Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Overexpression of sedoheptulose-1,7-bisphosphatase enhances photosynthesis and growth under salt stress in transgenic rice plants

Lingling Feng A B , Yujun Han A , Gai Liu A , Baoguang An A , Jing Yang A , Guohua Yang A , Yangsheng Li A C and Yingguo Zhu A
+ Author Affiliations
- Author Affiliations

A Key Laboratory of MOE for Plant Developmental Biology, College of Life Sciences, Wuhan University, Wuhan 430072, PR China.

B Key laboratory of Pesticide and Chemical Biology (CCNU) of Ministry of Education, College of Chemistry, Central China Normal University, Wuhan 430079, PR China.

C Corresponding author. Email: yangshengl@yahoo.com.cn

Functional Plant Biology 34(9) 822-834 https://doi.org/10.1071/FP07074
Submitted: 27 March 2007  Accepted: 19 June 2007   Published: 30 August 2007

Abstract

Activity of the Calvin cycle enzyme sedoheptulose-1,7-bisphosphatase (SBPase; EC3.1.3.37) was increased in the transgenic rice cultivar zhonghua11 (Oryza sativa L. ssp. japonica) by overexpressing OsSbp cDNA from the rice cultivar 9311 (Oryza sativa ssp. indica). This genetic engineering enabled the transgenic plants to accumulate SBPase in chloroplasts and resulted in enhanced tolerance of transgenic rice plants to salt stress at the young seedlings stage. Moreover, CO2 assimilation in transgenic rice plants was significantly more tolerant to salt stress than in wild-type plants. The analysis of chlorophyll fluorescence and the activity of SBPase indicated that the enhancement of photosynthesis in salt stress was not related to the function of PSII but to the activity of SBPase. Western-blot analysis showed that salt stress led to the association of SBPase with the thylakoid membranes from the stroma fractions. However, this association was much more prominent in wild-type plants than in transgenic plants. Results suggested that under salt stress, SBPase maintained the activation of ribulose-1,5-bisphosphate carboxylase-oxygenase by providing more regeneration of the acceptor molecule ribulose-1,5-bisphosphate in the soluble stroma and by preventing the sequestration of Rubisco activase to the thylakoid membrane from the soluble stroma, and, thus, enhanced the tolerance of photosynthesis to salt stress. Results suggested that overexpression of SBPase was an effective method for enhanncing salt tolerance in rice.

Additional keywords: overexpression, photosynthesis, salt stress, sedoheptulose-1,7-bisphosphatase, transgenetic rice.


Acknowledgements

We are extremely grateful to Li-Zhong Xiong for a gift of the binary vector pU1301, to Christine A Raines for a gift of SBPase antibodies, to Henry Miziorko for a gift of PRK antibodies, and to Martin Parry for a gift of Rubisco antibodies. We would also like to thank Laurence Cantrill of www.outofsiteenglish.com.au for assistance with English expression. This work was supported by the State Key Basic Research and Development Plan of China (No. 2001CB108805), the National Natural Science Foundation of China for Innovative Research Team (No.30521004) and the Program for Changjiang Scholars and Innovative Research Team (PCSIRT). This work was also supported in part by the Hi-Tech Research and Development Program of China (Grant No. 2006AA10Z 1F 7) and the Key grant Project of Chinese Ministry of Education (Grant No. 307018).


References


Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiologia Plantarum 81, 563–570.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ball MC, Farquhar GD (1984) Photosynthetic and stomatal response of two mangrove species, Aegiceras corniculatum and Avicennia marina to long term salinity and humidity conditions. Plant Physiology 74, 1–6.
PubMed |
open url image1

Belkhodja R, Morales F, Abadia A, Gomez-Aparisi J, Abadia J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiology 104, 667–673.
PubMed |
open url image1

Brugnoli E, Björkman O (1992) Growth of cotton under continuous salinity stress: influence on allocation pattern, stomatal and non-stomatal components of photosynthesis and dissipation of excess light energy. Planta 187, 335–345.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chen XF, Xiong JH, Yu T, Li X, Li SQ, Hua Y, Li YS, Zhu YG (2004) Molecular cloning and characterization of rice Sedoheptulose-1,7-bisphosphatase gene that is regulated by environmental stresses. Journal of Plant Biochemistry and Biotechnology 13, 93–99. open url image1

Crafts-Brandner SJ, van de Loo FJ, Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiology 114, 439–444.
PubMed |
open url image1

Dionisio-Sese ML, Tobita S (2000) Effect of salinity on sodium content and photosynthetic responses of rice seedlings differing in salt tolerance. Journal of Plant Physiology 157, 54–58. open url image1

Dunkley PR, Anderson JM (1979) The light-harvesting chlorophyll a/b-protein complex from barley thylakoid membranes. Polypeptide composition and characterization of an oligomer. Biochimica et Biophysica Acta 545, 175–187.
Crossref | GoogleScholarGoogle Scholar | open url image1

