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

C4 rice: a challenge for plant phenomics

Robert T. Furbank A E , Susanne von Caemmerer B , John Sheehy C and Gerry Edwards D
+ Author Affiliations
- Author Affiliations

A CSIRO Plant Industry and High Resolution Plant Phenomics Centre, GPO Box 1600, Canberra, ACT 2601, Australia.

B Research School of Biology, Australian National University, GPO Box 475, Canberra, ACT 2601, Australia.

C International Rice Research Institute, DAPO Box 7777, Metro Manila, Philippines.

D School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA.

E Corresponding author. Email: robert.furbank@csiro.au

This paper originates from a presentation at the 1st International Plant Phenomics Symposium, Canberra, Australia, April 2009.

Functional Plant Biology 36(11) 845-856 https://doi.org/10.1071/FP09185
Submitted: 21 July 2009  Accepted: 15 September 2009   Published: 5 November 2009

Abstract

There is now strong evidence that yield potential in rice (Oryza sativa L.) is becoming limited by ‘source’ capacity, i.e. photosynthetic capacity or efficiency, and hence the ability to fill the large number of grain ‘sinks’ produced in modern varieties. One solution to this problem is to introduce a more efficient, higher capacity photosynthetic mechanism to rice, the C4 pathway. A major challenge is identifying and engineering the genes necessary to install C4 photosynthesis in rice. Recently, an international research consortium was established to achieve this aim. Central to the aims of this project is phenotyping large populations of rice and sorghum (Sorghum bicolor L.) mutants for ‘C4-ness’ to identify C3 plants that have acquired C4 characteristics or revertant C4 plants that have lost them. This paper describes a variety of plant phenomics approaches to identify these plants and the genes responsible, based on our detailed physiological knowledge of C4 photosynthesis. Strategies to asses the physiological effects of the installation of components of the C4 pathway in rice are also presented.

Additional keywords: carbon isotope discrimination, chlorophyll fluorescence, CO2 compensation point, Kranz anatomy, photosynthesis, photosynthetic efficiency.


Acknowledgements

The authors thank Abigail Elmido-Mabilangan (International Rice Research Institute) and Rosemary White (CSIRO Plant Industry) for the generation of the micrographs of rice and maize shown in this publication. We also acknowledge the support of the Bill and Melinda Gates Foundation-funded C4 rice program, International Rice Research Institute and the contributions of the associated international consortium members.


References


Badger MR (1985) Photosynthetic oxygen-exchange. Annual Review of Plant Physiology and Plant Molecular Biology 36, 27–53.
CrossRef | CAS | open url image1

Badger MR, von Caemmerer S, Ruuska S, Nakano H (2000) Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1433–1446.
CrossRef | CAS | PubMed | open url image1

Baker N (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
CrossRef | CAS | PubMed | open url image1

Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 130, 1992–1998.
CrossRef | CAS | PubMed | open url image1

Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light. Planta 165, 397–406.
CrossRef | CAS | open url image1

Cannell RQ, Bruns WA, Moss DN (1969) A search for high net photosynthetic rate among soybean genotypes. Crop Science 9, 840–841. open url image1

Chonan N, Kaneko M, Kawahara H, Matsuda T (1981) Ultrastructure of the large vascular bundles of the rice plant. Nihon Sakumotsu Gakkai Kiji 50, 323–331. open url image1

Cousins AB, Badger MR, Von Caemmerer S (2006) Carbonic anhydrase and its influence on carbon isotope discrimination during C4 photosynthesis: insights from antisense RNA in Flaveria bidentis. Plant Physiology 141, 232–242.
CrossRef | CAS | PubMed | open url image1

Delgado E, Azcon-Bieto J, Aranda X, Palazon J, Medrano H (1992) Leaf photosynthesis and respiration of high CO2-grown tobacco plants selected for survival under CO2 compensation point conditions. Plant Physiology 98, 949–954.
CrossRef | CAS | PubMed | open url image1

Delgado E, Parry MAJ, Lawlor DW, Keys AJ, Medrano H (1993) Photosynthesis, ribulose-1,5-bisphosphate carboxylase and leaf characteristics of Nicotiana tabacum L. genotypes selected by survival at low CO2 concentrations. Journal of Experimental Botany 44, 1–7.
CrossRef | CAS | open url image1

