Temperate and boreal plants show natural low temperature acclimation during autumn. This cold acclimation process results in increased freezing tolerance. Global climate change is leading to ...increasing spring and autumn temperatures that can trigger deacclimation and loss of freezing tolerance, making plants susceptible to both late-autumn and late-spring freezing events. In particular, spring frosts can have devastating effects on whole ecosystems and can significantly reduce the yield of crop plants. Although the timing and speed of deacclimation are clearly of crucial importance for plant winter survival, the molecular basis of this process is still largely unknown. The regulation of deacclimation is, however, not only related to freezing tolerance, but also to the termination of dormancy, and the initiation of growth and development. In this paper, we provide an overview of what is known about deacclimation in both woody and herbaceous plants. We use publicly available transcriptome data to identify a core set of deacclimation-related genes in Arabidopsis thaliana that highlight physiological determinants of deacclimation, and suggest important directions for future research in this area.
In plants from temperate climates such as Arabidopsis thaliana low, non-freezing temperatures lead to increased freezing tolerance in a process termed cold acclimation. This process is accompanied by ...massive changes in gene expression and in the content of primary metabolites and lipids. In addition, most flavonols and anthocyanins accumulate upon cold exposure, along with most transcripts encoding transcription factors and enzymes of the flavonoid biosynthetic pathway. However, no evidence for a functional role of flavonoids in plant freezing tolerance has been shown. Here, we present a comprehensive analysis using qRT-PCR for transcript, LC-MS for flavonoid and GC-MS for primary metabolite measurements, and an electrolyte leakage assay to determine freezing tolerance of 20 mutant lines in two Arabidopsis accessions that are affected in different steps of the flavonoid biosynthetic pathway. This analysis provides evidence for a functional role of flavonoids in plant cold acclimation. The accumulation of flavonoids in the activation tagging mutant line pap1-D improved, while reduced flavonoid content in different knock-out mutants impaired leaf freezing tolerance. Analysis of the different knock-out mutants suggests redundancy of flavonoid structures, as the lack of flavonols or anthocyanins could be compensated by other compound classes.
Plants need to adapt to fluctuating temperatures throughout their lifetime. Previous research showed that Arabidopsis memorizes a first cold stress (priming) and improves its primed freezing ...tolerance further when subjected to a second similar stress after a lag phase. This study investigates primary metabolomic and transcriptomic changes during early cold priming or triggering after 3 days at 4°C interrupted by a memory phase. DREB1 family transcription factors DREB1C/CBF2, DREB1D/CBF4, DREB1E/DDF2, and DREB1F/DDF1 were strongly significantly induced throughout the entire triggering. During triggering, genes encoding Late Embryogenesis Abundant (LEA), antifreeze proteins or detoxifiers of reactive oxygen species (ROS) were higher expressed compared with priming. Examples of early triggering responders were xyloglucan endotransglucosylase/hydrolase genes encoding proteins involved in cell wall remodeling, while late responders were identified to act in fine‐tuning the stress response and developmental regulation. Induction of non‐typical members of the DREB subfamily of ERF/AP2 transcription factors, the relatively small number of induced CBF regulon genes and a slower accumulation of selected cold stress associated metabolites indicate that a cold triggering stimulus might be sensed as milder stress in plants compared with priming. Further, strong induction of CBF4 throughout triggering suggests a unique function of this gene for the response to alternating temperatures.
In plants from temperate climates such as Arabidopsis thaliana, low, non‐freezing temperatures lead to increased freezing tolerance in a process termed cold acclimation. During cold acclimation, ...massive changes in gene expression and in the content of primary metabolites and lipids have been observed. Here, we have analysed the influence of cold acclimation on flavonol and anthocyanin content and on the expression of genes related to flavonoid metabolism in 54 Arabidopsis accessions covering a wide range of freezing tolerance. Most flavonols and anthocyanins accumulated upon cold exposure, but the extent of accumulation varied strongly among the accessions. This was also true for most of the investigated transcripts. Correlation analyses revealed a high degree of coordination among metabolites and among transcripts, but only little correlation between metabolites and transcripts, indicating an important role of post‐transcriptional regulation in flavonoid metabolism. Similarly, levels of many flavonoid biosynthesis genes were correlated with freezing tolerance after cold acclimation, but only the pool sizes of a few flavonols and anthocyanins. Collectively, our data provide evidence for an important role of flavonoid metabolism in Arabidopsis freezing tolerance and point to the importance of post‐transcriptional mechanisms in the regulation of flavonoid metabolism in response to cold.
