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Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin

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Abstract

Chilling depresses seed germination and seedling establishment, and is one major constraint to grain yield formation in late sown winter wheat. Seeds of winter wheat (Triticum aestivum L.) were separately pre-soaked with sodium nitroprusside (SNP, as nitric oxide donor) and Gibberellic acid (GA3) before germination and then germinated under low temperature. SNP and GA3 pre-treatment increased seed germination rate, germination index, weights and lengths of coleoptile and radicle, while they decreased mean germination time and weight of seeds germinating under low temperature. Exogenous NO and GA3 increased seed respiration rate and promoted starch degradation along with increased amylase activities. In addition, efficient antioxidant systems were activated by NO, and which effectively reduced concentrations of malondialdehyde and hydrogen peroxide (H2O2). Seedling growth was also enhanced by exogenous NO and GA3 as a result of improved seed germination and maintenance of better reactive oxygen species homeostasis in seedling growing under chilling temperatures. It is indicated that exogenous NO was more effective than GA3 in alleviating chilling stress during seed germination and seedling establishment in wheat.

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Abbreviations

ANOVA:

One-way analysis of variance

APX:

Ascorbate peroxidase

BSA:

Bovine serum albumin

DOG:

Days of germination

GA:

Gibberellic acid

GI:

Germination index

GPX:

Guaiacol peroxidase

GR:

Germination rate

H2O2 :

Hydrogen peroxide

MDA:

Malondialdehyde

MGT:

Mean germination time

NBT:

Nitro blue tetrazolium

PCD:

Programmed cell death

POD:

Peroxidase

PPO:

Polyphenol oxidase

PVP:

Polyvinylpoly pyrrolidone

ROS:

Reactive oxygen species

SNP:

Sodium nitroprusside

SOD:

Superoxide dismutase

TiCl4 :

Titanium tetrachloride

References

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in β vulgaris. Plant Physiol 24:1–15

    Article  PubMed  CAS  Google Scholar 

  • Beligni M, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  PubMed  CAS  Google Scholar 

  • Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Ann Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Browse J, Xin Z (2001) Temperature sensing and cold acclimation. Curr Opin Plant Biol 4:241–246

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  PubMed  CAS  Google Scholar 

  • Cui JX, Zhou YH, Ding JG, Xia XJ, Shi K, Chen SC, Asami T, Chen ZX, Yu JQ (2011) Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell Environ 34:347–358

    Article  PubMed  CAS  Google Scholar 

  • Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459

    Article  PubMed  CAS  Google Scholar 

  • Du Z, Bramlage WJ (1992) Modified thiobarbituric acid assay for measuring lipid peroxidation in sugar rich plant tissue extracts. J Agr Food Chem 40:1566–1570

    Article  CAS  Google Scholar 

  • Ellis RH, Roberts EH (1980) Towards a rational basis for testing seed quality. Seed Production, Butterworths

    Google Scholar 

  • Esim N, Atici O, Mutlu S (2012) Effects of exogenous nitric oxide in wheat seedlings under chilling stress. Toxicol Ind Health. doi: 10.1177/0748233712457444

  • Fales FW (1951) The assimilation and degradation of carbohydrates by yeast cells. J Biol Chem 193:113–124

    PubMed  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  PubMed  CAS  Google Scholar 

  • Guo Z, Ou W, Lu S, Zhong Q (2006) Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836

    Article  PubMed  CAS  Google Scholar 

  • Itoh H, Ueguchi TM, Matsuoka M (2008) Molecular biology of gibberellins signaling in higher plants. Elsevier, Waltham

    Google Scholar 

  • Keeley JE, Fotheringham CJ (1997) Trace gas emissions and smoke-induced seed germination. Science 276:1248–1250

    Article  CAS  Google Scholar 

  • Kishorekumar A, Abdul JC, Manivannan P (2007) Comparative effects of different triazole compounds on growth, photosynthetic pigments and carbohydrate metabolism of Solenostemon rotundifolius. Colloids Surf B Biointerfaces 60:207–212

    Article  PubMed  CAS  Google Scholar 

  • Lamattina L, Beligni MV, Garcia-Mata C (2001) Method of enhancing the metabolic function and the growing conditions of plants and seeds. US Patent. Patent No. US 6242384B1

  • Lenton J, Appleford N (1991) Gibberellin production and action during germination of wheat. Springer-Verlag, New York

    Google Scholar 

  • Li QY, Niu HB, Yin J, Wang MB, Shao HB, Deng DZ, Chen XX, Ren JP, Li YC (2008) Protective role of exogenous nitric oxide against oxidative-stress induced by salt stress in barley (Hordeum vulgare). Colloids Surf B Biointerfaces 65:220–225

    Article  PubMed  CAS  Google Scholar 

  • Li QZ, Li CH, Yu XC, Shi QH (2011) Gibberellin A3 pre-treatment increased antioxidative capacity of cucumber radicles and hypocotyls under suboptimal temperature. Afr J Agric Res 6:4091–4098

