The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water

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Abstract

Living organisms must acquire new biological functions to adapt to changing and hostile environments. Deepwater rice has evolved and adapted to flooding by acquiring the ability to significantly elongate its internodes, which have hollow structures and function as snorkels to allow gas exchange with the atmosphere, and thus prevent drowning1,2,3. Many physiological studies have shown that the phytohormones ethylene, gibberellin and abscisic acid are involved in this response4,5,6,7,8, but the gene(s) responsible for this trait has not been identified. Here we show the molecular mechanism of deepwater response through the identification of the genes SNORKEL1 and SNORKEL2, which trigger deepwater response by encoding ethylene response factors involved in ethylene signalling. Under deepwater conditions, ethylene accumulates in the plant and induces expression of these two genes. The products of SNORKEL1 and SNORKEL2 then trigger remarkable internode elongation via gibberellin. We also demonstrate that the introduction of three quantitative trait loci from deepwater rice into non-deepwater rice enabled the latter to become deepwater rice. This discovery will contribute to rice breeding in lowland areas that are frequently flooded during the rainy season.

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Figure 1: Identification of genes responsible for deepwater response in rice.
Figure 2: Molecular characterization of SK1 and SK2.
Figure 3: GA response and molecular mechanism of deepwater response.
Figure 4: SK genes in wild rice species and QTL pyramiding.

Accession codes

Primary accessions

DDBJ/GenBank/EMBL

Data deposits

The DDBJ accession numbers for SNORKEL1 and SNORKEL2 are as follows (rice variety, accession numbers): C9285, AB510478 and AB510479; Bhadua, AB510480 and AB510481; O. rufipogon (W0120), AB510482 and AB510483; and in O. nivara (W0106), AB510484 and AB510485. SNORKEL2 and SNORKEL2-like genes in O. glumaepatula (IRGC105668) are AB510486 and AB510487.

References

  1. 1

    Vergara, B. S., Jackson, B. & De Datta, S. K. in Climate and Rice (eds IRRI) 301–319 (IRRI, Los Baños, 1976)

  2. 2

    Catling, D. Rice in Deepwater (Macmillan, London, 1992)

  3. 3

    Kende, H., Van der Knaap, E. & Cho, H.-T. Deepwater rice: a model plant to study stem elongation. Plant Physiol. 118, 1105–1110 (1998)

  4. 4

    Métraux, J.-P. & Kende, H. The role of ethylene in the growth response of submerged deep water rice. Plant Physiol. 72, 441–446 (1983)

  5. 5

    Raskin, I. & Kende, H. Role of gibberellin in the growth response of submerged deep water rice. Plant Physiol. 76, 947–950 (1984)

  6. 6

    Hoffmann-Benning, S. & Kende, H. On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol. 99, 1156–1161 (1992)

  7. 7

    Azuma, T. et al. Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice. J. Plant Physiol. 14, 323–328 (1995)

  8. 8

    Bailey-Serres, J. & Voesenek, L. A. C. J. Flooding stress: acclimations and genetic diversity. Annu. Rev. Plant Biol. 59, 313–339 (2008)

  9. 9

    Hattori, Y. et al. A major QTL confers rapid internode elongation in response to water rise in deepwater rice. Breed. Sci. 57, 305–314 (2007)

  10. 10

    Hattori, Y. et al. Mapping of three QTLs that regulate internode elongation in deepwater rice. Breed. Sci. 58, 39–46 (2008)

  11. 11

    Nemoto, K. et al. Inheritance of early elongation ability in floating rice revealed by diallel and QTL analyses. Theor. Appl. Genet. 109, 42–47 (2004)

  12. 12

    Kawano, R. et al. Mapping of QTLs for floating ability in rice. Breed. Sci. 58, 47–53 (2008)

  13. 13

    Nakano, T., Suzuki, K., Fujimura, T. & Shinshi, H. Genome-wide analysis of the ERF gene family in Arabidopsis and Rice. Plant Physiol. 140, 411–432 (2006)

  14. 14

    Xu, K. et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442, 705–708 (2006)

  15. 15

    Fukao, T., Xu, K., Ronald, P. C. & Bailey-Serres, J. A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18, 2021–2034 (2006)

  16. 16

    Solano, R., Stepanova, A., Chao, Q. & Ecker, J. R. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1. Genes Dev. 12, 3703–3714 (1998)

  17. 17

    Jackson, M. B. Ethylene and responses of plants to soil waterlogging and submergence. Annu. Rev. Plant Physiol. 36, 145–174 (1985)

