Skip to main content
SpringerLink
Log in

Role of Ethylene and Other Plant Hormones in Orchestrating the Responses to Low Oxygen Conditions

  • Chapter
  • First Online:
Low-Oxygen Stress in Plants

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 21))

Abstract

Flooding results in an altered physical environment with a drastically reduced diffusion rate for gases into and from the submerged plant parts. The gaseous hormone ethylene inevitably accumulates in submerged tissue even at low rates of synthesis. Not surprisingly, ethylene is used by plants to regulate many of the adaptations plants have evolved to cope with submergence stress. Even more so, the ethylene precursor 1-aminocyclopropane-1-carboxylic acid acts as a mobile signal to promote a systemic response in root waterlogged plants. Regulation of ethylene synthesis and signaling contribute to timely and coordinated adaptive responses. In many instances ethylene acts in concert with gibberellic acid (GA) and abscisic acid (ABA) signaling either by interacting with the biosynthetic or catabolic pathways or with signaling pathways. Changes in ethylene, GA and ABA levels, and consequently in hormone signaling bring about many of the adaptive responses to flooding including acceleration or deceleration of shoot growth, adventitious root growth, and aerenchyma formation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Amrhein N, Breuing F, Eberle J, Skorupka H, Tophof S (1982) The metabolism of 1-aminocycloproprane-1-carboxylic acid. In: Waering PF (ed) Plant growth substances. Academic, New York, pp 249–258

    Google Scholar 

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–232

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LA, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138

    Article  CAS  PubMed  Google Scholar 

  • Banga M, Slaa EJ, Blom C, Voesenek L (1996) Ethylene biosynthesis and accumulation under drained and submerged conditions (A comparative study of two Rumex species). Plant Physiol 112:229–237

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benschop JJ, Jackson MB, Gühl K, Vreeburg RA, Croker SJ, Peeters AJ, Voesenek LA (2005) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768

    Article  CAS  PubMed  Google Scholar 

  • Bradford KJ, Yang SF (1980) Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol 65:322–326

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bradford KJ, Hsiao T, Yang SF (1982) Inhibition of ethylene synthesis in tomato plants subjected to anaerobic root stress. Plant Physiol 70:1503–1507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cao Y, Song F, Goodman RM, Zheng Z (2006) Molecular characterization of four rice genes encoding ethylene-responsive transcriptional factors and their expressions in response to biotic and abiotic stress. J Plant Physiol 163:1167–1178

    Article  CAS  PubMed  Google Scholar 

  • Chae HS, Kieber JJ (2005) Eto Brute? The role of ACS turnover in regulating ethylene biosynthesis. Trends Plant Sci 10:291–296

    Article  CAS  PubMed  Google Scholar 

  • Cox MC, Benschop JJ, Vreeburg RA, Wagemaker CA, Moritz T, Peeters AJ, Voesenek LA (2004) The roles of ethylene, auxin, abscisic acid, and gibberellin in the hyponastic growth of submerged Rumex palustris petioles. Plant Physiol 136:2948–2960

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dorling SJ, McManus MT (2012) The fate of ACC in higher plants. In: McManus M (ed) The plant hormone ethylene. Annual plant reviews, vol 44. Wiley-Blackwell Press, Massey, New Zealand, pp 83–115

    Chapter  Google Scholar 

  • Else MA, Coupland D, Dutton L, Jackson MB (2001) Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiol Plant 111:46–54

    Article  CAS  Google Scholar 

  • Else MA, Taylor JM, Atkinson CJ (2006) Anti-transpirant activity in xylem sap from flooded tomato (Lycopersicon esculentum Mill.) plants is not due to pH-mediated redistributions of root- or shoot-sourced ABA. J Exp Bot 57:3349–3357

    Article  CAS  PubMed  Google Scholar 

  • English PJ, Lycett GW, Roberts JA, Jackson MB (1995) Increased 1-aminocyclopropane-1-carboxylic acid oxidase activity in shoots of flooded tomato plants raises ethylene production to physiologically active levels. Plant Physiol 109:1435–1440

