Skip to main content

Thank you for visiting 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.

A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice


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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it


Prices may be subject to local taxes which are calculated during checkout

Figure 1: Phenotypes of OsTPP7 present and absent lines.
Figure 2: Sugar metabolism related to trehalose-6-phosphate is influenced by OsTPP7.
Figure 3: OsTPP7 promoter–GUS expression and effects of OsTPP7 expression on global transcript levels.


  1. Kumar, V. & Ladha, J. K. in Advances in Agronomy, Vol. 111 (ed. Sparks, D. L. ) 297–413 (Elsevier Academic Press Inc, 2011).

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Ismail, A. M., Ella, E. S., Vergara, G. V. & Mackill, D. J. Mechanisms associated with tolerance to flooding during germination and early seedling growth in rice (Oryza sativa). Ann. Bot. 103, 197–209 (2009).

    Article  CAS  Google Scholar 

  6. Septiningsih, E. M. 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).

    Article  Google Scholar 

  7. Angaji, S., Septiningsih, E., Mackill, D. & Ismail, A. QTLs associated with tolerance to flooding during germination in rice (Oryza sativa). Euphytica 172, 159–168 (2010).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Sasaki, K. 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).

    Article  CAS  Google Scholar 

  11. Schatz, M. C. 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).

    PubMed  PubMed Central  Google Scholar 

  12. 3,000 Rice Genomes Project. The 3,000 rice genomes project. Gigascience 3, 7 (2014).

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  15. Voesenek, L. A. C. J. & Bailey-Serres, J. Flood adaptive traits and processes: an overview. New Phytol. 206, 57–73 (2015).

    Article  CAS  Google Scholar 

  16. Edwards, J. M., Roberts, T. H. & Atwell, B. J. 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).

    Article  CAS  Google Scholar 

  17. Loreti, E., Yamaguchi, J., Alpi, A. & Perata, P. Sugar modulation of alpha-amylase genes under anoxia. Ann. Bot. 91 Spec No, 143–148 (2003).

  18. Park, M. 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).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  20. Lee, K.-W., Chen, P. W. & Yu, S.-M. Metabolic adaptation to sugar/O2 deficiency for anaerobic germination and seedling growth in rice. Plant Cell Environ. 37, 2234–2244 (2014).

    CAS  PubMed  Google Scholar 

  21. Ge, L.-F. 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).

    Article  CAS  Google Scholar 

  22. Shima, S., Matsui, H., Tahara, S. & Imai, R. Biochemical characterization of rice trehalose-6-phosphate phosphatases supports distinctive functions of these plant enzymes. FEBS J. 274, 1192–1201 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  25. O'Hara, L. E., Paul, M. J. & Wingler, A. How do sugars regulate plant growth and development? New insight into the role of Trehalose-6-Phosphate. Mol. Plant 6, 261–274 (2012).

    Article  Google Scholar 

  26. Lunn, J. E., Delorge, I., Figueroa, C. M., Van Dijck, P. & Stitt, M. Trehalose metabolism in plants. Plant J. 79, 544–567 (2014).

    Article  CAS  Google Scholar 

  27. Schluepmann, H., Pellny, T., van Dijken, A., Smeekens, S. & Paul, M. Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 100, 6849–6854 (2003).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  29. Lu, C.-A. 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).

    Article  CAS  Google Scholar 

  30. Radchuk, R. 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).

    Article  CAS  Google Scholar 

  31. Martínez-Barajas, E. 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).

    Article  Google Scholar 

  32. Valluru, R. & Van den Ende, W. Myo-inositol and beyond—emerging networks under stress. Plant Sci. 181, 387–400 (2011).

    Article  CAS  Google Scholar 

  33. Narsai, R., Rocha, M., Geigenberger, P., Whelan, J. & van Dongen, J. T. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol. 190, 472–487 (2011).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  36. Luo, M. & Wing, R. A. An improved method for plant BAC library construction. Methods Mol. Biol. 236, 3–20 (2003).

    CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  38. Slamet-Loedin, I., Chada-Mohanty, P. & Torizzo, L. Agrobacterium-mediated transformation: rice transformation. Methods Mol. Biol. 1099, 261–271 (2014).

    Article  CAS  Google Scholar 

  39. Ella, E. S., Dionisio-Sese, M. L. & Ismail, A. M. Seed pre-treatment in rice reduces damage, enhances carbohydrate mobilization and improves emergence and seedling establishment under flooded conditions. AoB Plants 2011, plr007 (2011).

    Article  Google Scholar 

  40. Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. & Fernie, A. R. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protoc. 1, 387–396 (2006).

    Article  CAS  Google Scholar 

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

Authors and Affiliations



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.

Corresponding author

Correspondence to Endang M. Septiningsih.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kretzschmar, T., Pelayo, M., Trijatmiko, K. et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants 1, 15124 (2015).

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI:

This article is cited by


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