  18. 18

    Hooley, R. Gibberellins: perception, transduction and responses. Plant Mol. Biol. 26, 1529–1555 (1994)

  19. 19

    Cheng, C., Tsuchimoto, S., Ohtsubo, H. & Ohtsubo, E. Evolutionary relationships among rice species with AA genome based on SINE insertion analysis. Genes Genet. Syst. 77, 323–334 (2002)

  20. 20

    Vaughan, D. A., Lu, B.-R. & Tomooka, N. The evolving story of rice evolution. Plant Sci. 174, 394–408 (2008)

  21. 21

    Ashikari, M. et al. Cytokinin oxidase regulates rice grain production. Science 309, 741–745 (2005)

  22. 22

    Ashikari, M. & Matsuoka, M. Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci. 11, 344–350 (2006)

  23. 23

    Fan, C. et al. GS3, a major QTL for grain length and weight and minor QTL for grain width and thickness in rice, encodes a putative transmembrane protein. Theor. Appl. Genet. 112, 1164–1171 (2006)

  24. 24

    Song, X.-J. et al. A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nature Genet. 39, 623–630 (2007)

  25. 25

    Shomura, A. et al. Deletion in a gene associated with grain size increased yields during rice domestication. Nature Genet. 40, 1023–1028 (2008)

  26. 26

    Huang, X. et al. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genet. 41, 494–497 (2009)

  27. 27

    Fukao, T. & Bailey-Serres, J. Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proc. Natl Acad. Sci. USA 105, 16814–16819 (2008)

  28. 28

    Morishima, H., Hinata, K. & Oka, H. I. Floating ability and drought resistance in wild and cultivated species of rice. Ind. J. Genet. Plant Breed. 22, 1–11 (1962)

  29. 29

    Hood, E. E., Helmer, G. L., Fraley, R. T. & Chilton, M.-D. The hypervirulence of Agrobacterium tumefaciens A281 is encoded in a region of pTiBo542 outside of T-DNA. J. Bacteriol. 168, 1291–1301 (1986)

  30. 30

    Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1989)

  31. 31

    Kaneko, M. et al. Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J. 35, 104–115 (2003)

  32. 32

    Hiei, Y., Ohta, S., Komari, T. & Kumashiro, T. 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)

  33. 33

    Hirano, K. et al. Comprehensive transcriptome analysis of phytohormone biosynthesis and signaling genes in microspore/pollen and tapetum of rice. Plant Cell Physiol. 49, 1429–1450 (2008)

  34. 34

    Mao, C., Wang, S., Jia, Q. & Wu, P. OsEIL1, a rice homolog of the Arabidopsis EIN3 regulates the ethylene response as a positive component. Plant Mol. Biol. 61, 141–152 (2006)

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Acknowledgements

We thank I. Aichi for helping to produce the transgenic lines and M. Ito for helping to map the genes. We also thank P. Chaiyawat for the opportunity to photograph the deepwater rice specimen and M. Kojima for technical assistance with the hormone analysis. This work was supported by a grant from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Integrated Research Project for Plants, Insects, and Animals using Genome Technology, QT-2003 and QT-4002) and a research fellowship from the Japan Society for the Promotion of Science (Y.H.). The wild rice lines used in this study were obtained from the National Institute of Genetics supported by the National Bioresource Project, MEXT, Japan and the International Rice Research Institute, Philippines.

Author Contributions M.A. conceived the project and designed the experiments. Y.H. identified the genes and Y.H., K.N., S.F., X.-J.S. and R.K. performed molecular characterization of the genes. H.S. and H.M. surveyed the hormone contents. J.W. and T.M. performed BAC clone analysis. A.Y., H.K. and M.M. provided advice regarding the experiments. M.A. and Y.H. wrote the manuscript.

Author information

Correspondence to Motoyuki Ashikari.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary Figures 1-11 with Legends and Supplementary Tables 1-4. (PDF 2255 kb)

Supplementary Movie 1

This movie shows temporal elongation phenotype under deepwater conditions. Plants were submerged in water up to 70% of the plant height, and the water level was then increased by 10 cm every day until the tank was full. Control, T65; DWR, C9285. (MOV 5759 kb)

Supplementary Movie 2

This movie shows temporal elongation phenotype under complete submergence. The tank was filled with water on the first day of the deepwater treatment. Control, T65; DWR, C9285. (MOV 6225 kb)

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