POWERDRESS and Diversified Expression of the MIR172 Gene Family Bolster the Floral Stem Cell Network

Yumul, Rae Eden; Kim, Yun Ju; Liu, Xigang; Wang, Ruozhong; Ding, Junhui; Xiao, Langtao; Chen, Xuemei

doi:10.1371/journal.pgen.1003218

Cited by 69 publications

(70 citation statements)

References 51 publications

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“…We reported previously that PWR regulates floral stem cell fate through promotion of miR172 and CRC expression (34), but its molecular function was unknown. The paired SANT domains (SANT1 and SANT2), a distinct feature of PWR, were found to have high sequence similarity with the animal HDAC subunits SMRT and N-CoR (52% and 63% similarity, respectively) (Fig.…”

Section: Resultsmentioning

confidence: 99%

POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis

Kim

Wang

Gao

et al. 2016

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

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102

133

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Histone acetylation is a major epigenetic control mechanism that is tightly linked to the promotion of gene expression. Histone acetylation levels are balanced through the opposing activities of histone acetyltransferases (HATs) and histone deacetylases (HDACs). Arabidopsis HDAC genes (AtHDACs) compose a large gene family, and distinct phenotypes among AtHDAC mutants reflect the functional specificity of individual AtHDACs. However, the mechanisms underlying this functional diversity are largely unknown. Here, we show that POWERDRESS (PWR), a SANT (SWI3/DAD2/N-CoR/TFIII-B) domain protein, interacts with HDA9 and promotes histone H3 deacetylation, possibly by facilitating HDA9 function at target regions. The developmental phenotypes of pwr and hda9 mutants were highly similar. Three lysine residues (K9, K14, and K27) of H3 retained hyperacetylation status in both pwr and hda9 mutants. Genome-wide H3K9 and H3K14 acetylation profiling revealed elevated acetylation at largely overlapping sets of target genes in the two mutants. Highly similar gene-expression profiles in the two mutants correlated with the histone H3 acetylation status in the pwr and hda9 mutants. In addition, PWR and HDA9 modulated flowering time by repressing AGAMOUS-LIKE 19 expression through histone H3 deacetylation in the same genetic pathway. Finally, PWR was shown to physically interact with HDA9, and its SANT2 domain, which is homologous to that of subunits in animal HDAC complexes, showed specific binding affinity to acetylated histone H3. We therefore propose that PWR acts as a subunit in a complex with HDA9 to result in lysine deacetylation of histone H3 at specific genomic targets.SANT domain | POWERDRESS | HDA9 | histone deacetylation | AGL19 P osttranslational modifications of histones-including acetylation, methylation, phosphorylation, and ubiquitinationplay important roles in plant development, genome integrity, and stress responses. Histone acetylation/deacetylation, a reversible process, promotes/represses gene expression (1) and occurs at lysine residues within histone N-terminal tails. The histone acetylation status is regulated by counteracting enzymes: histone acetyltransferases (HATs) and histone deacetylases (HDACs). The 18 HDACs identified in Arabidopsis (2) can be categorized into three groups based on phylogenetic analysis: reduced potassium dependency-3/histone deacetylase-1 (RPD3/HDA1), histone deacetylase-2 (HD2), and silent information regulator-2 (SIR2)-like (3). Twelve HDACs belong to the RPD3/HDA1 group (3) and are involved in various biological processes, such as organ development, reproductive processes, hormone signaling, and DNA methylation (4-9). They can be further classified into three classes based on sequence homology (3). The HD2 group is plant-specific and includes four HDACs that act in plant development and stress responses (10-13). The two HDACs encoded by the SIR2 family genes in Arabidopsis, SRT1 and SRT2, regulate mitochondrial energy metabolism and cellular dedifferentiation, respectively (14,15).I...