    CAS  PubMed Central  PubMed  Google Scholar 

  • Finlayson SA, Foster KR, Reid DM (1991) Transport and metabolism of 1-aminocyclopropane-1-carboxylic acid in sunflower (Helianthus annuus L.) seedlings. Plant Physiol 96:1360–1367

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gao XH, Xiao SL, Yao QF, Wang YJ, Fu XD (2011) An updated GA signaling ‘relief of repression’ regulatory model. Mol Plant 4:601–606

    Article  CAS  PubMed  Google Scholar 

  • Geisler-Lee J, Caldwell J, Gallie DR (2010) Expression of the ethylene biosynthetic machinery in maize roots is regulated in response to hypoxia. J Exp Bot 61:857–871

    Article  CAS  PubMed  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene related mutants. Plant Cell 2:513–523

    CAS  PubMed Central  PubMed  Google Scholar 

  • Harpaz-Saad S, Yoon GM, Mattoo AK, Kieber JJ (2012) The formation of ACC and competition between polyamines and ethylene for SAM. In: McManus M (ed) The plant hormone ethylene. Annual plant reviews, vol 44. Wiley-Blackwell Press, Massey, New Zealand, pp 53–81

    Chapter  Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto 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 460:1026–1030

    Article  CAS  PubMed  Google Scholar 

  • He CJ, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiol 112:1679–1685

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hess N, Klode M, Anders M, Sauter M (2011) The hypoxia responsive transcription factor genes ERF71/HRE2 and ERF73/HRE1 of Arabidopsis are differentially regulated by ethylene. Physiol Plant 143:41–49

    Article  CAS  PubMed  Google Scholar 

  • Hoffman NE, Yang SF, McKeon T (1982) Identification of 1-(malonylamino)cyclopropane-1-carboxylic acid as a major conjugate of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor in higher plants. Biochem Biophys Res Commun 104:765–770

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hsu FC, Chou MY, Peng HP, Chou SJ, Shih MC (2011) Insights into hypoxic systemic responses based on analyses of transcriptional regulation in Arabidopsis. PLoS One 6(12):e28888

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ikeda A, Ueguchi-Tanaka M, Sonoda Y, Kitano H, Koshioka M, Futsuhara Y, Matsuoka M, Yamaguchi J (2001) Slender rice, a constitutive gibberellin response mutant, is caused by a null mutation of the SLR1 gene, an ortholog of the height-regulating gene GAI/RGA/RHT/D8. Plant Cell 13:999–1010

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ikeda A, Sonoda Y, Vernieri P, Perata P, Hirochika H, Yamaguchi J (2002) The slender rice mutant, with constitutively activated gibberellin signal transduction, has enhanced capacity for abscisic acid level. Plant Cell Physiol 43:974–979

    Article  CAS  PubMed  Google Scholar 

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Itoh H, Asako Shimada A, Ueguchi-Tanaka M, Kamiya N, Hasegawa Y, Ashikari M, Matsuoka M (2005) Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. Plant J 44:669–679

    Article  CAS  PubMed  Google Scholar 

  • Jackson MB (2002) Long-distance signalling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–181

    Article  CAS  PubMed  Google Scholar 

  • Jiao XZ, Philosophhadas S, Su LY, Yang SF (1986) The conversion of 1-(malonylamino)cyclopropane-1-carboxylic acid to 1-aminocyclopropane-1-carboxylic acid in plant tissues. Plant Physiol 81:637–641

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joshi-Saha A, Valon C, Leung J (2012) A brand new START: abscisic acid perception and transduction in the guard cell. Sci Signal 4(201):re4

    Google Scholar 

  • Kamiyoshihara Y, Iwata M, Fukaya T, Tatsuki M, Mori H (2010) Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphyrylation/dephosphorylation. Plant J 64:140–150

