The regulation of antioxidant enzymes in two Plantago species differing in salinity tolerance under combination of waterlogging and salinity
Ismail Turkan A C , Tijen Demiral B and Askim Hediye Sekmen A
+ Author Affiliations
- Author Affiliations
A Department of Biology, Faculty of Science, Ege University, Bornova 35100, Izmir, Turkey.
B Department of Biology, Faculty of Science and Arts, Harran University, Sanliurfa, Turkey.
C Corresponding author. Email: ismail.turkan@ege.edu.tr
Functional Plant Biology 40(5) 484-493 https://doi.org/10.1071/FP12147
Submitted: 15 May 2012 Accepted: 15 December 2012 Published: 18 February 2013
Abstract
Natural waterlogging affects vegetation dynamics in many areas of the world. Goose-tongue (Plantago spp.) plants include diverse group of species differing in salt tolerance, some of which are adapted to live in saline wetlands, which makes the genus Plantago a good model for comparative studies on the responses to waterlogging and salinity stresses. The aim of this study was to determine how waterlogging in combination with 200 mM NaCl affect the tolerance mechanism of Plantago maritima L. (salt-tolerant) and Plantago media L. (salt-sensitive). Combination of salinity and waterlogging treatments (WLS) decreased shoot and root dry weights (DW) and leaf relative water content (RWC) of both P. maritima and P. media and these decreases were more dramatic in the latter. Lipid peroxidation level as measured by thiobarbutiric acid reactive substances (TBARS) content was increased in P. maritima by the combined salinity and waterlogging treatment, whereas in P. media it was increased by all stress treatments applied. Peroxidases (POX), ascorbate peroxidase (APX), catalase (CAT) and glutathione reductase (GR) activities of P. maritima were increased whereas only POX and CAT activities of P. media were increased by salinity treatment alone. WLS treatment increased POX, APX and GR activities but did not affect CAT activities of both Plantago species. NADPH oxidase (NOX) activity did not seem to have any effect to control the level of lipid peroxidation. This study is the first to demonstrate that increased antioxidant activity protected against lipid peroxidation resulting from waterlogging and salinity stresses. In conclusion, we suggest that a salt-tolerant species would also have a higher tolerance of the combination of waterlogging and salinity stress than a salt-sensitive one.
Additional keywords: antioxidant defence, salt tolerance, waterlogging.
References
Abbott JD, Gough RE (1987a) Reproductive response of the highbush blueberry to root-zone flooding. HortScience 22, 40–42.Abbott JD, Gough RE (1987b) Prolonged flooding effects on anatomy of highbush blueberry. HortScience 22, 622–625.
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 Science 163, 117–123.
| Alterations in photosynthesis and some antioxidant enzymatic activities of mungbean subjected to waterlogging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVOku74%3D&md5=f814171e4290dff627ba44f28e73e5c2CAS |
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373–399.
| Reactive oxygen species: metabolism, oxidative stress, and signal transduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFeisL0%3D&md5=bb62c10883f0f45b9778cbbe05a12a70CAS |
Arbona V, Hossain Z, Lpez-Climent MF, Pe’rez-Clemente RM, Go’mez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiologia Plantarum 132, 452–466.
| Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktb8%3D&md5=ac8a97c7785b34414cb304de0737e80aCAS |
Barrett-Lennard EG (1986) Wheat growth on saline waterlogged soils. Journal of Agriculture of Western Australia 27, 118–119.
Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant and Soil 253, 35–54.
| The interaction between waterlogging and salinity in higher plants: causes, consequences and implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsbk%3D&md5=a46fbd122186d4e690bf50aab4cd8500CAS |
Bergmeyer N (1970) ‘Methoden der enzymatischen analyse. Vol. 1.’ pp. 636–647. (Akademie Verlag, Berlin)
Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany 91, 179–194.
| Antioxidants, oxidative damage and oxygen deprivation stress: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVCksbw%3D&md5=7eb817ec347d1442f49f210c3a527914CAS |
Blumwald E, Aharon GS, Apse MP (2000) Sodium transport in plant cells. Biochimica et Biophysica Acta (BBA) – Biomembranes 1465, 140–151.
