Expression of barley SUSIBA2 transcription factor yields high-starch low-methane rice

  • Nature volume 523, pages 602606 (30 July 2015)
  • doi:10.1038/nature14673
  • Download Citation


Atmospheric methane is the second most important greenhouse gas after carbon dioxide, and is responsible for about 20% of the global warming effect since pre-industrial times1,2. Rice paddies are the largest anthropogenic methane source and produce 7–17% of atmospheric methane2,3. Warm waterlogged soil and exuded nutrients from rice roots provide ideal conditions for methanogenesis in paddies with annual methane emissions of 25–100-million tonnes3,4. This scenario will be exacerbated by an expansion in rice cultivation needed to meet the escalating demand for food in the coming decades4. There is an urgent need to establish sustainable technologies for increasing rice production while reducing methane fluxes from rice paddies. However, ongoing efforts for methane mitigation in rice paddies are mainly based on farming practices and measures that are difficult to implement5. Despite proposed strategies to increase rice productivity and reduce methane emissions4,6, no high-starch low-methane-emission rice has been developed. Here we show that the addition of a single transcription factor gene, barley SUSIBA2 (refs 7, 8), conferred a shift of carbon flux to SUSIBA2 rice, favouring the allocation of photosynthates to aboveground biomass over allocation to roots. The altered allocation resulted in an increased biomass and starch content in the seeds and stems, and suppressed methanogenesis, possibly through a reduction in root exudates. Three-year field trials in China demonstrated that the cultivation of SUSIBA2 rice was associated with a significant reduction in methane emissions and a decrease in rhizospheric methanogen levels. SUSIBA2 rice offers a sustainable means of providing increased starch content for food production while reducing greenhouse gas emissions from rice cultivation. Approaches to increase rice productivity and reduce methane emissions as seen in SUSIBA2 rice may be particularly beneficial in a future climate with rising temperatures resulting in increased methane emissions from paddies9,10.

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Data deposits

The sequence of construct containing HvSBEIIb p:HvSUSIBA2 has been deposited in GenBank under accession number KR935231.


  1. 1.

    et al. Three decades of global methane sources and sinks. Nature Geosci. 6, 813–823 (2013)

  2. 2.

    , , & Methane emissions from wetlands: biogeochemical, microbial, and modeling perspectives from local to global scales. Glob. Change Biol. 19, 1325–1346 (2013)

  3. 3.

    & Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann. NY Acad. Sci. 1125, 171–189 (2008)

  4. 4.

    & Photosynthate allocations in rice plants: Food or atmospheric methane. Proc. Natl Acad. Sci. USA 99, 11993–11995 (2002)

  5. 5.

    China cuts methane emissions from rice fields. Nature (2009)

  6. 6.

    et al. Optimizing grain yields reduces CH4 emission from rice paddy fields. Proc. Natl Acad. Sci. USA 99, 12021–12024 (2002)

  7. 7.

    et al. A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 15, 2076–2092 (2003)

  8. 8.

    , , , & Antisense oligodeoxynucleotide inhibition as a potent strategy in plant biology: identification of SUSIBA2 as a transcriptional activator in plant sugar signaling. Plant J. 44, 128–138 (2005)

  9. 9.

    et al. Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507, 488–491 (2014)

  10. 10.

    & Methane minimalism. Nature 507, 436–437 (2014)

  11. 11.

    , , & WRKY transcription factors. Trends Plant Sci. 15, 247–258 (2010)

  12. 12.

    , , & Steady-state and time-resolved spectroscopy of F420 extracted from methanogen cells and its utility as a marker for fecal contamination. J. Agric. Food Chem. 49, 1123–1127 (2001)

  13. 13.

    , , & Response of a rice paddy soil methanogen to syntrophic growth as revealed by transcriptional analyses. Appl. Environ. Microbiol. 80, 4668–4676 (2014)

  14. 14.

    , & Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 6, 847–862 (2012)

  15. 15.

    et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA 112, E911–E920 (2015)

  16. 16.

    , , & Methanogenic pathway and archaeal communities in three different anoxic soils amended with rice straw and maize straw. Frontiers Microbiol. 3 (2012)

  17. 17.

    , , & Dynamics of the methanogenic archaeal community during plant residue decomposition in an anoxic rice field soil. Appl. Environ. Microbiol. 74, 2894–2901 (2008)

  18. 18.

    et al. Molecular insights into how a deficiency of amylose affects carbon allocation-carbohydrate and oil analysis and gene expression profiling in the seeds of a rice waxy mutant. BMC Plant Biol. 12, 230 (2012)

  19. 19.

    , , , & Development of an efficient tissue culture after crossing (TCC) system for transgenic improvement of barley as a bioenergy crop. Appl. Energy 91, 405–411 (2012)

  20. 20.

