Abstract
The antioxidant enzyme activities and gene expressions in leaves of Kentucky bluegrass (Poa pratensis L.) were investigated in response to waterlogging stress and subsequent drainage. Two cultivars contrasting in waterlogging tolerance, ‘Moonlight’ (waterlogging-tolerant) and ‘Kenblue’ (waterlogging-sensitive), were subjected to waterlogging for 28 days (d) followed by 7 d of drainage recovery. Waterlogging stress increased malondialdehyde (MDA), superoxide anion (O ·−2 ) and hydrogen peroxide (H2O2) in both cultivars. Moonlight exhibited greater turfgrass quality (TQ) rating and chlorophyll (Chl) content than Kenblue during the waterlogging and drainage period. After 7 d of drainage, all physiological parameters returned to the control level for Moonlight, but not for Kenblue. Higher activities of superoxide dismutase (SOD), catalase (CAT) and ascorbate peroxidase (APX) as well as more abundance of isozymes were found in Moonlight relative to Kenblue under waterlogging stress. Moonlight showed higher SOD and APX activity and isozymes intensity when compared with Kenblue during the drainage period. The transcript levels of chloroplastic Cu/ZnSOD (Chl Cu/ZnSOD), MnSOD, FeSOD, POD and cytosolic APX (Cyt APX) were higher in Moonlight relative to Kenblue under waterlogging conditions, and higher transcript activities of Chl Cu/ZnSOD, FeSOD and Cyt APX were observed in Moonlight than in Kenblue at 7 d of drainage. The results of this study indicate that higher SOD and APX activity, isozymes intensity and gene expression level in Moonlight relative to Kenblue may play crucial roles in Kentucky bluegrass tolerance to waterlogging stress.
Similar content being viewed by others
Abbreviations
- APX:
-
Ascorbate peroxidase
- CAT:
-
Catalase
- Chl:
-
Chlorophyll
- H2O2 :
-
Hydrogen peroxide
- MDA:
-
Malondialdehyde
- O ·−2 :
-
Superoxide anion
- PAR:
-
Photosynthetically active radiation
- POD:
-
Guaiacol peroxidase
- ROS:
-
Reactive oxygen species
- SOD:
-
Superoxide dismutase
- TQ:
-
Turfgrass quality
References
Ahmed S, Nawata E, Hosokawa M, Domae Y, Sakuratani T (2002) Alterations in photosynthesis and some antioxidant enzymatic activities of mungbean subjected to waterlogging. Plant Sci 163:117–123
Amako K, Chen GX, Asada K (1994) Separate assays specific for ascorbate peroxidase and guaiacol peroxidase and for the chloroplastic and cytosolic isozymes of ascorbate peroxidase in plants. Plant Cell Physiol 35:497–504
Bai TH, Li CY, Ma FW, Feng FJ, Shu HR (2010) Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant Soil 327:95–105
Beauchamp CO, Fridovich I (1973) Isozymes of superoxide dismutase from wheat germ. Biochim Biophys Acta 317:50–64
Bian SM, Jiang YW (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Sci Hortic 120:264–270
Blokhina O, Virolainen E, Fagestedt KV (2003) Antioxidants, oxidative damage, and oxygen deprivation stress: a review. Ann Bot 91:179–194
Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Mol Biol 43:83–116
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chen FM (1984) Determining the chlorophyll contents of plant leaves by acetone/ethanol mixture assay. For Sci Commun 2:4–8
Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 342:89–97
Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91
Dolferus R, Klok EJ, Delessert C, Wilson S, Ismond KP, Good AG, Peacock WJ, Dennis ES (2003) Enhancing the anaerobic response. Ann Bot 91:111–117
Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Mol Biol 48:223–250
Fielding JL, Hall JL (1978) A biochemical and cytological study of peroxidase activity in roots of Pisum sativum. J Exp Bot 29:969–981
Garnczarska M (2005) Responses of the ascorbate-glutathione cycle to re-aeration following hypoxia in lupine roots. Plant Physiol Biochem 43:583–590
Giannopolities CN, Rise SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol 59:309–314
