Skip to main content
Log in

Brassinosteroid signaling modulates submergence-induced hyponastic growth in Arabidopsis thaliana

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The role of brassinosteroids (BRs) in hyponastic growth induced by submergence was investigated in Arabidopsis thaliana. Under flooding conditions, exogenously applied BRs increased hyponastic growth of rosette leaves. This hyponastic growth was reduced in a BR insensitive mutant (bri1-5), while it was increased in a BR dominant mutant (bes1-D). Further, expression of hypoxia marker genes, HRE1 and HRE2, was elevated in submerged bes1-D. These results indicate that BRs exert a positive action on hyponastic growth of submerged Arabidopsis leaves. Expression of ethylene biosynthetic genes, such as ACS6, ACS8 and ACO1, which are up-regulated by submergence, was also activated by application of BRs and in bes1-D. The enhanced hyponastic growth in submerged bes1-D was significantly reduced by application of cobalt ion, suggesting that BRs control hyponastic growth via ethylene, which seems to be synthesized by ACO6 and ACO8 followed by ACO1 in submerged leaves. A double mutant, bes1-Dxaco1-1, showed hyponastic growth activity similar to that seen in aco1-1, demonstrating that the BR signaling for regulation of hyponastic growth seems to be an upstream event in ethylene-induced hyponastic growth under submergence in Arabidopsis.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Arteca RN, Tsai DS, Schlagnhaufer C, Mandava NB (1983) The effect of brassinosteroid on auxin-induced ethylene production by etiolated mung bean segments. Physiol Plant 59:539–544

    Article  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 

  • Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: Essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451

    Article  CAS  PubMed  Google Scholar 

  • Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36

    Article  CAS  Google Scholar 

  • Colmer TD, Gibberd MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solutions. J Exp Bot 49:1431–1436

    Article  CAS  Google Scholar 

  • Cox MCH, Benschop JJ, Vreeburg RAM, Wagemaker CA, Moritz T, Peeters AJM, Voesenek LACJ (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  PubMed Central  Google Scholar 

  • Cox MCH, Millenaar FF, de Jong vanBerkel YEM, Peeters AJM, Voesenek LACJ (2003) Plant movement. Submergence-induced petiole elongation in Rumex palustris depends on hyponastic growth. Plant Physiol 132:282–291

    CAS  PubMed  Google Scholar 

  • Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49

    Article  Google Scholar 

  • Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia. Is survival a balancing act? Trends Plant Sci 9:1403–1409

    Google Scholar 

  • Gendron JM, Haque A, Gendron N, Chang T, Asami T, Wang Z (2008) Chemical genetic dissection of brassinosteroid-ethylene interaction. Mol Plant 1:368–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbs J, Greenway H (2003) Review: Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47

    Article  CAS  Google Scholar 

  • Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004). Comprehensive comparison brassinosteroid-regulated of auxinregulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 134:1555–1573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Lim MA, Valdes-Lopez V, Cruz-Hernandez A, Saucedo-Arias LJ (1993) Isolation and characterization of a gene involved in ethylene biosynthesis from Arabidopsis thaliana. Gene 134: 217–221

    Article  CAS  PubMed  Google Scholar 

  • Halliday KJ (2004) Plant hormones: the interplay of brassinosteroids and auxin. Curr Biol 14:1008–1010

    Article  Google Scholar 

  • Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot 101:229–248

    Article  CAS  PubMed  Google Scholar 

  • Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxiainducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62:302–315

    Article  CAS  PubMed  Google Scholar 

  • Lim SH, Chang SC, Lee JS, Kim SK, Kim SY (2002) Brassinosteroids affect ethylene production in the primary roots of maize (Zea mays L.) J Plant Biol 45:148–153

    Article  CAS  Google Scholar 

  • Millenaar FF, Cox MCH, de Jong-van Berkel YEM, Welschen RAM, Pierik R, Voesenek LACJ, Peeters AJM (2005) Ethylene-induced differential growth of petioles in Arabidopsis Analyzing natural variation, response kinetics, and regulation. Plant Physiol 137: 998–1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Millenaar FF, van Zanten M, Cox MCH, Pierik R, Voesenek LACJ, Peeters AJM (2009) Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation. New Phytol 184:141–152

    Article  CAS  PubMed  Google Scholar 

  • Mitchell JW, Mandava N, Worley JF, Plimmer JR, Smith MV (1970) Brassins: a new family of plant hormones from rape pollen. Nature 225:1065–1066