Eckhardt NA, Portis AR (1997) Heat denaturation profiles of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and Rubisco activase and the inability of Rubisco activase to restore activity of heat-denaturated Rubisco. Plant Physiology 113, 243–248.
PubMed |
open url image1

Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH (1994) Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiology 106, 281–292.
PubMed |
open url image1

Banks FM, Driscoll SP, Parry MAJ, Lawlor DW, Knight JS, Gray JC, Paul MJ (1999) Decrease in phosphoribulokinase activity by antisense RNA in transgenic tobacco. Relationship between photosynthesis, growth, and allocation at different nitrogen levels. Plant Physiology 119, 1125–1136.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gardemann A, Stitt M, Heldt HW (1983) Regulation of spinach ribulose-5-phosphate kinase by stromal metabolite levels. Biochimica et Biophysica Acta 722, 51–60.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harrison EP, Willingham NM, Lloyd JC, Raines CA (1997) Reduced sedoheptulose-1,7-bisphosphatase levels in transgenic tobacco lead to decreased photosynthetic capacity and altered carbohydrate accumulation. Planta 204, 27–36.
Crossref | GoogleScholarGoogle Scholar | open url image1

Harrison EP, Olcer H, Lloyd JC, Long SP, Raines CA (2001) Small decreases in SBPase cause a linear decline in the apparent RuBP regeneration rate, but do not affect Rubsico carboxylation capacity. Journal of Experimental Botany 52, 1779–1784.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463–499.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Havaux M (1993) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Science 94, 19–33.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hoque MS, Masle J, Udvardi MK, Ryan PR, Upadhyaya NM (2006) Over-expression of the rice OsAMT1–1 gene increases ammonium uptake and content, but impairs growth and development of plants under high ammonium nutrition. Functional Plant Biology 33, 153–163.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kagawa T (1982) Isolation and purification of ribulose-5-phosphate kinase from Nicotiana glutinosa. In ‘Methods in chloroplast molecular biology’. (Eds M Edelman, KB Hallick, N-H Chua) pp. 695–705. (Elsevier Biomedical Press: Amsterdam)

Kossmann J, Sonnewald U, Willmitzer L (1994) Reduction of the chloroplastic fructose-1,6-bisphosphatase in transgenic potato plants impairs photosynthesis and plant growth. The Plant Journal 6, 637–650.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42, 313–349.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kumar A, Kaiser BN, Siddiqi MY, Glass ADM (2006) Functional characterisation of OsAMT1.1 overexpression lines of rice, Oryza sativa. Functional Plant Biology 33, 339–346.
Crossref | GoogleScholarGoogle Scholar | open url image1

Laing WA, Stitt M, Heldt HW (1981) Changes in the activity of ribulosephosphate kinase and fructose- and sedoheptulose-bisphophatase in chloroplasts. Biochimica et Biophysica Acta 637, 348–359.
Crossref | GoogleScholarGoogle Scholar | open url image1

Leegood RC (1990) Enzymes of the Calvin cycle. In ‘Methods in plant biochemistry. Vol. 3’. (Ed. PJ Lea) pp. 16–20. (Academic Press: London)

Leegood RC (1993) Carbon Metabolism. In ‘Photosynthesis and production in a changing environment: a field and laboratory manual’. (Eds DO Hall, JMO Scurlock, HR Bolhar-Nordenkampf, RC Leegood, SP Long) pp. 247–267. (Academic Press: London.)

Lefebvre S, Lawson T, Zakhleniuk OV, Lloyd JC, Raines CA (2005) Increased sedoheptulose-1,7-bisphosphatase activity in transgenic tobacco plants stimulates photosynthesis and growth from an early stage in development. Plant Physiology 138, 451–460.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lin T-P, Caspar T, Somerville C, Preiss J (1988) Isolation and characterization of a starchless mutant of Arabidopsis thaliana (L.) Heynh lacking ADP glucose pyrophosphorylase activity. Plant Physiology 86, 1131–1135.
PubMed |
open url image1

Masojidek J, Hall DO (1992) Salinity and drought stresses are amplified by high irradiance in sorghum. Photosynthetica 27, 159–171. open url image1

Mitsuya S, Kawasaki M, Taniguchi M, Miyake H (2003) Light dependency of salinity-induced chloroplast degradation. Plant Production Science 6, 219–223.
Crossref | GoogleScholarGoogle Scholar | open url image1

Miyagawa Y, Tamoi M, Shigeoka S (2001) Overexpression of a cyanobacterial fructose-1,6-/sedohetulose-1,7-bisphosphatase in tobacco enhances photosynthesis and growth. Nature Biotechnology 19, 965–969.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Morales F, Abadia A, Gomez-Aparis J, Abadia J (1992) Effects of combined NaCl and CaCl2 salinity on photosynthetic parameters of barley grown in nutrient solution. Physiologia Plantarum 86, 419–426.
Crossref | GoogleScholarGoogle Scholar | open url image1

