Integration of low temperature and light signaling during cold acclimation response in Arabidopsis.
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ABSTRACT:
SUBMITTER: Catala R
PROVIDER: S-EPMC3182711 | biostudies-literature | 2011 Sep
REPOSITORIES: biostudies-literature
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Project description:Plant survival in temperate zones requires efficient cold acclimation, which is strongly affected by light and temperature signal crosstalk, which converge in modulation of hormonal responses. Cold under low light conditions affected Arabidopsis responses predominantly in apices, possibly because energy supplies were too limited for requirements of these meristematic tissues, despite a relatively high steady-state quantum yield. Comparing cold responses at optimal light intensity and low light, we found activation of similar defence mechanisms-apart from CBF1-3 and CRF3-4 pathways, also transient stimulation of cytokinin type-A response regulators, accompanied by fast transient increase of trans-zeatin in roots. Upregulated expression of components of strigolactone (and karrikin) signalling pathway indicated involvement of these phytohormones in cold responses. Impaired response of phyA, phyB, cry1 and cry2 mutants reflected participation of these photoreceptors in acquiring freezing tolerance (especially cryptochrome CRY1 at optimal light intensity and phytochrome PHYA at low light). Efficient cold acclimation at optimal light was associated with upregulation of trans-zeatin in leaves and roots, while at low light, cytokinin (except cis-zeatin) content remained diminished. Cold stresses induced elevation of jasmonic acid and salicylic acid (in roots). Low light at optimal conditions resulted in strong suppression of cytokinins, jasmonic and salicylic acid.
| S-EPMC7962961 | biostudies-literature
Project description:Photosynthetic organisms are able to sense energy imbalances brought about by the overexcitation of photosystem II (PSII) through the redox state of the photosynthetic electron transport chain, estimated as the chlorophyll fluorescence parameter 1-qL, also known as PSII excitation pressure. Plants employ a wide array of photoprotective processes that modulate photosynthesis to correct these energy imbalances. Low temperature and light are well established in their ability to modulate PSII excitation pressure. The acquisition of freezing tolerance requires growth and development a low temperature (cold acclimation) which predisposes the plant to photoinhibition. Thus, photosynthetic acclimation is essential for proper energy balancing during the cold acclimation process. Eutrema salsugineum (Thellungiella salsuginea) is an extremophile, a close relative of Arabidopsis thaliana, but possessing much higher constitutive levels of tolerance to abiotic stress. This comparative study aimed to characterize the photosynthetic properties of Arabidopsis (Columbia accession) and two accessions of Eutrema (Yukon and Shandong) isolated from contrasting geographical locations at cold acclimating and non-acclimating conditions. In addition, three different growth regimes were utilized that varied in temperature, photoperiod and irradiance which resulted in different levels of PSII excitation pressure. This study has shown that these accessions interact differentially to instantaneous (measuring) and long-term (acclimation) changes in PSII excitation pressure with regard to their photosynthetic behaviour. Eutrema accessions contained a higher amount of photosynthetic pigments, showed higher oxidation of P700 and possessed more resilient photoprotective mechanisms than that of Arabidopsis, perhaps through the prevention of PSI acceptor-limitation. Upon comparison of the two Eutrema accessions, Shandong demonstrated the greatest PSII operating efficiency (ΦPSII) and P700 oxidizing capacity, while Yukon showed greater growth plasticity to irradiance. Both of these Eutrema accessions are able to photosynthetically acclimate but do so by different mechanisms. The Shandong accessions demonstrate a stable response, favouring energy partitioning to photochemistry while the Yukon accession shows a more rapid response with partitioning to other (non-photochemical) strategies.
| S-EPMC5620588 | biostudies-literature
Project description:BACKGROUND:Cold stress causes dynamic changes in gene expression that are partially caused by small non-coding RNAs since they regulate protein coding transcripts and act in epigenetic gene silencing pathways. Thus, a detailed analysis of transcriptional changes of small RNAs (sRNAs) belonging to all known sRNA classes such as microRNAs (miRNA) and small interfering RNA (siRNAs) in response to cold contributes to an understanding of cold-related transcriptome changes. RESULT:We subjected A. thaliana plants to cold acclimation conditions (4?°C) and analyzed the sRNA transcriptomes after 3?h, 6?h and 2 d. We found 93 cold responsive differentially expressed miRNAs and only 14 of these were previously shown to be cold responsive. We performed miRNA target prediction for all differentially expressed miRNAs and a GO analysis revealed the overrepresentation of miRNA-targeted transcripts that code for proteins acting in transcriptional regulation. We also identified a large number of differentially expressed cis- and trans-nat-siRNAs, as well as sRNAs that are derived from long non-coding RNAs. By combining the results of sRNA and mRNA profiling with miRNA target predictions and publicly available information on transcription factors, we reconstructed a cold-specific, miRNA and transcription factor dependent gene regulatory network. We verified the validity of links in the network by testing its ability to predict target gene expression under cold acclimation. CONCLUSION:In A. thaliana, miRNAs and sRNAs derived from cis- and trans-NAT gene pairs and sRNAs derived from lncRNAs play an important role in regulating gene expression in cold acclimation conditions. This study provides a fundamental database to deepen our knowledge and understanding of regulatory networks in cold acclimation.
