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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339
Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: Essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451
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
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
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
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
Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49
Fukao T, Bailey-Serres J (2004) Plant responses to hypoxia. Is survival a balancing act? Trends Plant Sci 9:1403–1409
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
Gibbs J, Greenway H (2003) Review: Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Funct Plant Biol 30:1–47
Goda H, Shimada Y, Asami T, Fujioka S, Yoshida S (2002) Microarray analysis of brassinosteroid-regulated genes in Arabidopsis. Plant Physiol 130:1319–1334
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
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
Halliday KJ (2004) Plant hormones: the interplay of brassinosteroids and auxin. Curr Biol 14:1008–1010
Jackson MB (2008) Ethylene-promoted elongation: an adaptation to submergence stress. Ann Bot 101:229–248
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
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
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
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
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
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
Mommer L, Visser EJW (2005) Underwater photosynthesis in flooded terrestrial plants: a matter of leaf plasticity. Ann Bot 96:581–589
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
Nemhauser J, Mockler T, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:1460–1471
Perata P, Voesenek LACJ (2007) Submergence tolerance in rice requires Sub1A, an ethylene-response-factor-like gene. Trends Plant Sci 12:43–46
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
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
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
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
Raz V, Ecker JR. (1999) Regulation of differential growth in the apical hook of Arabidopsis. Development 126:3661–3668
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
Sasse, JM (2003) Physiological actions of brassinosteroids: An update. J Plant Growth Regul 22:276–288
Sauter M (2000) Rice in deep water: “How to take heed against a sea of trouble”. Naturwissenschaften 87:289–303
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
Setter TL, Laureles EV (1996) The beneficial effect of reduced elongation growth on submergence tolerance of rice. J Exp Bot 47:1551–1559
Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34
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
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
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
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
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
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence. New Phytol 170:213–226
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
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
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
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contribute equally to this work.
Electronic supplementary material
Rights and permissions
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-016-0160-y