Climate-Resilient Future Crop: Development of C4 Rice

  • Hsiang Chun Lin
  • Robert A. Coe
  • W. Paul Quick
  • Anindya BandyopadhyayEmail author


Rice is the most important crop in the world. It is a staple food for more than half of the human population and a primary food source for the world’s poorest people. Asia currently accounts for 90% of global rice production but it will need to increase this by 50% within the next 30 years. By this time the region will be home to nearly 90% of the global population increase and will likely be experiencing extreme climatic conditions. Agriculture will be challenged by diminishing water resources, reduced nutrient inputs and an increase in abiotic stresses. Rice yield increases have already stagnated and so a new paradigm is needed to meet these future challenges. Most crop plants, like rice and wheat, have a simple and less efficient photosynthetic mechanism (C3 photosynthesis) that as a consequence results in considerable loss of water through stomatal pores on their leaves that open widely to let in more carbon dioxide. They also make a large amount of photosynthetic protein to maximise their photosynthetic rate that requires a large investment of nitrogen and hence fertiliser application. However, a few plants have evolved a more efficient C4 photosynthetic pathway that greatly alleviates these problems. The installation of a C4 photosynthetic pathway into major crops like rice could potentially increase yields by 50%, double the water-use efficiency and reduce fertiliser use by 40%. This is because plants with a C4 photosynthetic pathway concentrate CO2 within the leaf prior to photosynthetic fixation leading to increased photosynthetic efficiency and large reductions in the requirement for scarce resources like water and nitrogen (fertiliser). These modifications would be particularly advantageous in future climate scenarios where water scarcity and global temperature are predicted to increase.


