|
|
|
|
|
| Effects of chilling tolerance induced by spermidine pretreatment on antioxidative activity, endogenous hormones and ultrastructure of indica-japonica hybrid rice seedlings |
| ZENG Yan-hua, ZAHNG Yu-ping, XIANG Jing, WU Hui, CHEN Hui-zhe, ZHANG Yi-kai, ZHU De-feng |
1、College of Agronomy, Nanjing Agricultural University, Nanjing 210095, P.R.China
2、State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou 310006, P.R.China |
|
|
|
摘要 Spermidine (Spd) is known to be involved in the regulation of plant responses to chilling stress and counteract the adverse effect of stress conditions. Antioxidant activities, endogenous hormones and ultrastructure change under chilling stress were investigated in indica-japonica hybrid rice seedlings. 12-d-old seedlings were subjected to exogenous Spd (1 mmol L–1) and then a chilling stress (6°C, 4 d) was induced, followed by a subsequent recovery (25°C, 4 d). Results showed that malondialdehyde (MDA) and proline content were enhanced significantly, whereas shoot fresh and dry weights decreased during chilling stress and after recovery; chlorophyll content of chilling-stressed seedlings increased slightly but declined after recovery; additionally, total soluble sugar, sucrose, fructose and starch contents increased significantly during chilling stress, and only soluble sugar and fructose contents were observed in increase after recovery; chilling stress-induced increases in superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) activities, but declined after recovery, and the level of ascorbate peroxidase was lower during chilling stress and after recovery; however, endogenous indole-3-acetic acid (IAA), zeatin riboside (ZR), gibberellic acid (GA3), and abscisic acid (ABA) levels were induced decreased compared with Spd pretreatment. The microscopic analysis revealed that chilling stress-induced destruction of the chloroplast envelope during chilling stress and increased the number of plastoglobuli along with aberrations in thylakoid membranes after recovery. In contrast, exogenous Spd protected rice seedlings from chilling-induced injuries in terms of lower malondialdehyde, proline and carbohydrates accumulation coupled with increased endogenous hormones metabolism. After recovery, Spd pretreatment chilling-exposed seedlings showed higher activities of antioxidant enzymes and normal physiological function of chloroplasts. These results suggest that Spd could promote effectively chilling tolerance which might be largely attributable to the integrity of cell structure and normal metabolism of endogenous hormones in indica-japonica hybrid rice seedlings.
Abstract Spermidine (Spd) is known to be involved in the regulation of plant responses to chilling stress and counteract the adverse effect of stress conditions. Antioxidant activities, endogenous hormones and ultrastructure change under chilling stress were investigated in indica-japonica hybrid rice seedlings. 12-d-old seedlings were subjected to exogenous Spd (1 mmol L–1) and then a chilling stress (6°C, 4 d) was induced, followed by a subsequent recovery (25°C, 4 d). Results showed that malondialdehyde (MDA) and proline content were enhanced significantly, whereas shoot fresh and dry weights decreased during chilling stress and after recovery; chlorophyll content of chilling-stressed seedlings increased slightly but declined after recovery; additionally, total soluble sugar, sucrose, fructose and starch contents increased significantly during chilling stress, and only soluble sugar and fructose contents were observed in increase after recovery; chilling stress-induced increases in superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT) activities, but declined after recovery, and the level of ascorbate peroxidase was lower during chilling stress and after recovery; however, endogenous indole-3-acetic acid (IAA), zeatin riboside (ZR), gibberellic acid (GA3), and abscisic acid (ABA) levels were induced decreased compared with Spd pretreatment. The microscopic analysis revealed that chilling stress-induced destruction of the chloroplast envelope during chilling stress and increased the number of plastoglobuli along with aberrations in thylakoid membranes after recovery. In contrast, exogenous Spd protected rice seedlings from chilling-induced injuries in terms of lower malondialdehyde, proline and carbohydrates accumulation coupled with increased endogenous hormones metabolism. After recovery, Spd pretreatment chilling-exposed seedlings showed higher activities of antioxidant enzymes and normal physiological function of chloroplasts. These results suggest that Spd could promote effectively chilling tolerance which might be largely attributable to the integrity of cell structure and normal metabolism of endogenous hormones in indica-japonica hybrid rice seedlings.
