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.

  • Letter
  • Published:

Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice


Most Oryza sativa cultivars die within a week of complete submergence—a major constraint to rice production in south and southeast Asia that causes annual losses of over US$1 billion and affects disproportionately the poorest farmers in the world1,2. A few cultivars, such as the O. sativa ssp. indica cultivar FR13A, are highly tolerant and survive up to two weeks of complete submergence owing to a major quantitative trait locus designated Submergence 1 (Sub1) near the centromere of chromosome 9 (refs 3, 4, 5–6). Here we describe the identification of a cluster of three genes at the Sub1 locus, encoding putative ethylene response factors. Two of these genes, Sub1B and Sub1C, are invariably present in the Sub1 region of all rice accessions analysed. In contrast, the presence of Sub1A is variable. A survey identified two alleles within those indica varieties that possess this gene: a tolerance-specific allele named Sub1A-1 and an intolerance-specific allele named Sub1A-2. Overexpression of Sub1A-1 in a submergence-intolerant O. sativa ssp. japonica conferred enhanced tolerance to the plants, downregulation of Sub1C and upregulation of Alcohol dehydrogenase 1 (Adh1), indicating that Sub1A-1 is a primary determinant of submergence tolerance. The FR13A Sub1 locus was introgressed into a widely grown Asian rice cultivar using marker-assisted selection. The new variety maintains the high yield and other agronomic properties of the recurrent parent and is tolerant to submergence. Cultivation of this variety is expected to provide protection against damaging floods and increase crop security for farmers.

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

Access options

Buy this article

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

Figure 1: Sub1 region gene composition and submergence-induced mRNA accumulation in rice.
Figure 2: Characterization of submergence response in transgenic rice ectopically expressing Sub1A-1.
Figure 3: Introgression of the FR13A Sub1 haplotype into an intolerant variety by MAS confers submergence tolerance.

Similar content being viewed by others


  1. Dey, M. & Upadhyaya, H. in Rice Research in Asia: Progress and Priorities (eds Evenson, R., Herdt, R. & Hossain, M.) 291–303 (CAB International, Wallingford, 1996)

    Google Scholar 

  2. Herdt, R. W. in Rice Biotechnology (eds Khush, G. S. & Toenniessen, G. H.) 19–54 (CAB International, Wallingford, 1991)

    Google Scholar 

  3. Xu, K. & Mackill, D. J. A major locus for submergence tolerance mapped on rice chromosome 9. Mol. Breed. 2, 219–224 (1996)

    Article  CAS  Google Scholar 

  4. Xu, K., Xu, X., Ronald, P. C. & Mackill, D. J. A high-resolution linkage map in the vicinity of the rice submergence tolerance locus Sub1. Mol. Gen. Genet. 263, 681–689 (2000)

    Article  CAS  PubMed  Google Scholar 

  5. Harushima, Y. et al. A high-density rice genetic linkage map with 2275 markers using a single F2 population. Genetics 148, 479–494 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Chen, M. et al. An integrated physical and genetic map of the rice genome. Plant Cell 14, 537–545 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  7. Fukao, T. & Bailey-Serres, J. Plant responses to hypoxia—is survival a balancing act? Trends Plant Sci. 9, 449–456 (2004)

    Article  CAS  PubMed  Google Scholar 

  8. Sauter, M. Rice in deep water: “How to take heed against a sea of troubles”. Naturwissenschaften 87, 289–303 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Catling, D. Rice in Deep Water 5 (Macmillan, London, 1992)

    Book  Google Scholar 

  10. Ram, P. C. et al. Submergence tolerance in rainfed lowland rice: physiological basis and prospects for cultivar improvement through marker-aided breeding. Field Crops Res. 76, 131–152 (2002)

    Article  Google Scholar 

  11. International Rice Genome Sequencing Project. The map-based sequence of the rice genome. Nature 436, 793–800 (2005)

    Article  Google Scholar 

  12. Arumanagathan, K. & Earle, E. D. Nuclear DNA content of some important plant species. Plant Mol. Biol. Rep. 9, 229–241 (1991)

    Article  Google Scholar 

  13. Wu, J. et al. A comprehensive rice transcript map containing 6591 expressed sequence tag sites. Plant Cell 14, 525–535 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gutterson, N. & Reuber, T. L. Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr. Opin. Plant Biol. 7, 465–471 (2004)

