Review
A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis

https://doi.org/10.1016/S1369-5266(02)00258-3Get rights and content

Abstract

Low temperatures lead to the inhibition of sucrose synthesis and photosynthesis. The biochemical and physiological adaptations of plants to low temperatures 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 the leaf protein content. Recent progress has been made in understanding both the signals that trigger these processes and how the regulation of photosynthetic carbon metabolism interacts with other processes during cold acclimation.

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

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