Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes

BMC Plant Biology, Aug 2015

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.

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Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes

Raschke et al. BMC Plant Biology Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes Anja Raschke 0 Carla Ibañez 0 Kristian Karsten Ullrich 0 Muhammad Usman Anwer 3 Sebastian Becker 0 Annemarie Glöckner 0 Jana Trenner 0 Kathrin Denk 0 Bernhard Saal 2 Xiaodong Sun 6 Min Ni 6 Seth Jon Davis 3 5 Carolin Delker 0 Marcel Quint 0 1 4 0 Department of Molecular Signal Processing, Leibniz Institute of Plant Biochemistry , Weinberg 3, 06120 Halle, Saale , Germany 1 Martin Luther University Halle‐Wittenberg, Institute of Agricultural and Nutritional Sciences , Betty-Heimann-Str. 5, Halle (Saale) 06120 , Germany 2 PlantaServ GmbH , Erdinger Straße 82a, 85356 Freising , Germany 3 Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research , 50829 Cologne , Germany 4 Martin Luther University Halle‐Wittenberg, Institute of Agricultural and Nutritional Sciences , Betty-Heimann-Str. 5, Halle (Saale) 06120 , Germany 5 Department of Biology, University of York , York YO10 5DD , UK 6 Department of Plant Biology, University of Minnesota Twin Cities , Saint Paul, MN , USA 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. Ambient temperature signaling; Auxin; ELF3; PIF4; Thermomorphogenesis - Background In analogy to photomorphogenesis, the term thermomorphogenesis describes the effect of temperature on morphogenesis [1]. Hypocotyl elongation [2] and leaf hyponasty [3] belong to the most sensitive thermomorphogenic changes in plant development. Physiologically, these coordinated responses likely enhance evaporative leaf cooling [4, 5] and thus enable plants to adapt to warmth. Within the context of globally increasing ambient temperatures, it is imperative to improve our understanding of the basic processes plants employ to react to such environmental perturbations. A major hub in the ambient temperature signaling network is the basic helix-loop-helix (bHLH) transcription factor PHYTOCHROME-INTERACTING FACTOR4 (PIF4). PIF4 protein binds to the promoters of auxin biosynthesis and response genes [6–9]. It thereby transcriptionally activates auxin responses, resulting in elongation growth. PIF4 itself seems to be transcriptionally regulated in a temperature-dependent manner by the bZIP transcription factor ELONGATED HYPOCOTYL5 (HY5) [10]. © 2015 Raschke et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Accumulating data on PIF4 regulation from light signaling, photomorphogenesis and the circadian clock [11–13] indicate a more complex regulation of PIF4 activity on several levels. The objective of this study was to exploit natural variation within the gene pool of Arabidopsis thaliana to identify additional components of the complex signaling network that (...truncated)


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Anja Raschke, Carla Ibañez, Kristian Ullrich, Muhammad Anwer, Sebastian Becker, Annemarie Glöckner, Jana Trenner, Kathrin Denk, Bernhard Saal, Xiaodong Sun, Min Ni, Seth Davis, Carolin Delker, Marcel Quint. Natural variants of ELF3 affect thermomorphogenesis by transcriptionally modulating PIF4-dependent auxin response genes, BMC Plant Biology, 2015, pp. 197, 15, DOI: 10.1186/s12870-015-0566-6