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Y, Hoffman NE, Yang SF (1983) Relationship between the malonylation of 1-aminocyclopropane-1-carboxylic acid and D-amino acids in mung-bean hypocotyls. Planta 158:437–441

    Article  CAS  PubMed  Google Scholar 

  • Lorbiecke R, Sauter M (1999) Adventitious root growth and cell cycle induction in deepwater rice (Oryza sativa L.). Plant Physiol 119:21–29

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Martin MN, Saftner RA (1995) Purification and characterization of 1-aminocyclopropane-1-carboxylic acid N-malonyltransferase from tomato fruit. Plant Physiol 108:1241–1249

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mergemann H, Sauter M (2000) Programmed death of epidermal cells facilitates emergence of adventitious roots in deepwater rice. Plant Physiol 124:609–614

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peiser G, Yang SF (1998) Evidence for 1-(malonylamino)cyclopropane-1-carboxylic acid being the major conjugate of aminocyclopropane-1-carboxylic acid in tomato fruit. Plant Physiol 116:1527–1532

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peng HP, Lin T-Y, Wang N-N, Shih MC (2005) Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58:15–25

    Article  CAS  PubMed  Google Scholar 

  • Qi W, Sun F, Wang Q, Chen M, Huang Y, Feng YQ, Luo X, Yang J (2011) Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a gibberellin biosynthetic gene. Plant Physiol 157:216–228

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rodriguez-Gamir J, Ancillo G, Gonzalez-Mas MC, Millo E, Iglesias DJ, Forner-Giner MA (2011) Root signalling and modulation of stomatal closure in flooded citrus seedlings. Plant Physiol Biochem 49:636–645

    Article  CAS  PubMed  Google Scholar 

  • Rzewuski G, Sauter M (2008) Ethylene biosynthesis and signaling in rice. Plant Sci 175:32–42

    Article  CAS  Google Scholar 

  • Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K et al (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sasidharan R, Mustroph A (2011) Plant oxygen sensing is mediated by the N-end rule pathway: a milestone in plant anaerobiosis. Plant Cell 23:4173–4183

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sauter M (1997) Differential expression of a CAK (cdc2-activating kinase)-like protein kinase, cyclins and cdc2 genes from rice during the cell cycle and in response to gibberellin. Plant J 11:181–190

    Article  CAS  PubMed  Google Scholar 

  • Sauter M, Kende H (1992) Gibberellin-induced growth and regulation of the cell division cycle in deepwater rice. Planta 188:362–368

    Article  CAS  PubMed  Google Scholar 

  • Sauter M, Mekhedov SL, Kende H (1995) Gibberellin promotes histone H1 kinase activity and the expression of cdc2 and cyclin genes during the induction of rapid growth in deepwater rice internodes. Plant J 7:623–632

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Tan BC, Gage DA, Zeevaart JA, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874

    Article  CAS  PubMed  Google Scholar 

  • Shiu OY, Oetiker JH, Yip WK, Yang SF (1998) The promoter of LE-ACS7, an early flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of the tomato, is tagged by a Sol3 transposon. Proc Natl Acad Sci U S A 95:10334–10339

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Skottke KR, Yoon GM, Kieber JJ (2011) Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet 7:e1001370

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steffens B, Sauter M (2009) Epidermal cell death in rice is confined to cells with a distinct molecular identity and is mediated by ethylene and H2O2 through an autoamplified signal pathway. Plant Cell 21:184–196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Steffens B, Wang J, Sauter M (2006) Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice. Planta 223:604–612

    Article  CAS  PubMed  Google Scholar 

  • Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21:R338–R3345

    Article  CAS  PubMed  Google Scholar 

  • Tsuchisaka A, Theologis A (2004) Unique and overlapping expression patterns among the Arabidopsis 1-aminocyclopropane-1-carboxylate synthase gene family members. Plant Physiol 136:2982–3000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tsuchisaka A, Yu G, Jin H, Theologis A (2009) A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate synthase isoforms regulates ethylene biosyntehsis. Genetics 183:979–1003