It is well known that acclimation of plants to low temperatures elicits massive changes in gene expression and in the content of primary metabolites and lipids, but changes in secondary metabolites have not been characterized previously. We have analyzed the effect of cold on flavonol and anthocyanin content and on the expression of genes related to flavonoid metabolism in 54 Arabidopsis accessions covering a wide range of freezing tolerance. Most flavonols, anthocyanins and the related transcripts accumulated in the cold and for some, a correlation of pool sizes with freezing tolerance was found. There was little correlation between metabolite and transcript levels, indicating an important role of post‐transcriptional regulation in flavonoid metabolism.
Understanding the response to cold temperature stress is relevant for both basic biology and application. Here we report on ERF105, which is a novel cold‐regulated transcription factor gene of ...Arabidopsis that makes a significant contribution to freezing tolerance and cold acclimation. The expression of cold‐responsive genes in erf105 mutants suggests that its action is linked to the CBF regulon mediating cold responses.
Low temperature is an environmental factor that adversely affects plant growth and development and limits the geographical distribution of species; it impacts also the agronomical performance of crop plants. Therefore, understanding the response to cold‐temperature stress is relevant for both basic biology and application. In this work, we report the characterization of an APETALA2 (AP2)/ERF domain‐containing transcription factor gene of Arabidopsis, ERF105. ERF105 expression is induced by cold, and we show that the gene is functionally important for the cold stress response. Its effect on freezing tolerance is comparable or even higher than the one of components of the well‐studied CBF regulon, and the expression behaviour of cold‐responsive genes indicates that ERF105 may act upstream of the well‐known CBF regulon. Taken together, we think that this is a novel and relevant contribution for our understanding of the response of plants to cold stress.
Arabidopsis thaliana is a geographically widely spread species consisting of local accessions differing both genetically and phenotypically. These differences may constitute environmental adaptations ...and a latitudinal cline in freezing tolerance has been shown previously. Many plants, including Arabidopsis, exhibit increased freezing tolerance after cold exposure (cold acclimation). Here we present evidence for geographical clines (both latitudinal and longitudinal) in acclimated (ACC) and non‐acclimated (NA) freezing tolerance, estimated from electrolyte leakage measurements on 54 accessions. Leaf Pro contents were not correlated with freezing tolerance, while sugar contents (Glc, Fru, Suc, Raf) were in the ACC, but not the NA state. Expression levels of 14 cold‐induced genes were investigated before and after 2 weeks of cold acclimation by quantitative RT‐PCR. Expression of the CBF1, 2 and 3 genes was not correlated with freezing tolerance. The expression of some CBF‐regulated (COR) genes, however, was correlated specifically with ACC freezing tolerance. A tight correlation between CBF and COR gene expression was only observed under non‐acclimating conditions, where CBF and COR expression were also correlated with the expression of PRR5, a component of the circadian clock. Collectively, this study sheds new light on the molecular determinants of plant‐freezing tolerance and cold acclimation and their geographical dependence.
During low temperature exposure, temperate plant species increase their freezing tolerance in a process termed cold acclimation. This is accompanied by dampened oscillations of circadian clock genes ...and disrupted oscillations of output genes and metabolites. During deacclimation in response to warm temperatures, cold acclimated plants lose freezing tolerance and resume growth and development. While considerable effort has been directed toward understanding the molecular and metabolic basis of cold acclimation, much less information is available about the regulation of deacclimation.
We report metabolic (gas chromatography-mass spectrometry) and transcriptional (microarrays, quantitative RT-PCR) responses underlying deacclimation during the first 24 h after a shift of Arabidopsis thaliana (Columbia-0) plants cold acclimated at 4 °C back to warm temperature (20 °C). The data reveal a faster response of the transcriptome than of the metabolome and provide evidence for tightly regulated temporal responses at both levels. Metabolically, deacclimation is associated with decreasing contents of sugars, amino acids, glycolytic and TCA cycle intermediates, indicating an increased need for carbon sources and respiratory energy production for the activation of growth. The early phase of deacclimation also involves extensive down-regulation of protein synthesis and changes in the metabolism of lipids and cell wall components. Hormonal regulation appears particularly important during deacclimation, with extensive changes in the expression of genes related to auxin, gibberellin, brassinosteroid, jasmonate and ethylene metabolism. Members of several transcription factor families that control fundamental aspects of morphogenesis and development are significantly regulated during deacclimation, emphasizing that loss of freezing tolerance and growth resumption are transcriptionally highly interrelated processes. Expression patterns of some clock oscillator components resembled those under warm conditions, indicating at least partial re-activation of the circadian clock during deacclimation.
This study provides the first combined metabolomic and transcriptomic analysis of the regulation of deacclimation in cold acclimated plants. The data indicate cascades of rapidly regulated genes and metabolites that underlie the developmental switch resulting in reduced freezing tolerance and the resumption of growth. They constitute a large-scale dataset of genes, metabolites and pathways that are crucial during the initial phase of deacclimation. The data will be an important reference for further analyses of this and other important but under-researched stress deacclimation processes.
