Global socioeconomic developments create strong incentives for farmers to shift from transplanted to direct-seeded rice (DSR) as a means of intensification and economization1. Rice production must increase to ensure food security2 and the bulk of this increase will have to be achieved through intensification of cultivation, because expansion of cultivated areas is reaching sustainable limits3. Anaerobic germination tolerance, which enables uniform germination and seedling establishment under submergence4, is a key trait for the development of tropical DSR varieties5,6. Here, we identify a trehalose-6-phosphate phosphatase gene, OsTPP7, as the genetic determinant in qAG-9-2, a major quantitative trait locus (QTL) for anaerobic germination tolerance7. OsTPP7 is involved in trehalose-6-phosphate (T6P) metabolism, central to an energy sensor that determines anabolism or catabolism depending on local sucrose availability8,9. OsTPP7 activity may increase sink strength in proliferating heterotrophic tissues by indicating low sugar availability through increased T6P turnover, thus enhancing starch mobilization to drive growth kinetics of the germinating embryo and elongating coleoptile, which consequently enhances anaerobic germination tolerance.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. 1.

    & in Advances in Agronomy, Vol. 111 (ed. Sparks, D. L.) 297–413 (Elsevier Academic Press Inc, 2011).

  2. 2.

    et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).

  3. 3.

    et al. Solutions for a cultivated planet. Nature 478, 337–342 (2011).

  4. 4.

    & Rice germination and seedling growth in the absence of oxygen. Ann. Bot. 103, 181–196 (2009).

  5. 5.

    , , & Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann. Bot. 103, 197–209 (2009).

  6. 6.

    et al. QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan Red. Theor. Appl. Genet. 126, 1357–1366 (2013).

  7. 7.

    , , & QTLs associated with tolerance to flooding during germination in rice (Oryza sativa). Euphytica 172, 159–168 (2010).

  8. 8.

    Trehalose 6-phosphate: a signal of sucrose status. Biochem J 412, 1–2 (2008).

  9. 9.

    et al. Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 149, 1860–1871 (2009).

  10. 10.

    et al. Fine mapping of a major quantitative trait locus, qLG-9, that controls seed longevity in rice (Oryza sativa L.). Theor. Appl. Genet. TAG. 128, 769–778 (2015).

  11. 11.

    et al. Whole genome de novo assemblies of three divergent strains of rice, Oryza sativa, document novel gene space of aus and indica. Genome Biol. 15, 506 (2014).

  12. 12.

    3,000 Rice Genomes Project. The 3,000 rice genomes project. Gigascience 3, 7 (2014).

  13. 13.

    et al. Transcript profiling of the anoxic rice coleoptile. Plant Physiol. 144, 218–231 (2007).

  14. 14.

    Oxygen as an environmental factor in influencing normal morphogenetic development in germinating rice seedlings. J. Exp. Bot. 27, 947–952 (1976).

  15. 15.

    & Flood adaptive traits and processes: an overview. New Phytol. 206, 57–73 (2015).

  16. 16.

    , & Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. J. Exp. Bot. 63, 4389–4402 (2012).

  17. 17.

    , , & Sugar modulation of alpha-amylase genes under anoxia. Ann. Bot. 91 Spec No, 143–148 (2003).

  18. 18.

    et al. Interference with oxidative phosphorylation enhances anoxic expression of rice alpha-amylase genes through abolishing sugar regulation. J. Exp. Bot. 61, 3235–3244 (2010).

  19. 19.

    et al. Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci. Signal. 2, ra61 (2009).

  20. 20.

    , & Metabolic adaptation to sugar/O2 deficiency for anaerobic germination and seedling growth in rice. Plant Cell Environ. 37, 2234–2244 (2014).

  21. 21.

    et al. Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228, 191–201 (2008).

  22. 22.

    , , & Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. FEBS J. 274, 1192–1201 (2007).

  23. 23.

    et al. The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J. Exp. Bot. 65, 1051–1068 (2014).

  24. 24.

    & Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat. Front Plant Sci. 5, 418 (2014).

  25. 25.

    , & How do sugars regulate plant growth and development? New insight into the role of Trehalose-6-Phosphate. Mol. Plant 6, 261–274 (2012).

  26. 26.

    , , , & Trehalose metabolism in plants. Plant J. 79, 544–567 (2014).

  27. 27.

    , , , & Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6849–6854 (2003).

  28. 28.

    & SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci. 12, 20–28 (2007).

  29. 29.

    et al. The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19, 2484–2499 (2007).

  30. 30.

    et al. Sucrose non-fermenting kinase 1 (SnRK1) coordinates metabolic and hormonal signals during pea cotyledon growth and differentiation. Plant J. 61, 324–338 (2010).

  31. 31.

    et al. Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol. 156, 373–381 (2011).

