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Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14.

ABSTRACT: The histone demethylase JMJ14 catalyzes histone demethylation at lysine 4 of histone 3 and is involved in transcriptional repression and flowering time control in Arabidopsis. Here, we report that JMJ14 is physically associated with two previously uncharacterized NAC transcription factors, NAC050 and NAC052. The NAC050/052-RNAi plants and the CRISPR-CAS9-mediated nac050/052 double mutant plants show an early flowering phenotype, which is similar to the phenotype of jmj14, suggesting a functional association between JMJ14 and NAC050/052. RNA-seq data indicated that hundreds of common target genes are co-regulated by JMJ14 and NAC50/052. Our ChIP analysis demonstrated that JMJ14 and NAC050 directly bind to co-upregulated genes shared in jmj14 and NAC050/052-RNAi, thereby facilitating H3K4 demethylation and transcriptional repression. The NAC050/052 recognition DNA cis-element was identified by an electrophoretic mobility shift assay at the promoters of its target genes. Together, our study identifies two novel NAC transcription repressors and demonstrates that they are involved in transcriptional repression and flowering time control by associating with the histone demethylase JMJ14.

SUBMITTER: Ning YQ

PROVIDER: S-EPMC4330355 | biostudies-literature | 2015 Feb

REPOSITORIES: biostudies-literature

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Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14.

Ning Yong-Qiang YQ Ma Ze-Yang ZY Huang Huan-Wei HW Mo Huixian H Zhao Ting-ting TT Li Lin L Cai Tao T Chen She S Ma Ligeng L He Xin-Jian XJ

Nucleic acids research 20150110 3

The histone demethylase JMJ14 catalyzes histone demethylation at lysine 4 of histone 3 and is involved in transcriptional repression and flowering time control in Arabidopsis. Here, we report that JMJ14 is physically associated with two previously uncharacterized NAC transcription factors, NAC050 and NAC052. The NAC050/052-RNAi plants and the CRISPR-CAS9-mediated nac050/052 double mutant plants show an early flowering phenotype, which is similar to the phenotype of jmj14, suggesting a functional ...[more]

PMID: 25578968

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Project description:In spite of short-day (SD) nature, rice (Oryza sativa) shares a conserved photoperiodic network for flowering control with long-day plants like Arabidopsis thaliana. Flowering or heading is an important agronomic trait in rice. NAC transcription factors (TFs) are well-conserved and one of the largest families of plant TFs. However, their function in flowering or heading time is not well-known yet. A preferential expression of a membrane-bound NAC-like TF OsNTL5 in developing leaves and panicles of rice indicated to us its putative role in flowering. To examine its function, three independent constructs was generated, one with a deletion in the C terminus membrane-spanning domain (OsNTL5?C), OsNTL5?C fused with the SRDX transcriptional repressor motif and OsNTL5?C used with the VP16 activation domain under the Ubiquitin promoter to produce the overexpressing lines OsNTL5?C, OsNTL5?C-SRDX, and OsNTL5?C-VP, respectively in rice. The OsNTL5?C-VP line showed an early-flowering phenotype. In contrast to this, the plants with OsNTL5?C and OsNTL5?C-SRDX showed a very strong late-flowering phenotype, suggesting that OsNTL5 suppresses flowering as a transcriptional repressor. The protein subcellular localization assay suggested that N-terminal part of the OsNTL5 is localized to the nucleus after the protein is cleaved from its membrane-spanning domain at the C-terminal end and functions as a TF. Expression of flowering genes responsible for day length signals such as Early Heading Date 1 (Ehd1), Heading Date 3a (Hd3a), and Rice Flowering Locus T1 (RFT1) was significantly changed in the overexpression lines of OsNTL5?C-VP, OsNTL5?C, and OsNTL5?C-SRDX as analyzed by Quantitative Real-time PCR. ChIP-qPCR and rice protoplasts assays indicate that OsNTL5 directly binds to the promoter of Ehd1 and negatively regulates the expression of Ehd1, which shows antagonistic photoperiodic expression patterns of OsNTL5 in a 24-h SD cycle. Hence in conclusion, the NAC-like TF OsNTL5 functions as a transcriptional repressor to suppress flowering in rice as an upstream factor of Ehd1.

Project description:BackgroundPlants must integrate complex signals from environmental and endogenous cues to fine-tune the timing of flowering. Low temperature is one of the most common environmental stresses that affect flowering time; however, molecular mechanisms underlying the cold temperature regulation of flowering time are not fully understood.Methodology/principal findingsWe report the identification of a novel regulator, LONG VEGETATIVE PHASE 1 (LOV1), that controls flowering time and cold response. An Arabidopsis mutant, longvegetative phase 1-1D (lov1-1D) showing the late-flowering phenotype, was isolated by activation tagging screening. Subsequent analyses demonstrated that the phenotype of the mutant resulted from the overexpression of a NAC-domain protein gene (At2g02450). Both gain- and loss-of-function alleles of LOV1 affected flowering time predominantly under long-day but not short-day conditions, suggesting that LOV1 may act within the photoperiod pathway. The expression of CONSTANS (CO), a floral promoter, was affected by LOV1 level, suggesting that LOV1 controls flowering time by negatively regulating CO expression. The epistatic relationship between CO and LOV1 was consistent with this proposed regulatory pathway. Physiological analyses to elucidate upstream signalling pathways revealed that LOV1 regulates the cold response in plants. Loss of LOV1 function resulted in hypersensitivity to cold temperature, whereas a gain-of-function allele conferred cold tolerance. The freezing tolerance was accompanied by upregulation of cold response genes, COLD-REGULATED 15A (COR15A) and COLD INDUCED 1 (KIN1) without affecting expression of the C-repeat-binding factor/dehydration responsive element-binding factor 1 (CBF/DREB1) family of genes.ConclusionsOur study shows that LOV1 functions as a floral repressor that negatively regulates CO expression under long-day conditions and acts as a common regulator of two intersecting pathways that regulate flowering time and the cold response, respectively. Our results suggest an overlapping pathway for controlling cold stress response and flowering time in plants.

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Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14.

Publications

Two novel NAC transcription factors regulate gene expression and flowering time by associating with the histone demethylase JMJ14.

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