Alleviation of salt stress effects on physiology of leaves in two cultivars of pigmented rice by application of spermidine
Article Sidebar
Main Article Content
Abstract
Treating plants with plant growth regulators to alleviate adverse effects of stresses such as drought and salinity has received growing attentions in recent years. In this study, the mitigation of salt stress effects induced by application of spermidine (Spd) in two indigenous pigmented rice cultivars, namely Niewdam Gs.no.00621 (salt-tolerant, having violet leaf color) and KKU-LLR-039 (salt-sensitive, having green leaf color) was investigated. Rice seedlings were grown in plastic pots filled with paddy soils mixed with farmyard manure (3:1) in a net-house under natural light conditions. Sixty days after planting the plants of each cultivar were divided into 3 groups: (1) control group; plants irrigated with tap water, (2) NaCl group; plants sprayed with distilled water for 7 days prior to being irrigated with 25 mM NaCl and (3) NaCl+Spd group; plants sprayed with 1 mM Spd for 7 days prior to being irrigated with 25 mM NaCl. The salt stress treatment was conducted for 20 days. Sampling of leaves was performed at 10-day intervals (days 0, 10 and 20) to determine changes in the physiological characteristics of the leaves. Salt stress triggered an increase in electrolyte leakage (EL), malondialdehyde (MDA), hydrogen peroxide (H2O2), proline, protein and Na+ but caused a decrease in Fv/Fm, total chlorophyll and K+/Na+ ratio. Rice plants subjected to Spd pre-treatment showed, in comparison to the salt-stress treatment, a decrease in EL, MDA, H2O2, proline, protein and Na+ but increase in Fv/Fm, total chlorophyll and K+/Na+ ratio. The alleviative effects of Spd were more prominent in the sensitive cultivar (KKU-LLR-039). Spd can improve salt tolerance of rice, particularly the salt-sensitive genotype, by enhancing several physiological mechanisms such as maintaining ion homeostasis, water balance and membrane integrity as well as protecting pigments and photosynthetic machinery.
Article Details
References
Sudhir P, S.D.S. Murthy SDS. Effect of salt stress on basic processes of photosynthesis.
Photosynthetica. 2004; 42: 481-486.
Chen HJ, Chen JY, Wang JY. Molecular regulation of starch accumulation in rice
seedling leaves in response to salt stress. Acta Physiol Plant. 2008; 30: 135-142.
Ashraf M, Harris PJC. Potential biochemical indicators of salinity tolerance in plant. Plant Sci. 2004; 166: 3-16.
Verma S, Mishra SN. Putrescine alleviation of growth in salt stressed Brassica juncea
by inducing antioxidative defense system. J Plant Physiol. 2005; 162: 669-677.
Roychoudhury A, Basu S, Sengupta DN. Amelioration of salinity stress by exogenously
applied spermidine or spermine in three varieties of indica rice differing in their level of
salt tolerance. J Plant Physiol. 2011; 168: 317-328.
Parida AK, Das AB. Salt tolerance and salinity effects on plant: a review. Ecotoxicol
Environ Saf. 2005; 60: 324-349.
Gill S, Tuteja N. Polyamines and abiotic stress tolerance in plants Plant Signal Behav.
; 5(1): 26-33.
Kubiś J. Polyamines and “scavenging system”: influence of exogenous spermidine on
catalase and quaiacol peroxidase activities, and free polyamine level in barley leaves
under water deficit. Acta Physiol Plant. 2003; 25: 337-343.
Jiménez-Bremount JF, Ruiz OA, Rodríguez-Kessler M. Modulation of spermidine and
spermine levels in maize seedling subjected to long-term salt stress. Plant Physiol Biochem. 2007; 45: 812-821.
Saleethong P, Sanitchon J, Kong-ngern, K, Theerakulpisut P. Pretreatment
with spermimide reverses inhibitory effects of salt stress in two rice (Oryza sativa L.)
cultivars differing in salinity tolerance. Asian J Plant Sci. 2011; 10: 245-254.
Roy M, Wu R. Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhance sodium chloride-stress tolerance. Plant Sci.
; 163: 987-992.
Krishnamurthy R, Bhagwat KA. Polyamines as modulators of salt tolerance in rice
cultivars. Plant Physiol. 1989; 91: 500-504.
Ndayiragije A, Lutts S. Do exogenous polyamines have an impact on the response of a salt-sensitive rice cultivar to NaCl?. J Plant Physiol. 2006; 163: 506-516.
Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B. Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant. 2002; 116: 192-199.
Chunthaburee S, Sanitchon J, Pattanagul W, Theerakulpisut P. Effects of salt stress after late booting stage on yield and antioxidant capacity in pigmented rice grains and alleviation of the salt-induced yield reduction by exogenous spermidine. Plant Prod Sci. 2015; 18: 32-42.
