Low temperature is a primary determinant of plant growth and survival. Using accessions of Arabidopsis (Arabidopsis thaliana) originating from Scandinavia to the Cape Verde Islands, we show that freezing tolerance of natural accessions correlates with habitat winter temperatures, identifying low temperature as an important selective pressure for Arabidopsis. Combined metabolite and transcript profiling show that during cold exposure, global changes of transcripts, but not of metabolites, correlate with the ability of Arabidopsis to cold acclimate. There are, however, metabolites and transcripts, including several transcription factors, that correlate with freezing tolerance, indicating regulatory pathways that may be of primary importance for this trait. These data identify that enhanced freezing tolerance is associated with the down-regulation of photosynthesis and hormonal responses and the induction of flavonoid metabolism, provide evidence for naturally increased nonacclimated freezing tolerance due to the constitutive activation of the C-repeat binding factors pathway, and identify candidate transcriptional regulators that correlate with freezing tolerance.
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.
Numerous studies have been published that attempted to correlate fructan concentrations with freezing and drought tolerance. Studies investigating the effect of fructan on liposomes indicated that a direct interaction between membranes and fructan was possible. This new area of research began to move fructan and its association with stress beyond mere correlation by confirming that fructan has the capacity to stabilize membranes during drying by inserting at least part of the polysaccharide into the lipid headgroup region of the membrane. This helps prevent leakage when water is removed from the system either during freezing or drought. When plants were transformed with the ability to synthesize fructan, a concomitant increase in drought and/or freezing tolerance was confirmed. These experiments indicate that besides an indirect effect of supplying tissues with hexose sugars, fructan has a direct protective effect that can be demonstrated by both model systems and genetic transformation.
Desiccation in general leads to severe damage of cellular structures, which commonly results in the death of cells and the organism. However, a number of so-called anhydrobiotic organisms have developed remarkable mechanisms, allowing them to minimize or avoid such damage and survive extreme dehydration in a cryptobiotic state [1][2][3][4][5][6]. Several species of invertebrate taxa have this ability, including the embryonic cysts of crustaceans, rotifers, insect larvae, nematodes and tardigrades [2,3,[7][8][9][10][11][12]. Additionally, many procaryotes, such as bacteria and cyanobacteria [13,14], and even plant seeds [15][16][17][18][19] and adult plants, for example the resurrection lycopode Selaginella lepidophylla [5,20], demonstrate dehydration tolerance. Although Antonin van Leuwenhoek described anhydrobiosis over 300 years ago [21], the underlying mechanisms are still not fully understood. However, over the last three decades, researchers have come to recognize the important role of polyhydroxy compounds such as the non-reducing disaccharide trehalose [22][23][24]. This sugar is found in high concentrations in a wide variety of anhydrobiotic organisms, including nematodes, embryonic cysts of crustaceans, and yeast. Trehalose concentrations as high as 13-18% of the dry weights have been reported for anhydrobiotic cysts of the crustacean Artemia franciscana [25][26][27] whereas the nematode Aphelenchus avenae can accumulate 10-15% of its dry weight as trehalose during anhydrobiosis [8,9]. Studies on the anhydrobiotic insect larvae Polypedilum vanderplanki report up to 18% trehalose in the dry body mass [11]. Significantly increased trehalose levels also have been found in the Arctic collembolan Onychiurus arcticus during partial desiccation, induced by sub-zero temperatures [28]. The disaccharide sucrose fulfils a similar role in plants and accumulates in desiccation-tolerant plant seeds and resurrection To withstand desiccation, many invertebrates such as rotifers, nematodes and tardigrades enter a state known as anhydrobiosis, which is thought to require accumulation of compatible osmolytes, such as the non-reducing disaccharide trehalose to protect against dehydration damage. The trehalose levels of eight tardigrade species comprising Heterotardigrada and Eutardigrada were observed in five different states of hydration and dehydration. Although many species accumulate trehalose during dehydration, the data revealed significant differences between the species. Although trehalose accumulation was found in species of the order Parachela (Eutardigrada), it was not possible to detect any trehalose in the species Milnesium tardigradum and no change in the trehalose level has been observed in any species of Heterotardigrada so far investigated. These results expand our current understanding of anhydrobiosis in tardigrades and, for the first time, demonstrate the accumulation of trehalose in developing tardigrade embryos, which have been shown to have a high level of desiccation tolerance.Abbreviations HPAEC, h...
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