Heath RL, Packer L (1968) Photoperoxiation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agr Exp Sta Circ 347:1–32
Hsu FH, Lin JB, Vhang SR (2000) Effects of waterlogging on seed germination, electric conductivity of seed leakage and developments of hypocotyl and radicle in sudangrass. Bot Bull Acad Sin 41:267–273
Hu LX, Li HY, Pang HC, Fu JM (2012) Responses of antioxidant gene, protein and enzymes to salinity stress in two genotypes of perennial ryegrass (Lolium perenne L.) differing in salt tolerance. J Plant Physiol 169:146–156
Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96:501–505
Kato C, Ohshima N, Kamada H, Satoh S (2001) Enhancement of the inhibitory activity for greening in xylem sap of squash root with waterlogging. Plant Physiol Biochem 39:513–519
Kumutha D, Ezhilmathi K, Sairam RK, Srivastava GC, Deshmukh PS, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. Biol Plant 53:75–84
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lee YH, Kim KS, Jang YS, Hwang JH, Lee DH, Choi IH (2014) Global gene expression responses to waterlogging in leaves of rape seedlings. Plant Cell Rep 33:289–299
Li HB, Vaillancourt R, Mendham N, Zhou M (2008) Comparative mapping of quantitative trait loci associated with waterlogging tolerance in barley (Hordeum vulgare L.). BMC Genom 9:401
Lin KHR, Weng CC, Lo HF, Chen JT (2004) Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. Plant Sci 167:355–365
Lin KH, Chao PY, Yang CM (2006) The effects of flooding and drought stresses on the antioxidant constituents in sweet potato leaves. Bot Stud 47:417–426
Luna C, Garcia-Seffino L, Arias C, Taleisnik E (2008) Oxidative stress indicators as selection tools for salt tolerance. Plant Breed 119:341–345
Malik AI, Colmer TD, Lambers H, Schortemeyer M (2001) Changes in physiological and morphological traits of roots and shoots of wheat in response to different depths of waterlogging. Aust J Plant Physiol 28:1121–1131
Menezes-Benavente L, Teixeira FK, Kamei CLA, Margis-Pinheiro M (2004) Salt stress induces altered expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.). Plant Sci 166:323–331
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Mittler R, Zilinskas BA (1993) Detection of ascorbate peroxidase activity in native gels by inhibition of the ascorbate-dependent reduction of nitroblue tetrazolium. Anal Biochem 212:540–546
Ou LJ, Dai XZ, Zhang ZQ, Zou XX (2011) Responses of pepper to waterlogging stress. Photosynthetica 49:339–345
Özçubukçu S, Ergün N, Ílhan E (2014) Waterlogging and nitric oxide induce gene expression and increase antioxidant enzyme activity in wheat (Triticum aestivum L.). Acta Biol Hung 65:47–60
Qi XH, Xu XW, Lin XJ, Zhang WJ, Chen XH (2012) Identification of differentially expressed genes in cucumber (Cucumis sativus L.) root under waterlogging stress by digital gene expression profile. Genomics 99:160–168
Sairam RK, Dharmar K, Chinnusamy V, Meena RC (2009) Waterlogging-induced increase in sugar mobilization, fermentation, and related gene expression in the roots of mung bean (Vigna radiata). J Plant Physiol 166:602–616
Schneider K, Schlegel HG (1981) Production of superoxide radical by soluble hydrogenase from Alcaligenes eutrophus H16. Biochem J 193:99–107
Simon EW (1974) Phospholipids and plant membrane permeability. New Phytol 73:377–420
Smethurst CF, Shabala S (2003) Screening methods for waterlogging tolerance in lucerne: comparative analysis of waterlogging effects on chlorophyll fluorescence, photosynthesis, biomass and chlorophyll content. Funct Plant Biol 30:335–343
Smethurst CF, Garnett T, Shabala S (2005) Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. Plant Soil 270:31–45
Smirnoff N (1993) The role of active oxygen in the response of plants to water-deficit and desiccation. New Phytol 125:27–58
Stoilova LS, Demirevska K, Smith AK, Feller U (2012) Involvement of the leaf antioxidant system in the response to soil flooding in two Trifolium genotypes differing in their tolerance to waterlogging. Plant Sci 183:43–49