    Article  CAS  PubMed  Google Scholar 

  15. McGrath, K. C. et al. Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol. 139, 949–959 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Magnani, E., Sjolander, K. & Hake, S. From endonucleases to transcription factors: evolution of the AP2 DNA binding domain in plants. Plant Cell 16, 2265–2277 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Parnell, S. C. et al. Phosphorylation of the RGS protein Sst2 by the MAP kinase Fus3 and use of Sst2 as a model to analyse determinants of substrate sequence specificity. Biochemistry 44, 8159–8166 (2005)

    Article  CAS  PubMed  Google Scholar 

  18. Cheong, Y. H. et al. BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol. 132, 1961–1972 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Christensen, A. H. & Quail, P. H. Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res. 5, 213–218 (1996)

    Article  CAS  PubMed  Google Scholar 

  20. Chern, M.-S., Fitzgerald, H. A., Canlas, P. E., Navarre, D. A. & Ronald, P. C. Overexpression of a rice NPR1 homolog leads to constitutive activation of defense response and hypersensitivity to light. Mol. Plant Microbe Interact. 18, 511–520 (2005)

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Jackson, M. B. & Ram, P. C. Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann. Bot. 91, 227–241 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fukao, T., Xu, K., Ronald, P. & Bailey-Serres, J. A variable cluster of ethylene responsive-like factors regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell (in the press)

  24. Fujimoto, S. Y., Ohta, M., Usui, A., Shinshi, H. & Ohme-Takagi, M. Arabidopsis ethylene-responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell 12, 393–404 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Song, C.-P. et al. Role of an Arabidopsis AP2/EREBP-type transcriptional repressor in abscisic acid and drought stress responses. Plant Cell 17, 2384–2396 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Chen, X., Temnykh, S., Xu, Y., Cho, Y. G. & McCouch, S. R. Development of a microsatellite framework map providing genome-wide coverage in rice (Oryza sativa L.). Theor. Appl. Genet. 95, 553–567 (1997)

    Article  CAS  Google Scholar 

  27. Temnykh, S. et al. Mapping and genome organization of microsatellite sequences in rice (Oryza sativa L.). Theor. Appl. Genet. 100, 697–712 (2000)

    Article  CAS  Google Scholar 

  28. Xu, K., Deb, R. & Mackill, D. J. A microsatellite marker and a codominant PCR-based marker for marker-assisted selection of submergence tolerance in rice. Crop Sci. 44, 248–253 (2004)

    Article  CAS  Google Scholar 

  29. Siangliw, M., Toojinda, T., Tragoonrung, S. & Vanavichit, A. Thai jasmine rice carrying QTLch9 (SubQTL) is submergence tolerant. Ann. Bot. 91, 255–261 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Setter, T. L. et al. Physiology and genetics of submergence tolerance in rice. Ann. Bot. 79, 67–77 (1997)

    Article  CAS  Google Scholar 

Download references


We thank J. Dvorak for discussions of experimental design, H. Zhang for providing BAC clones, D. Chen, J. S. Jeon, J. Ni, P. Colowit, D. Ruan, R. Bruskiewich, G. Vergara, M. Nas, A. Pamplona, C. N. Neeraja, and S. Singh for their technical assistance and suggestions, support and discussions, and the IRRI Grain Quality, Nutrition, and Postharvest Center for amylose data. This work was supported by USDA-NRICGP grants to D.J.M. and P.C.R., and to J.B.-S. and P.C.R., and USAID Linkage Project funds to J.B.-S. and P.C.R. The work on transferring Sub1 to Swarna was supported by a grant from the German Federal Ministry for Economic Cooperation and Development (BMZ) to D.J.M. and A.M.I.

Author information

Authors and Affiliations


Corresponding authors

Correspondence to Pamela C. Ronald or David J. Mackill.

Ethics declarations

Competing interests

Sequences were submitted to GenBank/EMBL/DDJB under accession numbers DQ011597–DQ011607 and DQ453964–DQ453966. Reprints and permissions information is available at The authors declare no competing financial interests.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI:

This article is cited by


By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.


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