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Enhancing photosynthetic CO2 use efficiency in rice: approaches and challenges

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Abstract

It is estimated that 925 million people mainly in developing countries suffer from malnutrition due to food shortage. This situation will deteriorate as world population will reach 9 billion by 2050. It is obvious that current rate of increase in crop yields is not sufficient to solve the problem of food security worldwide, especially in Asia, where at least 50 % increase in rice yield is needed to satisfy the increasing population. Depending on advanced development of modern biotechnology, several strategies have been provided for ‘supercharging’ photosynthesis to increase rice yield. In this review, we updated four major approaches: namely improving the performance of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco), establishment of photorespiratory bypass, installing single-cell and two-celled C4 photosynthesis. The first approach aimed at direct manipulation of Rubisco for more efficient catalytic character by directed molecular evolution. The second approach focused on reducing the loss of photorespiratory CO2 by direct manipulation of photorespiratory pathway. The last two concentrated on introduction of C4 pathway into rice, based on the observation that the efficiency of C4 photosynthesis is 50 % higher than that of C3 photosynthesis.

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Abbreviations

2-PG:

2-Phosphoglycolate

3-PGA:

3-Phosphoglycerate

BS:

Bundle sheath

CA:

Carbonic anhydrase

GCL:

Glyoxylate carboligase

GDC:

Glycine decarboxylase

GDH:

Glycolate dehydrogenase

GO:

Glycolate oxidase

HI:

Harvest index

MS:

Mesophyll

NADP-ME:

NADP-malic enzyme

NADP-MDH:

NADP-malate dehydrogenase

OAA:

Oxaloacetate

PEPC:

Phosphoenolpyruvate carboxylase

PEPCK:

Phosphoenolpyruvate carboxykinase

PPDK:

Pyruvate, orthophosphate dikinase

Rubisco:

Ribulose 1,5-bisphosphate carboxylase/oxygenase

RuBP:

Ribulose 1,5-bisphosphate

RUE:

Photosynthetically active radiation use efficiency

TSR:

Tartronic semialdehyde reductase

References

  • Akyildiz M, Gowik U, Engelmann S, Koczor M, Streubel M, Westhoff P (2007) Evolution and function of a cis-regulatory module for mesophyll-specific gene expression in the C4 dicot Flaveria trinervia. Plant Cell 19:3391–3402

    Article  CAS  PubMed  Google Scholar 

  • Aloni R (1987) Differentiation of vascular tissues. Annu Rev Plant Physiol 38:179–204

    Article  Google Scholar 

  • Alonso H, Blayney MJ, Beck JL, Whitney SM (2009) Substrate-induced assembly of Methanococcoides burtonii d-ribulose-1,5-bisphosphate carboxylase/oxygenase dimers into decamers. J Biol Chem 284:33876–33882

    Article  CAS  PubMed  Google Scholar 

  • Anderson LE (1971) Chloroplast and cytoplasmic enzymes II. Pea leaf triose phosphate isomerases. Biochim Biophys Acta 235:237–244

    Article  CAS  PubMed  Google Scholar 

  • Andersson I (2008) Catalysis and regulation in Rubisco. J Exp Bot 59:1555–1568

    Article  CAS  PubMed  Google Scholar 

  • Aubry S, Brown NJ, Hibberd JM (2011) The role of proteins in C3 plants prior to their recruitment into the C4 pathway. J Exp Bot 62:3049–3059

    Article  CAS  PubMed  Google Scholar 

  • Bainbridge G, Madgwick P, Parmar S, Mitchell R, Paul M, Pitts J, Keys AJ, Parry MAJ (1995) Engineering Rubisco to change its catalytic properties. J Exp Bot 46:1269–1276

    Article  CAS  Google Scholar 

  • Bandyopadhyay A, Datta K, Zhang J, Yang W, Raychaudhuri S, Miyao M, Dattaa SK (2007) Enhanced photosynthesis rate in genetically engineered indica rice expressing pepc gene cloned from maize. Plant Sci 172:1204–1209

