Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field

Abstract

The green revolution’s breeding of semi-dwarf rice cultivars in the 1960s improved crop yields, with large increases in the use of nitrogen (N) fertilizer. However, excess N application has caused serious environmental problems, including acid rain and the eutrophication of rivers and oceans. To use N to improve crop yields, while minimizing the associated environmental costs, there is a need to produce crops with higher N-use efficiency and higher yield components. Here we show that transgenic rice overproducing ribulose 1,5-bisphosphate carboxylase–oxygenase (Rubisco)—the key enzyme of photosynthesis—exhibits increased yields with improved N-use efficiency for increasing biomass production when receiving sufficient N fertilization in an experimental paddy field. This field experiment demonstrates an improvement in photosynthesis linked to yield increase due to a higher N-use efficiency in a major crop.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: The effect of N fertilizer on the plant N content of the above-ground section of plants and the total dry matter of wild-type, RBCS-sense and RBCS-antisense rice plants at the full-heading and harvesting stages.
Fig. 2: Relationships between grain (brown rice) yield, yield components and the plant N content of the above-ground section per unit land area in wild-type, RBCS-sense and RBCS-antisense plants at the harvesting stage.
Fig. 3: Changes in the Rubisco content per unit land area in flag leaves of wild-type, RBCS-sense and RBCS-antisense rice plants during the ripening stages.

Data availability

Source data for Figs. 1, 2 and 3 are provided with the paper. The data that support the findings of this study are available from the corresponding author upon request.

References

  1. 1.

    Evans, L. T. Feeding the Ten Billion: Plants and Population Growth (Cambridge Univ. Press, 1998).

  2. 2.

    Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth’s nitrogen cycle. Science 330, 192–196 (2010).

    CAS  ADS  Article  Google Scholar 

  3. 3.

    Good, A. G. & Beatty, P. H. Fertilizing nature: a tragedy of excess in the commons. PLoS Biol. 9, e1001124 (2011).

    CAS  Article  Google Scholar 

  4. 4.

    Köhler, I. H. et al. Expression of cyanobacterial FBP/SBPase in soybean prevents yield depression under future climate conditions. J. Exp. Bot. 68, 715–726 (2016).

    PubMed Central  Google Scholar 

  5. 5.

    Lopez-Calcagno, P. E. et al. Overexpressing the H-protein of the glycine cleavage system increases biomass yield in the glasshouse and field grown transgenic tobacco plants. Plant Biotech. J. 17, 141–151 (2019).

    CAS  Article  Google Scholar 

  6. 6.

    South, P. F., Cavanagh, A. P., Liu, H. W. & Ort, D. R. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363, eaat9077 (2019).

    CAS  Article  Google Scholar 

  7. 7.

    Sinclair, T. R., Rufty, T. W. & Lewis, R. S. Increasing photosynthesis: unlikely solution for world food problem. Trends Plant Sci. 24, 1032–1039 (2019).

    CAS  Article  Google Scholar 

  8. 8.

    Evans, J. R. The relationship between carbon-dioxide-limited photosynthetic rate and ribulose-1,5-bisphosphate-carboxylase content in two nuclear-cytoplasm substitution lines of wheat, and the coordination of ribulose-bisphosphate-carboxylation and electron-transport capacities. Planta 167, 351–358 (1986).

    CAS  Article  Google Scholar 

  9. 9.

    Makino, A., Mae, T. & Ohira, K. Differences between wheat and rice in the enzymic properties of ribulose-1,5-bisphosphate carboxylase/oxygenase and the relationship to photosynthetic gas exchange. Planta 174, 30–38 (1988).

    CAS  Article  Google Scholar 

  10. 10.

    Suzuki, Y. et al. Increased Rubisco content in transgenic rice transformed with the ‘sense’ rbcS gene. Plant Cell Physiol. 48, 626–637 (2007).

    CAS  Article  Google Scholar 

  11. 11.

    Makino, A., Nakano, H., Mae, T., Shimada, T. & Yamamoto, N. Photosynthesis, plant growth and N allocation in transgenic rice plants with decreased Rubisco under CO2 enrichment. J. Exp. Bot. 51, 383–389 (2000).

    CAS  Article  Google Scholar 

  12. 12.

    Sudo, E., Suzuki, Y. & Makino, A. Whole-plant growth and N utilization in transgenic rice plants with increased or decreased Rubisco content under different CO2 partial pressures. Plant Cell Physiol. 55, 1905–1911 (2014).