| S-EPMC7325139 | biostudies-literature
Project description:Arabidopsis REIL proteins are cytosolic ribosomal 60S-biogenesis factors. After shift to 10 °C, reil mutants deplete and slowly replenish non-translating eukaryotic ribosome complexes of root tissue, while controlling the balance of non-translating 40S- and 60S-subunits. Reil mutations respond by hyper-accumulation of non-translating subunits at steady-state temperature; after cold-shift, a KCl-sensitive 80S sub-fraction remains depleted. We infer that Arabidopsis may buffer fluctuating translation by pre-existing non-translating ribosomes before de novo synthesis meets temperature-induced demands. Reil1 reil2 double mutants accumulate 43S-preinitiation and pre-60S-maturation complexes and alter paralog composition of ribosomal proteins in non-translating complexes. With few exceptions, e.g. RPL3B and RPL24C, these changes are not under transcriptional control. Our study suggests requirement of de novo synthesis of eukaryotic ribosomes for long-term cold acclimation, feedback control of NUC2 and eIF3C2 transcription and links new proteins, AT1G03250, AT5G60530, to plant ribosome biogenesis. We propose that Arabidopsis requires biosynthesis of specialized ribosomes for cold acclimation.
| S-EPMC7844247 | biostudies-literature
Project description:Plant metabolism is broadly reprogrammed during acclimation to abiotic changes. Most previous studies have focused on transitions from standard to single stressful conditions. Here, we systematically analyze acclimation processes to levels of light, heat, and cold stress that subtly alter physiological parameters and assess their reversibility during de-acclimation. Metabolome and transcriptome changes were monitored at 11 different time points. Unlike transcriptome changes, most alterations in metabolite levels did not readily return to baseline values, except in the case of cold acclimation. Similar regulatory networks operate during (de-)acclimation to high light and cold, whereas heat and high-light responses exhibit similar dynamics, as determined by surprisal and conditional network analyses. In all acclimation models tested here, super-hubs in conditional transcriptome networks are enriched for components involved in translation, particularly ribosomes. Hence, we suggest that the ribosome serves as a common central hub for the control of three different (de-)acclimation responses.
| S-EPMC7364123 | biostudies-literature
Project description:Animals have evolved sophisticated temperature-sensing systems and mechanisms to detect and respond to ambient temperature changes. As a relict species endemic to the Qinghai-Tibet Plateau, hot-spring snake (Thermophis baileyi) survived the dramatic changes in climate that occurred during plateau uplift and ice ages, providing an excellent opportunity to explore the evolution of temperature sensation in ectotherms. Based on distributional information and behavioral experiments, we found that T. baileyi prefer hot-spring habitats and respond more quickly to warmth than other two snakes, suggesting that T. baileyi may evolve an efficient thermal-sensing system. Using high-quality chromosome-level assembly and comparative genomic analysis, we identified cold acclimation genes experiencing convergent acceleration in high-altitude lineages. We also discovered significant evolutionary changes in thermosensation- and thermoregulation-related genes, including the transient receptor potential (TRP) channels. Among these genes, TRPA1 exhibited three species-specific amino acid replacements, which differed from those found in infrared imaging snakes, implying different temperature-sensing molecular strategies. Based on laser-heating experiments, the T. baileyi-specific mutations in TRPA1 resulted in an increase in heat-induced opening probability and thermal sensitivity of the ion channels under the same degree of temperature stimulation, which may help the organism respond to temperature changes more quickly. These results provide insight into the genetic mechanisms underpinning the evolution of temperature-sensing strategies in ectotherms as well as genetic evidence of temperature acclimation in this group.