Dever LV, Blackwell RD, Fullwood NJ, Lacuesta M, Leegood RC, Onek LA, Pearson M, Lea PJ (1995) The isolation and characterization of mutants of the C4 photosynthetic pathway. Journal of Experimental Botany 46, 1363–1376.
CAS |
open url image1

Earl HJ, Tollenaar M (1998) Relationship between thylakoid electron transport and photosynthetic CO2 uptake in leaves of three maize (Zea mays L.) hybrids. Photosynthesis Research 58, 245–257.
CrossRef | CAS | open url image1

Edwards GE, Baker NR (1993) Can CO2 assimilation in maize leaves be predicted accurately from chlorophyll fluorescence analysis? Photosynthesis Research 37, 89–102.
CrossRef | CAS | open url image1

Edwards GE, Furbank RT, Hatch MD, Osmond CB (2001) What does it take to be C4? Lessons from the evolution of C4 photosynthesis. Plant Physiology 125, 46–49.
CrossRef | CAS | PubMed | open url image1

Edwards GE, Franceschi VR, Voznesenskaya EV (2004) Single-cell C4 photosynthesis versus the dual-cell (Kranz) paradigm. Annual Review of Plant Biology 55, 173–196.
CrossRef | CAS | PubMed | open url image1

Evans LT, Fischer RA (1999) Yield potential: its definition, measurement, and significance. Crop Science 39, 1544–1551. open url image1

Evans JR, Sharkey TD, Berry JA, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas-exchange to investigate CO2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281–292.
CrossRef | CAS | open url image1

Farquhar GD (1983) On the nature of carbon isotope discrimination in C4 species. Australian Journal of Plant Physiology 10, 205–226.
CrossRef | CAS | open url image1

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical-model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
CrossRef | CAS | open url image1

Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon isotope discrimination and the intercellular carbon-dioxide concentration in leaves. Australian Journal of Plant Physiology 9, 121–137.
CrossRef | CAS | open url image1

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
CrossRef | CAS | open url image1

Food and Agricultural Organisation of the United Nations Food Security Statistics (2008) Food and agricultural statistics global outlook. Food and Agricultural Organisation of the United Nations. Available at http://faostat.fao.org/Portals/_Faostat/documents/pdf/world.pdf [Verified 7 October 2009]

Furbank RT, Badger MR (1982) Photosynthetic oxygen-exchange in attached leaves of C4 monocotyledons. Australian Journal of Plant Physiology 9, 553–558.
CrossRef | CAS | open url image1

Furbank RT, Walker DA (1986) Chlorophyll a fluorescence as a quantitative probe of photosynthesis: effects of CO2 concentration during gas transients on chlorophyll fluorescence in spinach leaves. New Phytologist 104, 207–213.
CrossRef | CAS | open url image1

Furbank RT, Chitty JA, Jenkins CLD, Taylor WC, Trevanion SJ, von Caemmerer S, Ashton AR (1997) Genetic manipulation of key photosynthetic enzymes in the C4 plant Flaveria bidentis. Australian Journal of Plant Physiology 24, 477–485.
CrossRef | CAS | open url image1

Galmes J, Flexas J, Keys AJ, Cifre J, Mitchell RAC, Madgwick PJ, Haslam RP, Medrano H, Parry MAJ (2005) Rubisco specificity factor tends to be larger in plant species from drier habitats and in species with persistent leaves. Plant, Cell & Environment 28, 571–579.
CrossRef | CAS | open url image1

Genty B, Briantais J-M, Baker N (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta 990, 87–92.
CAS |
open url image1

Ghannoum O, Siebke K, Von Caemmerer S, Conroy JP (1998) The photosynthesis of young Panicum C-4 leaves is not C-3-like. Plant, Cell & Environment 21, 1123–1131.
CrossRef | CAS | open url image1

Gunning BES (2007) ‘Plant cell biology.’ (CD-ROM). Available from http://www.plantcellbiologyondvd.com/

Hattersley PW, Watson L (1975) Anatomical parameters for predicting photosynthetic pathways of grass leaves: the ‘maximal lateral cell count’ and the ‘maximum cells distant count’. Phytomorphology 25, 325–333. open url image1

Henderson S, von Caemmerer S, Farquhar GD (1992) Short-term measurements of carbon isotope discrimination in several C4 species. Australian Journal of Plant Physiology 19, 263–285.
CrossRef | CAS | open url image1

Holaday AS, Chollet R (1983) Photosynthetic/photorespiratory carbon metabolism in the C3–C4 intermediate species, Moricandia arvensis and Panicum milioides. Plant Physiology 73, 740–745.
CrossRef | CAS | PubMed | open url image1