Celotno besedilo
Dostopno za:
DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Freezing injury is a major factor limiting the geographical distribution of plant species and the growth and yield of crop plants. Plants from temperate climates are able to increase their freezing ...tolerance during exposure to low but non‐freezing temperatures in a process termed cold acclimation. Damage to cellular membranes is the major cause of freezing injury in plants, and membrane lipid composition is strongly modified during cold acclimation. Forward and reverse genetic approaches have been used to probe the role of specific lipid‐modifying enzymes in the freezing tolerance of plants. In the present paper we describe an alternative ecological genomics approach that relies on the natural genetic variation within a species. Arabidopsis thaliana has a wide geographical range throughout the Northern Hemisphere with significant natural variation in freezing tolerance that was used for a comparative analysis of the lipidomes of 15 Arabidopsis accessions using ultra‐performance liquid chromatography coupled to Fourier‐transform mass spectrometry, allowing the detection of 180 lipid species. After 14 days of cold acclimation at 4°C the plants from most accessions had accumulated massive amounts of storage lipids, with most of the changes in long‐chain unsaturated triacylglycerides, while the total amount of membrane lipids was only slightly changed. Nevertheless, major changes in the relative amounts of different membrane lipids were also evident. The relative abundance of several lipid species was highly correlated with the freezing tolerance of the accessions, allowing the identification of possible marker lipids for plant freezing tolerance.
Heat and drought stress are projected to become major challenges to sustain rice (Oryza sativa L.) yields with global climate change. Both stresses lead to yield losses when they coincide with ...flowering. A significant knowledge gap exists in the mechanistic understanding of the responses of rice floral organs that determine reproductive success under stress. Our work connects the metabolomic and transcriptomic changes in anthers, pistils before pollination and pollinated pistils in a heat‐tolerant (N22) and a heat‐sensitive (Moroberekan) cultivar. Systematic analysis of the floral organs revealed contrasts in metabolic profiles across anthers and pistils. Constitutive metabolic markers were identified that can define reproductive success in rice under stress. Six out of nine candidate metabolites identified by intersection analysis of stressed anthers were differentially accumulated in N22 compared with Moroberekan under non‐stress conditions. Sugar metabolism was identified to be the crucial metabolic and transcriptional component that differentiated floral organ tolerance or susceptibility to stress. While susceptible Moroberekan specifically showed high expression of the Carbon Starved Anthers (CSA) gene under combined heat and drought, tolerant N22 responded with high expression of genes encoding a sugar transporter (MST8) and a cell wall invertase (INV4) as markers of high sink strength.
A novel attempt was made to associate temporal and spatial dynamics with the transcriptome and the metabolome of the anther, pistil before pollination and pollinated pistil exposed to heat or combined drought and heat stress, with key physiological processes determining stress induced spikelet sterility. Our work identifies key constitutive metabolite markers specific to reproductive organs that could be extremely valuable particularly with constrains associated with infrastructural challenges for precision stress phenotyping. We demonstrate that the tolerant cultivar N22 having the potential to avoid carbon starvation through e.g. the operation of sugar transporters and a cell wall invertase to reduce the impact of heat or drought stress on anthers, unlike the susceptible cultivar Moroberekan.
Freezing triggers extracellular ice formation leading to cell dehydration and deformation during a freeze–thaw cycle. Many plant species increase their freezing tolerance during exposure to low, ...non‐freezing temperatures, a process termed cold acclimation. In addition, exposure to mild freezing temperatures after cold acclimation evokes a further increase in freezing tolerance (sub‐zero acclimation). Previous transcriptome and proteome analyses indicate that cell wall remodelling may be particularly important for sub‐zero acclimation. In the present study, we used a combination of immunohistochemical, chemical and spectroscopic analyses to characterize the cell walls of Arabidopsis thaliana and characterized a mutant in the XTH19 gene, encoding a xyloglucan endotransglucosylase/hydrolase (XTH). The mutant showed reduced freezing tolerance after both cold and sub‐zero acclimation, compared to the Col‐0 wild type, which was associated with differences in cell wall composition and structure. Most strikingly, immunohistochemistry in combination with 3D reconstruction of centres of rosette indicated that epitopes of the xyloglucan‐specific antibody LM25 were highly abundant in the vasculature of Col‐0 plants after sub‐zero acclimation but absent in the XTH19 mutant. Taken together, our data shed new light on the potential roles of cell wall remodelling for the increased freezing tolerance observed after low temperature acclimation.
xth19 mutant had reduced freezing tolerance after cold or sub‐zero acclimation. Microscopic and biochemical characterization of the cell wall indicated altered xyloglucan deposition in xth19 after sub‐zero acclimation showing the importance of cell wall remodelling for increased freezing tolerance.
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