|
|
Received: 06 February 2015
Accepted:
|
| Fund: This work was supported by grants from the the Earmarked Fund for Modern Agro-industry Technology Research System of China (CARS-01-09B), the Natural Science Foundation of Zhejiang Province, China (Y13C130013) and the Special Fund for Basic Scientific Research Business of Central Public Research Tnstitutes, Chinese Academy of Agricultural Sciences (2012RG004-2). |
|
Corresponding Authors:
ZHU De-feng, Tel/Fax: +86-571-63370373,E-mail: cnrice@qq.com; ZAHNG Yu-ping, Tel/Fax: +86-571-63371376, E-mail: cnrrizyp@163.com
E-mail: cnrice@qq.com; cnrrizyp@163.com
|
Cite this article:
ZENG Yan-hua, ZAHNG Yu-ping, XIANG Jing, WU Hui, CHEN Hui-zhe, ZHANG Yi-kai, ZHU De-feng.
2016.
Effects of chilling tolerance induced by spermidine pretreatment on antioxidative activity, endogenous hormones and ultrastructure of indica-japonica hybrid rice seedlings. Journal of Integrative Agriculture, 15(2): 295-308.
|
| Arnon D I. 1949. Copper enzymes in isolated chloroplasts.Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24,1-15Bates L S, Waldren R P, Teare I D. 1973. Rapid determinationof free proline for water-stress studies. Plant and Soil, 39,205-207Boyer J S. 1982. Plant productivity and environment. Science,218, 443-448Cakmak I, Marschner H. 1992. Magnesium deficiency and highlight intensity enhance activities of superoxide dismutase,ascorbate peroxidase, and glutathione reductase in beanleaves. Plant Physiology, 98, 1222-1227 Dai A H, Nie Y X, Yu B, Li Q, Lu L Y, Bai J G. 2012. Cinnamicacid pretreatment enhances heat tolerance of cucumberleaves through modulating antioxidant enzyme activity.Environmental and Experimental Botany, 79, 1-10Gulen H, Cansev A, Eris A. 2009. Cold hardiness of olive(Olea europaea L.) cultivars in cold-acclimated and nonacclimatedstages: Seasonal alteration of soluble sugarsand phospholipids. Journal of Agriculture Science, 147,459-467Guo Z F, Ou W B, Lu S Y, Zhong Q. 2006. Differential responsesof antioxidative system to chilling and drought in fourrice cultivars differing in sensitivity. Plant Physiology andBiochemistry, 44, 828-836Heath R L, Packer L. 1968. Photoperoxidation in isolatedchloroplasts: I. Kinetics and stoichiometry of fatty acidperoxidation. Archives of Biochemistry and Biophysics,125, 189-198He L, Ban Y, Inoue H, Matsuda N, Liu J, Moriguchi T. 2008.Enhancement of spermidine content and antioxidantcapacity in transgenic pear shoots overexpressingapple spermidine synthase in response to salinity andhyperosmosis. Phytochemistry, 69, 2133-2141He L X, Nada K, Kasukabe Y, Tachibana S. 2002. Enhancedsusceptibility of photosynthesis to low temperaturephotoinhibition due to interruption of chill-induced increaseof S-adenosylmethionine decarboxylase activity in leavesof spinach (Spinacia Oleracea L.). Plant Cell Physiology,43, 196-206Hunt R. 2003. Growth analysis, individual plants. Encyclopaediaof Applied Plant Sciences, 2, 579-588Jouve L, Hoffmann L, Hausman J F. 2004. Polyamine,carbohydrate, and proline content changes during saltstress exposure of Aspen (Populus tremula L.): Involvementof oxidation and osmoregulation metabolism. Plant Biology,6, 74-80Keunen E, Peshev D, Vangronsveld J, Van Den Ende W,Cuypers A. 2013. Plant sugars are crucial players inthe oxidative challenge during abiotic stress: Extendingthe traditional concept. Plant, Cell & Environment, 36,1242-1255Klotke J, Kopka J, Gatzke N, Heyer A G. 2004. Impact of solublesugar concentrations on the acquisition of freezing tolerancein accessions of Arabidopsis thaliana with contrastingcold adaptation - evidence for a role of raffinose in coldacclimation. Plant, Cell & Environment, 27, 1395-1404Konstrantinos P A, Imene T, Panagiotis M N, Roubelakis-Angelakis K A. 2010. ABA-dependent amine oxidasesdrivedH2O2 affects stomata conductance. Plant SignalBehavior, 5, 1153-1156Kubis J. 2008. Exogenous spermidine differentially altersactivities of some scavenging system enzymes, H2O2 