Zeng L, Shannon M. Salinity effects on seedling growth and yield components of rice. Crop Sci. 2000; 40: 996-1003.
Guo H, Ling W, Wang Q, Xia X. Effect of anthocyanin-rich extract from black rice (Oryza sativa L. indica) on hyperlipidemia and insulin resistance in fructose- fed rats. Plant Foods Hum Nutr. 2007; 62: 1-6.
Suzuki M, Kimura T, Yamagishi K, Shinmoto H, Yamaki K. Comparison of mineral contents in 8 cultivars of pigmented brown rice. Nippon Shokuhin Kagaku Kogaku Kaishi. 2004; 51: 424-427.
Lee J-C, Kim J-D, Hsieh F-H, Eun J-B. Production of black rice cake using ground
black rice and medium-grain brown rice. Int J Food Sci Technol. 2008; 43: 1078-1082.
VelikovaV, Yordanov I, Edreva A. Oxidative stress and some antioxidant system in
acid rain-treated bean plant: protective role of exogenous polyamine. Plant Sci. 2000; 15: 59-66.
Heath RL, Packer L. 1968. Photoperoxidation in isolated chloroplast: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys. 1968; 125: 189-198.
Dionisio-Sese ML, Tobita S. Antioxidant responses of rice seedling to salinity stress.
Plant Sci. 1998; 135: 1-9.
Turner NC. Techniques and experimental approaches for the measurement of plant water status. Plant Soil. 1981; 58: 339-366.
Lutts S, Kinet JM, Bouharmont J. NaCl-induced senescence in leave of rice (Oryza
sativa L.) cultivars differing in salinity resistance. Ann Bot. 1996; 78: 389-398.
Moradi F, Ismail ABM. Responses of photosynthesis, chlorophyll fluorescence and
ROS-scavenging systems to salt stress during seedling and reproductive stage in rice.
Ann Bot. 2007; 99: 1161-1173.
Abdel-Aal ESM, Hucl PA, 1999. A rapid method for quantifying total anthocyanins in blue aleurone and purple pericarp wheats. Cereal Chem.1999; 76: 350-354.
Arnon DI.1949. Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta
vulgaris. Plant Physiol. 1949; 24: 2-25.
Kähkönen MP, Hopia AI, Vuorela HJ, Rauha JP, Pihlaja K, Kujaa KS, Meinonen M.
Antioxidant activity of plant extracts containing phenolic compound. J Agric Food
Chem. 1999; 47: 3954-3962.
Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil 1973; 39: 205-207.
Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;
: 248-254.
Mahajan S, Tuteja N. Cold, salinity and drought stresses: An overview. Arch Biochem
Biophys. 2005; 444: 139-158.
Dionisio-Sese ML, Tobita S. Effects of salinity on sodium content and photosynthetic
responses of rice seedlings differing in salt tolerance. J Plant Physiol. 2000; 157: 54-58.
Suping W, Yongxia J, Shirong G, Guoxian Z. Effect of polyamines on K+, Na+ and Cl-
content and distribution in different organs of cucumber (Cucumis sativus L.) seedling
under NaCl stress. Front Agric China. 2007; 1: 430-437.
Saleethong P, Sanitchon J, Kong-Ngern K, Theerakulpisut P. Effects of exogenous
spermidine (Spd) on yield, yield-related pretreatment and mineral composition of rice
(Oryza sativa L. ssp. indica) grains under salt stress. Aust J Crop Sci. 2013; 7: 1293-
Zhu H, Ding GH, Fang K, Zhao FG, Qin P. New perspective on the mechanism of alleviating salt stress by spermidine in barley seedlings. Plant Growth Regul. 2006; 49:
-156.
Roy P, Niyogi K, SenGupta DN, Ghosh B. Spermidine treatment to rice seedlings
recovers salinity stress-induced damage of plasma membrane and PM-bound H+-
ATPase in salt-tolerant and salt-sensitive rice cultivars. Plant Sci. 2005; 168: 583-591.
Zhao FG, Qin P. Protective effect of exogenous polyamines on root tonoplast function against salt stress in barley seedlings. Plant Growth Regul. 2004; 42: 97-103.
Duan J, Li J, Guo S, Kang Y. Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J
Plant Physiol. 2008; 165: 1620-1635.
Bajji M, Kinet J-M, Lutts S. The use of the electrolyte leakage method for assessing cell membrane stability as water stress tolerance test in durum wheat. Plant Growth Regul.
; 00:1-10.
