Abstract
Regulation of sucrose-starch accumulation and its effect on CO2 gas exchange and electron transport were studied in low-temperature-stressed and cold-acclimated spring (Katepwa) and winter (Monopol) cultivars of wheat (Triticum aestivum L.). Low-temperature stress of either the spring or winter cultivar was associated with feedback-limited photosynthesis as indicated by a 50–60% reduction in CO2 assimilation rates, twofold lower ATP/ADP ratio, and threefold lower electron transport rate than 20°C-grown control plants. However, no limitations were evident at the level of ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco) in low-temperature-stressed plants. Cold acclimation of the spring cultivar resulted in similar feedback-limited photosynthesis observed during low-temperature stress. In contrast, cold acclimation of the winter cultivar resulted in an adjustment of CO2 assimilation rates to that of control plants. However, we show, for the first time, that this capacity to adjust CO2 assimilation still appeared to be associated with limited triose phosphate utilisation, a twofold lower ATP/ADP ratio, a reduction in electron transport rates but no restriction at the level of Rubisco compared to controls grown at 20°C. Thus, contrary to previous suggestions, we conclude that cold-acclimated Monopol appears to exhibit feedback limitations at the level of electron transport characteristic of cold-stressed plants despite the maintenance of high rates of CO2 assimilation. Furthermore, the differential capacity of the winter cultivar to adjust CO2 assimilation rates was associated with higher levels of sucrose accumulation and a threefold higher sucrose-phosphate synthase activity despite an apparent limitation in triose phosphate utilisation.
Similar content being viewed by others
Abbreviations
- AGPase:
-
ADP-glucose pyrophosphorylase
- FBPase:
-
fructose-1,6-bisphosphatase
- Fru 6-P:
-
fructose 6-phosphate
- Fru 1,6-BP:
-
fructose 1,6-bisphosphate
- Glc 6-P:
-
glucose 6-phosphate
- PGA:
-
3-phosphoglyceric acid
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase-oxygenase
- RuBP:
-
ribulose 1,5-bisphosphate
- SPS:
-
sucrose-phosphate synthase
- Triose-P:
-
triose phosphate
References
Battistelli A, Adcock MD, Leegood RC (1991) The relationship between the activation state of sucrose-phosphate synthase and the rate of CO2 assimilation in spinach leaves. Planta 183: 620–622
Dietz K-J, Heber U (1986) Light and CO2 limitation of photosynthesis and states of the reactions regenerating ribulose-1,5-bisphosphate or reducing 3-phosphoglycerate. Biochim Biophys Acta 848: 392–401
Galtier N, Foyer CH, Huber J, Voelker TA, Huber SC (1993) Effects of elevated sucrose-phosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycopersicon esculentum var UC82B). Plant Physiol 101: 535–543
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87–92
Gray GR, Savitch LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photo-inhibition. II. Adjustment of photosynthetic capacity inTriticum aestivum andSecale cereale. Plant Physiol 110: 61–71
Guy CL, Huber JLA, Huber SC (1992) Sucrose phosphate synthase and sucrose accumulation at low-temperature. Plant Physiol 100: 502–508
Holaday AS, Martindale W, Alred R, Brooks AL, Leegood RC (1992) Changes in activities of enzymes of carbon metabolism in leaves during exposure of plants to low-temperature. Plant Physiol 98: 1105–1114
Huber JL, Hite DRC, Outlaw JWH, Huber SC (1991) Inactivation of highly activated spinach leaf sucrose-phosphate synthase by dephosphorylation. Plant Physiol 95: 291–297
Hurry VM, Huner NPA (1991) Low growth temperature effects a differential inhibition of photosynthesis in spring and winter wheat. Plant Physiol 96: 491–497
Hurry VM, Gardeström P, Öquist G (1993) Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. Planta 190: 484–490
Hurry VM, Malmberg G, Gardeström P, Öquist G (1994a) 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 106: 983–990
Hurry VM, Keerberg O, Parnik T, Gardeström P, Öquist G (1994b) Cold hardening results in increased activity of enzymes involved in carbon metabolism in leaves of winter rye (Secale cereale L.). Planta 195: 554–562
Hurry VM, Strand C, Tobiaeson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism and carbohydrate content. Plant Physiol 109: 697–706
Krause K-P, Stitt M (1992) Sucrose-6-phosphate levels in spinach leaves and their effects on sucrose phosphate synthase. Phytochemistry 131: 1143–1146
Labate CA, Leegood RC (1988) Limitation of photosynthesis by changes in temperature. Planta 173: 519–527
Labate CA, Adcock MD, Leegood RC (1990) Effects of temperature on the regulation of photosynthetic carbon accumulation in leaves of maize and barley. Planta 181: 547–554
Leegood RC, Walker DA (1983) The role of transmembrane solute flux in regulation of CO2 fixation in chloroplasts. Biochem Soc Trans 11: 74–76
Loreto F, Sharkey TD (1993) On the relationship between isoprene emission and photosynthetic metabolites under different environmental conditions. Planta 189: 420–424
Öquist G, Hurry VM, Huner NPA (1993) Low temperature effects on photosynthesis and correlation with freezing tolerance in spring and winter cultivars of wheat and rye. Plant Physiol 101: 245–250
Pammenter NW, Loreto F, Sharkey TD (1993) End product feedback effects on photosynthetic electron transport. Photosyn Res 35: 5–14
Pollock CJ, Lloyd EJ (1987) The effect of low temperature upon starch, sucrose and fructan synthesis in leaves. Ann Bot 60: 231–235
Rufty TWI, Huber SC (1983) Changes in starch formation and activities of sucrose phosphate synthase and cytoplasmic fructose 1,6-bisphosphatase in response to source-sink alterations. Plant Physiol 72: 474–480
Sage RF, Sharkey TD (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol 84: 658–664
Sharkey TD (1990) Feedback limitation of photosynthesis and the physiological role of ribulose bisphosphate carboxylase carbamylation. Bot Mag Tokyo 2: 87–105
Sharkey TD, Vassey TL, Vanderveer PJ, Vierstra RD (1991a) Carbon metabolism enzymes and photosynthesis in transgenic tobacco (Nicotiana tabacum L.) having excess phytochrome. Planta 185: 287–296
Sharkey TD, Savitch LV, Butz ND (1991b) Photometric method for routine determination of kcat and carbamylation of rubisco. Photosynth Res 28: 41–48
Vassey TL, Sharkey TD (1989) Mild water stress ofPhaseolus vulgaris plants leads to reduced starch synthesis and extractable sucrose phosphate synthase activity. Plant Physiol 89: 1066–1070
Weber H, Heim U, Borisjuk L, Wobus U (1995) Cell-type specific, coordinate expression of two ADP-glucose pyrophosphorylase genes in relation to starch biosynthesis during seed development ofVicia faba L. Planta 195: 352–361
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Savitch, L.V., Gray, G.R. & Huner, N.P.A. Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201, 18–26 (1997). https://doi.org/10.1007/BF01258676
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01258676