Abstract
We investigated the effect of large isoform of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBPCO) activase (RuBPCO-A) on photosynthesis and constructed two plant expression vectors and introduced them into rice cultivars (Oryza sativa f. japonica cv. Nipponbare) through Agrobacterium tumefaciens-mediated transformation. Plasmid pCBrbcSRca contained the cDNA of RuBPCO-A large isoform (rca) controlled by RuBPCO small subunit gene promoter (rbcS), and plasmid pCBUbi-antirca contained a reversed rca sequence driven by maize ubiquitin promoter. Transformants were screened by polymerase chain reaction (PCR), Southern and Western blot analysis. Compared to the control rice plants, RuBPCO activity was improved in the pCBrbcSRca rice plants, which is opposite to RuBPCO activity in the pCBUbi-antirca rice plants. Net photosynthetic rate, quantum yield of electron transport in photosystem 2, and steady state photochemical fluorescence quenching increased in the pCBrbcSRca plants, but decreased in the pCBUbi-antirca plants as compared to the controls. The pCBrbcSRca plants had heavier grains and accelerated development, while the pCBUbi-antirca plants showed reverse changes. Thus RuBPCO-A large isoform exerts considerable effect on photosynthesis and is a promising target for plant breeding to improve rice crop yield.
Similar content being viewed by others
Abbreviations
- ADP:
-
adenosine 5′-diphosphate
- ATP:
-
adenosine 5′-triphosphate
- Car:
-
carotene
- Chl:
-
chlorophyll
- Fv/Fm :
-
maximal photochemical efficiency of PS2
- F′v/F′m :
-
efficiency of excitation energy captured by open PS2 centres
- NADH:
-
reduced nicotinamide adenine dinucleotide
- PCR:
-
polymerase chain reaction
- PEPC:
-
phosphoenolpyruvate carboxylase
- P N :
-
steady state net photosynthetic rate
- PS:
-
photosystem
- qN :
-
proportion of excitation energy dissipated as thermal energy
- qP :
-
proportion of excitation energy captured by PS2 and used in photochemical electron transport
- rbcS:
-
gene for ribulose-1,5-bisphosphate carboxylase/oxygenase small subunit
- RC:
-
reaction centre
- rca:
-
cDNA of ribulose-1,5-bisphosphate carboxylase/oxygenase activase
- RuBP:
-
ribulose-1,5-bisphosphate
- RuBPCO:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase
- RuBPCO-A:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase activase
- Xan:
-
xanthophyll
- Γ:
-
CO2 compensation concentration
- ΦPS2 :
-
quantum yield of electron transport in PS2
References
Arnon, D.I.: Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.-Plant Physiol. 24: 1–15, 1949.
Baker, J.T., Allen, L.H., Jr., Boote, K.J., Jones, P., Jones, J.W.: Developmental responses of rice to photoperiod and carbon dioxide concentration.-Agr. Forest Meteorol. 50: 201–210, 1990.
Bowes, G.: Facing the inevitable: Plants and increasing atmospheric CO2.-Annu. Rev. Plant Physiol. Plant mol. Biol. 44: 309–332, 1993.
Cheng, S.H., Moore, B.D., Seemann, J.R.: Effects of short and long term elevated CO2 on the expression of ribulose-1,5-bisphosphate carboxylase/oxygenase genes and carbohydrate accumulation in leaves of Arabidopsis thaliana (L.) Heynh.-Plant Physiol. 116: 715–723, 1998.
De Nisi, P., Zocchi, G.: Phosphoenolpyruvate carboxylase in cucumber (Cucumis sativus L.) roots under iron deficiency: activity and kinetic characterization.-J. exp. Bot. 51: 1903–1909,2000.
Devanand, P.S., Rangaswamy, M., Ikehashi, H.: Identification of hybrid sterility gene loci in two cytoplasmic male sterile lines in rice.-Crop Sci. 40: 640–646, 2000.
Ditta, G., Stanfield, S., Corbin, D., Helinsnki, D.R.: Broad host range cloning system for gram negative bacteria: construction of gene bank of Rhizobium meliloti.-Proc. nat. Acad. Sci. USA 77: 7374–7351, 1980.
Eckardt, N.A., Snyder, G.W., Portis, A.R., Jr., Ogren, W.L.: Growth and photosynthesis under high and low irradiance of Arabidopsis thaliana antisense mutants with reduced ribulose-1,5-bisphosphate carboxylase/oxygenase activase content.-Plant Physiol. 113: 575–586, 1997.
Genty, B., Briantais, J.-M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.-Biochim. biophys. Acta 990: 87–92, 1989.
Gifford, R.M., Jenkins, C.L.D.: Prospects of applying knowledge of photosynthesis toward improving crop production.-In: Govindjee (ed.): Photosynthesis. Vol. II. Pp. 419–457. Academic Press, New York-London-Paris-San Diego-San Francisco-Sao Paulo-Sydney-Tokyo-Toronto 1982.