  32. 32.

    & Myo-inositol and beyond—emerging networks under stress. Plant Sci. 181, 387–400 (2011).

  33. 33.

    , , , & Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol. 190, 472–487 (2011).

  34. 34.

    et al. Mechanisms of growth and patterns of gene expression in oxygen-deprived rice coleoptiles. Plant J. 82, 25–40 (2015).

  35. 35.

    et al. Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breed. Biotech. 3, 77–87 (2015).

  36. 36.

    & An improved method for plant BAC library construction. Methods Mol. Biol. 236, 3–20 (2003).

  37. 37.

    et al. SNP-Seek database of SNPs derived from 3000 rice genomes. Nucleic Acids Res. 43, D1023–D1027 (2015).

  38. 38.

    , & Agrobacterium-mediated transformation: rice transformation. Methods Mol. Biol. 1099, 261–271 (2014).

  39. 39.

    , & Seed pre-treatment in rice reduces damage, enhances carbohydrate mobilization and improves emergence and seedling establishment under flooded conditions. AoB Plants 2011, plr007 (2011).

  40. 40.

    , , , & Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protoc. 1, 387–396 (2006).

Download references


We thank I. Tamisin, J. Mendoza, G. Reynaldo, P. Sendon, J.C. Ignacio, C. Casal, D. Sanchez, G. Vergara, S. Catausan, L. Torrizo, C. Duenas, R. Anacleto and C. Llorente for technical assistance; D. Kudrna, W. Golser, J. Talag and R. Wing from Arizona Genomics Institute (AGI) for providing BAC clones, Metabolomic Discoveries GmbH for quantification of sucrose, trehalose-6-phosphate (T6P) and trehalose. This work was supported by the Stress Tolerant Rice for Africa and South Asia (STRASA) project funded by the Bill and Melinda Gates Foundation (BMGF), Global Rice Science Partnership (GRiSP), a grant from the German Federal Ministry of Economic Cooperation and Development (BMZ) #81157485 to E.M.S. and A.M.I, and the US National Science Foundation #IOS-1121626 to J.B.-S. T.K's fellowship was supported by a BMZ Post Doc grant to E.M.S. and R.A.'s PhD was supported by the Monsanto Beachell-Borlaug International Scholars Program (MBBISP) under supervision of J.B.-S. and E.M.S.

Author information

Author notes

    • David J. Mackill
    •  & Endang M. Septiningsih

    Present address: MARS Inc., Department of Plant Sciences, University of California Davis, California 95616, USA (D.J.M.); Department of Soil and Crop Sciences, Texas A&M University, College Station, Texas 77843, USA (E.M.S.).


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

    • Tobias Kretzschmar
    • , Margaret Anne F. Pelayo
    • , Kurniawan R. Trijatmiko
    • , Lourd Franz M. Gabunada
    • , Rosario Jimenez
    • , Inez H. Slamet-Loedin
    • , Nese Sreenivasulu
    • , Abdelbagi M. Ismail
    • , David J. Mackill
    •  & Endang M. Septiningsih
  2. University of the Philippines, Los Banos, Laguna 4031, Philippines

    • Lourd Franz M. Gabunada
    •  & Merlyn S. Mendioro
  3. Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California Riverside, Riverside, California 92521, USA

    • Rejbana Alam
    •  & Julia Bailey-Serres


  1. Search for Tobias Kretzschmar in:

  2. Search for Margaret Anne F. Pelayo in:

  3. Search for Kurniawan R. Trijatmiko in:

  4. Search for Lourd Franz M. Gabunada in:

  5. Search for Rejbana Alam in:

  6. Search for Rosario Jimenez in:

  7. Search for Merlyn S. Mendioro in:

  8. Search for Inez H. Slamet-Loedin in:

  9. Search for Nese Sreenivasulu in:

  10. Search for Julia Bailey-Serres in:

  11. Search for Abdelbagi M. Ismail in:

  12. Search for David J. Mackill in:

  13. Search for Endang M. Septiningsih in:


E.M.S., T.K., D.J.M. and A.M.I. designed the experiments; E.M.S. fine-mapped the QTL; K.R.T. developed the OX lines; L.F.G. performed phenotyping in the laboratory; J.B.-S. assisted in analysing RNA-Seq data; R.A. performed qRT–PCR; N.S. and R.J. performed metabolomics profiling; T.K. with assistance of M.A.P. performed the rest of the experiments; J.B.-S and M.S.M. provided advice about the experiments; I.S.-L. provided technical assistance and infrastructure for rice transformation; T.K. and E.M.S. wrote the manuscript; J.B.-S., N.S., D.J.M. and A.M.I. edited the manuscript; all authors read and approved the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Endang M. Septiningsih.

Supplementary information

About this article

Publication history






Further reading Further reading