Skip to main content
Log in

Spermidine enhanced the antioxidant capacity of rice seeds during seed aging

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Seed aging is a problem during long-term seed storage, affecting the commercial and germplasm value of seeds. In this study, a widely cultivated rice (Oryza sativa L.) cultivar, Huanghuazhan, was used to investigate the effects of exogenous spermidine (Spd) on accelerated aging (AA). The results showed that the speed of germination and the activities of catalase (CAT), ascorbate peroxidase (APX) and β-amylase were reduced by AA, and more H2O2 accumulated in aged seeds than in normal seeds. As compared with aged seeds pretreated with water, seed vigor and the gibberellic acid (GA) content in aged seeds pretreated with Spd were increased by 47% and 17%, respectively. Furthermore, antioxidant enzyme activity and related gene expression were also higher in aged seeds pretreated with Spd. It is speculated that CAT and APX are the two primary enzymes involved in the effects of Spd to AA. These results suggest that the adverse effect of AA stress on seeds may be partially alleviated by the application of exogenous Spd, which may affect the scavenging of reactive oxygen species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

AA:

Accelerated aging

PAs:

Polyamines

Spd:

Spermidine

CAT:

Catalase

APX:

Ascorbate peroxidases

GA:

Gibberellin acid

ABA:

Abscisic acid

ROS:

Reactive oxygen species

PCD:

Programmed cell death

MDA:

Malondialdehyde

POD:

Peroxidase

MT:

Metallothionein

GR:

Glutathione reductase

H2O2 :

Hydrogen peroxide

GE:

Germination energy

GI:

Germination index

GP:

Germination percentage

HAI:

Hours after imbibition

MGT:

Mean germination time

SL:

Seedling length

DW:

Dry weight of 10 seedlings

qRT-PCR:

Quantitative real-time PCR

CK:

Control

WBA:

Seeds treated with water before AA

SBA:

Seeds treated with Spd before AA

References

  • Agacka-Mołdoch M, Nagel M, Lewis R, Börner A (2015) Mapping quantitative trait loci determining seed longevity in tobacco (Nicotiana tabacum L.). Euphytica 202:1–8

    Article  CAS  Google Scholar 

  • Anguillesi MC, Grilli I, Tazziolo R, Floris C (1990) Polyamine accumulation in aged wheat seeds. Biol Plant 32:189–197

    Article  CAS  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bailly C, Benamar A, Corbineau F, Come D (1996) Changes in malondialdehyde content and in superoxide dismutase, catalase and glutathione reductase activities in sunflower seeds as related to deterioration during accelerated aging. Physiol Plant 97:104–110

    Article  CAS  Google Scholar 

  • Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107

    Article  CAS  Google Scholar 

  • Bajaj S, Rajam MV (1995) Efficient plant regeneration from long-term callus cultures of rice by spermidine. Plant Cell Rep 14:717–720

    Article  CAS  PubMed  Google Scholar 

  • Benamar A, Tallon C, Macherel D (2007) Membrane integrity and oxidative properties of mitochondria isolated from imbibing pea seeds after priming or accelerated ageing. Seed Sci Res 13:35–45

    Article  CAS  Google Scholar 

  • Besford R, Richardson C, Campos L, Tiburcio A (1993) Effect of polyamines on stabilization of molecular complexes in thylakoid membranes of osmotically stressed oat leaves. Planta 189:201–206

    Article  CAS  Google Scholar 

  • Bhukel A, Madeo F, Sigrist SJ (2017) Spermidine boosts autophagy to protect from synapse aging. Autophagy 13:444–445

    Article  CAS  PubMed  Google Scholar 

  • Cao YY, Chen YH, Chen MX, Wang ZQ, Wu CF, Bian XC, Yang JC, Zhang JH (2016) Growth characteristics and endosperm structure of superior and inferior spikelets of indica rice under high-temperature stress. Biol Plant 60:1–11

    Article  CAS  Google Scholar 

  • Chen MX, Zhu FY, Gao B, Ma KL, Ye NH, Zhang YJ, Fernie AR, Chen X, Hu QJ, Tian Y, Zhang D, Liu TY, Zhang JH, Liu YG (2020) Full-length transcript-based proteogenomics of rice improves its genome and proteome annotation. Plant Physiol 182:1–17

    Article  CAS  Google Scholar 

  • de Cabo R, Navas P (2016) Spermidine to the rescue for an aging heart. Nat Med 22:1389

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Draper HH, Hadley M (1990) Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    Article  CAS  PubMed  Google Scholar 

  • Edreva AM, Velikova VB, Tsonev TD (2007) Phenylamides in plants. Russ J Plant Physl 54:287–301

    Article  CAS  Google Scholar 

  • El-Maarouf-Bouteau H, Mazuy C, Corbineau F, Bailly C (2011) DNA alteration and programmed cell death during ageing of sunflower seed. J Exp Bot 62:5003–5011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng F, Li Y, Qin X, Liao Y, Siddique K (2017) Changes in rice grain quality of indica and japonica type varieties released in China from 2000 to 2014. Front Plant Sci 8:1066–1072

    Article  Google Scholar 

  • Fu Y, Ahmed Z, Diederichsen A (2015) Towards a better monitoring of seed ageing under ex situ seed conservation. Conserv Physiol 3:v26

    Article  CAS  Google Scholar 

  • Fu YY, Gu QQ, Dong Q, Zhang ZH, Lin C, Hu WM, Pan RH, Guan YJ, Hu J (2019) Spermidine enhances heat tolerance of rice seeds by modulating endogenous starch and polyamine metabolism. Molecules 24:1395

