Cross‐species complementation reveals conserved functions for EARLY FLOWERING 3 between monocots and dicots

Huang, He; Gehan, Malia; Huss, Sarah E.; Alvarez, Sophie; Lizárraga, César; Gruebbling, Ellen L.; Gierer, John; Naldrett, Michael J.; Bindbeutel, Rebecca K.; Evans, Bradley S.; Mockler, Todd C.; Nusinow, Dmitri A.

doi:10.1002/pld3.18

Cited by 22 publications

(11 citation statements)

References 101 publications

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“…The ELF3 coding region cloned into the pENTR/D-TOPO vector, originally published in Huang et al (2017) , was obtained from Dmitri Nusinow. Cloning of ELF3 into pANIC10a was done as described in Ream et al (2014) .…”

Section: Methodsmentioning

confidence: 99%

“…In wheat, the thermosensitive earliness per se locus Eps-A m 1 ( Bullrich et al, 2002 ) was shown to be linked to mutations in ELF3 ( Alvarez et al, 2016 ). The conserved role of ELF3 across the monocot/eudicot divide is indicated by the ability of the B. distachyon ELF3 gene to rescue the hypocotyl elongation, clock arrhythmicity, and flowering phenotypes of the Arabidopsis elf3 mutant ( Huang et al, 2017 ). Here, we describe a new mutant allele of elf3 that was identified in a mutagenized population grown under short days (SD), highlighting that the role of ELF3 in circadian clock function and mediating the photoperiodic induction of flowering genes is conserved.…”

Section: Introductionmentioning

confidence: 99%

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EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon

et al. 2022

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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.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon

et al. 2022

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“…Moreover, loss of function of ELF3 in B. distachyon also results in rapid flowering under SD and LD, and expression of the B. distachyon ELF3 protein is able to rescue the A. thaliana elf3 mutant, demonstrating a conserved role of ELF3 in flowering across angiosperm diversification [29][30][31].…”

Section: Introductionmentioning

confidence: 99%

PHYTOCHROME C regulation ofPHOTOPERIOD1is mediated byEARLY FLOWERING 3inBrachypodium distachyon

Woods

Sibout

et al. 2022

Preprint

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Daylength sensing in many plants is critical for coinciding 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, 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 levels and extremely delayed flowering consistent with reports 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, which is associated with a reduction of PPD1 and FT1, demonstrating 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.

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“…ELF3 functions as a scaffold to directly bind ELF4 and LUX to form the EC [ 12 , 13 ]. ELF3 has essential functions in crops [ 14 – 19 ]. Loss-of-function of elf3 results in arrhythmic circadian output in Arabidopsis and barley [ 8 , 44 , 45 ].…”

Section: Discussionmentioning

confidence: 99%

“…ELF3 has essential functions in crops. Its monocot homologs BdELF3 and SvELF3 can functionally complement loss of ELF3 in the dicot Arabidopsis [ 14 ]. Both Earliness per se-D1 ( Eps-D1 ) in bread wheat ( Triticum aestivum ) and Eps-A m 1 in T. monococcum [ 15 ] were proposed to be ELF3 genes.…”

Section: Introductionmentioning

confidence: 99%

Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars

Yue

Sapey

et al. 2021

BMC Genomics

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Background In soybean, some circadian clock genes have been identified as loci for maturity traits. However, the effects of these genes on soybean circadian rhythmicity and their impacts on maturity are unclear. Results We used two geographically, phenotypically and genetically distinct cultivars, conventional juvenile Zhonghuang 24 (with functional J/GmELF3a, a homolog of the circadian clock indispensable component EARLY FLOWERING 3) and long juvenile Huaxia 3 (with dysfunctional j/Gmelf3a) to dissect the soybean circadian clock with time-series transcriptomal RNA-Seq analysis of unifoliate leaves on a day scale. The results showed that several known circadian clock components, including RVE1, GI, LUX and TOC1, phase differently in soybean than in Arabidopsis, demonstrating that the soybean circadian clock is obviously different from the canonical model in Arabidopsis. In contrast to the observation that ELF3 dysfunction results in clock arrhythmia in Arabidopsis, the circadian clock is conserved in soybean regardless of the functional status of J/GmELF3a. Soybean exhibits a circadian rhythmicity in both gene expression and alternative splicing. Genes can be grouped into six clusters, C1-C6, with different expression profiles. Many more genes are grouped into the night clusters (C4-C6) than in the day cluster (C2), showing that night is essential for gene expression and regulation. Moreover, soybean chromosomes are activated with a circadian rhythmicity, indicating that high-order chromosome structure might impact circadian rhythmicity. Interestingly, night time points were clustered in one group, while day time points were separated into two groups, morning and afternoon, demonstrating that morning and afternoon are representative of different environments for soybean growth and development. However, no genes were consistently differentially expressed over different time-points, indicating that it is necessary to perform a circadian rhythmicity analysis to more thoroughly dissect the function of a gene. Moreover, the analysis of the circadian rhythmicity of the GmFT family showed that GmELF3a might phase- and amplitude-modulate the GmFT family to regulate the juvenility and maturity traits of soybean. Conclusions These results and the resultant RNA-seq data should be helpful in understanding the soybean circadian clock and elucidating the connection between the circadian clock and soybean maturity.

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Cross‐species complementation reveals conserved functions for EARLY FLOWERING 3 between monocots and dicots

Cited by 22 publications

References 101 publications

EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon

EARLY FLOWERING 3 and Photoperiod Sensing in Brachypodium distachyon

PHYTOCHROME C regulation ofPHOTOPERIOD1is mediated byEARLY FLOWERING 3inBrachypodium distachyon

Transcriptomal dissection of soybean circadian rhythmicity in two geographically, phenotypically and genetically distinct cultivars

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