    Article  CAS  Google Scholar 

  • Barnola JM, Raynaud D, Lorius C, Barkov N (1999) Historical CO2 record from the Vostok ice core. In trends: a compendium of data on global change, Carbon Dioxide Information Analysis Center, U.S. Department of Energy. http://cdiac.ornl.gov/trends/co2/vostok.html

  • Bauwe H (2011) Photorespiration: the bridge to C4 photosynthesis. In: Raghavendra AS, Sage RF (eds) C4 Photosynthesis and related CO2 concentrating mechanisms. Advances in photosynthesis and respiration, vol 32. Springer, Dordrecht, pp 81–108

  • Berleth T, Scarpella E, Prusinkiewicz P (2007) Towards the systems biology of auxin-transport-mediated patterning. Trends Plant Sci 12:151–159

    Article  CAS  PubMed  Google Scholar 

  • Bowes G, Rao SK, Estavillo GM, Reiskind JB (2002) C4 mechanisms in aquatic angiosperms: comparisons with terrestrial C4 systems. Funct Plant Biol 29:379–392

    Article  CAS  Google Scholar 

  • Brown NJ, Newell CA, Stanley S, Chen JE, Perrin AJ, Kajala K, Hibberd JM (2011) Independent and parallel recruitment of preexisting mechanisms underlying C4 photosynthesis. Science 331:1436–1439

    Article  CAS  PubMed  Google Scholar 

  • Christin PA, Besnard G (2009) Two independent C4 origins in Aristidoideae (Poaceae) revealed by the recruitment of distinct phosphoenolpyruvate carboxylase genes. Am J Bot 96:2234–2239

    Article  CAS  PubMed  Google Scholar 

  • Christin PA, Salamin N, Savolainen V, Duvall MR, Besnard G (2007) C4 photosynthesis evolved in grasses via parallel adaptive genetic changes. Curr Biol 17:1241–1247

    Article  CAS  PubMed  Google Scholar 

  • Christin PA, Salamin N, Muasya AM, Roalson EH, Russier F, Besnard G (2008) Evolutionary switch and genetic convergence on rbcL following the evolution of C photosynthesis. Mol Biol Evol 25:2361–2368

    Article  CAS  PubMed  Google Scholar 

  • Christin PA, Salamin N, Kellogg EA, Vicentini A, Besnard G (2009) Integrating phylogeny into studies of C4 variation in the grasses. Plant Physiol 149:82–87

    Article  CAS  PubMed  Google Scholar 

  • Cousins AB, Adam NR, Wall GW, Kimball BA, Pinter PJ Jr, Ottman MJ, Leavitt SW, Webber AN (2003) Development of C4 photosynthesis in sorghum leaves grown under free-air CO2 enrichment (FACE). J Exp Bot 54:1969–1975

    Article  CAS  PubMed  Google Scholar 

  • Donner TJ, Sherr I, Scarpella E (2009) Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136:3235–3246

    Article  CAS  PubMed  Google Scholar 

  • Engelmann S, Blasing OE, Gowik U, Svensson P, Westhoff P (2003) Molecular evolution of C4 phosphoenolpyruvate carboxylase in the genus Flaveria—a gradual increase from C3 to C4 characteristics. Planta 217:717–725

    Article  CAS  PubMed  Google Scholar 

  • Fukayama H, Imanari E, Tsuchida H, lzui K, Maysuoka M, Miyao TM (2000) In vivo activity of maize phosphoenolpyruvate carboxylase in transgenic rice plant. Plant Cell Physiol 41:S112

    Google Scholar 

  • Fukayama H, Tsuchida H, Agarie S, Nomura M, Onodera H (2001) Significant accumulation of C4-specific pyruvate, orthophosphate dikinase in a C3 plant, rice. Plant Physiol 127:1136–1146

    Article  CAS  PubMed  Google Scholar 

  • Fukayama H, Hatch MD, Tamai T, Tsuchida H, Sudoh S, Furbank RT, Miyao M (2003) Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants. Photosynth Res 77:227–239

