Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes.
BACKGROUND
Perception and transduction of temperature changes result in altered growth enabling plants to adapt to increased ambient temperature. While PHYTOCHROME-INTERACTING FACTOR4 (PIF4) has been identified as a major ambient temperature signaling hub, its upstream regulation seems complex and is poorly understood. Here, we exploited natural variation for thermo-responsive growth in Arabidopsis thaliana using quantitative trait locus (QTL) analysis.


RESULTS
We identified GIRAFFE2.1, a major QTL explaining ~18 % of the phenotypic variation for temperature-induced hypocotyl elongation in the Bay-0 x Sha recombinant inbred line population. Transgenic complementation demonstrated that allelic variation in the circadian clock regulator EARLY FLOWERING3 (ELF3) is underlying this QTL. The source of variation could be allocated to a single nucleotide polymorphism in the ELF3 coding region, resulting in differential expression of PIF4 and its target genes, likely causing the observed natural variation in thermo-responsive growth.


CONCLUSIONS
In combination with other recent studies, this work establishes the role of ELF3 in the ambient temperature signaling network. Natural variation of ELF3-mediated gating of PIF4 expression during nightly growing periods seems to be affected by a coding sequence quantitative trait nucleotide that confers a selective advantage in certain environments. In addition, natural ELF3 alleles seem to differentially integrate temperature and photoperiod information to induce architectural changes. Thus, ELF3 emerges as an essential coordinator of growth and development in response to diverse environmental cues and implicates ELF3 as an important target of adaptation.
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. anja.raschke@landw.uni-halle.de.
Anja
A
Raschke
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. cibanez@ipb-halle.de.
Carla
C
Ibañez
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. Kristian.Ullrich@biologie.uni-marburg.de.
Kristian Karsten
KK
Ullrich
Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, 50829, Cologne, Germany. anwer@mpipz.mpg.de.
Muhammad Usman
MU
Anwer
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. sebastian.becker@student.uni-halle.de.
Sebastian
S
Becker
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. annemarie.gloeckner@uni-hamburg.de.
Annemarie
A
Glöckner
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. Jana.Trenner@ipb-halle.de.
Jana
J
Trenner
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. kdenk@ipb-halle.de.
Kathrin
K
Denk
PlantaServ GmbH, Erdinger Straße 82a, 85356, Freising, Germany. saal@baypmuc.de.
Bernhard
B
Saal
Department of Plant Biology, University of Minnesota Twin Cities, Saint Paul, MN, USA. xdsun@plantsciences.ucdavis.edu.
Xiaodong
X
Sun
Department of Plant Biology, University of Minnesota Twin Cities, Saint Paul, MN, USA. nixxx008@umn.edu.
Min
M
Ni
Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, 50829, Cologne, Germany. seth.davis@york.ac.uk.|Department of Biology, University of York, York, YO10 5DD, UK. seth.davis@york.ac.uk.
Seth Jon
SJ
Davis
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. cdelker@ipb-halle.de.
Carolin
C
Delker
Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry, Weinberg 3, 06120, Halle, Saale, Germany. mquint@ipb-halle.de.|Martin Luther University Halle-Wittenberg, Institute of Agricultural and Nutritional Sciences, Betty--Heimann-Str. 5, Halle (Saale), 06120, Germany. mquint@ipb-halle.de.
Marcel
M
Quint
D000222:Adaptation, Physiological; D017360:Arabidopsis / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D051792:Basic Helix-Loop-Helix Proteins / Q000235:genetics* / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D017440:Photoperiod; D040641:Quantitative Trait Loci; D015398:Signal Transduction; D014157:Transcription Factors / Q000235:genetics* / Q000378:metabolism
D029681:Arabidopsis Proteins; D051792:Basic Helix-Loop-Helix Proteins; D014157:Transcription Factors; C432430:At2g25930 protein, Arabidopsis; C459466:PIF4 protein, Arabidopsis