Hammond, E.T., Andrews, T.J., Mott, K.A., Woodrow, I.E.: Regulation of Rubisco activation in antisense plants of tobacco containing reduced levels of Rubisco activase.-Plant J. 14: 101–110, 1998.
Hartman, F.C., Harpel, M.R.: Structure, function, regulation, and assembly of D-ribulose-l,5-bisphosphate carboxylase/oxygenase.-Annu. Rev. Biochem. 63: 197–234, 1994.
He, Z., Caemmerer, S. von, Hudson, G.S., Price, G.D., Badger, M.R., Andrews, T.J.: Ribulose-l,5-bisphosphate carboxylase/oxygenase activase deficiency delays senescence of ribulose-1,5-bisphosphate carboxylase/oxygenase but progressively impairs its catalysis during tobacco leaf development.-Plant Physiol. 115: 1569–1580, 1997.
Horton, P.: Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture.-J. exp. Bot. 51: 475–485, 2000.
Ishi, R.: Leaf/canopy photosynthesis and crop productivity.-In: Raghavendra, A.S. (ed.): Photosynthesis: A Comprehensive Treatise. Pp. 215–225. Cambridge University Press, Cambridge 1998.
Jiang, C.Z., Quick, W.P., Aired, R., Kliebenstein, D., Rodermel, S.R.: Antisense RNA inhibition of Rubisco activase expression.-Plant J. 5: 787–798, 1994.
Khoo, G.H., He, J., Hew, C.S.: Photosynthetic utilization of radiant energy by CAM Dendrobium flowers.-Photosynthetica 34: 367–376, 1997.
Khrebtukova, I., Spreitzer, R.J.: Elimination of the Chlamydomonas gene family that encodes the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase.-Proc. nat. Acad. Sci. USA 93: 13689–13693, 1996.
Koch, K.E., Jones, P.H., Avigne, W.T., Allen, L.H., Jr.: Growth, dry matter partitioning, and diurnal activities of RuBP carboxylase in citrus seedlings maintained at two levels of CO2.-Physiol. Plant. 67: 477–484, 1986.
Rostov, R.V., McFadden, B.A.: A sensitive, simultaneous analysis of ribulose 1,5-bisphosphate carboxylase/oxygenase efficiencies: Graphical determination of the CO2/O2 specificity factor.-Photosynth. Res. 43: 57–66, 1995.
Krapp, A., Chaves, M.M., David, M.M., Rodriguez, M.L., Pereira, J.S., Stitt, M.: Decreased ribulose-1,5-bisphosphate carboxylase/oxygenase in transgenic tobacco transformed with “antisense” rbcS. VIII. Impact on photosynthesis and growth in tobacco growing under extreme high irradiance and high temperature.-Plant Cell Environ. 17: 945–953, 1994.
Larson, E.M., O’Brien, CM., Zhu, G., Spreitzer, R.J., Portis, A.R., Jr.: Specificity for activase is changed by a Pro-89 to Arg substitution in the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase.-J. biol. Chem. 272: 17033–17037, 1997.
Liu, Z., Taub, C.C., McClung, C.R.: Identification of an Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase activase (RCA) minimal promoter regulated by light and the circadian clock.-Plant Physiol. 112: 43–51, 1996.
Long, S.P., Drake, B.G.: Photo synthetic CO2 assimilation and rising atmospheric CO2 concentrations.-In Baker N.R., Thomas, H. (ed.): Crop Photosynthesis: Spatial and Temponl Determinants. Pp. 69–103. Elsevier Science Publ., Amsterdam 1992.
Mate, C.J., Hudson, G. S., Caemmerer, S. von, Evans, J.R., Andrews, T.J.: Reduction of ribulose biphosphate carboxylase activase levels in tobacco (Nicotiana tabacum) by antisense RNA reduces ribulose bisphophate carboxylase carbamylation and impairs photosynthesis.-Plant Physiol. 102: 1119–1128, 1993.
Peng, S., Laza, R.C., Visperas, R.M., Sanico A.L., Cassman, K.G., Khush, G.S.: Crop breeding, genetics and cytology. Grain yield of rice cultivars and lines developed in the Philippines since 1966.-Crop Sci. 40: 307–314 2000.
Pich, U., Schubert, I.: Midiprep method for isolation of DNA from plants with a high content of polyphenolics.-Nucleic Acids Res. 21: 3328, 1993.
Portis, A.R., Jr.: Rubisco activase-Rubisco’s catalytic chaperone.-Photosynth. Res. 75: 11–27, 2003.
Quick, W.P., Schurr, U., Fichtner, K., Schulze, E.-D., Rodermel, S.R., Bogorad, L., Stitt, M.: The impact of decreased Rubisco on photosynthesis, growth, allocation and storage in tobacco plants which have been transformed with antisense rbcS.-Plant J. 1: 51–58, 1991.