C4 photosynthesis Rubisco Photorespiration C4 evolution Rice 


  1. Ainsworth, E. A., & Long, S. P. (2005). What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist, 165(2), 351–372.CrossRefGoogle Scholar
  2. Bräutigam, A., Hofmann-Benning, S., & Weber, A. P. M. (2008). Comparative proteomics of chloroplast envelopes from C(3) and C(4) plants reveals specific adaptations of the plastid envelope to C(4) photosynthesis and candidate proteins required for maintaining C(4) metabolite fluxes. Plant Physiology, 148(1), 568–579.CrossRefGoogle Scholar
  3. Brutnell, T. P., et al. (2010). Setaria viridis: A model for C4 photosynthesis. The Plant Cell, 22(8), 2537–2544.CrossRefGoogle Scholar
  4. von Caemmerer, S., Quick, W. P., & Furbank, R. T. (2012). The development of C4 rice: Current progress and future challenges. Science (New York, N.Y.), 336(6089), 1671–1672.CrossRefGoogle Scholar
  5. Edwards, E. J., Smith, S. A., & Crossing Environmental Thresholds. (2010). The origins of C 4 grasslands: Integrating evolutionary and ecosystem science. Science, 328(April), 587–590.CrossRefGoogle Scholar
  6. Evans, J. R., & von Caemmerer, S. (2000). Would C4 rice produce more biomass than C3 rice? In J. E. Sheehy, P. L. Mitchell, & B. Hardy (Eds.), Redesigning rice photosynthesis to increase yield (pp. 53–72). Amsterdam: Elsevier.CrossRefGoogle Scholar
  7. Furbank, R. T. (2011). Evolution of the C 4 photosynthetic mechanism: Are there really three C 4 acid decarboxylation types? Journal of Experimental Botany, 62(9), 3103–3108.CrossRefGoogle Scholar
  8. Ghannoum, O., Evans, J. R., & von Caemmerer, S. (2011). Nitrogen and water use efficiency in C4 plants. In A. S. Raghavendra & R. F. Sage (Eds.), C4 photosynthesis and related CO2 concentrating mechanisms (pp. 129–146). Dordrecht: Springer.Google Scholar
  9. Hatch, M. D. (1999). C4 photosynthesis: A historical overview. In R. Sage & R. Monson (Eds.), C4 plant biology (pp. 175–196). New York, NY: Academic Press.Google Scholar
  10. Hatch, M. D., Kagawa, T., & Craig, S. (1975). Subdivision of C4-pathway species based on differing C4 acid decarboxylating systems and ultrastructural features. Australian Journal of Plant Physiology, 2, 111–128.Google Scholar
  11. Hibberd, J. M., & Covshoff, S. (2010). The regulation of gene expression required for C 4 photosynthesis. Annual Review of Plant Biology, 61, 181–207.CrossRefGoogle Scholar
  12. Hibberd, J. M., Sheehy, J. E., & Langdale, J. A. (2008). Using C4 photosynthesis to increase the yield of rice—Rationale and feasibility. Current Opinion in Plant Biology, 11(2), 228–231.CrossRefGoogle Scholar
  13. Hsing, Y. I., et al. (2007). A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Molecular Biology, 63(3), 351–364.CrossRefGoogle Scholar
  14. Jenkins, C. L. D., Furbank, R. T., & Hatch, M. D. (1989). Mechanism of C4 photosynthesis - A model describing the inorganic carbon pool in bundle sheath-cells. Plant Physiology, 91(4), 1372–1381.CrossRefGoogle Scholar
  15. Jeong, D. H., et al. (2002). T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiology, 130(4), 1636–1644.CrossRefGoogle Scholar
  16. Kajala, K., et al. (2011). Strategies for engineering a two-celled C4 photosynthetic pathway into rice. Journal of Experimental Botany, 62(9), 3001–3010.CrossRefGoogle Scholar
  17. Kanai, R., & Edwards, G. E. (2001). The biochemistry of C4 photosynthesis. In C4 plant biology (pp. 49–87). New York, NY: Academic Press.Google Scholar
  18. Kocacinar, F., McKown, A. D., Sage, T. L., & Sage, R. F. (2008). Photosynthetic pathway influences xylem structure and function in flaveria (Asteraceae). Plant, Cell and Environment, 31(10), 1363–1376.CrossRefGoogle Scholar
  19. Ku, S.-b., & Edwards, G. E. (1977). Oxygen inhibition of photosynthesis. Plant Physiology, 59, 986–990.CrossRefGoogle Scholar
  20. Leegood, R. C. (2002). C4 photosynthesis: Principles of CO2 concentration and prospects for its introduction into C3 plants. Journal of Experimental Botany, 53(369), 581–590.CrossRefGoogle Scholar
  21. Leegood, R. C. (2013). Strategies for engineering C 4 photosynthesis. Journal of Plant Physiology, 170(4), 378–388.CrossRefGoogle Scholar
  22. Lin, H., et al. (2016). Targeted knockdown of GDCH in rice leads to a photorespiratory-deficient phenotype useful as a building block for C4 rice. Plant and Cell Physiology, 57(5), 919–932.CrossRefGoogle Scholar
  23. Majeran, W., Cai, Y., Sun, Q., & van Wijk, K. J. (2005). The plant cell functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. Plant Cell, 17, 3111.CrossRefGoogle Scholar