    Google Scholar 

  • Lovegrove A, Hooley R (2000) Gibberellin and abscisic acid signalling in aleurone. Trends Plant Sci 5:102–110

    Article  PubMed  CAS  Google Scholar 

  • Mata CG, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  CAS  Google Scholar 

  • Moloi MJ, Westhuizen AJ (2006) The reactive oxygen species are involved in resistance responses of wheat to the Russian wheat aphid. J Plant Physiol 163:1118–1125

    Article  PubMed  CAS  Google Scholar 

  • Pimenta Lange MJ, Lange T (2006) Gibberellin biosynthesis and the regulation of plant development. Plant Biol 8:281–290

    Article  PubMed  CAS  Google Scholar 

  • Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Elsevier, Waltham

    Google Scholar 

  • Siddiqui KS, Cavicchioli R (2006) Cold-adapted enzymes. Annu Rev Biochem 75:403–433

    Article  PubMed  CAS  Google Scholar 

  • Skadsen R (1998) Physiological and molecular genetic mechanisms regulating hydrolytic enzyme gene expression in cereal grains. Physiol Plant 104:486–502

    Article  CAS  Google Scholar 

  • Skinner DZ, Mackey B (2009) Freezing tolerance of winter wheat plants frozen in saturated soil. Field Crops Res 113:335–341

    Article  Google Scholar 

  • Song LL, Ding W, Zhao MG, Sun BT, Zhang LX (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171:449–458

    Article  CAS  Google Scholar 

  • Srivastava LM (2002) Gibberellins, plant growth and development. Academic Press, San Diego

    Google Scholar 

  • Sun TP (2000) Gibberellin signal transduction. Curr Opin Plant Biol 3:374–380

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos L. New Phytol 174:322–331

    Article  PubMed  CAS  Google Scholar 

  • Tuna AL, Kaya C, Dikilitas M, Higgs D (2008) The combined effects of gibberellic acid and salinity on some antioxidant enzyme activities, plant growth parameters and nutritional status in maize plants. Environ Exp Bot 62:1–9

    Article  CAS  Google Scholar 

  • Wang YR, Yu L, Nan ZB, Liu YL (2004) Vigor tests used to rank seed lot quality and predict field emergence in four forage species. Crop Sci 44:535–541

    Article  Google Scholar 

  • Xie Z, Jiang D, Cao W, Dai T, Jing Q (2003) Relationships of endogenous plant hormones to accumulation of grain protein and starch in winter wheat under different post-anthesis soil water statuses. Plant Growth Regul 41:117–127

    Article  CAS  Google Scholar 

  • Zhang H, Shen WB, Xu LL (2003) Effects of nitric oxide on the germination of wheat seeds and its reactive oxygen species metabolisms under osmotic stress. Acta Bot Sin 45:901–905

    CAS  Google Scholar 

  • Zhang H, Shen WB, Zhang W, Xu LL (2005) A rapid response of β-amylase to nitric oxide but not gibberellin in wheat seeds during the early stage of germination. Planta 220:708–716

    Article  PubMed  CAS  Google Scholar 

  • Zhang Y, Liu Z, Wang L, Zheng S, Xie J, Bi Y (2010) Sucrose-induced hypocotyl elongation of Arabidopsis seedlings in darkness depends on the presence of gibberellins. J Plant Physiol 167:1130–1136

    Article  PubMed  CAS  Google Scholar 

  • Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217

    Article  PubMed  CAS  Google Scholar 

  • Zhao M, Chen L, Zhang L, Zhang W (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767

    Article  PubMed  CAS  Google Scholar 

  • Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67:222–227

    Article  CAS  Google Scholar 

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Acknowledgments

This study is supported by projects of projects of PAPD, the National Natural Science Foundation of China (30971734, 31028017, 31000686, 31171484), the Specialized Research Fund for the Doctoral Program of Higher Education (20090097110009), the National Non-profit Program by Ministry of Agriculture (200903003), and the China Agriculture Research System (CARS-03).

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Authors and Affiliations

  1. National Engineering and Technology Center for Information Agriculture, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Xiangnan Li, Haidong Jiang, Jian Cai, Tingbo Dai, Weixing Cao & Dong Jiang

  2. Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, Nanjing Agricultural University, Nanjing, 210095, China

    Xiangnan Li, Haidong Jiang, Jian Cai, Tingbo Dai, Weixing Cao & Dong Jiang

  3. Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Højbakkegaard Allé 13, 2630, Taastrup, Denmark

    Xiangnan Li & Fulai Liu

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  1. Xiangnan Li
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  2. Haidong Jiang
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  3. Fulai Liu
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  4. Jian Cai
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  7. Dong Jiang
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Correspondence to Haidong Jiang or Dong Jiang.

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Li, X., Jiang, H., Liu, F. et al. Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin. Plant Growth Regul 71, 31–40 (2013). https://doi.org/10.1007/s10725-013-9805-8

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  • DOI: https://doi.org/10.1007/s10725-013-9805-8

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