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.

ANAC075, a putative regulator of VASCULAR-RELATED NAC-DOMAIN7, is a repressor of flowering

“…Recent reports show that some NAC transcription factors are also involved in flowering-time regulation (Ning et al 2015;Yoo et al 2007). Among them, NAC050 and NAC052 were reported to function as negative regulators of flowering (Ning et al 2015). Similarly to anac075 mutants, loss-offunction lines of NAC050/NAC052 flower early under both long-and short-day conditions.…”

“…Loss of function of JMJ14, a JmjC-domain containing histone demethylase, leads to early flowering under both long-and short-day conditions, and overexpression of JMJ14 (JMJ14-ox) leads to late flowering, indicating that JMJ14 functions as a floral repressor (Jeong et al 2009;Lu et al 2010;Ning et al 2015;Searle et al 2010;Yang et al 2010). jmj14 under short days flowers considerably later than that under long days, suggesting that the mutants retain photoperiod sensitivity.…”

“…The mechanism by which JMJ14 represses flowering is controversial. Jeong et al (2009) reported that JMJ14 directly demethylates H3K4, an active-mark modification, of the FT locus, but Lu et al (2010) and Ning et al (2015) indicated that FT locus is not the direct target of demethylation by JMJ14. JMJ14 is reported to mediate H3K4 demethylation of TSF loci as well (Yang et al 2010).…”

“…JMJ14 is reported to mediate H3K4 demethylation of TSF loci as well (Yang et al 2010). Interestingly, JMJ14 physically interacts with the NAC-family transcription factors ANAC050 and ANAC052 (Ning et al 2015). Loss of function of ANAC050 and ANAC052 results in early flowering and overexpression of ANAC050 delays flowering, indicating that ANAC050 and ANAC052 function as floral repressors.…”

Genome-Wide Analysis of Soybean JmjC Domain-Containing Proteins Suggests Evolutionary Conservation Following Whole-Genome Duplication

“…In addition, AtJMJ14, an active histone H3K4 demethylase (Lu et al, 2010; Yang et al, 2010), was also implicated in preventing early flowering by repressing the expression of FLOWERING LOCUS T ( FT ) and its homologs. Recently, Ning reported that AtJMJ14 associates with two NAC transcription factors, NAC050 and NAC052, and co-occupies hundreds of common target genes, resulting in H3K4 demethylation and transcriptional repression (Ning et al, 2015). Apart from controlling flowering time, there is also evidence that AtJMJ14 functions in RNA silencing and cell-to-cell movement of an RNA silencing signal (Lu et al, 2010).…”