Abstract
The role of ethylene in induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema zawadskii and D. nankingense, two species that differ with respect to waterlogging tolerance, was examined. In the more tolerant D. zawadskii, but not in D. nankingense, ethylene accelerated programmed cell death and promoted formation of lysigenous aerenchyma, both of which were inhibited by treatment with the ethylene inhibitor 1-methylcyclopropene. Waterlogged D. zawadskii roots generated a higher quantity of endogenous ethylene than did those of D. nankingense. In waterlogged D. zawadskii roots, transcription of the genes encoding alcohol dehydrogenase (EC 1.1.1.1) and pyruvate decarboxylase (EC 4.1.1.1) increased rapidly but transiently, whereas expression of these genes in D. nankingense increased gradually and over a longer period. In D. nankingense, waterlogging elevated both alcohol dehydrogenase and pyruvate decarboxylase activity, and the production of ethanol and acetaldehyde was increased in the presence of exogenous ethylene and inhibited by 1-methylcyclopropene. In D. zawadskii, in contrast, after a prolonged episode of waterlogging stress, exogenous supply of ethylene suppressed the production of ethanol and acetaldehyde, whereas exogenous 1-methylcyclopropene enhanced their production. In the more tolerant Dendranthema species, ethylene appeared to signal an acceleration of both waterlogging-induced programmed cell death and aerenchyma formation and to alleviate ethanolic fermentation, whereas in the more sensitive species ethylene activated fermentation and increased the release of ethanol and acetaldehyde, which are by-products probably responsible for the collapse of the waterlogging-damaged root.
Similar content being viewed by others
References
Bleecker A, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18
Yang S, Hoffman N (1984) Ethylene biosynthesis and its regulation in higher plants. Ann Rev Plant Physiol 35:155–189
Geisler-Lee J, Caldwell C, Gallie DR (2010) Expression of the ethylene biosynthetic machinery in maize roots is regulated in response to hypoxia. J Exp Bot 61:857–871
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 18:2021–2034
Peeters AJM, Cox MCH, Benschop JJ, Vreeburg RAM, Voesenek LACJ (2002) Submergence research using Rumex palustris as a model; looking back and going forward. J Exp Bot 53:391–398
Cox JW, Pitman A, Bellotti WD (2004) The role of shallow drains in removing ‘Excess’ water from texture-contrast soils. In: Dogramaci S, Waterhouse A (eds) Engineering salinity Solutions: 1st national salinity engineering conference Barton ACT: engineers australia, pp 78–83
Banga M, Bogemann GM, Blom CWPM, Voesenek LACJ (1997) Flooding resistance of Rumex species strongly depends on their response to ethylene: rapid shoot elongation or foliar senescence. Physiol Plant 99:415–422
Hattori Y, Nagai K, Furukawa S, Song X, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters AJM (2006) How plants cope with complete submergence? New Phytol 170:213–226
Jackson MB, Ishizawa K, Ito O (2009) Evolution and mechanisms of plant tolerance to flooding stress. Ann Bot 103:137–142
Evans D (2004) Tansley review: aerenchyma formation. New Phytol 161:35–49
Kratsch HA, Graves WR (2005) Oxygen concentration affects nodule anatomy and nitrogenase activity of Alnus maritime. Plant Cell Environ 28:688–696
Pang J, Cuin T, Shabala L, Zhou M, Mendham N, Shabala S (2007) Effect of secondary metabolites associated with anaerobic soil conditions on ion fluxes and electrophysiology in barley roots. Plant Physiol 145:266–276
Pennell RI, Lamb C (1997) Programmed cell death in plants. Plant Cell 9:1157–1168
Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127
Steffens B, Sauter M (2005) Epidermal cell death in rice is regulated by ethylene gibberellin and abscisic acid. Plant Physiol 139:713–721
Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378
Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124:609–614
Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190:289–298
Visser E, Bögemann G (2006) Aerenchyma formation in the wetland plant Juncus effusus is independent of ethylene. New Phytol 171:305–314
