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. 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. 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.
Abstract Increase in ambient temperatures caused by climate change affects various morphological and developmental traits of plants, threatening crop yield stability. In the model plant Arabidopsis thaliana, EARLY FLOWERING 3 ( ELF3 ) plays prominent roles in temperature sensing and thermomorphogenesis signal transduction. However, how crop species respond to elevated temperatures is poorly understood. Here, we show that the barley ortholog of AtELF3 interacts with high temperature to control growth and development. We used heterogeneous inbred family (HIF) pairs generated from a segregating mapping population and systematically studied the role of exotic ELF3 variants in barley temperature responses. An exotic ELF3 allele from Syrian origin promoted elongation growth in barley at elevated temperatures, whereas plant area and estimated biomass were drastically reduced, resulting in an open canopy architecture. The same allele accelerated inflorescence development at high temperature, which correlated with early transcriptional induction of MADS-box floral identity genes BM3 and BM8 . Consequently, barley plants carrying the exotic ELF3 allele displayed stable total grain number and mitigated yield loss at elevated temperatures. Our findings therefore demonstrate that exotic ELF3 variants can contribute to phenotypic and developmental acclimation to elevated temperatures, providing a stimulus for breeding of climate resilient crops. Highlight We demonstrate that an exotic allele of EARLY FLOWERING 3 ( ELF3 ) contributes to plant architectural and developmental acclimation, and thereby improves yield stability at high ambient temperatures.
This record contains additional information and a supplementary dataset of sequence alignment files and phylograms that support the publication: Trenner J, Monaghan J, Saeed B, Quint M, Shabek N, Trujillo M. 2022. Evolution and Functions of Plant U-box proteins (PUBs): From protein quality control to signalling. (submitted to Annual Review of Plant Biology) Included files: Additional information.pdf This file contains Supplementary Methods and References. Supp_Fig1_Ubox_full_protein_maximum_likelihood_phylogram_linear.pdf A multiple protein sequence alignment by MAFFT of 1121 U-box protein sequences from 21 species and four outgroup sequences containing a RING finger domain (A. thaliana RBX1, A. thaliana RMA1, S. cerevisiae RAD18, Homo sapiens TRAF6 ) was used to infer a phylogenetic tree by maximum likelihood with IQ-TREE. The implemented ultrafast bootstrap approximation, set to 2000 bootstrap samples, was used for branch support. The consensus tree was annotated using iTOL. Supp_Fig2_Ubox_domain_maximum_likelihood_phylogram_linear.pdf In order to analyse specifically the evolution of the U-box domain, the U-box domain of the final 1121 U-box protein sequences as well as the RING finger domain of the four outgroup sequences were isolated and aligned by MAFFT. The U-box domain alignment was then used to infer a phylogenetic tree by maximum likelihood with IQ-TREE. The implemented ultrafast bootstrap approximation, set to 2000 bootstrap samples, was used for branch support. The consensus tree was annotated using iTOL. This tree was used to interpret the evolutionary history of U-box proteins in the main text. MAFFT_alignment _1121seqs_Ubox_full_protein_plus_4seqs_RING_outgroup.fasta Multiple protein sequences alignment by MAFFT of 1121 U-box full length protein sequences and four RING finger protein sequences, FASTA formatted. MAFFT_alignment _1121seqs_Ubox_domain_plus_4seqs_RING_outgroup.fasta Multiple protein sequences alignment by MAFFT of U-box domain sequences of 1121 U-box protein and four RING finger domain sequences of outgroup sequences, FASTA formatted. Ubox_protein_sequences_information.xlsx Spreadsheet with sequence ID information and source databases.
Plants have a remarkable capacity to adjust their growth and development to elevated ambient temperatures. Increased elongation growth of roots, hypocotyls, and petioles in warm temperatures are hallmarks of seedling thermomorphogenesis. In the last decade, significant progress has been made to identify the molecular signaling components regulating these growth responses. Increased ambient temperature utilizes diverse components of the light sensing and signal transduction network to trigger growth adjustments. However, it remains unknown whether temperature sensing and responses are universal processes that occur uniformly in all plant organs. Alternatively, temperature sensing may be confined to specific tissues or organs, which would require a systemic signal that mediates responses in distal parts of the plant. Here, we show that Arabidopsis (Arabidopsis thaliana) seedlings show organ-specific transcriptome responses to elevated temperatures and that thermomorphogenesis involves both autonomous and organ-interdependent temperature sensing and signaling. Seedling roots can sense and respond to temperature in a shoot-independent manner, whereas shoot temperature responses require both local and systemic processes. The induction of cell elongation in hypocotyls requires temperature sensing in cotyledons, followed by the generation of a mobile auxin signal. Subsequently, auxin travels to the hypocotyl, where it triggers local brassinosteroid-induced cell elongation in seedling stems, which depends upon a distinct, permissive temperature sensor in the hypocotyl.