| Sodium transport in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Wgtrs%3D&md5=0bc2ce62783cc3db8047740db60cda3dCAS |
Bradford MM (1976) A rapid and sensitive method for quantification of proteins utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for quantification of proteins utilizing the principle of protein dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS |
Candan N, Tarhan L (2012) Tolerance or sensitivity responses of Mentha pulegium to osmotic and waterlogging stress in terms of antioxidant defense systems and membrane lipid peroxidation. Environmental and Experimental Botany 75, 83–88.
| Tolerance or sensitivity responses of Mentha pulegium to osmotic and waterlogging stress in terms of antioxidant defense systems and membrane lipid peroxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFSksbrN&md5=cdf13e3ec5d8c8344b4cca60ad3f0a4cCAS |
Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
| Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurnE&md5=00b92cbcc1649e26a963a26ffc260d5dCAS |
Erdei L, Kuiper PJC (1979) The effect of salinity on growth, cation content, Na+ uptake and translocation in salt-sensitive and salt-tolerant Plantago species. Physiologia Plantarum 47, 95–99.
| The effect of salinity on growth, cation content, Na+ uptake and translocation in salt-sensitive and salt-tolerant Plantago species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhvV2huw%3D%3D&md5=ddbfc2e795d56412063276fd9223671dCAS |
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21–25.
| The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism.Crossref | GoogleScholarGoogle Scholar |
Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiologia Plantarum 92, 696–717.
| Photooxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXivVSlsLc%3D&md5=3c764ed4a57179a0e5bea1b73b44003dCAS |
Guan B, Yu J, Wang X, Fu Y, Kan X, Lin Q, Han G, Lu Z (2011) Physiological responses of halophyte Suaeda salsa to water table and salt stresses in coastal wetland of Yellow River delta. CLEAN – Soil, Air, Water 39, 1029–1035.
| Physiological responses of halophyte Suaeda salsa to water table and salt stresses in coastal wetland of Yellow River delta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVagu73O&md5=08324874725582f36b1fb6fd44ff1806CAS |
Halliwell B (1987) Oxidative damage, lipid peroxidation, and antioxidant protection in chloroplasts. Chemistry and Physics of Lipids 44, 327–340.
| Oxidative damage, lipid peroxidation, and antioxidant protection in chloroplasts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXjtlym&md5=c9b31e71e5224aca35fb23f7af9aad8bCAS |
Herzog V, Fahimi H (1973) Determination of the activity of peroxidase. Analytical Biochemistry 55, 554–562.
| Determination of the activity of peroxidase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXlt1aqsLw%3D&md5=3bbf06952c5ef339cb6326dc19c14c65CAS |
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, University of California, Berkeley.
Jiang M, Zhang J (2002) Involvement of plasma membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings. Planta 215, 1022–1030.
| Involvement of plasma membrane NADPH oxidase in abscisic acid-and water stress-induced antioxidant defense in leaves of maize seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovValu74%3D&md5=f52f526bc1d6fd35c428cf1d0b334fe9CAS |
Kozlowski TT (1984) Plant responses to flooding of soil. Bioscience 34, 162–167.
| Plant responses to flooding of soil.Crossref | GoogleScholarGoogle Scholar |
Kumutha D, Ezhilmathi K, Sairam RK, Srivastava GC, Deshmukh PS, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. Biologia Plantarum 53, 75–84.
| Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsVOmsLo%3D&md5=c9efcaf535abf1b53922eacff02085c4CAS |
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.
| Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFags7s%3D&md5=445d75904529d747c279af05b4e6db88CAS |
Maathuis FJM, Prins HBA (1990) Electrophysiological membrane characteristics of the salt-tolerant Plantago maritima and the salt-sensitive Plantago media. Plant and Soil 123, 233–238.
| Electrophysiological membrane characteristics of the salt-tolerant Plantago maritima and the salt-sensitive Plantago media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXlt12mtr4%3D&md5=faa0dc4f1b9af5876e71f3ce26ce8329CAS |
Madhava Rao KV, Sresty TVS (2000) Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses. Plant Science 157, 113–128.
| Antioxidative parameters in the seedlings of pigeonpea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsFCjtL4%3D&md5=a5cb855c820bdc6b5f2a1ff70bf7996cCAS |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=6fc277d70817036dd692121577a2da70CAS |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant & Cell Physiology 22, 867–880.
