Natural Variants of<i>ELF3</i>Affect Thermomorphogenesis by Transcriptionally Modulating<i>PIF4</i>-Dependent Auxin Response Genes

Raschke, Anja; Ibáñez, Carla; Ullrich, Kristian K.; Anwer, Muhammad; Becker, S.; Glöckner, Annemarie; Trenner, Jana; Denk, Kathrin; Saal, Bernhard; Sun, Xiaodong; Ni, Min; Davis, Seth J; Delker, Carolin; Quint, Marcel

doi:10.1101/015305

Cited by 20 publications

(32 citation statements)

References 39 publications

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“…The EC is a transcriptional repressor made up of the proteins EARLY FLOWERING3 (ELF3), ELF4 and LUX ARRHYTHMO (LUX) (7)(8)(9). To test if the EC is also required for hypocotyl elongation responses below 22ºC, we examined the behavior of elf3-1 and lux-4 at 12 and 17ºC.…”

Section: ) Growth At 27ºc Reduces the Activity Of The Evening Complmentioning

confidence: 99%

Phytochromes function as thermosensors inArabidopsis

Jung

Domijan

Klose

et al. 2016

Science

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Plants are responsive to temperature, and can distinguish differences of 1ºC. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). The mechanisms of temperature perception are however largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm temperature response, and consistent with this, we show in this background that the warm temperature transcriptome 2 becomes de-repressed at low temperatures. We have discovered phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature dependent manner.The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers, integrating temperature information over the course of the night. One Sentence Summary:The plant temperature transcriptome is controlled at night by phytochromes, acting as thermoresponsive transcriptional repressors. Main Text:Plant development is responsive to temperature, and the phenology and distribution of crops and wild plants have already altered in response to climate change (1, 2). In Arabidopsis thaliana, warm temperature-mediated elongation growth and flowering is dependent on the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR4 and 5 (PIF4 and 5) (3-6). Growth at 27ºC reduces the activity of the Evening Complex (EC) resulting in greater PIF4 transcription. The EC is a transcriptional repressor made up of the proteins EARLY FLOWERING3 (ELF3), ELF4 and LUX ARRHYTHMO (LUX) (7-9). To test if the EC is also required for hypocotyl elongation responses below 22ºC, we examined the behavior of elf3-1 and lux-4 at 12 and 17ºC. Hypocotyl elongation in elf3-1 and lux-4 is largely suppressed at lower temperatures (Fig. 1A, B), which is consistent with cold temperatures being able to suppress PIF4 overexpression phenotypes (10). Since PHYTOCHROME B (PHYB) was identified as a QTL for thermal responsiveness and PIF4 activity is regulated by phytochromes (8, 11), we investigated whether these red light receptors control hypocotyl elongation in the range 12 to 22ºC. Plants lacking phytochrome activity (12) show constitutively long hypocotyls at 12ºC and 17ºC. Thus phytochromes are essential for responding to temperature (Fig. 1C, D and Fig. S1).We used transcriptome analysis to determine whether disrupted thermomorphogenesis in phyABCDE is specific for temperature signaling or is a consequence of misregulated growth pathways. To capture diurnal variation in thermoresponsiveness, we sampled seedlings over 24 hours at 22 and 27ºC. Clustering analysis reveals 20 groups of transcripts ( Fig. 2A and Fig. S3; described in supplement). Thermomorphogenesis occurs predominantly at night and is driven by PIF4. Consistent with this, we observe PIF4 is present in cluster 20, which is more highly expressed at 27ºC during darkness. Clusters 15 and 16 represent the other major groups of 3 nighttim...

