skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Thursday, February 13 until 2:00 AM ET on Friday, February 14 due to maintenance. We apologize for the inconvenience.


Title: The H3K4 demethylase JMJ1 is required for proper timing of flowering in Brachypodium distachyon
Abstract

Flowering is a key developmental transition in the plant life cycle. In temperate climates, flowering often occurs in response to the perception of seasonal cues such as changes in day-length and temperature. However, the mechanisms that have evolved to control the timing of flowering in temperate grasses are not fully understood. We identified a Brachypodium distachyon mutant whose flowering is delayed under inductive long-day conditions due to a mutation in the JMJ1 gene, which encodes a Jumonji domain-containing protein. JMJ1 is a histone demethylase that mainly demethylates H3K4me2 and H3K4me3 in vitro and in vivo. Analysis of the genome-wide distribution of H3K4me1, H3K4me2, and H3K4me3 in wild-type plants by chromatin immunoprecipitation and sequencing combined with RNA sequencing revealed that H3K4m1 and H3K4me3 are positively associated with gene transcript levels, whereas H3K4me2 is negatively correlated with transcript levels. Furthermore, JMJ1 directly binds to the chromatin of the flowering regulator genes VRN1 and ID1 and affects their transcription by modifying their H3K4me2 and H3K4me3 levels. Genetic analyses indicated that JMJ1 promotes flowering by activating VRN1 expression. Our study reveals a role for JMJ1-mediated chromatin modification in the proper timing of flowering in B. distachyon.

 
more » « less
PAR ID:
10520255
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
The Plant Cell
Volume:
36
Issue:
7
ISSN:
1040-4651
Format(s):
Medium: X Size: p. 2729-2745
Size(s):
p. 2729-2745
Sponsoring Org:
National Science Foundation
More Like this
  1. SUMMARY

    Flowering of the reference legumeMedicago truncatulais promoted by winter cold (vernalization) followed by long‐day photoperiods (VLD) similar to winter annual Arabidopsis. However, Medicago lacksFLCandCO, key regulators of Arabidopsis VLD flowering.Most plants have twoINHIBITOR OF GROWTH(ING) genes (ING1andING2), encoding proteins with an ING domain with two anti‐parallel alpha‐helices and a plant homeodomain (PHD) finger, but their genetic role has not been previously described.In Medicago,Mting1gene‐edited mutants developed and flowered normally, but anMting2‐1 Tnt1insertion mutant and gene‐editedMting2mutants had developmental abnormalities including delayed flowering particularly in VLD, compact architecture, abnormal leaves with extra leaflets but no trichomes, and smaller seeds and barrels.Mting2mutants had reduced expression of activators of flowering, including theFT‐like geneMtFTa1, and increased expression of the candidate repressorMtTFL1c, consistent with the delayed flowering of the mutant.MtING2overexpression complementedMting2‐1, but did not accelerate flowering in wild type. The MtING2 PHD finger bound H3K4me2/3 peptides weaklyin vitro, but analysis of gene‐edited mutants indicated that it was dispensable to MtING2 function in wild‐type plants. RNA sequencing experiments indicated that >7000 genes are mis‐expressed in theMting2‐1mutant, consistent with its strong mutant phenotypes. Interestingly, ChIP‐seq analysis identified >5000 novel H3K4me3 locations in the genome ofMting2‐1mutants compared to wild type R108. Overall, our mutant study has uncovered an important physiological role of a plantING2gene in development, flowering, and gene expression, which likely involves an epigenetic mechanism.