andsuperoxide radical levels in water-stressed cucumberleaves. Journal of Plant Physiology, 165, 397-406Kumar S, Kaur R, Kaur N, Bhandhari K, Kaushal N, Gupta K,Bains T S, Nayyar H. 2011. Heat-stress induced inhibitionin growth and chlorosis in mungbean (Phaseolus aureusRoxb.) is partly mitigated by ascorbic acid application andis related to reduction in oxidative stress. Acta PhysiologyPlant, 33, 2091-2101Laloi C, Apel K, Danon A. 2004. Reactive oxygen signaling:The latest news. Current Opinon Plant Biology, 7, 323-328Li H B, Wang J, Liu A M, Liu K D, Zhang Q F, Zou J S. 1997.Genetic basis of low-temperature-sensitive sterility in indicajaponicahybrids of rice as determined by RFLP analysis.Theoretical and Applied Genetics, 95, 1092-1097Liu J, Jiang M Y, Zhou Y F, Liu Y L. 2005. Production ofpolyamines is enhanced by endogenous abscisic acidin maize seedlings subjected to salt stress. Journal ofIntegrative Plant Biology, 47, 1326-1334Liu X G, Xu H, Zhang J Y, Liang G W, Liu Y T, Guo A G. 2012.Effect of low temperature on chlorophyll biosynthesis inalbinism line of wheat (Triticum aestivum) FA85. PhysiologiaPlantarum, 145, 384-394Luomala E M, Laitinen K, Sutinen S, Kellomäki S, Vapaavuori E.2005. Stomatal density, anatomy and nutrient concentrationsof Scots pine needles are affected by elevated CO2 andtemperature. Plant Cell and Environment, 28, 733-749Madhava Rao K V, Sresty T V. 2000. Antioxidative parameters inthe seedlings of pigeonpea (Cajanus cajan (L.) Millspaugh)in response to Zn and Ni stresses. Plant Science, 157,113-128Morsy M R, Jouve L, Hausman J F, Hoffmann L, Stewart J M.2007. Alteration of oxidative and carbohydrate metabolismunder abiotic stress in two rice (Oryza sativa L.) genotypescontrasting in chilling tolerance. Journal of Plant Physiology,164, 157-167Mostofa M G, Yoshida N, Fujita M. 2014. Spermidinepretreatment enhances heat tolerance in rice seedlingsthrough modulating antioxidative and glyoxalase systems.Plant Growth Regulation, 73, 31-44Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T,Motohashi R, Shono Y, Nagata N, Ikeuchi M, ShinozakiK. 2008. A heterocomplex of iron superoxide dismutasesdefends chloroplast nucleoids against oxidative stress andis essential for chloroplast development in Arabidopsis. ThePlant Cell, 20, 3148-3162Nakano Y, Asada K. 1981. Hydrogen peroxide is scavengedby ascorbate-specific peroxidase in spinach chloroplasts.Plant and Cell Physiology, 22, 867-880Nickel K S, Cunningham B A. 1969. Improved peroxidaseassay method using leuco 2,3’,6-trichloroindophenol andapplication to comparative measurements of peroxidaticcatalysis. Analytical Biochemistry, 27, 292-299Palonen P, Buszard D, Donnelly D. 2000. Changes incarbohydrates and freezing tolerance during coldacclimation of red raspberry cultivars grown in vitro andin vivo. Physiologia Plantarum, 110, 393-401Parida A B, Das A, Das P. 2002. NaCl stress causes changesin photosynthetic pigments, proteins, and other metaboliccomponents in the leaves of a true mangrove, Bruguiera parviflora, in hydroponic cultures. Journal of Plant Biology,45, 28-36Polanská L, Vicankova A, Novakova M, Malbeck J, Dobrev PI, Brzobohaty B, Vankova R, Machackova I. 2007. Alteredcytokinin metabolism affects cytokinin, auxin, and abscisicacid contents in leaves and chloroplasts, and chloroplastultrastructure in transgenic tobacco. Journal of ExperimentalBotany, 58, 637-649Purvis A C, Grierson W. 1982. Accumulation of reducing sugarand resistance of grapefruit peel to chilling injury as relatedto winter temperatures. Journal of the American Society forHorticultural Science, 107, 139-142Pusittigul I, Kondo S, Siriphanich J. 2012. Internal browningof pineapple (Ananas comosus L.) fruit and endogenousconcentrations of abscisic acid and gibberellins during lowtemperature storage. Scientia Horticulturae, 146, 45-51Qiu J, Wang R M, Yan J Z, Hu J. 2005. Seed film coating withuniconazole improves rape seedling growth in relation tophysiological