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Section: ) Growth At 27ºc Reduces the Activity Of The Evening Complmentioning

confidence: 99%

Phytochromes function as thermosensors inArabidopsis

Jung

Domijan

Klose

et al. 2016

Science

759

752

View full text Add to dashboard Cite

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“…PIF4 is inhibited by phyB and cry1 (Ma et al, 2016;Qiu et al, 2019), while PIF4 function depends on HEMERA that regulates both PIF4 abundance and its transactivating potential (Qiu et al, 2019). A key role of PIF4 is to induce expression of auxin biosynthetic and signalling genes ultimately leading to hypocotyl elongation (Franklin et al, 2011;Sun et al, 2012;Raschke et al, 2015). Hypocotyl elongation in response to shade and temperature elevation also depends on other phytohormones including gibberellic acid (GA) and brassinosteroids (BR) (Quint et al, 2016;Legris et al, 2017;Casal & Balasubramanian, 2019).…”

Section: Introductionmentioning

confidence: 99%

PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings

et al. 2019

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Summary In response to elevated ambient temperature Arabidopsis thaliana seedlings display a thermomorphogenic response that includes elongation of hypocotyls and petioles. Phytochrome B and cryptochrome 1 are two photoreceptors also playing a role in thermomorphogenesis. Downstream of both environmental sensors PHYTOCHROME INTERACTING FACTOR 4 (PIF4) is essential to trigger this response at least in part through the production of the growth promoting hormone auxin. Using a genetic approach, we identified PHYTOCHROME INTERACTING FACTOR 7 (PIF7) as a novel player for thermomorphogenesis and compared the phenotypes of pif7 and pif4 mutants. We investigated the role of PIF7 during temperature‐regulated gene expression and the regulation of PIF7 transcript and protein by temperature. Furthermore, pif7 and pif4 loss‐of‐function mutants were similarly unresponsive to increased temperature. This included hypocotyl elongation and induction of genes encoding auxin biosynthetic or signalling proteins. PIF7 bound to the promoters of auxin biosynthesis and signalling genes. In response to temperature elevation PIF7 transcripts decreased while PIF7 protein levels increased rapidly. Our results reveal the importance of PIF7 for thermomorphogenesis and indicate that PIF7 and PIF4 likely depend on each other possibly by forming heterodimers. Elevated temperature rapidly enhances PIF7 protein accumulation, which may contribute to the thermomorphogenic response.

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“…The transcriptional factor ELF3 controlling thermo-responsive hypocotyl elongation was identified from a study on 19 MAGIC parental lines (Box et al, 2015). It was also identified as a major quantitative trait locus (QTL) for temperature-induced hypocotyl elongation in the Bay-0 9 Sha recombinant inbred line population (Raschke et al, 2015). However, thermo-responsiveness variations in a larger natural population have not been examined, and therefore the molecular nature of common variants is unknown.…”

Section: Introductionmentioning

confidence: 99%

Natural variations of growth thermo‐responsiveness determined by SAUR26/27/28 proteins in Arabidopsis thaliana

et al. 2019

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Summary How diversity in growth thermo‐responsiveness is generated for local adaptation is a long‐standing biological question. We investigated molecular genetic basis of natural variations in thermo‐responsiveness of plant architecture in Arabidopsis thaliana. We measured the extent of rosette architecture at 22°C and 28°C in a set of 69 natural accessions and determined their thermo‐responsiveness of plant architecture. A genome‐wide association study was performed to identify major loci for variations in thermo‐responsiveness. The SAUR26 subfamily, a new subfamily of SAUR genes, was identified as a major locus for the thermo‐responsive architecture variations. The expression of SAUR26/27/28 is modulated by temperature and PIF4. Extensive natural polymorphisms in these genes affect their RNA expression levels and protein activities and influence the thermo‐responsiveness of plant architecture. In addition, the SAUR26 subfamily genes exhibit a high variation frequency and their variations are associated with the local temperature climate. This study reveals that the SAUR26 subfamily is a key variation for thermo‐responsive architecture and suggests a preference for generating diversity for local adaptation through signaling connectors.

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Natural Variants ofELF3Affect Thermomorphogenesis by Transcriptionally ModulatingPIF4-Dependent Auxin Response Genes

Cited by 20 publications

References 39 publications

Phytochromes function as thermosensors inArabidopsis

Phytochromes function as thermosensors inArabidopsis

PHYTOCHROME INTERACTING FACTOR 7 is important for early responses to elevated temperature in Arabidopsis seedlings

Natural variations of growth thermo‐responsiveness determined by SAUR26/27/28 proteins in Arabidopsis thaliana

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