    Article  CAS  PubMed  Google Scholar 

  • Mommer L, Pons TL, Wolters-Arts M, Venema JH, Visser EJW (2005) Submergence-induced morphological, anatomical, and biochemical responses in a terrestrial species affects gas diffusion resistance and photosynthetic performance. Plant Physiol 139:497–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann Bot 96:581–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura A, Higuchi K, Goda H, Fujiwara MT, Sawa S, Koshiba T, Shimada Y, Yoshida S (2003) Brassinolide induces IAA5, IAA19, and DR5, a synthetic auxin response element in Arabidopsis, implying a cross talk point of brassinosteroid and auxin signaling. Plant Physiol 133:1843–1853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nemhauser J, Mockler T, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:1460–1471

    Article  CAS  Google Scholar 

  • Perata P, Voesenek LACJ (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci 12:43–46

    Article  CAS  PubMed  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    Article  CAS  PubMed  Google Scholar 

  • Polko JK, van Zanten M, van Rooij JA, Marée AFM, Voesenek LACJ, Peeters AJM, Pierik R (2012) Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion. New Phytol 193:339–348

    Article  CAS  PubMed  Google Scholar 

  • Polko JK, Pierik R, van Zanten M, Tarkowská D, Strnad M, Voesenek LACJ, Peeters AJM (2013) Ethylene promotes hyponastic growth through interaction with ROTUNDIFOLIA3/CYP90C1 in Arabidopsis. J Exp Bot 64:613–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rauf M, Arif M, Fisahn J, Xue GP, Balazadeh S, Mueller-Roeber B (2013) NAC transcription factor SPEEDY HYPONASTIC GROWTH regulates flooding-induced leaf movement in Arabidopsis. Plant Cell 25:4941–4955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raz V, Ecker JR. (1999) Regulation of differential growth in the apical hook of Arabidopsis. Development 126:3661–3668

    CAS  PubMed  Google Scholar 

  • Rieu I, Cristescu SM, Harren FJM, Huibers W, Voesenek LACJ, Mariani C, Vriezen WH (2005) RP-ACS1, a flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of Rumex palustris, is involved in rhythmic ethylene production. J Exp Bot 56:841–849

    Article  CAS  PubMed  Google Scholar 

  • Sasse, JM (2003) Physiological actions of brassinosteroids: An update. J Plant Growth Regul 22:276–288

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schmitz AJ, Folsom JJ, Jikamaru Y, Ronald P, Walia H (2013) SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. New Phytol 198:1060–1070

    Article  CAS  PubMed  Google Scholar 

  • Setter TL, Laureles EV (1996) The beneficial effect of reduced elongation growth on submergence tolerance of rice. J Exp Bot 47:1551–1559

    Article  CAS  Google Scholar 

  • Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34

    Article  CAS  Google Scholar 

  • Van der Straeten D, Zhou Z, Prinsen E, Van Onckelen HA, 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 

  • Van Zanten M, Basten Snoek L, van Eck-Stouten E, Proveniers MCG, Torii KU, Voesenek LACJ, Peeters AJM, Millenaar FF (2010) Ethylene-induced hyponastic growth in Arabidopsis thaliana is controlled by ERECTA. Plant J 61:83–95

    Article  PubMed  Google Scholar 

  • Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by auxin response factor 2. Proc Natl Acad Sci USA 105:9829–9834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Visser EJW, Blom CWPM, Voesenek LACJ (1996) Flooding-induced adventitious rooting in Rumex: morphology and development in an ecological perspective. Acta Bot Neerl 45:17–28

    Article  Google Scholar 

  • Visser EJW, Bögemann GM, Van de Steeg HM, Pierik R, Blom CWPM (2000) Flooding tolerance of Carex species in relation to field distribution and aerenchyma formation. New Phytol 148:93–103

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Voesenek LACJ, Rijnders JHGM, Peeters AJM, Van de Steeg HM, de Kroon H (2004) Plant hormones regulate fast shoot elongation under water: from genes to community. Ecology 85:16–27

    Article  Google Scholar 

  • Vriezen WH, De Graaf B, Mariani C, Voesenek LACJ (2000) Submergence induces expansin gene expression in floodingtolerant Rumex palustris and not in flooding-intolerant R. acetosa. Planta 210:956–963

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Seong-Ki Kim.

Additional information

These authors contribute equally to this work.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Youn, J.H., Kang, S.H., Roh, J. et al. Brassinosteroid signaling modulates submergence-induced hyponastic growth in Arabidopsis thaliana . J. Plant Biol. 59, 397–404 (2016). https://doi.org/10.1007/s12374-016-0160-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0160-y

Keywords

Navigation