    Article  CAS  PubMed  Google Scholar 

  • Greene DN, Whitney SM, Matsumura I (2007) Artificially evolved Synechococcus PCC6301 Rubisco variants exhibit improvements in folding and catalytic efficiency. Biochem J 404:517–524

    Article  CAS  PubMed  Google Scholar 

  • Hatch MD (1987) C4 photosynthesis: a unique blend of modified biochemistry, anatomy and ultrastructure. Biochim Biophys Acta 895:81–106

    Article  CAS  Google Scholar 

  • Hibberd JM, Covshoff S (2010) The regulation of gene expression required for C4 photosynthesis. Annu Rev Plant Biol 61:181–207

    Article  CAS  PubMed  Google Scholar 

  • Hibberd JM, Sheehy JE, Langdale JA (2008) Using C4 photosynthesis to increase the yield of rice—rationale and feasibility. Curr Opin Plant Bio 11:228–231

    Article  CAS  Google Scholar 

  • Jiao DM, Hang XQ, Chi W, Kuang TY, Ku MSB (2001) The characteristics of CO2 assimilation of photosynthesis and chlorophyll fluorescence in transgenic PEPC rice. Chin Sci Bull 46:414–418

    Google Scholar 

  • Jiao DM, Huang XQ, Li X, Chi W, Kuang TY, Zhang QD, Ku MSB, Chao DG (2002) Photosynthetic characteristics and tolerance to photooxidation of transgenic rice expressing C4 photosynthesis enzymes. Photosynth Res 72:85–93

    Article  CAS  PubMed  Google Scholar 

  • Kajala K, Covshoff S, Karki S, Woodfield H, Tolley BJ, Dionora MJA, Mogul RT, Mabilangan AE, Danila FR, Hibberd JM, Quick WP (2011) Strategies for engineering a two-celled C4 photosynthetic pathway into rice. J Exp Bot 62:3001–3010

    Article  CAS  PubMed  Google Scholar 

  • Kebeish R, Niessen M, Thiruveedhi K, Bari R, Hirsch HJ, Rosenkranz R, Stäbler N, Schönfeld B, Kreuzaler F, Peterhänsel C (2007) Chloroplastic photorespiratory bypass increases photosynthesis and biomass production in Arabidopsis thaliana. Nat Biotechnol 25:593–599

    Google Scholar 

  • King JL, Edwards GE, Cousins AB (2012) The efficiency of the CO2-concentrating mechanism during single-cell C4 photosynthesis. Plant Cell Environ 35:513–523

    Article  CAS  PubMed  Google Scholar 

  • Kurek I, Chang TK, Bertain SM, Madrigal A, Liu L, Lassner MW, Zhu G (2007) Enhanced thermostability of Arabidopsis Rubisco activase improves photosynthesis and growth rates under moderate heat stress. Plant Cell 19:3230–3241

    Article  CAS  PubMed  Google Scholar 

  • Langdale JA, Zelitch I, Miller E, Nelson T (1988) Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J 7:3643–3651

    CAS  PubMed  Google Scholar 

  • Langdale JA, Nelson T (1991) Spatial regulation of photosynthetic development in C4 plants. Trends Genet 7:191–196

    Google Scholar 

  • Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330

    Article  CAS  PubMed  Google Scholar 

  • Ludwig M (2011) The molecular evolution of β-carbonic anhydrase in Flaveria. J Exp Bot 62:3071–3081

    Article  CAS  PubMed  Google Scholar 

  • Marshall DM, Muhaida R, Brown NJ, Liu Z, Stanley S, Griffiths H, Sage RF, Hibberd JM (2007) Cleome, a genus closely related to Arabidopsis, contains species spanning a developmental progression from C3 to C4 photosynthesis. Plant J 51:886–896

    Article  CAS  PubMed  Google Scholar 

  • Mattsson J, Sung ZR, Berleth T (1999) Responses of plant vascular systems to auxin transport inhibition. Development 126:2979–2991