| S-EPMC9405097 | biostudies-literature
Project description:Many temperate plant species such as Arabidopsis thaliana are able to increase their freezing tolerance when exposed to low, nonfreezing temperatures in a process called cold acclimation. This process is accompanied by complex changes in gene expression. Previous studies have investigated these changes but have mainly focused on individual or small groups of genes. We present a comprehensive statistical analysis of the genome-wide changes of gene expression in response to 14 d of cold acclimation in Arabidopsis, and provide a large-scale validation of these data by comparing datasets obtained for the Affymetrix ATH1 Genechip and MWG 50-mer oligonucleotide whole-genome microarrays. We combine these datasets with existing published and publicly available data investigating Arabidopsis gene expression in response to low temperature. All data are integrated into a database detailing the cold responsiveness of 22,043 genes as a function of time of exposure at low temperature. We concentrate our functional analysis on global changes marking relevant pathways or functional groups of genes. These analyses provide a statistical basis for many previously reported changes, identify so far unreported changes, and show which processes predominate during different times of cold acclimation. This approach offers the fullest characterization of global changes in gene expression in response to low temperature available to date.
| S-EPMC1189076 | biostudies-literature
Project description:Overwintering plants are capable of exhibiting high levels of cold tolerance, which is acquired through the process of cold acclimation (CA). In contrast to CA, the acquired freezing tolerance is rapidly reduced during cold de-acclimation (DA) and plants resume growth after sensing warm temperatures. In order to better understand plant growth and development, and to aid in the breeding of cold-tolerant plants, it is important to decipher the functional mechanisms of the DA process. In this study, we performed comparative transcriptomic and proteomic analyses during CA and DA. As revealed by shotgun proteomics, we identified 3987 peptides originating from 1569 unique proteins and the corresponding mRNAs were analyzed. Among the 1569 genes, 658 genes were specifically induced at the transcriptional level during the process of cold acclimation. In order to investigate the relationship between mRNA and the corresponding protein expression pattern, a Pearson correlation was analyzed. Interestingly, 199 genes showed a positive correlation of mRNA and protein expression pattern, indicating that both their transcription and translation occurred during CA. However, 226 genes showed a negative correlation of mRNA and protein expression pattern, indicating that their mRNAs were transcribed during CA and were stored for the subsequent DA step. Under this scenario, those proteins were specifically increased during DA without additional transcription of mRNA. In order to confirm the negative correlation of mRNA and protein expression patterns, qRT-PCR and western blot analyses were performed. Mitochondrial malate dehydrogenase 1 (mMDH1) exhibited a negative correlation of mRNA and protein levels, which was characterized by CA-specific mRNA induction and protein accumulation specifically during DA. These data indicate that the expression of specific mRNAs and subsequent accumulation of corresponding proteins are not always in accordance under low temperature stress conditions in plants.
| S-EPMC4256508 | biostudies-literature
Project description:We conducted microarray analysis to study comprehensive changes of gene expression profile under long-term low-temperature (LT) treatment and to identify other LT-responsive genes related with cold acclimation in seedling leaves and crown tissues (shoots containing apical meristems) of a synthetic hexaploid wheat line. The microarray analysis revealed marked up-regulation of a number of Cor/Lea genes and fructan biosynthesis-related genes under the long-term LT treatment. For validation of the microarray data, we selected four synthetic wheat lines, which contained the A and B genomes from a tetraploid wheat cultivar Langdon and the diverse D genomes originating from the different Ae. tauschii accessions, with distinct levels of freezing tolerance after cold acclimation. Quantitative RT-PCR analyses showed that the transcription accumulated levels of the Cor/Lea, CBF, and fructan biosynthesis-related genes were higher in more freezing-tolerant lines than those in the sensitive lines. The fructan biosynthesis pathway would be associated with cold acclimation to develop wheat freezing tolerance and related with diversity of the freezing tolerance level in addition to the CBF-mediated Cor/Lea expression pathway.
2014-10-10 | GSE61621 | GEO
Project description:Because stress experiences are often recurrent plants have developed strategies to remember a first so-called priming stress to eventually respond more effectively to a second triggering stress. Here, we have studied the impact of discontinuous or sustained cold stress (4 °C) on in vitro grown Arabidopsis thaliana seedlings of different age and their ability to get primed and respond differently to a later triggering stress. Cold treatment of 7-d-old seedlings induced the expression of cold response genes but did not cause a significantly enhanced freezing resistance. The competence to increase the freezing resistance in response to cold was associated with the formation of true leaves. Discontinuous exposure to cold only during the night led to a stepwise modest increase in freezing tolerance provided that the intermittent phase at ambient temperature was less than 32 h. Seedlings exposed to sustained cold treatment developed a higher freezing tolerance which was further increased in response to a triggering stress during three days after the priming treatment had ended indicating cold memory. Interestingly, in all scenarios the primed state was lost as soon as the freezing tolerance had reached the level of naïve plants indicating that an effective memory was associated with an altered physiological state. Known mutants of the cold stress response (cbfs, erf105) and heat stress memory (fgt1) did not show an altered behaviour indicating that their roles do not extend to memory of cold stress in Arabidopsis seedlings.
| S-EPMC6971231 | biostudies-literature