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

Nature Plants volume 1, Article number: 15124 (2015) Cite this article

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Abstract

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.

Anaerobic germination tolerance is characterized by rapid coleoptile elongation under submergence, with concomitant delay of radicle development13, eventually enabling allocation of surface oxygen towards the developing embryo14—a submergence escape strategy15. Developmental restrictions associated with anaerobic germination are linked to the abolition of respiratory ATP regeneration16. Consequently, efficient use of starch reserves is pivotal in attenuating energy starvation symptoms and maintaining growth under anaerobic germination4,6,17–19.

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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.

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Acknowledgements

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.

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Author notes

  1. David J. Mackill & Endang M. Septiningsih

    Present address: †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.).,

Authors and Affiliations

  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, 4031, Laguna, Philippines

    Lourd Franz M. Gabunada & Merlyn S. Mendioro

  3. Department of Botany and Plant Sciences, Center for Plant Cell Biology, University of California Riverside, Riverside, 92521, California, USA

    Rejbana Alam & Julia Bailey-Serres

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Contributions

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.

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Correspondence to Endang M. Septiningsih.

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Kretzschmar, T., Pelayo, M., Trijatmiko, K. et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nature Plants 1, 15124 (2015). https://doi.org/10.1038/nplants.2015.124

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