    CAS  PubMed  Google Scholar 

  • McKown AD, Dengler NG (2007) Key innovations in the evolution of Kranz anatomy and C4 vein pattern in Flaveria (Asteraceae). Am J Bot 94:382–399

    Article  PubMed  Google Scholar 

  • Mitchell PL, Sheehy JE (2006) Supercharging rice photosynthesis to increase yield. New Phytol 171:688–693

    Article  CAS  PubMed  Google Scholar 

  • Miyao M, Masumoto C, Miyazawa S, Fukayama H (2011) Lessons from engineering a single-cell C4 photosynthetic pathway into rice. J Exp Bot 62:3021–3029

    Article  CAS  PubMed  Google Scholar 

  • Muhaidat R, Sage TL, Frohlich MW, Dengler NG, Sage RF (2011) Characterization of C3-C4 intermediate species in the genus Heliotropium L. (Boraginaceae): anatomy, ultrastructure and enzyme activity. Plant Cell Environ 34(10):1723–1736

    Google Scholar 

  • Nelson T, Dengler NG (1997) Leaf vascular pattern formation. Plant Cell 9:1121–1135

    Article  CAS  PubMed  Google Scholar 

  • Parry MAJ, Madgwick PJ, Carvalho JFC, Andralojc PJ (2007) Prospects for increasing photosynthesis by overcoming the limitations of Rubisco. J Agric Sci 145:31–43

    Article  CAS  Google Scholar 

  • Peterhansel C, Maurino VG (2011) Photorespiration redesigned. Plant Physiol 155:49–55

    Article  CAS  PubMed  Google Scholar 

  • Peterhansel C, Horst I, Niessen M, Blume C, Kebeish R, Kurkcuoglu S, Kreuzaler F (2010) Photorespiration. The Arabidopsis book. American Society of Plant Biologists, Rockville. doi:10.1199/tab.0130

  • Portis AR, Li CS, Wang DF, Salvucci ME (2008) Regulation of Rubisco activase and its interaction with Rubisco. J Exp Bot 59:1597–1604

    Article  CAS  PubMed  Google Scholar 

  • Rao SK, Fukayama H, Reiskind JB, Miyao M, Bowes G (2006) Identification of C4 responsive genes in the facultative C4 plant Hydrilla verticillata. Photosynth Res 88:173–183

    Article  CAS  PubMed  Google Scholar 

  • Rolland-Lagan AG, Prusinkiewicz P (2005) Reviewing models of auxin canalization in the context of leaf vein pattern formation in Arabidopsis. Plant J 44:854–865

    Article  CAS  PubMed  Google Scholar 

  • Rondeau P, Rouch C, Besnard G (2005) NADP-malate dehydrogenase gene evolution in Andropogoneae (Poaceae): gene duplication followed by sub-functionalization. Ann Bot 96:1307–1314

    Article  CAS  PubMed  Google Scholar 

  • Sachs T (1981) The control of the patterned differentiation of vascular tissues. Adv Bot Res 9:152–262

    Google Scholar 

  • Sage RF, Sage TL (2008) Learning from nature to develop strategies for the directed evolution of C4 rice. In: Sheehy JE, Mitchell PL, Hardy B (eds) Charting new pathways to C4 rice. World Scientific Publishing Co. Pte, Ltd., Singapore, pp 195–216

    Chapter  Google Scholar 

  • Sage TL, Sage RF, Vogen PJ, Rahman B, Johnson DC, Oakley JC, Heckel MA (2011a) The occurrence of C2 photosynthesis in Euphorbia subgenus Chamaesyce (Euphorbiaceae). J Exp Bot 62:3183–3195

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Christin PA, Edwards EJ (2011b) The C4 plant lineages of planet Earth. J Exp Bot 62:3155–3169

    Article  CAS  PubMed  Google Scholar 

  • Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Annu Rev Plant Biol 63:19–47

    Article  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  CAS  PubMed  Google Scholar 

