Increased Sedoheptulose-1,7-Bisphosphatase Activity in Transgenic Tobacco Plants Stimulates Photosynthesis and Growth from an Early Stage in Development1

Activity of the Calvin cycle enzyme sedoheptulose-1,7-bisphosphatase (SBPase) was increased by overexpression of an Arabidopsis (Arabidopsis thaliana) cDNA in tobacco (Nicotiana tabacum) plants. In plants with increased SBPase activity, photosynthetic rates were increased, higher levels of Suc and starch accumulated during the photoperiod, and an increase in leaf area and biomass of up to 30% was also evident. Light saturated photosynthesis increased with increasing SBPase activity and analysis of CO2 response curves revealed that this increase in photosynthesis could be attributed to an increase in ribulose 1,5-bisphosphate regenerative capacity. Seedlings with increased SBPase activity had an increased leaf area at the 4 to 5 leaf stage when compared to wild-type plants, and chlorophyll fluorescence imaging of these young plants revealed a higher photosynthetic capacity at the whole plant level. Measurements of photosynthesis, made under growth conditions integrated over the day, showed that mature plants with increased SBPase activity fixed 6% to 12% more carbon than equivalent wild-type leaves, with the young leaves having the highest rates. In this paper, we have shown that photosynthetic capacity per unit area and plant yield can be increased by overexpressing a single native plant enzyme, SBPase, and that this gives an advantage to the growth of these plants from an early phase of vegetative growth. This work has also shown that it is not necessary to bypass the normal regulatory control of SBPase, exerted by conditions in the stroma, to achieve improvements in carbon fixation.

[1]  M. Stitt,et al.  Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology , 1994 .

[2]  C. Raines.  Review article. New insights into the structure and function of sedoheptulose-1,7-bisphosphatase; an important but neglected Calvin cycle enzyme , 1999 .

[3]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS , 1991, Planta.

[4]  C. Raines,et al.  Photosynthetic capacity is differentially affected by reductions in sedoheptulose-1,7-bisphosphatase activity during leaf development in transgenic tobacco plants. , 2001, Plant physiology.

[5]  M. Stitt,et al.  A Small Decrease of Plastid Transketolase Activity in Antisense Tobacco Transformants Has Dramatic Effects on Photosynthesis and Phenylpropanoid Metabolism , 2001, Plant Cell.

[6]  T. Andrews,et al.  Reduction of ribulose-1,5-bisphosphate carboxylase/oxygenase content by antisense RNA reduces photosynthesis in transgenic tobacco plants. , 1992, Plant physiology.

[7]  Julie C. Lloyd,et al.  Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation , 1997, Planta.

[8]  L. Willmitzer,et al.  Reduction of the chloroplastic fructose‐1,6‐bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth , 1994 .

[9]  M. Stitt,et al.  A moderate decrease of plastid aldolase activity inhibits photosynthesis, alters the levels of sugars and starch, and inhibits growth of potato plants. , 1998, The Plant journal : for cell and molecular biology.

[10]  R. Richards.  Selectable traits to increase crop photosynthesis and yield of grain crops. , 2000, Journal of experimental botany.

[11]  U. Sonnewald,et al.  Small changes in the activity of chloroplastic NADP(+)-dependent ferredoxin oxidoreductase lead to impaired plant growth and restrict photosynthetic activity of transgenic tobacco plants. , 2002, The Plant journal : for cell and molecular biology.

[12]  J. Lloyd,et al.  New insights into the structure and function of sedoheptulose-1,7-bisphosphatase; an important but neglected Calvin cycle enzyme , 1999 .

[13]  N. Baker,et al.  Rapid, Noninvasive Screening for Perturbations of Metabolism and Plant Growth Using Chlorophyll Fluorescence Imaging1 , 2003, Plant Physiology.

[14]  E. Harrison,et al.  Investigating the role of the thiol‐regulated enzyme sedoheptulose‐1,7‐bisphosphatase in the control of photosynthesis , 2000 .

[15]  J. Wiseman,et al.  Limits to efficiencies of primary production - constraints and opportunities. , 2005 .

[16]  Donald R. Geiger,et al.  Diurnal Regulation of Photosynthetic Carbon Metabolism in C3 Plants , 1994 .

[17]  K. Siebke,et al.  Photosynthesis is strongly reduced by antisense suppression of chloroplastic cytochrome bf complex in transgenic tobacco , 1998 .

[18]  M. Stitt,et al.  Pathway of starch breakdown in photosynthetic tissues of Pisum sativum. , 1978, Biochimica et biophysica acta.

[19]  E. Schulze,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1991, Planta.

[20]  M. Badger,et al.  Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants , 2004, Planta.

[21]  M. Tamoi,et al.  Overexpression of a cyanobacterial fructose-1,6-/sedoheptulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth , 2001, Nature Biotechnology.

[22]  L. T. Evans,et al.  Yield potential: its definition, measurement, and significance , 1999 .

[23]  C. Raines,et al.  Molecular cloning of the Arabidopsis thaliana sedoheptulose-1,7-biphosphatase gene and expression studies in wheat and Arabidopsis thaliana , 1994, Plant Molecular Biology.

[24]  R. Loomis,et al.  Yield Potential, Plant Assimilatory Capacity, and Metabolic Efficiencies , 1999 .

[25]  M. Stitt,et al.  Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with “antisense” rbcS , 1993, Planta.

[26]  D. R. Hoagland,et al.  The Water-Culture Method for Growing Plants Without Soil , 2018 .

[27]  G. Farquhar,et al.  Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves , 1981, Planta.

[28]  J. Fry,et al.  A simple and general method for transferring genes into plants. , 1985, Science.

[29]  Eva Rosenqvist,et al.  Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. , 2004, Journal of experimental botany.

[30]  E. Harrison,et al.  Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubisco carboxylation capacity. , 2001, Journal of experimental botany.

[31]  S. V. Caemmerer,et al.  Biochemical models of leaf photosynthesis. , 2000 .

[32]  C. Raines.  The Calvin cycle revisited , 2004, Photosynthesis Research.

[33]  G. Farquhar,et al.  Effects of partial defoliation, changes of irradiance during growth, short-term water stress and growth at enhanced p(CO2) on the photosynthetic capacity of leaves of Phaseolus vulgaris L. , 1984, Planta.

[34]  M. Stitt,et al.  Metabolite levels in specific cells and subcellular compartments of plant leaves , 1989 .

[35]  Dimah Z. Habash,et al.  Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco: effect on CO2 assimilation and growth in low irradiance , 1995 .