Irfan M, Hayat S, Hayat Q, Afroz S, Ahmad A (2010) Physiological and biochemical changes in plants under waterlogging. Protoplasma 241:3–17
Peng HP, Chan CS, Shih MC, Yang SF (2001) Signaling events in the hypoxic induction of alcohol dehydrogenase gene in Arabidopsis. Plant Physiol 126:742–749
Yin D, Chen S, Chen F, Guan Z, Fang W (2009) Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. Environ Exp Bot 67:87–93
Yin D, Chen S, Chen F, Guan Z, Fang W (2010) Morpho-anatomical and physiological responses of two Dendranthema species to waterlogging. Environ Exp Bot 68:122–130
Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208
Gaff DF, Okong’O-Ogola O (1971) The use of nonpermeating pigments for testing the survival of cells. J Exp Bot 22:756–758
Kato-Noguchi H, Watada A (1997) Effects of low-oxygen atmosphere on ethanolic fermentation in fresh-cut carrots. J Am Soc Hortic Sci 122:107–111
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding. Anal Biochem 72:248–254
Yang D, Yun P, Park S, Plaha P, Lee D, Lee I, Kim Y, Hwang Y, Lee J, Han B, Lee S, Suh E, Lim Y (2005) Cloning characterization and expression of a lateral supperessor-like gene from chrysanthemum (Dendranthema grandiflorum Kitamura). Plant Physiol Biochem 43:1044–1051
Mühlenbock P, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell 19:3819–3830
Drew MC, He CJ, Morgan PW (2000) Ethylene-triggered cell death during aerenchyma formation in roots. Symp Soc Exp Biol 52:183–192
Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500
Baxter-Burrell A, Chang R, Springer P, Bailey-Serres J (2003) Gene and enhancer trap transposable elements reveal oxygen deprivation-regulated genes and their complex patterns of expression in Arabidopsis. Ann Bot 9:129–141
Kürsteiner O, Dupuis I, Kuhlemeier C (2003) The pyruvate decarboxylase1 gene of Arabidopsis is required during anoxia but not other environmental stresses. Plant Physiol 132:968–978
Chen HJ, Qualls RG, Miller GC (2002) Adaptive responses of Lepidium latifolium to soil flooding: biomass allocation adventitious rooting aerenchyma formation and ethylene production. Environ Exp Bot 48:119–128
Hinz M, Wilson I, Yang J, Buerstenbinder K, Llewellyn D, Dennis E, Sauter M, Dolferus R (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 153:757–772
Gunawardena A, Pearce D, Jackson M, Hawes C, Evans D (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L). Planta 212:205–214
Perata P, Voesenek L (2007) Submergence tolerance in rice requires Sub1A an ethylene-response-factor-like gene. Trends Plant Sci 12:43–46
Suralta RR, Yamauchi A (2008) Root growth aerenchyma development and oxygen transport in rice genotypes subjected to drought and waterlogging. Environ Exp Bot 64:75–82
Vodnik D, Strajnar P, Jemc S, Macek I (2009) Respiratory potential of maize (Zea mays L) roots exposed to hypoxia. Environ Exp Bot 65:107–110
Acknowledgments
This work was supported by the Fundamental Research Fund for Central Universities (KYJ 200907), the National Natural Science Foundation of China (grant nos. 30872064, 31071820, and 31071825), the Jiangsu Province Research and Innovation Program for College Graduates (CX10B_320Z), the Program for New Century Excellent Talents in University of the Chinese Ministry of Education (grant no. NCET-10-0492), and the Shanghai Institute of Technology Scientific Research Foundation for Introduced Talent (YJ2012-25) and the Excellent Young Teachers Training Program of Shanghai University (ZZyyy12038). We are grateful to Professor David B. Hannaway of the College of Agricultural Sciences, Department of Crop and Soil Science, Oregon State University, USA, for helpful discussions and improvements to the manuscript. The authors thank AgroFresh Inc. China for providing the 1-MCP (SmartFresh™).
Author information
Authors and Affiliations
Corresponding author
Additional information
Dongmei Yin and Sumei Chen contributed equally to this work.
Rights and permissions
About this article
Cite this article
Yin, D., Chen, S., Chen, F. et al. Ethylene promotes induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema spp.. Mol Biol Rep 40, 4581–4590 (2013). https://doi.org/10.1007/s11033-013-2550-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-013-2550-2