  • Sharwood RE, von Caemmerer S, Maliga P, Whitney SM (2008) The catalytic properties of hybrid Rubisco comprising tobacco small and sunflower large subunits mirror the kinetically equivalent source Rubiscos and can support tobacco growth. Plant Physiol 146:83–96

    Article  CAS  PubMed  Google Scholar 

  • Sheehy JE, Mitchell PL (2011) Rice and global food security: the race between scientific discovery and catastrophe. In: Pasternak C (ed) Access not excess. The search for better nutrition, Smith-Gordon and Company, Cambs, pp 81–90

  • Sieburth LE (1999) Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol 121:1179–1190

    Article  CAS  PubMed  Google Scholar 

  • Taniguchi Y, Ohkawa H, Masumoto C, Fukuda T, Tamai T, Lee K, Sudoh S, Tsuchida H, Sasaki H, Fukayama H, Miyao M (2008) Overproduction of C4 photosynthetic enzymes in transgenic rice plants: an approach to introduce the C4-like photosynthetic pathway into rice. J Exp Bot 59:1799–1809

    Article  CAS  PubMed  Google Scholar 

  • Tsuchida H, Tamai T, Agarie S, Nomura M, Onodera H, Toki S, Ku MSB, Matsuoka M, Miyao M (2001) High level expression of C4-specific NADP-malic enzyme in leaves and impairment of photoautotrophic growth of a C3 plant, rice. Plant Cell Physiol 42:138–145

    Article  CAS  PubMed  Google Scholar 

  • Uhl D, Mosbrugger V (1999) Leaf venation density as a climate and environmental proxy: a critical review and new data. Palaeogeogr Palaeocl 149:15–26

    Article  Google Scholar 

  • Wang J, Li R (2008) Integration of C4-specific ppdk gene of Echinochloa to C3 upland rice and its photosynthesis characteristics analysis. Afr J Biotechnol 7:783–787

    CAS  Google Scholar 

  • Wang XY, Gowik U, Tang HB, Bowers JE, Westhoff P, Paterson AH (2009) Comparative genomic analysis of C4 photosynthetic pathway evolution in grasses. Genome Biol 10:R68

    Article  PubMed  Google Scholar 

  • Whitney SM, Andrews TJ (2001) Plastome-encoded bacterial ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) supports photosynthesis and growth in tobacco. Proc Natl Acad Sci USA 98:14738–14743

    Article  CAS  PubMed  Google Scholar 

  • Whitney SM, Houtz RL, Alonso H (2011) Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiol 155:27–35

    Article  CAS  PubMed  Google Scholar 

  • Xie XJ, Shen SHH, Li YX, Zhao XY, Li BB, Xu DF (2011) Effect of photosynthetic characteristic and dry matter accumulation of rice under high temperature at heading stage. Afr J Agric Res 6:1931–1940

    Google Scholar 

  • Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP (2009) High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiol 149:195–204

    Article  CAS  PubMed  Google Scholar 

  • Zhu XG, Portis AR Jr, Long SP (2004) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165

    Article  CAS  Google Scholar 

  • Zhu G, Kurek I, Liu L (2010a) Engineering photosynthetic enzymes involved in CO2-assimilation by gene shuffling. In: Govindjee (ed) The chloroplast: advances in photosynthesis and respiration, vol 31. Springer, Amsterdam, pp 307–322

  • Zhu XG, Long SP, Ort DR (2010b) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the Scientific Research Foundation for the Returned Overseas Chinese Scholars by State Education Ministry of P. R. China (No. 2011-1139) and the Talent Introduction Project of Hebei University (No. 2010-185) for funding.

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The authors declare that they have no conflict of interest.

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Correspondence to Zheng Liu.

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Communicated by A. K. Kononowicz.

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Liu, Z., Sun, N. Enhancing photosynthetic CO2 use efficiency in rice: approaches and challenges. Acta Physiol Plant 35, 1001–1009 (2013). https://doi.org/10.1007/s11738-012-1171-z

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