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Section: Resultsmentioning

confidence: 99%

POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis

Kim

Wang

Gao

et al. 2016

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

Self Cite

102

133

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“…CPM, counts per million; FC, fold change. Arabidopsis (Wu and Poethig, 2006;Chuck et al, 2007a), and ts4 has more severe phenotypes than loss of single miR172 genes in Arabidopsis (Chuck et al, 2007b;Wu et al, 2009;Yumul et al, 2013). It is possible that the gene networks regulated by miRNAs are more robust in Arabidopsis than in maize, such that in maize, reduction of only a handful of miRNAs leads to severe phenotypic consequences.…”

Section: Discussion Fzt Contains a Mutation In Dcl1 And Is Defective mentioning

confidence: 99%

The dicer-like1 Homolog fuzzy tassel Is Required for the Regulation of Meristem Determinacy in the Inflorescence and Vegetative Growth in Maize

et al. 2014

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Plant architecture is determined by meristems that initiate leaves during vegetative development and flowers during reproductive development. Maize (Zea mays) inflorescences are patterned by a series of branching events, culminating in floral meristems that produce sexual organs. The maize fuzzy tassel (fzt) mutant has striking inflorescence defects with indeterminate meristems, fasciation, and alterations in sex determination. fzt plants have dramatically reduced plant height and shorter, narrower leaves with leaf polarity and phase change defects. We positionally cloned fzt and discovered that it contains a mutation in a dicer-like1 homolog, a key enzyme required for microRNA (miRNA) biogenesis. miRNAs are small noncoding RNAs that reduce target mRNA levels and are key regulators of plant development and physiology. Small RNA sequencing analysis showed that most miRNAs are moderately reduced in fzt plants and a few miRNAs are dramatically reduced. Some aspects of the fzt phenotype can be explained by reduced levels of known miRNAs, including miRNAs that influence meristem determinacy, phase change, and leaf polarity. miRNAs responsible for other aspects of the fzt phenotype are unknown and likely to be those miRNAs most severely reduced in fzt mutants. The fzt mutation provides a tool to link specific miRNAs and targets to discrete phenotypes and developmental roles.

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“…The five MIR172 genes in the Arabidopsis genome produce three mature miR172 sequences (one from MIR172a and MIR172b, one from MIR172c and MIR172d, and one from MIR172e). A point mutation in MIR172d was found to enhance the FM determinacy defects of ag-10, a weak ag allele, in an AP2-dependent manner, clearly showing that miR172d contributes to FM determinacy by repressing AP2 expression (Yumul et al, 2013). From the same ag-10 genetic screen, a mutation in POWERDRESS (PWR), which encodes a SANT (for switching-defective protein3, adaptor2, nuclear receptor corepressor, transcription factor IIIB) domaincontaining protein, was isolated based on its enhanced ag-10 indeterminate phenotype.…”

Section: Noncoding Rnasmentioning

confidence: 95%

Epigenetic Mechanisms Are Critical for the Regulation of WUSCHEL Expression in Floral Meristems

Cao

He²,

Guo³

et al. 2015

Plant Physiol.

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The floral meristem (FM), which develops from the inflorescence meristem upon completion of the floral transition, terminates after producing a defined number of floral organs. This is in contrast to the shoot apical meristem, which is active throughout the entire life span of plants. WUSCHEL (WUS) encodes a homeodomain-containing protein and plays a critical role in shoot apical meristem, inflorescence meristem, and FM establishment and maintenance as well as FM determinacy. Although many genes have been implicated in FM determinacy through the regulation of WUS expression, precisely how these genes are coordinated to regulate WUS and consequently dictate FM fate remains unclear. Emerging lines of evidence indicate that epigenetic mechanisms, such as histone modification, chromatin remodeling, noncoding RNAs, and DNA methylation, play vital roles in meristem maintenance and termination. Here, recent findings demonstrating the involvement of the epigenetic network in the regulation of WUS expression in the context of FM determinacy are summarized and discussed.

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POWERDRESS and Diversified Expression of the MIR172 Gene Family Bolster the Floral Stem Cell Network

Cited by 69 publications

References 51 publications

POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis

POWERDRESS and HDA9 interact and promote histone H3 deacetylation at specific genomic sites in Arabidopsis

The dicer-like1 Homolog fuzzy tassel Is Required for the Regulation of Meristem Determinacy in the Inflorescence and Vegetative Growth in Maize

Epigenetic Mechanisms Are Critical for the Regulation of WUSCHEL Expression in Floral Meristems

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