Mullet JE, Chua NH (1983) In vitro reconstitution of synthesis, uptake, and assembly of cytoplasmically synthesized chloroplast proteins. Methods in Enzymology 97, 502–509. open url image1

Munns R, Termaat A (1986) Whole plant responses to salinity. Australian Journal of Plant Physiology 13, 143–160. open url image1

Olcer H, Lloyd JC, Raines CA (2001) Photosynthetic capacity is differentially affected by reductions in sedoheptulose-1,7-bisphosphatase activity during leaf development in transgenic tobacco plants. Plant Physiology 125, 982–989.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans. I. Oxygen evolution and chlorophyll fluorescence. Plant Physiology 112, 1245–1251.
PubMed |
open url image1

Paul MJ, Knight JS, Habash D, Parry MAJ, Lawlor DW, Barnes SA, Loynes A, Gray JC (1995) Reduction in phosphoribulokinase activity by antisense RNA in transgenic tobacco: effect on CO2 assimilation and growth in low irradiance. The Plant Journal 7, 535–542.
Crossref | GoogleScholarGoogle Scholar | open url image1

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Crossref | GoogleScholarGoogle Scholar | open url image1

Portis AR (1992) Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity. Annual Review of Plant Physiology and Plant Molecular Biology 43, 415–437.
Crossref | GoogleScholarGoogle Scholar | open url image1

Portis AR (1995) The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany 46, 1285–1291. open url image1

Price GD, Evans JR, von Caemmerer S, Yu J-W, Badger MR (1995) Specific reduction of chloroplast glyceraldehydes-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195, 369–378.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Raines CA (2003) The Calvin cycle revised. Photosynthesis Research 75, 1–10.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Raines CA, Lloyd JC, Dyer TA (1999) New sight into the structure and function of sedoheptulose-1,7-bisphosphatase: an important but neglected Calvin cycle enzyme. Journal of Experimental Botany 50, 1–8.
Crossref | GoogleScholarGoogle Scholar | open url image1

Raines CA, Harrison EP, Olcer H, Lloyd JC (2000) Investigating the role of the thiol-regulated enzyme sedoheptulose-1,7-bisphosphatase in the control of photosynthesis. Physiologia Plantarum 110, 303–308.
Crossref | GoogleScholarGoogle Scholar | open url image1

Rokka A, Zhang L, Aro E-M (2001) Rubisco activase: an enzyme with a temperature-dependent dual function? The Plant Journal 25, 463–471.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Salvucci ME, Portis AR, Ogren WL (1985) A soluble chloroplast protein catalyzes ribulosebisphosphate carboxylase oxygenase activation in vivo (technical note). Photosynthesis Research 7, 193–201.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salvucci ME, Ogren WL (1996) The mechanism of Rubisco activase: insights from studies of the properties and strycture of the enzyme. Photosynthesis Research 47, 1–11.
Crossref | GoogleScholarGoogle Scholar | open url image1

Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant, Cell & Environment 27, 725–735.
Crossref | GoogleScholarGoogle Scholar | open url image1

Seemann JR, Sharkey TD (1986) Salinity and nitrogen effects on photosynthesis, ribulose-1,5-bisphosphatase and metabolite pool size in Phaseolus vulgaris L. Plant Physiology 82, 555–560.
PubMed |
open url image1

Stitt M, Schulze E-D (1994) Does Rubisco control the rate of photosynthesis and plant growth? An exercise in molecular ecophysiology. Plant, Cell & Environment 17, 465–487.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tamoi M, Nagaoka M, Shigeoka S (2005) Immunological properties of sedoheptulose-1,7-bisphosphatase from Chlamydomonas sp.w80. Bioscience, Biotechnology, and Biochemistry 69, 848–851.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Toki S (1997) Rapid and efficient Agrobacterium-mediated transformation in rice. Plant Molecular Biology Reporter 15, 16–21. open url image1

Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown Pima cotton plants at high temperature. Plant, Cell & Environment 27, 717–724.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yamane K, Kawasaki M, Taniguchi M, Miyake H (2003) Differential effect of NaCl and polyethylene glycol on the ultrastructure of chloroplasts in rice seedlings. Journal of Plant Physiology 160, 573–575.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yoshida S , Forno DA , Cook JH , Gomez KA (1976) ‘Laboratory manual for physiological studies of rice.’ 3rd edn. (International Rice Research Institute: Manila, Philippines)

Zhang J, Klueva NY, Wang Z, Wu R, Ho DTH, Nguyen HT (2000) Genetic engineering for abiotic stress resistance in crop plants. Biologia Plantarum 36, 108–114. open url image1

Zhu JK (2001) Plant salt tolerance. Trends in Plant Science 6, 66–71.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ziska LH, Seemann JR, DeJong TM (1990) Salinity induced limitations on photosynthesis in Prunus salicina, a deciduous tree species. Plant Physiology 93, 864–870.
PubMed |
open url image1