ReviewA plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis
Introduction
Low temperature is one of the most important factors affecting plant performance and distribution 1., 2.. At high latitudes or altitudes, the problem of coping with low temperatures is exacerbated by the need to prolong the growing season beyond the short summer. Low temperatures slow down enzyme-catalysed reactions and modify the conformation of lipids and other macromolecules, with consequences for most biological processes. It is difficult to determine which processes are affected most severely by cold, and differential responses generate complex indirect effects. Sub-freezing temperatures lead to severe damage caused by dehydration when ice forms outside the cell or, in extreme cases, to freezing of the cytoplasm.
Many species, including crops such as maize, bean, tomato and potato, have only a limited capacity to cope with low temperatures [2]. Cold-hardy herbaceous species, including Arabidopsis 3., 4., 5••. and crops such as winter cereals, winter rape, spinach and cabbage 6., 7., 8., 9., grow at low temperatures and survive freezing temperatures. Biennials and woody perennials that are adapted to high latitudes cope with temperatures down to –40°C or lower [2]. Low temperature tolerance develops in cold-hardy species during a period of exposure to low but non-freezing temperatures in a multi-facetted process termed cold-acclimation [10•]. In this review, we discuss the biochemical and physiological adaptations of plants to low temperature. These include the post-translational activation and increased expression of enzymes of the sucrose synthesis pathway, the changed expression of Calvin cycle enzymes, and changes in leaf protein content. We then discuss signals that may trigger these processes and consider how the regulation of photosynthetic carbon metabolism interacts with other processes during cold acclimation.
Section snippets
An important role for sugars in cold acclimation
Descriptive ecological and agronomic studies have uncovered a strong correlation between sugar concentrations and frost resistance 2., 7., 11., 12., 13., 14.. Likewise, changes of light regime during cold acclimation revealed a strong correlation between sugar levels and frost tolerance in Arabidopsis [15]. The sugar concentrations in transformants with antisense inhibition of cytosolic fructose-1,6-bisphosphatase (cFBPase) and sucrose phosphate synthase (SPS) expression, or with overexpression
An over-proportional inhibition of sucrose synthesis reduces photosynthesis at low temperatures
During photosynthesis, CO2 combines with ribulose-1,5-bisphosphate (Ru1,5bisP) to form glycerate-3-phosphate, which is reduced to triose-phosphate using NADPH and ATP that is generated by photosynthetic electron transport. The majority of the triose phosphates are retained in the chloroplast to regenerate Ru1,5bisP. The surplus is converted to end products, releasing inorganic orthophosphate (Pi) that recombines with ADP to regenerate ATP. The most important pathway for end-product synthesis
Cold acclimation includes a selective stimulation of sucrose synthesis and re-establishment of high rates of photosynthesis
Recent studies with Arabidopsis have shown that a sequence of events reverses the inhibition of sucrose synthesis and photosynthesis as the plants acclimate to low temperatures 3., 4., 5••., 16.. Short- and mid-term adjustments act primarily on sucrose synthesis but also stimulate photosynthesis by relieving the acute Pi-limitation. Longer-term adjustments affect photosynthesis directly. The recovery has two important functions: increased sucrose production [4] and protection against
Acclimation of photosynthetic metabolism is triggered in part by acute Pi-limitation
As already discussed, decreased temperatures lead to an acute Pi-limitation of photosynthesis. Intriguingly, some of the changes in photosynthetic metabolism that occur during cold acclimation are reminiscent of the response to low Pi 23., 40., 41.. Evidence that changes in Pi concentration or availability to metabolism contribute to cold acclimation has been provided by studies [5••] of pho1 [42] and pho2 [43] mutants. These mutants have decreased and increased shoot Pi concentrations,
Further components of the cold-acclimation response include novel cold-induced polypeptides, changes in membrane fluidity and proline accumulation
Low temperatures induce many other biochemical changes in addition to increased sugar levels. These include the accumulation of proline and, in some species, of other cryoprotectants including glycylbetaine 17., 18••., 44.; increased levels of antioxidants [10•]; and increased lipid desaturation to restore membrane fluidity 45., 46.. Chilling also induces the expression of a number of cold REGULATED (COR) genes 47., 48., 49•.. COR15a encodes a protein that interacts with lipids of the
Carbon metabolism interacts with other processes during cold acclimation
In Synechocystis, two histidine kinases and a regulator response element are required for the induction at low temperatures of desB [57], a fatty acid desaturase implicated in increasing membrane fluidity at low temperatures. This pathway acts via additional uncharacterised response receptors to regulate the expression of many other genes, and parallel receptors may act on further groups of targets 57., 58.. In higher plants, the primary temperature-sensing mechanism(s) have not yet been
Possible interactions with vernalisation
Studies with cereals have recently drawn attention to a further fascinating facet of cold acclimation. A set of COR genes have been identified in barley and winter wheat 68., 69., 70••.. In these species, prolonged exposure to low temperatures leads to a gradual decrease in the levels of COR transcripts and proteins, which is accompanied by a loss of cold tolerance 69., 70••.. This loss of cold tolerance may be linked to the switch from the vegetative to the reproductive state as a result of
The physiological contribution of sugars in cold acclimation
Sugars could act in several ways to promote cold acclimation (Fig. 2) with most hypothetical mechanisms involving interactions with other components of the acclimation response. Dissection of the role of sugars in cold acclimation is a major task for the future.