Rance, I.M., Tian, W.Z., Mathews, H., Kochko, A.D., Beachy, R.N., Fauquet, C: Partial desiccation of mature embryo-derived calluses, a simple treatment that dramatically enhances the regeneration ability of India rice.-Plant Cell Rep. 13: 647–651, 1994.
Robinson, S.P., Portis, A.R., Jr.: Release of the nocturnal inhibitor, carboxyarabinitol-1-phosphate, from ribulose bisphosphate carboxylase/oxygenase by rubisco activase.-FEBS Lett. 233: 413–416, 1988.
Rodermel, S., Haley, J., Jiang, C, Tsai, C, Bogora, L.: A mechanism for intergenomic integration: Abundance of ribulose bisphosphate carboxylase small-subunit protein influences the translation of the large-subunit mRNA.-Proc. nat. Acad. Sci. USA 93: 3881–3885, 1996.
Sambrook, J., Fritsch, E.F., Maniatis, T.: Molecular Cloning-a Laboratory Manual. 2nd Ed.-Pp. 469–490. Cold Spring Harbor Laboratory Publ., Cold Spring Harbor 1989.
Satagopan, S., Spreitzer, R.J.: Substitutions at the Asp-473 latch residue of Chlamydomonas ribulosebisphosphate carboxylase/oxygenase cause decreases in carboxylation efficiency and CO2/O2 specificity.-J. biol. Chem. 279: 14240–14244, 2004.
Somerville, C.R., Portis, A.R., Jr., Ogren, W.L.: A mutant of Arabidopsis thaliana which lacks activation of RuBP carboxylase in vivo.-Plant Physiol. 70: 381–387, 1982.
Spreitzer, R.J.: Questions about the complexity of chloroplast nbulose-1,5-bisphosphate carboxylase/oxygenase.-Photosynth. Res. 60: 29–42, 1999.
Spreitzer, R.J., Thow, G., Zhu, G.H.: Pseudoreversion substitution at large-subunit residue 54 influences the CO2/O2 specificity of chloroplast ribulose-bisphosphate carboxylase/oxygenase.-Plant Physiol. 109: 681–685, 1995.
Stitt, M.: Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells.-Plant Cell Environ. 14: 741–762, 1991.
Stitt, M., Quick, W.P., Schurr, U., Schulze, E.-D., Rodermel, S.R., Bogorad, L.: Decreased ribulose-1,5-bisphosphate carboxylase-oxygenase in transgenic tobacco transformed with ‘antisense’ rbcS. II. Flux-control coefficients tor photosynthesis in varying light, CO2, and air humidity.-Planta 183: 555–566, 1991.
Tenhunen, J.D., Lange, O.L., Gebel, J., Beyschlag, W., Weber, J.A.: Changes in photosynthetic capacity, carboxylation efficiency and CO2 compensation point associated with midday stomatal closure and midday depression of net CO2 exchange in leaves of Quercus suber.-Planta 193: 193–203, 1984.
van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology.-Photosynth. Res. 25: 147–150, 1990.
Xu, D.Q., Shen, Y.K.: Photosynthetic efficiency and crop yield.-In: Pessarakli, M. (ed): The Handbook of Plant and Crop Physiology. 2nd Ed. Pp. 821–834. M. Dekker Publ., New York 2001.
Yuan, L.P., Yang, Z.Y., Yang, J.B.: Hybrid rice technology: New developments and future prospects.-In: Virmani, S.S. (ed.): Hybrid Rice in China. Pp. 143–147. IRRI Publ., Manila 1994.
Werneke, J.W., Chatfield, J.M., Ogren, W.L.: Alternative mRNA splicing generates the two ribulosebisphosphate carboxylase/oxygenase activase polypeptides in spinach and Arabidopsis.-Plant Cell 1: 815–825, 1989.
Wittwer, S.H.: Food, Climate and Carbon Dioxide: The Global Environment and World Food Production.-Lewis Publ., New York 1995.
Zhang, N, Kallis, R.P., Ewy, R.G., Potis, A.R., Jr.: Light modulation of Rubisco in Arabidopsis requires a capacity for redox regulation of the larger Rubisco activase isoform.-Proc. nat. Acad. Sci. USA 99: 3330–3334, 2002.
Zhang, N, Potis, A.R., Jr.: Mechanism of light regulation of Rubisco: A specific role for the larger Rubisco activase isonat. Acad. Sci. USA 96: 9438–9443, 1999.
Zhang, Z.L., Komatsu, S.: Molecular cloning and characterization of cDNAs encoding two isoforms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase in rice (Oryza sativa L.).-J. Biochem. 128: 383–389, 2000.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wu, H.R., Li, L.B., Jing, Y.X. et al. Over-and anti-sense expressions of the large isoform of ribulose-1,5-bisphosphate carboxylase/oxygenase activase gene in Oryza sativa affect the photosynthetic capacity. Photosynthetica 45, 194–201 (2007). https://doi.org/10.1007/s11099-007-0032-2
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11099-007-0032-2