ABSTRACT 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. 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. 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 cues 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.
This record contains additional information and a supplementary dataset of sequence alignment files and phylograms that support the publication: Saeed B, Trenner J, Monaghan J, Quint M, Shabek N, Trujillo M. 2021. Evolution and Functions of Plant U-box proteins (PUBs): From protein quality control to signalling. (submitted to Annual Review of Plant Biology) included files: Additional information.pdf This file contains Supplementary Methods and References for the phylogenetic analyses. Ubox_full_protein_maximum_likelihood_phylogram_linear.pdf A multiple protein sequence alignment by MAFFT (22) of 1121 U-box protein sequences from 21 species and four outgroup sequences containing a RING finger domain (A. thaliana RBX1, A. thaliana RMA1, S. cerevisiae RAD18, Homo sapiens TRAF6 ) was used to infer a phylogenetic tree by maximum likelihood with IQ-TREE (31, 32). The implemented ultrafast bootstrap approximation, set to 2000 bootstrap samples, was used for branch support (17). The consensus tree was annotated using iTOL (25). Ubox_domain_maximum_likelihood_phylogram_linear.pdf In order to analyse specifically the evolution of the U-box domain, the U-box domain of the final 1121 U-box protein sequences as well as the RING finger domain of the four outgroup sequences were isolated and aligned by MAFFT (22). The U-box domain alignment was then used to infer a phylogenetic tree by maximum likelihood with IQ-TREE (31, 32). The implemented ultrafast bootstrap approximation, set to 2000 bootstrap samples, was used for branch support (17). The consensus tree was annotated using iTOL (25). This tree was used to interpret the evolutionary history of U-box proteins in the main text. MAFFT_alignment _1121seqs_Ubox_full_protein_plus_4seqs_RING_outgroup.fasta Multiple protein sequences alignment by MAFFT (22) of 1121 U-box full length protein sequences and four RING finger protein sequences, FASTA formatted. MAFFT_alignment _1121seqs_Ubox_domain_plus_4seqs_RING_outgroup.fasta Multiple protein sequences alignment by MAFFT (22) of U-box domain sequences of 1121 U-box protein and four RING finger domain sequences of outgroup sequences, FASTA formatted. Ubox_protein_sequences_information.xlsx Spreadsheet with sequence ID information and source databases.
Supplementary Dataset 1. Phenotypic data used for QTL mapping. This dataset has been uploaded to figshare and can be accessed via http://dx.doi.org/ 10.6084/m9.figshare.1339892 .
Abstract Plants have evolved to anticipate and adjust their growth and development in response to environmental changes. To mitigate the negative influence of global climate change on crop production, understanding the key regulators of plant performance is imperative. EARLY FLOWERING 3 ( ELF3 ) is such a regulator involved in the circadian clock and thermomorphogenesis. Arabidopsis thaliana ELF3 contains a prion-like domain (PrLD) that functions as a thermosensor, enabling its liquid-liquid phase separation at high ambient temperatures. To understand the conservation of this function across the plant kingdom, we traced the evolutionary emergence of ELF3 with a focus on PrLD existence. We observed that the presence of the domain within ELF3, mainly contributed by the length of polyglutamine (polyQ) repeats, is most prominent Brassicales . By analyzing 319 natural Arabidopsis thaliana accessions, we detected a wide range of polyQ length variation in ELF3. However, it is only weakly associated with geographic origin, climate conditions and classic temperature-responsive phenotypes. Based on available prediction tools and limited experimental evidence, we conclude that although the emergence of PrLD is not likely to be a key driver of environmental adaptation, it adds an extra layer to ELF3’s role in thermomorphogenesis.
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