    Article  CAS  PubMed  Google Scholar 

  • Tudela D, Primo-Millo E (1992) 1-Aminocyclopropane-1-carboxylic acid transported from roots to shoots promotes leaf abscission in Cleopatra Mandarin (Citrus reshni Hort. ex Tan.) seedlings rehydrated after water stress. Plant Physiol 100:131–137

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van der Straeten D, Zhou HA, Van Onckelen MC, Van Montagu MC (2001) A comparative molecular-physiological study of submergence response in lowland and deepwater rice. Plant Physiol 125:955–968

    Article  Google Scholar 

  • Vandenbussche F, Vaseva I, Vissenberg K, Van Der Straeten D (2012) Ethylene in vegetative development: a tale with a riddle. New Phytol 194:895–909

    Article  CAS  PubMed  Google Scholar 

  • Voesenek LA, Colmer TD, Pierik R, Millenaar FF, Peeters AJ (2006) How plants cope with complete submergence. New Phytol 170:213–226

    Article  CAS  PubMed  Google Scholar 

  • Vriezen WH, Hulzink R, Mariani C, Voesenek LA (1999) 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. Plant Physiol 121:189–196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 442:705–708

    Article  CAS  PubMed  Google Scholar 

  • Yaish MW, El-Kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ (2010) The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genet 6(9):e1001098

    Article  PubMed Central  PubMed  Google Scholar 

  • Yang S-H, Choi D (2006) Characterization of genes encoding ABA 8′-hydroxylase in ethylene-induced stem growth of deepwater rice (Oryza sativa L.). Biochem Biophys Res Commun 350:685–690

    Article  CAS  PubMed  Google Scholar 

  • Yang SF, Hoffman NE (1984) Ethylene biosynthesis and its regulation in higher plants. Annu Rev Plant Physiol 35:155–189

    Article  CAS  Google Scholar 

  • Yasumura Y, Pierik R, Fricker MD, Voesenek LA, Harberd NP (2012) Studies of Physcomitrella patens reveal that ethylene-mediated submergence responses arose relatively early in land-plant evolution. Plant J 72:947–959

    Google Scholar 

  • Yip W-K, Jiao X-Z, Yang SF (1988) Dependence of in vivo ethylene production rate on 1-aminocyclopropane-1-carboxylic acid content and oxygen concentrations. Plant Physiol 88:553–558

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshida H, Nagata M, Saito K et al (2005) Arabidopsis ETO1 specifically interacts with and negatively regulates type-2 1-aminocyclopropane-1-carboxylate synthases. BMC Biol 5:14

    Google Scholar 

  • Zarembinski TI, Theologis A (1997) Expression characteristics of Os-ACS1 and Os-ACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase family in rice (Oryza sativa L., cv. Habiganj Aman II) during partial submergence. Plant Mol Biol 33:71–77

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plant Developmental Biology and Plant Physiology, Institute of Botany, University of Kiel, 24118, Kiel, Germany

    Bianka Steffens & Margret Sauter

Authors
  1. Bianka Steffens
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Margret Sauter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Margret Sauter .

Editor information

Editors and Affiliations

  1. RWTH Aachen University, Aachen, Germany

    Joost T. van Dongen

  2. Scuola Superiore Sant´Anna, Pisa, Italy

    Francesco Licausi

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Wien

About this chapter

Cite this chapter

Steffens, B., Sauter, M. (2014). Role of Ethylene and Other Plant Hormones in Orchestrating the Responses to Low Oxygen Conditions. In: van Dongen, J., Licausi, F. (eds) Low-Oxygen Stress in Plants. Plant Cell Monographs, vol 21. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1254-0_7

Download citation

Publish with us

Policies and ethics

Search

Navigation