    , , , & The two genes encoding starch-branching enzymes IIa and IIb are differentially expressed in barley. Plant Physiol. 118, 37–49 (1998)

  21. 21.

    , , & Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271–282 (1994)

  22. 22.

    , , & Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem. Biophys. Res. Commun. 345, 646–651 (2006)

  23. 23.

    , , & A quantitative RT–PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3, 7 (2007)

  24. 24.

    , , & Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 89, 670–679 (2005)

  25. 25.

    et al. Quantification of syntrophic acetate-oxidizing microbial communities in biogas processes. Environ. Microbiol. Rep. 3, 500–505 (2011)

  26. 26.

    & Oligonucleotide primers, probes and molecular methods for the environmental monitoring of methanogenic archaea. Microb. Biotechnol. 4, 585–602 (2011)

  27. 27.

    , , & Effect of fertilizer application on NO and N2O fluxes from agricultural fields. J. Geophys. Res. 100, 25923–25931 (1995)

  28. 28.

    , & Improved biogas production from whole stillage by co-digestion with cattle manure. Bioresour. Technol. 114, 314–319 (2012)

  29. 29.

    , , , & Methane and nitrous oxide emissions from paddy field as affected by water-saving irrigation. Phys. Chem. Earth 53–54, 30–37 (2012)

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Special thanks to S. Stymne. We would also like to thank B. Müller, X. Feng, M. Erikson, L. Sun, S. Isaksson, J. Ascue and S. Mayer for their help in determining concentrations of methane and methanogens, and B. Ingemarsson for discussions concerning the work layout. This work was funded by the following organisations and foundations: The Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas) for Project No 219-2014-1172; the joint Formas/Sida-funded programme (Project No 220-2009-2069) on sustainable development in developing countries; the SLU Lärosätesansökan Programme (TC4F) for Team 4 supported by Vinnova; the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (Formas) under the Strategic Research Area for the TCBB Programme; National Natural Science Foundation of China (projects no 30771298 and no 31370389); the SLU programme BarleyFunFood; the Carl Trygger Foundation for Project No CTS 11: 450; funding in part by the US Department of Energy Contract DE-AC05-76RL01830 with the Pacific Northwest National Laboratory.

Author information

Author notes

    • J. Su
    • , C. Hu
    •  & X. Yan

    These authors contributed equally to this work.


  1. Institute of Biotechnology, Fujian Academy of Agricultural Sciences, Fuzhou 350003, China

    • J. Su
    • , C. Hu
    • , Z. Chen
    • , Q. Guan
    • , Y. Wang
    • , D. Zhong
    •  & F. Wang
  2. Department of Plant Biology, Uppsala BioCenter, Linnean Center for Plant Biology, Swedish University of Agricultural Sciences, PO Box 7080, SE-75007 Uppsala, Sweden

    • J. Su
    • , C. Hu
    • , X. Yan
    • , Y. Jin
    •  & C. Sun
  3. Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization, Hunan Agricultural University, Changsha 410128, China

    • Y. Jin
  4. The Environmental Molecular Sciences Laboratory (EMSL), Pacific Northwest National Laboratory, PO Box 999, K8-93 Richland, Washington 99352, USA

    • C. Jansson
  5. Department of Microbiology, Uppsala BioCenter, Swedish University of Agricultural Sciences, SE-75007 Uppsala, Sweden

    • A. Schnürer


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J.S., Z.C., Q.G., Y.W. and D.Z. performed measurements of methane emissions from paddies; J.S. also performed western blot and zymogram analyses, methanogen quantification and starch determination. C.H. was responsible for plasmid constructions, rice transformation, Southern blot analysis and phenotypic trait characterization. X.Y. carried out gene expression analysis, starch determination, sugar induction experiments and phenotypic trait characterization. Y.J. performed plasmid validation, insertion site identification, methanogen quantification, measurements of methane emissions in phytotrons and sugar induction experiments, electrophoretic mobility shift assay (EMSA), qPCR and light microscopy. C.J. was involved in the initiation, layout and discussions concerning the work and manuscript revision. F.W. was involved in the planning of rice transformation and field trial settings. A.S. revised the manuscript and helped with methane and methanogen determinations. C.S. initiated and coordinated the work, designed the experiments, performed some experiments, and drafted and revised the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to F. Wang or C. Sun.

Extended data

Supplementary information

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  1. 1.

    Supplementary Information

    This file contains Supplementary Table 1.

  2. 2.

    Supplementary Data

    This file contains the sequences of the construct and insertion sites in Extended Data Fig. 1.

Excel files

  1. 1.

    Supplementary Information

    This file contains Supplementary Table 2.


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