Janacek SH, Trenkamp S, Palmer B, Brown NJ, Parsley K , et al. (2009) Photosynthesis in cells around veins of the C3 plant Arabidopsis thaliana is important for both the shikimate pathway and leaf senescence as well as contributing to plant fitness. The Plant Journal 59, 329–343.
CrossRef | CAS | PubMed | open url image1

Jordan DB, Ogren WL (1984) The CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase. Planta 161, 308–313.
CrossRef | CAS | open url image1

Krall JP, Edwards GE, Ku MSB (1991) Quantum yield of photosystem II and efficiency of CO2 fixation in Flaveria (Asteraceae) species under varying light and CO2. Australian Journal of Plant Physiology 18, 369–383.
CrossRef | CAS | open url image1

Krishnan A, Guideroni E, An G, Hsing YC, Han C , et al. (2009) Mutant resources in rice for functional genomics of the grasses. Plant Physiology 149, 165–170.
CrossRef | CAS | PubMed | open url image1

Ku MSB, Wu JR, Dai ZY, Scott RA, Chu C, Edwards GE (1991) Photosynthetic and photorespiratory characteristics of Flaveria species. Plant Physiology 96, 518–528.
CrossRef | CAS | PubMed | open url image1

Laisk AK (1977) ‘Kinetics of photosynthesis and photorespiration in C3-plants.’ (Nauka: Moscow)

Laisk A, Edwards GE (1998) Oxygen and electron flow in C4 photosynthesis – mehler reaction, photorespiration and CO2 concentration in the bundle sheath. Planta 205, 632–645.
CrossRef | CAS | open url image1

Leegood RC (2000) Transport during C4 photosynthesis. In ‘Photosynthesis: physiology and metabolism’. (Eds RC Leegood, TD Sharkey, S von Caemmerer) pp. 459–469 (Kluwer Academic Publishers: The Netherlands)

Leegood RC (2002) C4 photosynthesis: principles of CO2 concentration and prospects for introduction into C3 plants. Journal of Experimental Botany 53, 581–590.
CrossRef | CAS | PubMed | open url image1

Leegood RC (2008) Roles of bundle sheath cells in leaves of C3 plants. Journal of Experimental Botany 59, 1663–1673.
CrossRef | CAS | PubMed | open url image1

Manning DT, Campbell AJ, Chen TM, Tolbert NE, Smith EW (1984) Detection of chemicals inhibiting photorespiratory senescence in a large scale survival chamber. Plant Physiology 76, 1060–1064.
CrossRef | CAS | PubMed | open url image1

Mayne BC, Dee AM, Edwards GE (1975) Photosynthesis in mesophyll protoplasts and bundle sheath cells of various type of C4 plants. III. Fluorescence emission spectra, delayed light emission, and P700 content. Zeitschrift Pflanzenphysiology 74, 275–291. open url image1

Menz KM, Moss DN, Cannell RQ, Brun WA (1969) Screening for photosynthetic efficiency. Crop Science 9, 692–694. open url image1

Nasyrov YS (1978) Genetic control of photosynthesis and improving of crop productivity. Annual Review of Plant Biology 29, 215–237.
CAS |
open url image1

Nelson T, Dengler NG (1992) Photosynthetic tissue differentiation in C4 plants. International Journal of Plant Physiology 153, 93–105. open url image1

Oberhuber W, Edwards GE (1993) Temperature dependence of the linkage of quantum yield of photosystem II to CO2 fixation in C4 and C3 plants. Plant Physiology 101, 507–512.
CAS | PubMed |
open url image1

O’Leary MH (1981) Carbon isotope fractionations in plants. Phytochemistry 20, 553–567.
CrossRef | CAS | open url image1

Parry MAJ, Andralojc PJ, Mitchell RAC, Madgwick PJ, Keys AJ (2003) Manipulation of Rubisco: the amount, activity, function and regulation. Journal of Experimental Botany 54, 1321–1333.
CrossRef | CAS | PubMed | open url image1

Peisker M (1979) Conditions of low, and oxygen-independent, CO2 compensation concentrations in C4 plants as derived from a simple model. Photosynthetica 13, 198–207.
CAS |
open url image1

Peng S, Khush GS, Virk P, Tang Q, Zou Y (2008) Progress in ideotype breeding to increase rice yield potential. Field Crops Research 108, 32–38.
CrossRef | open url image1

Pfundel E, Neubohn B (1999) Assessing photosystem I and II distribution in leaves from C4 plants using confocal laser scanning microscopy. Plant, Cell & Environment 22, 1569–1577.
CrossRef | CAS | open url image1

Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. Journal of Experimental Botany 51, 357–368.
CrossRef | CAS | PubMed | open url image1

Sage RF (2004) The evolution of C4 photosynthesis. The New Phytologist 161, 341–370.
CrossRef | CAS | open url image1

Sage TL, Sage RF (2009) The functional anatomy of rice leaves: implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant & Cell Physiology 50, 756–772.
CrossRef | CAS | PubMed | open url image1

Sheehy JE, Dionora MJA, Mitchell PL (2001) Spikelet numbers, sink size and potential yield in rice. Field Crops Research 71, 77–85.
CrossRef | open url image1

Sheehy JE , Ferrer AB , Mitchell PL , Elmido-Mabilangan A , Pablico P , Dionora MJA (2007 a) How the rice crop works and why it needs a new engine. In ‘Charting new pathways to C4 rice’. (Eds JE Sheehy, PL Mitchell, B Hardy) pp. 27–36. (International Rice Research Institute: Los Banos, Philippines)

Sheehy JE , Mitchell PL , Hardy B (Eds) (2007 b) ‘Charting new pathways to C4 rice.’ (International Rice Research Institute: Los Banos, Philippines)

Smith EW, Tolbert NE, Ku HS (1976) Variables affecting the CO2 compensation point. Plant Physiology 58, 143–146.
CrossRef | CAS | PubMed | open url image1

Vogan PJ, Frohlich MW, Sage RF (2007) The functional significance of C3–C4 intermediate traits in Heliotropium L. (Boraginaceae): gas exchange perspectives. Plant, Cell & Environment 30, 1337–1345.
CrossRef | CAS | PubMed | open url image1

von Caemmerer S (1989) A model of photosynthetic CO2 assimilation and carbon isotope discrimination in leaves of certain C3–C4 intermediate species. Planta 178, 463–474.
CrossRef | CAS | open url image1

von Caemmerer S (1992) Carbon isotope discrimination in C3–C4 intermediates. Plant, Cell & Environment 15, 1063–1072.
CrossRef | CAS | open url image1

von Caemmerer S , Furbank RT (1999) Modeling of C4 photosynthesis. In ‘C4 plant biology’. (Eds RF Sage and R Monson) pp. 169–207. (Academic Press: San Diego, CA)

von Caemmerer S (2000) ‘Biochemical models of leaf photosynthesis. Vol. 2.’ (CSIRO Publishing: Collingwood, Australia)

von Caemmerer S, Evans JR (1991) Determination of the average partial-pressure of CO2 in chloroplasts from leaves of several C3 plants. Australian Journal of Plant Physiology 18, 287–305.
CrossRef | CAS | open url image1

von Caemmerer S, Furbank RT (2003) The C4 pathway: an efficient CO2 pump. Photosynthesis Research 77, 191–207.
CrossRef | CAS | PubMed | open url image1

von Caemmerer S , Quick WP (2000) Rubisco: physiology in vivo. In ‘Photosynthesis: physiology and metabolism’. (Eds RC Leegood, TD Saharkey, S von Caemmerer) pp. 85–113. (Kluwer Academic Press: Dordrecht, The Netherlands)

von Caemmerer S, Evans JR, Hudson GS, Andrews TJ (1994) The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195, 88–97.
CAS |
open url image1

von Caemmerer S , Evans JR , Cousins AB , Badger MR , Furbank RT (2007) C4 photosynthesis and CO2 diffusion. In ‘Charting new pathways to C4 rice’. (Eds JE Sheehy, PL Mitchell, B Hardy) pp. 95–115. (International Rice Research Institute: Los Banos, Philippines)

Widholm JM, Ogren WL (1969) Photorespiratory-induced senescence of plants under conditions of low carbon dioxide. Proceedings of the National Academy of Sciences of the United States of America 63, 668–675.
CrossRef | CAS | PubMed | open url image1

Zhu X-G, Long SP, Ort DR (2008) What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? Current Opinion in Biotechnology 19, 153–159.
CrossRef | CAS | PubMed | open url image1








Rent Article (via Deepdyve) Export Citation Cited By (53)

View Altmetrics