Tan W, Liu J, Dai T, Jing Q, Cao W, Jiang D (2008) Alterations in photosynthesis and antioxidant enzyme activity in winter wheat subjected to post-anthesis water-logging. Photosynthetica 46:21–27
Turgeon AJ (2008) Turfgrass management, 8th edn. Pearson Prentice Hall, Upper Saddle River
Turkan I, Demiral T, Sekmen AH (2013) The regulation of antioxidant enzymes in two Plantago species differing in salinity tolerance under combination of waterlogging and salinity. Funct Plant Biol 40:484–493
Vartapetian BB, Jackson MB (1997) Plant adaptation to anaerobic stress. Ann Bot 79:3–20
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Sci 151:59–66
Voesenek LACJ, Colmer TD, Pierik R, Millenaar FF, Peeters JM (2006) How plants cope with complete submergence. New Phytol 170:213–226
Wang KH, Jiang YW (2006) Growth, physiological, and anatomical responses of creeping bentgrass cultivars to different depths of waterlogging. Crop Sci 46:2420–2426
Wang KH, Jiang YW (2007a) Waterlogging tolerance of Kentucky bluegrass cultivars. HortScience 42:386–390
Wang KH, Jiang YW (2007b) Antioxidant responses of creeping bentgrass roots to waterlogging. Crop Sci 47:232–238
Wang KH, Bian SM, Jiang YW (2009) Anaerobic metabolism in roots of Kentucky bluegrass in response to short-term waterlogging alone and in combination with high temperatures. Plant Soil 314:221–229
Wang LH, Zhang YX, Qi XQ, Li DH, Wei WL, Zhang XR (2012) Global gene expression responses to waterlogging in roots of sesame (Sesamum indicum L.). Acta Physiol Plant 34:2241–2249
Woodbury W, Spencer AK, Stahmann MA (1971) An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301
Xu LX, Han LB, Huang BR (2011) Antioxidant enzyme activities and gene expression patterns in leaves of Kentucky bluegrass in response to drought and post-drought recovery. J Am Soc Hort Sci 136:247–255
Xu LX, Yu JJ, Han LB, Huang BR (2013) Photosynthetic enzyme activities and gene expression associated with drought tolerance and post-drought recovery in Kentucky bluegrass. Environ Exp Bot 89:28–35
Yan B, Dai Q, Liu X, Huang S, Wang Z (1996) Flooding-induced membrane damage, lipid oxidation and activated oxygen generation in corn leaves. Plant Soil 179:261–268
Yin DM, Chen SM, Chen FD, Guan ZY, Fang WM (2009) Morphological and physiological responses of two chrysanthemum cultivars differing in their tolerance to waterlogging. Environ Exp Bot 67:87–93
Yin DM, Chen SM, Chen FD, Guan ZY, Fang WM (2010) Morpho-anatomical and physiological responses of two Dendranthema species to waterlogging. Environ Exp Bot 68:122–130
Yordanova RY, Alexieva VS, Popova LP (2003) Influence of root oxygen deficiency on photosynthesis and antioxidant status in barley plants. Russ J Plant Physiol 50:163–167
Zhang J, Kirkham MB (1996) Antioxidant responses to drought in sunflower and sorghum seedlings. New Phytol 132:361–373
Zhang GP, Tanakamaru K, Abe J, Morita S (2007) Influence of waterlogging on some anti-oxidative enzymatic activities of two barley genotypes differing in anoxia tolerance. Acta Physiol Plant 29:171–176
Zheng CF, Jiang D, Liu FL, Dai TB, Jing Q, Cao WX (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582
Acknowledgments
This research was supported by the National High Technology Research and Development Program of China (863 Program) (No. 2013AA102607) and the National Natural Science Foundation of China (No. 31172255).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Communicated by K. Apostol.
Rights and permissions
About this article
Cite this article
Puyang, X., An, M., Xu, L. et al. Antioxidant responses to waterlogging stress and subsequent recovery in two Kentucky bluegrass (Poa pratensis L.) cultivars. Acta Physiol Plant 37, 197 (2015). https://doi.org/10.1007/s11738-015-1955-z
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-015-1955-z