     
    more » « less
  2. The proper timing of flowering, which is key to maximize reproductive success and yield, relies in many plant species on the coordination between environmental cues and endogenous developmental programs. The perception of changes in day length is one of the most reliable cues of seasonal change, and this involves the interplay between the sensing of light signals and the circadian clock. Here, we describe a Brachypodium distachyon mutant allele of the evening complex protein EARLY FLOWERING 3 (ELF3). We show that the elf3 mutant flowers more rapidly than wild type plants in short days as well as under longer photoperiods but, in very long (20 h) days, flowering is equally rapid in elf3 and wild type. Furthermore, flowering in the elf3 mutant is still sensitive to vernalization, but not to ambient temperature changes. Molecular analyses revealed that the expression of a short-day marker gene is suppressed in elf3 grown in short days, and the expression patterns of clock genes and flowering time regulators are altered. We also explored the mechanisms of photoperiodic perception in temperate grasses by exposing B. distachyon plants grown under a 12 h photoperiod to a daily night break consisting of a mixture of red and far-red light. We showed that 2 h breaks are sufficient to accelerate flowering in B. distachyon under non-inductive photoperiods and that this acceleration of flowering is mediated by red light. Finally, we discuss advances and perspectives for research on the perception of photoperiod in temperate grasses. 
    more » « less
  3. Köhler, C (Ed.)
    Daylength sensing in many plants is critical for coordinating the timing of flowering with the appropriate season. Temperate climate-adapted grasses such as Brachypodium distachyon flower during the spring when days are becoming longer. The photoreceptor PHYTOCHROME C is essential for long-day (LD) flowering in B. distachyon. PHYC is required for the LD activation of a suite of genes in the photoperiod pathway including PHOTOPERIOD1 (PPD1) that, in turn, result in the activation of FLOWERING LOCUS T (FT1)/FLORIGEN, which causes flowering. Thus, B. distachyon phyC mutants are extremely delayed in flowering. Here we show that PHYC-mediated activation of PPD1 occurs via EARLY FLOWERING 3 (ELF3), a component of the evening complex in the circadian clock. The extreme delay of flowering of the phyC mutant disappears when combined with an elf3 loss-of-function mutation. Moreover, the dampened PPD1 expression in phyC mutant plants is elevated in phyC/elf3 mutant plants consistent with the rapid flowering of the double mutant. We show that loss of PPD1 function also results in reduced FT1 expression and extremely delayed flowering consistent with results from wheat and barley. Additionally, elf3 mutant plants have elevated expression levels of PPD1, and we show that overexpression of ELF3 results in delayed flowering associated with a reduction of PPD1 and FT1 expression, indicating that ELF3 represses PPD1 transcription consistent with previous studies showing that ELF3 binds to the PPD1 promoter. Indeed, PPD1 is the main target of ELF3-mediated flowering as elf3/ppd1 double mutant plants are delayed flowering. Our results indicate that ELF3 operates downstream from PHYC and acts as a repressor of PPD1 in the photoperiod flowering pathway of B. distachyon. 
    more » « less
  4. Abstract

    Environmental stimuli trigger rapid transcriptional reprogramming of gene networks. These responses occur in the context of the local chromatin landscape, but the contribution of organ-specific dynamic chromatin modifications in responses to external signals remains largely unexplored. We treated tomato seedlings with a supply of nitrate and measured the genome-wide changes of four histone marks, the permissive marks H3K27ac, H3K4me3, and H3K36me3 and repressive mark H3K27me3, in shoots and roots separately, as well as H3K9me2 in shoots. Dynamic and organ-specific histone acetylation and methylation were observed at functionally relevant gene loci. Integration of transcriptomic and epigenomic datasets generated from the same organ revealed largely syngenetic relations between changes in transcript levels and histone modifications, with the exception of H3K27me3 in shoots, where an increased level of this repressive mark is observed at genes activated by nitrate. Application of a machine learning approach revealed organ-specific rules regarding the importance of individual histone marks, as H3K36me3 is the most successful mark in predicting gene regulation events in shoots, while H3K4me3 is the strongest individual predictor in roots. Our integrated study substantiates a view that during plant environmental responses, the relationships between histone code dynamics and gene regulation are highly dependent on organ-specific contexts.

     
    more » « less
  5. Summary

    Many plants require prolonged exposure to cold to acquire the competence to flower. The process by which cold exposure results in competence is known as vernalization. InArabidopsis thaliana, vernalization leads to the stable repression of the floral repressorFLOWERING LOCUS Cvia chromatin modification, including an increase of trimethylation on lysine 27 of histone H3 (H3K27me3) by Polycomb Repressive Complex 2 (PRC2). Vernalization in pooids is associated with the stable induction of a floral promoter,VERNALIZATION1(VRN1). From a screen for mutants with a reduced vernalization requirement in the model grassBrachypodium distachyon, we identified two recessive alleles ofENHANCER OF ZESTELIKE 1(EZL1).EZL1is orthologous toA. thalianaCURLY LEAF 1, a gene that encodes the catalytic subunit ofPRC2.B. distachyon ezl1mutants flower rapidly without vernalization in long‐day (LD) photoperiods; thus,EZL1is required for the proper maintenance of the vegetative state prior to vernalization. Transcriptomic studies inezl1revealed mis‐regulation of thousands of genes, including ectopic expression of several floral homeotic genes in leaves. Loss ofEZL1results in the global reduction of H3K27me3 and H3K27me2, consistent with this gene making a major contribution toPRC2 activity inB. distachyon. Furthermore, inezl1mutants, the flowering genesVRN1andAGAMOUS(AG) are ectopically expressed and have reduced H3K27me3. Artificial microRNAknock‐down of eitherVRN1orAGinezl1‐1mutants partially restores wild‐type flowering behavior in non‐vernalized plants, suggesting that ectopic expression inezl1mutants may contribute to the rapid‐flowering phenotype.

     
    more » « less