Plant Growth Regulation

, Volume 85, Issue 1, pp 123–132 | Cite as

Internodal elongation under submergence in the Amazonian wild rice species Oryza glumaepatula: the growth response is induced by hypoxia but not by ethylene

  • Daisuke Sasayama
  • Takuma Okishio
  • Tatsuya Hirano
  • Hiroshi Fukayama
  • Tomoko Hatanaka
  • Masahiro Akimoto
  • Tetsushi Azuma
Original paper


Whole plants of Oryza glumaepatula (accession W1246) displayed rapid internodal elongation under partial submergence, comparable with those of deepwater or floating Oryza sativa cultivars. In excised stem segments of O. glumaepatula, submergence and hypoxia equally induced internodal elongation, whereas ethylene, which plays an important role in the rapid internodal elongation of deepwater rice, induced internodal elongation of only one-third relative to submergence or hypoxia. Pretreatments of stem segments with 1-methylcyclopropene (an ethylene action inhibitor) almost completely blocked ethylene-induced internodal elongation but had limited effects on submergence-induced internodal elongation. These results indicate that hypoxia, but not ethylene, triggers rapid internodal elongation during submergence in O. glumaepatula. O. glumaepatula W1246 possessed a homologue of SNORKEL1 (SK1) and two homologues of SNORKEL2 (SK2). SK1 and SK2 encode ethylene response factors and evoke rapid internodal elongation in response to ethylene in O. sativa. However, none of these homologues showed an increased expression level in internodes of stem segments treated with hypoxia.


Deepwater rice Escape strategy Ethylene response factor Floating rice Flood resistance SNORKEL 



We thank Rohm & Haas China Inc. for kindly providing 1-MCP. This work was supported by JSPS KAKENHI Grant No. 24580022.

Supplementary material

10725_2018_378_MOESM1_ESM.pdf (456 kb)
Supplementary material 1 (PDF 455 KB)


  1. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene analysis and properties of the gas. In: Ethylene in plant biology, 2nd edn. Academic Press, San Diego, pp 14–25CrossRefGoogle Scholar
  2. Akimoto M, Shimamoto Y, Morishima H (1998) Population genetic structure of wild rice Oryza glumaepatula distributed in the Amazon flood area influenced by its life-history traits. Mol Ecol 7:1371–1381CrossRefGoogle Scholar
  3. Azuma T, Mihara F, Uchida N, Yasuda T, Yamaguchi T (1990) Internodal elongation and ethylene concentration of floating rice stem sections submerged at different water depths. Jpn J Tropic Agric 34:265–270Google Scholar
  4. Azuma T, Mihara F, Uchida N, Yasuda T, Yamaguchi T (1991) Influence of humidity on ethylene-induced internodal elongation in floating rice. Plant Cell Physiol 32:307–309CrossRefGoogle Scholar
  5. Azuma T, Hirano T, Deki Y, Uchida N, Yasuda T, Yamaguchi T (1995) Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice. J Plant Physiol 146:323–328CrossRefGoogle Scholar
  6. Azuma T, Uchida N, Yasuda T (2001) Low levels of oxygen promote internodal elongation in floating rice independently of enhanced ethylene production. Plant Growth Regul 34:181–186CrossRefGoogle Scholar
  7. Azuma T, Hatanaka T, Uchida N, Yasuda T (2003) Enhancement of transpiration by ethylene is responsible for absence of internodal elongation in floating rice at low humidity. J Plant Physiol 160:1125–1128CrossRefPubMedGoogle Scholar
  8. Azuma T, Inoue Y, Hamada Y, Okishio T, Sasayama D, Itoh K (2013) Anoxia promotes gravitropic curvature in rice pulvini but inhibits it in wheat and oat pulvini. J Plant Physiol 170:1158–1164CrossRefPubMedGoogle Scholar
  9. Bailey-Serres J, Fukao T, Ronald P, Ismail A, Heuer S, Mackill D (2010) Submergence tolerance rice: SUB1’s journey from landrace to modern cultivar. Rice 3:138–147CrossRefGoogle Scholar
  10. Blom CWPM., Voesenek LACJ. (1996) Flooding: the survival strategies of plants. Trends Ecol Evol 11:290–295CrossRefPubMedGoogle Scholar
  11. Catling D (1992) Rice in deep water. MacMillan, LondonCrossRefGoogle Scholar
  12. Chu YE, Morishima H, Oka HI (1969) Reproductive barriers distributed in cultivated rice species and their wild relatives. Jpn J Genet 44:207–223CrossRefGoogle Scholar
  13. Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034CrossRefPubMedCentralPubMedGoogle Scholar
  14. Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030CrossRefPubMedGoogle Scholar
  15. Kende H, van der Knaap E, Cho HT (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110CrossRefPubMedCentralPubMedGoogle Scholar
  16. Okishio T, Sasayama D, Hirano T, Akimoto M, Itoh K, Azuma T (2014) Growth promotion and inhibition of the Amazonian wild rice species Oryza grandiglumis to survive flooding. Planta 240:459–469CrossRefPubMedGoogle Scholar
  17. Okishio T, Sasayama D, Hirano T, Akimoto M, Itoh K, Azuma T (2015) Ethylene in not involved in adaptive responses to flooding in the Amazonian wild rice species Oryza grandiglumis. J Plant Physiol 174:49–54CrossRefPubMedGoogle Scholar
  18. Piedade MTF, Junk WJ, Long SP (1991) The productivity of the C4 grass Echinochloa polystachya on the Amazon floodplain. Ecology 72:1456–1463CrossRefGoogle Scholar
  19. Raskin I, Kende H (1984) Regulation of growth in stem sections of deep-water rice. Planta 60:66–72CrossRefGoogle Scholar
  20. Setter TL, Laureles EV (1996) The beneficial effect of reduced elongation growth on submergence tolerance of rice. J Exp Bot 74:1551–1559CrossRefGoogle Scholar
  21. Vaughan DA (1994) The wild relatives of rice: a genetic resources handbook. International Rice Research Institute, ManilaGoogle Scholar
  22. Voesenek LACJ, Sasidharan R (2013) Ethylene– and oxygen signalling–drive plant survival during flooding. Plant Biol 15:426–435CrossRefPubMedGoogle Scholar
  23. Wang ZY, Second G, Tanksley SD (1992) Polymorphism and phylogenetic relationships among species in the genus Oryza as determined by analysis of nuclear RFLPs. Theor Appl Genet 83:565–581CrossRefPubMedGoogle Scholar
  24. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Daisuke Sasayama
    • 1
  • Takuma Okishio
    • 1
    • 2
  • Tatsuya Hirano
    • 3
  • Hiroshi Fukayama
    • 1
  • Tomoko Hatanaka
    • 1
  • Masahiro Akimoto
    • 4
  • Tetsushi Azuma
    • 1
  1. 1.Graduate School of Agricultural ScienceKobe UniversityKobeJapan
  2. 2.Leaf Tobacco Research CenterJapan Tobacco Inc.OyamaJapan
  3. 3.Graduate School of Agricultural ScienceMeijo UniversityNagoyaJapan
  4. 4.School of AgricultureObihiro University of Agriculture and Veterinary MedicineObihiroJapan

Personalised recommendations