Siringam K, Juntawong N, Cha-um S, Kirdmanee C. Salt stress induced ion
accumulation, ion homeostasis, membrane injury and sugar contents in salt-sensitive
rice (Oryza sativa L. spp. indica) roots under iso-osmotic conditions. Afr J Biotechnol.
; 10: 1340-1346.
Demiral T, Türkan I. Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp
Bot. 2005; 53: 247-257.
Lin CC, Kao CH. Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul. 2000; 30: 151-155.
Chunthaburee S, Dongsansuk A, Sanitchon J, Pattanagul W, Theerakulpisut P. Physiological and biochemical parameters for evaluation and clustering of rice cultivars differing in salt tolerance at seedling stage. Saudi J Biol Sci. 2016; 23: 467-477.
Pang X-M, Zhang Z-Y, Wen X-P, Ban Y, Moriguchi T. Polyamine, all-purposes players in response to environment stresses in plants. Plant Stress 2007; 1: 173-188.
Vysotskaya L, Hedley PE, Sharipova G, Veselov D, Kudoyarova G, Morris J, Jones HG. Effect of salinity on water relations of wild barley plants differing in salt tolerance. AoB Plants 2010; DOI:10.1093/aobpla/plq006.
Aroca R, Porcel R, Ruiz-Lozano JM. Regulation of root water uptake under abiotic
stress condition. J Exp Bot. 2012; 63: 43-57.
Belkheiri O, Mulas M. The effects of salt stress on growth, water relations and ion
accumulation in two halophyte Atriplex species. Environ Exp Bot. 2013; 86: 17-28.
Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H, Blazquez MA, Carbonell J. Role of polyamines in plant vascular development. Plant Physiol Biochem. 2010; 48: 534-539.
Pietrini F, Iannelli MA, Massacci A. Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low
temperature, without further limitation to photosynthesis. Plant Cell Environ. 2002; 25: 1251-1259.
Santos CV. Regulation of chlorophyll biosynthesis and degradation by salt stress
in sunflower leaves. Sci Hortic. 2004; 103: 93-99.
Chutipaijit S, Cha-um S, Sompornpailin K. High contents of proline and anthocyanin increase protective response to salinity in Oryza sativa L. spp. indica. Aust J Crop Sci. 2011; 5: 1191-1198.
Shabala S, Cuin TA, Prismall L, Nemchinov LG. Expression of animal CED-9 anti- apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta 2007; 227: 189-197.
Saha J, Brauer E, Sengupta A, Popescu S, Gupta K., Gupta B. Polyamines as redox
homeostasis regulators during salt stress in plant. Front Environ Sci. 2015; 3:21.
Maxwell K, Johnson GN. Chlorophyll fluorescence - A practical guide. J Exp Bot. 2000; 51: 659-668.
Shu S, Yuan L-Y, Guo S-R, Sun J., Yuan Y-H. Effect of exogenous spermine on
chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in
Cucumis sativus L. under salt stress. Plant Physiol Biochem. 2013; 63: 209-216.
Hamdani S, Yaakoubi H, Carpentier R. Polyamines interaction with thylakoid proteins during stress. J. Photochem. Photobiol. B, Biol. 2011; 104: 314-319.
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol. 2004; 55: 373-399.
Waśkiewicz A, Muzolf-Panek M, Goliński P. Phenolic content changes in plants under salt stress. In: Ecophysiology and Responses of Plants under Salt Stress. Parvaiz A,
Azooz MM, Prasad MNV. (Eds.). Springer, 2013; 283-314.
Yuan G, Wang X, Guo R, Wang Q. Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem. 2010; 121: 1014-1019.
Nilprapruck P, Meetum P, Chanthasa C. Influence of exogenous spermidine on the peel
color change and browning symptom of Musa (AAA group) cv. Kluai Hom Thong at
low temperature storage. SUSTJ. 2016; 10: 38-42.
Parvaiz A, Sayawati S. Salt stress and phyto-biochemical responses of plant-a review.
Plant Soil Environ. 2008; 60: 89-99.
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments. Plant Signal Behav. 2012; 7: 1456-1466.
Yamamoto A, Sawada H, Shim IS, Usui K, Fujihara S. Effect of salt stress on
physiological response and leaf polyamine content in NERICA rice seedling. Plant Soil
Environ. 2011; 57: 571-576.
Lutts S, Majerus V, Kinet JM. NaCl effects on proline metabolism in rice (Oryza sativa
L.) seedlings. Physiol Plant. 1999; 105: 450-458.
Balestrieri W, Cioni P, Romagnoli A, Bernini S, Fissi A, Felicioli R. Mechanism of polyamine inhibition of leaf protease. Arch Biochem Biophys. 1987; 255: 460-463.