Neill S, Desikan R, Hancock J (2002) Hydrogen peroxide signaling. Current Opinion in Plant Biology 5, 388–395.
| Hydrogen peroxide signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtlGjtL8%3D&md5=f018be519ef6d321ee6ea4024532c78bCAS |
Noble CL, Rogers ME (1994) Response of temperate forest legumes to waterlogging and salinity. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakli) pp. 473–496. (Marcel Dekker Inc.: New York)
Pezeshki SR (1994) Plant responses to flooding. In ‘Plant environment interactions’. (Ed. RE Wilkinson) pp. 289–312. (Marcel Dekker Inc.: New York)
Sairam RK, Kumutha D, Ezhilmathi K (2009) Waterlogging tolerance: nonsymbiotic haemoglobin-nitric oxide homeostasis and antioxidants. Current Science 96, 674–682.
Sairam RK, Dharmar K, Chinnnusamy V, Lekshmy S, Joshi R, Bhattacharya P (2011) NADPH oxidase as the source of ROS produced under waterlogging in roots of mung bean. Biologia Plantarum 55, 741–746.
| NADPH oxidase as the source of ROS produced under waterlogging in roots of mung bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlWrtb3O&md5=cdfd4a9b8d21be662f17d39a4a58069fCAS |
Sekmen AH, Turkan I, Takio S (2007) Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media. Physiologia Plantarum 131, 399–411.
| Differential responses of antioxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantago maritima and salt-sensitive Plantago media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1KqsrvM&md5=1735fc01ccfade2cbd6d75d5db1af6d4CAS |
Shi F, Yamamoto R, Shimamura S, Hiraga S, Nakayama N, Nakamura T, Yukawa K, Hachinohe M, Matsumoto H, Komatsu S (2008) Cytosolic ascorbate peroxidase 2 (cAPX 2) is involved in the soybean response to flooding. Phytochemistry 69, 1295–1303.
| Cytosolic ascorbate peroxidase 2 (cAPX 2) is involved in the soybean response to flooding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVCiurk%3D&md5=02d61f6e72c0600060b7dde230699659CAS |
Smart RE, Bingham GE (1974) Rapid estimates of relative water content. Plant Physiology 53, 258–260.
| Rapid estimates of relative water content.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnhtVylug%3D%3D&md5=ca3b7941cad853c8b1ece19390271c77CAS |
Wang K, Jiang Y (2007) Antioxidant responses of creeping bent-grass roots to water-logging. Crop Science 47, 232–238.
| Antioxidant responses of creeping bent-grass roots to water-logging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsF2nu7g%3D&md5=452cfc9d4661ac02fe58871a03cc5e0eCAS |
Ye Y, Tam NFY, Wong YS, Lu CY (2003) Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging. Environmental and Experimental Botany 49, 209–221.
| Growth and physiological responses of two mangrove species (Bruguiera gymnorrhiza and Kandelia candel) to waterlogging.Crossref | GoogleScholarGoogle Scholar |
Yin D, Chen S, Chen F, Guan Z, Fang W (2009) Morphological and physiological responses of two cultivars differing in their tolerance to waterlogging. Environmental and Experimental Botany 67, 87–93.
| Morphological and physiological responses of two cultivars differing in their tolerance to waterlogging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2qs7nN&md5=c8136261b39357b5f6994da86a9f43e7CAS |
Yordanova RY, Christov KN, Popova LP (2004) Antioxidative enzymes in barley plants subjected to soil flooding. Environmental and Experimental Botany 51, 93–101.
| Antioxidative enzymes in barley plants subjected to soil flooding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFCjt7w%3D&md5=424e9a3f122794f6c5c514230467db17CAS |
Zhou W, Lin X (1995) Effects of water logging at different growth stages on physiological characteristics and seed yield of winter rape. Field Crops Research 44, 103–110.
| Effects of water logging at different growth stages on physiological characteristics and seed yield of winter rape.Crossref | GoogleScholarGoogle Scholar |