changes under waterlogging stress. PlantGrowth Regulation, 47, 75-81Sanchez B, Rasmussen A, Porter J R. 2014. Temperatures andthe growth and development of maize and rice: A review.Global Change Biology, 20, 408-417Sasaki H, Ichimura K, Imada S, Yamaki S. 2001. Sucrosesynthase and sucrose phosphate synthase, but notacid invertase, are regulated by cold acclimation anddeacclimation in cabbage seedlings. Journal of PlantPhysiology, 158, 847-852Sevillano L, Sanchez-Ballesta M T, Romojaro F, Flores F B.2009. Physiological, hormonal and molecular mechanismsregulating chilling injury in horticultural species. Postharvesttechnologies applied to reduce its impact. Journal of theScience of Food and Agriculture, 89, 555-573Sheoran I S, Saini H S.1996. Drought-induced male sterility inrice: Changes in carbohydrate levels and enzyme activitiesassociated with the inhibition of starch accumulation inpollen. Sex Plant Reproduction, 9, 161-169Shu S, Guo S R, Sun J, Yuan L Y. 2012. Effects of salt stress onthe structure and function of the photosynthetic apparatusin Cucumis sativus and its protection by exogenousputrescine. Physiologia Plantarum, 146, 285-296Taylor A O, Craig A S. 1971. Plants under climatic stress: II. Lowtemperature, high light effects on chloroplast ultrastructure.Plant Physiology, 47, 719-725Tian J, Wang L P, Yang Y J, Sun J, Guo S R. 2012. Exogenousspermidine alleviates the oxidative damage in cucumberseedlings subjected to high temperatures. Journal ofAmerican Society Horticulture Science, 137, 11-19Wang B G, Wang J H, Liang H, Yi J Y, Zhang J J, Lin L, WuY, Feng X Y, Cao J K, Jiang W B. 2008. Reduced chillinginjury inmango fruit by 2,4-dichlorophenoxyacetic acidand the antioxidant response. Postharvest Biology andTechnology, 48, 172-181Wang F, Cheng F M, Liu Y i , Zhong L J, Zhang G P. 2006a.Dynamic changes of plant hormones in developing grainsat rice filling stage under different temperature. ActaAgronomica Sinca, 1, 25-29 (in Chinese)Wang F, Tan X H, Gan L, Wu Y Y, Wang R Z, Li Q M.2006b. Effects of cold shock treatments on endogenousphytohormones contents and proteins variations of naiplumefruits. Journal of Food Science, 1, 71-74Wang X, Yu J, Yang Y, Cang J, Li Z F. 2009. Changes ofendogenous hormones of winter wheat varieties withdifferent cold-resistances under low temperature. Journalof Triticeae Crops, 5, 827-831 (in Chinese)Xu P L, Guo Y K, Bai J G. 2008. Effects of long-term chillingon ultrastructure and antioxidant activity in leaves of twocucumber cultivars under low light. Physiologia Plantarum,132, 467-478Xu S C, Hu J, Li Y P, Ma W G, Zheng Y Y, Zhu S J. 2011. Chillingtolerance in Nicotiana tabacum induced by seed primingwith putrescine. Plant Growth Regulation, 63, 279-290Yamamoto A, Shim IS, Fujihara S. 2012. Chilling-stressresponses by rice seedlings grown with different ammoniumconcentrations and its relationship to leaf spermidinecontent. Journal of Plant Biology, 55, 191-197Yamane K, Kawasaki M, Taniguchi M, Miyake H. 2003.Differential effect of NaCl and polyethylene glycol on theultrastructure of chloroplasts in rice seedlings. Journal ofPlant Physiology, 160, 573-575Yang J C, Zhang J H, Wang Z Q, Zhu Q S, Wang W. 2001.Hormonal changes in the grains of rice subjected to waterstress during grain filling. Plant Physiology, 127, 315-323Yoshida S, Forno D A, Cock J H, Gomez K A.1976.Determination of sugar and starch in plant tissue. In:Yoshida S, ed., Laboratory Manual for Physiological Studiesof Rice. International Rice Research Institute, Los Banos,Laguna, Philippines. pp. 46-49Zhang M P, Zhang C J, Yu G H, Jiang Y Z, Strasser R J, YuanZ Y, Yang X S, Chen G X. 2010. Changes in chloroplastultrastructure, fatty acid components of thylakoid membraneand chlorophyll a fluorescence transient in flag leaves ofa super-high-yield hybrid rice and its parents during thereproductive stage. Journal of Plant Physiology, 167,277-285 |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