  24. Majeran, W., et al. (2008). Consequences of C4 differentiation for chloroplast membrane proteomes in maize mesophyll and bundle sheath cells. Molecular & Cellular Proteomics : MCP, 7(9), 1609–1638.CrossRefGoogle Scholar
  25. Majeran, W., et al. (2010). Structural and metabolic transitions of C4 leaf development and differentiation defined by microscopy and quantitative proteomics in maize. The Plant Cell, 22(11), 3509–3542.CrossRefGoogle Scholar
  26. Manandhar-Shrestha, K., et al. (2013). Comparative proteomics of chloroplasts envelopes from bundle sheath and mesophyll chloroplasts reveals novel membrane proteins with a possible role in c4-related metabolite fluxes and development. Frontiers in Plant Science, 4(March), 65.Google Scholar
  27. Mitchell, P. L., & Sheehy, J. E. (2006). Surveying the possible pathways to C 4 rice. In Charting new pathways to C4 rice (pp. 399–412). Los Banos: International Rice Research Institute.Google Scholar
  28. Miyao, M., Masumoto, C., Miyazawa, S. I., & Fukayama, H. (2011). Lessons from engineering a single-cell C 4 photosynthetic pathway into rice. Journal of Experimental Botany, 62(9), 3021–3029.CrossRefGoogle Scholar
  29. Monteith, J. L. (1978). Reassessment of maximum growth rates for C3 and C4 crops. Experimental Agriculture, 14, 1–5.CrossRefGoogle Scholar
  30. Morgan, J. a., et al. (2011). C4 grasses prosper as carbon dioxide eliminates desiccation in warmed semi-arid grassland. Nature, 476(7359), 202–205.CrossRefGoogle Scholar
  31. Osborn, H. L., et al. (2016). Effects of reduced carbonic anhydrase activity on co2 assimilation rates in setaria viridis: A transgenic analysis. Journal of Experimental Botany, 68(2), erw357.Google Scholar
  32. Peng, S., et al. (2004). Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences of the United States of America, 101(27), 9971–9975.CrossRefGoogle Scholar
  33. Rizal, G., et al. (2015). Two forward genetic screens for vein density mutants in sorghum converge on a cytochrome p450 gene in the brassinosteroid pathway. Plant Journal, 84(2), 257–266.CrossRefGoogle Scholar
  34. Sage, R. F. (1999). Why C4 photosynthesis? In R. F. Sage & R. K. Monson (Eds.), C4 plant biology (pp. 3–16). San Diego, CA: Academic Press.CrossRefGoogle Scholar
  35. Sage, R. F. (2004). The evolution of C 4 photosynthesis. New Phytologist, 161(2), 341–370.CrossRefGoogle Scholar
  36. Sage, R. F., & Zhu, X. G. (2011). Exploiting the engine of C 4 photosynthesis. Journal of Experimental Botany, 62(9), 2989–3000.CrossRefGoogle Scholar
  37. Sage, R. F., Christin, P. A., & Edwards, E. J. (2011). The C 4 plant lineages of planet earth. Journal of Experimental Botany, 62(9), 3155–3169.CrossRefGoogle Scholar
  38. Sheehy, J. E., et al. (2007). How the rice crop works and why it needs a new engine. In J. E. Sheehy, P. L. Mitchell, & B. Hardy (Eds.), Charting new pathways to C4 rice (pp. 3–26). Los Banos: International Rice Research Institute.Google Scholar
  39. Still, C. J., Berry, J. A., James Collatz, G., & DeFries, R. S. (2003). Global distribution of C 3 and C 4 vegetation: Carbon cycle implications. Global Biogeochemical Cycles, 17(1), 6-1–6-14.CrossRefGoogle Scholar
  40. 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. Journal of Experimental Botany, 59(7), 1799–1809.CrossRefGoogle Scholar
  41. Taylor, S. H., et al. (2010). Ecophysiological traits in C3 and C4 grasses: A phylogenetically controlled screening experiment. New Phytologist, 185, 780.CrossRefGoogle Scholar
  42. Wan, S., et al. (2009). Activation tagging, an efficient tool for functional analysis of the rice genome. Plant Molecular Biology, 69(1–2), 69–80.CrossRefGoogle Scholar
  43. Wang, P., Kelly, S., Fouracre, J. P., & Langdale, J. A. (2013). Genome-wide transcript analysis of early maize leaf development reveals gene cohorts associated with the differentiation of C4 kranz anatomy. Plant Journal, 75(4), 656–670.CrossRefGoogle Scholar
  44. Weber, A. P. M., & von Caemmerer, S. (2010). Plastid transport and metabolism of C3 and C4 plants — Comparative analysis and possible biotechnological exploitation. Current Opinion in Plant Biology, 13(3), 256–264.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Hsiang Chun Lin
    • 1
  • Robert A. Coe
    • 1
  • W. Paul Quick
    • 1
  • Anindya Bandyopadhyay
    • 1
    Email author
  1. 1.C4 Rice CentreInternational Rice Research Institute (IRRI)Los BañosPhilippines

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