DNA methylation within genes is widespread and is found in all major taxonomic groups of Viridiplantae investigated. Genes enriched with methylated CGs (mCG) were also identified in species sister to angiosperms. The proportion of genes and DNA methylation patterns associated with gbM are restricted to angiosperms with a functional CMT3 or ortholog. However, mCG-enriched genes in the gymnosperm Pinus taeda shared some similarities with gbM genes in Amborella trichopoda. Additionally, gymnosperms and ferns share a CMT homolog closely related to CMT2 and 3. Hence, the dependency of gbM on a CMT most likely extends to all angiosperms and possibly gymnosperms and ferns.

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“…CMT2 and CMT3 have DNA methylation activity at CHG sites ( Jones et al, 2001 ; Lindroth et al, 2001 ), and maintain CHH methylation at certain genomic loci ( Cao and Jacobsen, 2002a ; Cokus et al, 2008 ; Stroud et al, 2013 ). Zea mays methyltransferase 2 (ZMET2) and the Nicotiana benthamiana CMT3 homolog NbCMT3 were identified as CHG-specific DNMTs ( Papa et al, 2001 ; Hou et al, 2013 ). MET1 is a homolog of mammalian DNMT1 that catalyzes symmetric CG methylation ( Jones et al, 2001 ).…”

Section: Introductionmentioning

confidence: 99%

Ammonium Inhibits Chromomethylase 3-Mediated Methylation of the Arabidopsis Nitrate Reductase Gene NIA2

et al. 2016

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Gene methylation is an important mechanism regulating gene expression and genome stability. Our previous work showed that methylation of the nitrate reductase (NR) gene NIA2 was dependent on chromomethylase 3 (CMT3). Here, we show that CMT3-mediated NIA2 methylation is regulated by ammonium in Arabidopsis thaliana. CHG sequences (where H can be A, T, or C) were methylated in NIA2 but not in NIA1, and ammonium [(NH4)2SO4] treatment completely blocked CHG methylation in NIA2. By contrast, ammonium had no effect on CMT3 methylation, indicating that ammonium negatively regulates CMT3-mediated NIA2 methylation without affecting CMT3 methylation. Ammonium upregulated NIA2 mRNA expression, which was consistent with the repression of NIA2 methylation by ammonium. Ammonium treatment also reduced the overall genome methylation level of wild-type Arabidopsis. Moreover, CMT3 bound to specific promoter and intragenic regions of NIA2. These combined results indicate that ammonium inhibits CMT3-mediated methylation of NIA2 and that of other target genes, and CMT3 selectively binds to target DNA sequences for methylation.

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Functional characterization of Nicotiana benthamiana chromomethylase 3 in developmental programs by virus‐induced gene silencing

Cited by 11 publications

References 62 publications

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

The evolution of CHROMOMETHYLASES and gene body DNA methylation in plants

Ammonium Inhibits Chromomethylase 3-Mediated Methylation of the Arabidopsis Nitrate Reductase Gene NIA2

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