    CAS  Article  Google Scholar 

  13. 13.

    Wada, G., Shoji, S. & Mae, T. Relationship between nitrogen absorption and growth and yield of rice plants. Jpn Agric. Res. Q. 20, 135–145 (1986).

    Google Scholar 

  14. 14.

    Yoshida, H., Horie, T. & Shiraiwa, T. A model explaining genotypic and environmental variation of rice spikelet number per unit area measured by cross-locational experiments in Asia. Field Crops Res. 97, 337–343 (2006).

    Article  Google Scholar 

  15. 15.

    Wada, G., Matsushima, S. & Matsuzaki, A. Analysis of yield-determining process and its application to yield prediction and culture improvement of lowland rice. LXXXV. An investigation on the percentage of ripened grains from the point of analytical view of the number of spikelets per unit area. Jpn. J. Crop Sci. 35, 195–199 (1968).

    Article  Google Scholar 

  16. 16.

    Mae, T. & Ohira, K. The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryza sativa L.). Plant Cell Physiol. 22, 1067–1074 (1981).

    CAS  Google Scholar 

  17. 17.

    Hoshikawa, K. The Growing Rice Plant (Nosan Gyoson Bunka Kyokai, 1989).

  18. 18.

    Cook, M. G. & Evans, L. T. Some physiological aspects of the domestication and improvement of rice (Oryza spp). Field Crops Res. 6, 219–238 (1983).

    Article  Google Scholar 

  19. 19.

    Yoshida, S. Fundamentals of Rice Crop Science (The International Rice Research Institute, 1981).

  20. 20.

    Yamamuro, S., Ueno, H., Takahashi, S., Morita, S. & Matsuba, K. Evaluation of carbon dioxide assimilation and translocation by 13CO2-tracer method at ripening sage in two rice varieties which differ in the rate of ripened grain. Jpn. J. Soil Sci. Plant Nutr. 72, 379–384 (2001).

    Google Scholar 

  21. 21.

    Suzuki, Y., Miyamoto, T., Yoshizawa, R., Mae, T. & Makino, A. Rubisco content and photosynthesis of leaves at different positions in transgenic rice with an overexpression of RBCS. Plant Cell Environ. 32, 417–427 (2009).

    CAS  Article  Google Scholar 

  22. 22.

    Hossain, M. Z., Shibuya, K. & Saigusa, M. No-tillage transplanting system of rice with controlled availability fertilizer in the nursery box. 1. Growth characteristics and yield of rice in three representative paddy soil. Tohoku J. Agric. Res. 50, 71–86 (2000).

    Google Scholar 

  23. 23.

    Mae, T. et al. A large-grain rice cultivar, Akita 63, exhibits high yield with high physiological N-use efficiency. Field Crops Res. 97, 227–237 (2006).

    Article  Google Scholar 

  24. 24.

    Makino, A., Nakano, H. & Mae, T. Responses of ribulose-1,5-bisphosphate carboxylase, cytochrome f, and sucrose synthesis enzymes in rice leaves to leaf nitrogen and their relationships to photosynthesis. Plant Physiol. 105, 173–179 (1994).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was supported by KAKENHI Grant No. JP16H06379 (to A.M.) from the Japan Society for the Promotion of Science and by Core Research for Environmental Science and Technology Scientific Research Grant No. JPMJCR1503 (to Y.S. and A.M.) from the Japan Society for Technology. We are grateful to M. Seki of Kyusyu University for critical advice on statistical analyses and also thank our colleagues and laboratory members for technical support during our field experiments. This work was registered on 18 May 2016 at the Biosafety Clearing-House Management Centre, which is established under the Cartagena Protocol on Biosafety to the Convention on Biological Diversity (an international agreement on biosafety created as a supplement to the Convention on Biological Diversity effective since 2003).

Author information

Affiliations

Authors

Contributions

K.I., M. Obara, T.M. and A.M. designed the research. D.-K.Y., K.I., M.W., S.I., M. Ogura and Y.S. performed most of the experiments, as well as the growth, biomass and yield analyses. M.S. and Y.T. performed the biochemical and physiological experiments. K.I., H.I, T.M. and A.M. analysed the data, and K.I. and A.M. wrote most of the article.

Corresponding author

Correspondence to Amane Makino.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yoon, DK., Ishiyama, K., Suganami, M. et al. Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field. Nat Food 1, 134–139 (2020). https://doi.org/10.1038/s43016-020-0033-x

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing