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

Abstract

BackgroundPerception 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.ResultsWe 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.ConclusionsIn 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0566-6) contains supplementary material, which is available to authorized users.

PIF4 and ELF3 Act Independently in Arabidopsis thaliana Thermoresponsive Flowering

“…Like others [14–16], we observed an inverse relationship between ELF3 functionality and transcript levels of PIF4 and AtHB2 , with larger effects on PIF4 expression. The ELF3 lines with the strongest thermal response ( e .…”

“…Following the recent discoveries that ELF3 is involved with thermal response [14–16], we confirmed that ELF3 polyQ variation also affects thermal response phenotypes in a background-dependent fashion. However, we found little support for the hypothesis that the polyQ tract has a special role in temperature sensing.…”

“…Given known regulatory interactions between ELF3 and PIF4 [17–20], it is reasonable to predict that both operate in the same pathway for thermal response phenotypes [21]. Recent reports focusing on one such phenotype, hypocotyl elongation, support this expectation [14–16]. …”

TOC1–PIF4 interaction mediates the circadian gating of thermoresponsive growth in Arabidopsis

“…Consequently, both light condition and the circadian clock influence thermomorphogenesis by modulating the level of PIF4 (refs 3, 13). Recent studies have shown that the transcription factor EARLY FLOWERING3 (ELF3), a component of the evening complex (EC) of the circadian clock, represses PIF4 RNA expression and warm temperature induces PIF4 expression by inhibiting ELF3 binding to the PIF4 promoter161718. Furthermore, elf3 -null mutant plants grown under short-day conditions develop long hypocotyls that are insensitive to warm temperature1718.…”

Natural Variation of the Circadian Clock in Neurospora

“…Latitude-specific circadian variation has also been observed in other eukaryotes like plants, birds, and mammals. In Arabidopsis , natural allelic variations are associated with several circadian phenotypes like hypocotyl growth (Coluccio, Sanchez, Kasulin, Yanovsky, & Botto, 2011; Raschke et al, 2015), flowering time (Lempe et al, 2005; Press, Lanctot, & Queitsch, 2016), periodic leaf movements (Michael et al, 2003; Swarup et al, 1999) and temperature compensation (Edwards, Lynn, Gyula, Nagy, & Millar, 2005). These same allelic variations are also associated with the phenotypes for breeding time (Hau, 2001) and diurnal and seasonal variation of hormone secretion (Dawson, King, Bentley, & Ball, 2001; Reierth, Van’t Hof, & Stokkan, 1999) in birds, and seasonal variation of melatonin circadian rhythms (Adamsson, Laike, & Morita, 2016) and latitudinal and seasonal specific qualitative and quantitative variations of sleep (Friborg, Bjorvatn, Amponsah, & Pallesen, 2012) in humans.…”