It has been proposed that sugars either act as osmotica or protect specific macromolecules during dehydration 2., 71.. Changes in the subcellular concentration and distribution of sugars might also provide a mechanism to protect specific
Conclusions: wheels and roundabouts
Even though overexpression of CBF family members leads to enhanced frost tolerance, the transformants grow poorly at normal temperatures 54., 55.. This implies that at least some of the adjustments that occur during cold acclimation are detrimental at higher temperatures. The reasons for this will become clearer as more is learnt about the biochemical and cellular changes that occur during cold acclimation. Photosynthetic metabolism provides an easily approachable system to investigate the
Acknowledgements
The authors’ work was supported by the Alexander von Humboldt Society, the Deutsche Forschungsgemeinschaft, the GABI programme of the German Ministry for Education Research, and the Swedish Council for Forestry and Agricultural Research. We are grateful to Åsa Strand, Eike Hentschel and Per Gardeström for cooperation. This article is dedicated to the memory of Peter Steponkus.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
References (82)
- et al.
Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings
J Plant Physiol
(2001) - et al.
Interactions between sucrose synthesis and CO2 fixation. II. Alterations of fructose 2,6-bisphosphate during photosynthetic oscillations
J Plant Physiol
(1988) - et al.
Phospholipid, protein, and nucleic acid increases in protoplasm and membrane structures associated with development of extreme freezing resistance in black locust tree cells
Cryobiology
(1968) - et al.
Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus x canadensis Moench [robusta]) wood
J Plant Physiol
(1996) - et al.
The TAG1 locus of Arabidopsis encodes for a diacylglycerol acyltransferase
Plant Physiol Biochem
(1999) - et al.
Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana
FEBS Lett
(1999) - et al.
Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways
Curr Opin Plant Biol
(2000) - et al.
Temperature sensing and cold acclimation
Curr Opin Plant Biol
(2001) - et al.
Carbon and nitrogen metabolism and reversible protein phosphorylation
Adv Bot Res
(2000) - et al.
Developmental regulation of low-temperature tolerance in winter wheat
Ann Bot
(2001)
Consequences of omega-6-oleate desaturase deficiency on lipid dynamics and functional properties of mitochondrial membranes of Arabidopsis thaliana
J Biol Chem
Sugars as signaling molecules
Curr Opin Plant Biol
Plant productivity and environment
Science
Physiological Plant Ecology
Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates
Plant J.
Acclimation of Arabidopsis leaves developing at low temperatures. Increasing cytoplasmic volume accompanies increased activities of enzymes in the Calvin cycle and in the sucrose-biosynthesis pathway
Plant Physiol.
The role of inorganic phosphate in the development of freezing tolerance and the acclimatization of photosynthesis to low temperature is revealed by the pho mutants of Arabidopsis thaliana
Plant J
Acclimation of photosynthesis to low temperature in Spinacia oleracea L. 1. Effects of acclimation on CO2 assimilation and carbon partitioning
J Exp Bot
Effects of a short-term shift to low-temperature and of long-term cold hardening on photosynthesis and ribulose-1,5-bisphosphate carboxylase oxygenase and sucrose-phosphate synthase activity in leaves of winter rye (Secale cereale L)
Plant Physiol
Cold hardening of spring and winter-wheat and rape results in differential-effects on growth, carbon metabolism, and carbohydrate content
Plant Physiol
Cold comfort farm: the acclimation of plants to freezing temperatures
Plant Cell Environ
Cold acclimation and freezing stress tolerance — role of protein metabolism
Annu Rev Plant Physiol Plant Mol Biol
Sucrose phosphate synthase and sucrose accumulation at low-temperature
Plant Physiol
Non-structural carbohydrates and catalytic activities of sucrose metabolizing enzymes in trunks of two Juglans species and their role in heartwood formation
Holzforschung
Fast, nondestructive measurement of frost hardiness in conifer seedlings by VIS plus NIR spectroscopy
Tree Physiol
Cold-induced freezing tolerance in Arabidopsis
Plant Physiol
eskimo1 mutants of Arabidopsis are constitutively freezing-tolerant
Proc Natl Acad Sci USA
Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation
Plant Physiol
Cold responses of Arabidopsis mutants impaired in freezing tolerance
J Exp Bot
Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L) Heynh
Plant Physiol
C3–C4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis
Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells
Plant Cell Environ
Metabolic regulation of photosynthesis
Stimulation of photosynthesis by 2% oxygen at low-temperatures is restored by phosphate
Planta
Limitation of photosynthesis by carbon metabolism. II. O2-insensitive CO2 uptake results from limitations of triose phosphate utilization
Plant Physiol
Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability
Planta
Measurement of subcellular metabolite levels by fractionation of freeze-stopped material in non-aqueous media
Plant Physiol
Stromal phosphate concentration is low during feedback limited photosynthesis
Plant Physiol
Carbohydrate-modulated gene expression in plants
Annu Rev Plant Physiol Plant Mol Biol
The onset of sucrose accumulation in cold-stored potato tubers is caused by an increased rate of sucrose synthesis and coincides with low levels of hexose-phosphates, an activation of sucrose phosphate synthase and the appearance of a new form of amylase
Plant Cell Environ
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