    Article  CAS  PubMed Central  Google Scholar 

  • Galston AW (1990) Polyamines in Plant Physiology. Plant Physiol 94:406–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grappin P, Bouinot D, Sotta B, Miginiac E, Jullien M (2000) Control of seed dormancy in Nicotiana plumbaginifolia: post-imbibition abscisic acid synthesis imposes dormancy maintenance. Planta 210:279–285

    Article  CAS  PubMed  Google Scholar 

  • Harman D (2006) Free-Radical Theory of Aging. Ann N Y Acad Sci 717:1–15

    Article  Google Scholar 

  • He Y, Cheng J, He Y, Yang B, Cheng Y, Yang C, Zhang H, Wang Z (2019) Influence of isopropylmalate synthase OsIPMS1 on seed vigor associated with amino acid and energy metabolism in rice. Plant Biotechnol J 17:322–337

    Article  CAS  PubMed  Google Scholar 

  • Hu Q, Lin C, Guan Y, Sheteiwy MS, Hu W, Hu J (2017) Inhibitory effect of eugenol on seed germination and pre-harvest sprouting of hybrid rice (Oryza sativa L.). Sci Rep 7(1):5295

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang Y, Lin C, He F, Li Z, Guan Y, Hu Q, Hu J (2017) Exogenous spermidine improves seed germination of sweet corn via involvement in phytohormone interactions, H2O2 and relevant gene expression. BMC Plant Biol 17(1):1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jacobsen JV, Pearce DW, Poole AT, Pharis RP, Mander LN (2002) Abscisic acid, phaseic acid and gibberellin contents associated with dormancy and germination in barley. Physiol Plant 115:428–441

    Article  CAS  PubMed  Google Scholar 

  • Kibinza S, Vinel D, Côme D, Bailly C, Corbineau F (2006) Sunflower seed deterioration as related to moisture content during aging, energy metabolism and active oxygen species scavenging. Physiol Plant 128:496–506

    Article  CAS  Google Scholar 

  • Kocsy G (2015) Die or survive? Redox changes as seed viability markers. Plant Cell Environ 38:1008–1010

    Article  CAS  PubMed  Google Scholar 

  • Kranner I, Colville L (2011) Metals and seeds: Biochemical and molecular implications and their significance for seed germination. Environ Exp Bot 72(1):93–105

    Article  CAS  Google Scholar 

  • Kraus T, Fletcher R (1994) Paclobutrazol Protects Wheat Seedlings from Heat and Paraquat Injury. Is detoxification of active oxygen involved? Plant Cell Physiol 35:45–52

    CAS  Google Scholar 

  • Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8 ‘-hydroxylases: key enzymes in ABA catabolism. Embo J 23:1647–1656

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H (2000) Principle and technology of plant physiological and biochemical experiments. Higher Education Press, Beijing

    Google Scholar 

  • Li Z, Peng Y, Zhang X, Ma X, Huang L, Yan Y (2014) Exogenous spermidine improves seed germination of white clover under water stress via involvement in starch metabolism, antioxidant defenses and relevant gene expression. Molecules 19:18003–18024

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li J, Hu L, Zhang L, Pan X, Hu X (2015) Exogenous spermidine is enhancing tomato tolerance to salinity-alkalinity stress by regulating chloroplast antioxidant system and chlorophyll metabolism. BMC Plant Biol 15:303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Zhang Y, Wang D, Liu Y, Dirk LMA, Goodman J, Downie AB, Wang J, Wang G, Zhao T (2017) Regulation of seed vigor by manipulation of raffinose family oligosaccharides in maize and Arabidopsis thaliana. Mol Plant 10:1540–1555

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Gao Y, Lin C, Pan R, Ma W, Zheng Y, Guan Y, Hu J (2018) Suppression of LOX activity enhanced seed vigour and longevity of tobacco (Nicotiana tabacum L.) seeds during storage. Conserv Physiol 6:y47

    Article  CAS  Google Scholar 

  • Liu Y, Fang J, Xu F, Chu J, Yan C, Schläppi MR, Wang Y, Chu C (2014) Expression patterns of aba and ga metabolism genes and hormone levels during rice seed development and imbibition: a comparison of dormant and non-dormant rice cultivars. J Genet Genomics 41:327–338

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 –∆∆CT Method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Michalak M, Plitta-Michalak BP, Naskręt-Barciszewska M, Barciszewski J, Bujarska-Borkowska B, Chmielarz P (2015) Global 5-methylcytosine alterations in DNA during ageing of Quercus robur seeds. Ann Bot-London 116:369–376

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2009) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Miransari M, Smith DL (2014) Plant hormones and seed germination. Environ Exp Bot 99:110–121

    Article  CAS  Google Scholar 

  • Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: Epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709

    Article  CAS  PubMed  Google Scholar 

  • Nandi S, Das G, Sen-Mandi S (1995) β-Amylase activity as an index for germination potential in rice. Ann Bot 75:463–467

    Article  CAS  Google Scholar 

  • Noctor G, Foyer C (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Phys 49:249–279

    Article  CAS  Google Scholar 

  • Penfield S, King J (2009) Towards a systems biology approach to understanding seed dormancy and germination. Proc R Soc B 276:3561–3569

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi J, Wang J, Gong Z, Zhou JM (2017) Apoplastic ROS signaling in plant immunity. Curr Opin Plant Biol 38:92–100

    Article  CAS  PubMed  Google Scholar 

  • Raychaudhuri SS, Deng XW (2000) The role of superoxide dismutase in combating oxidative stress in higher plants. Bot Rev 66:89–98

    Article  Google Scholar 

  • Revilla P, Butron A, Rodriguez VM, Malvar RA, Ordas A (2009) Identification of genes related to germination in aged maize seed by screening natural variability. J Exp Bot 60:4151–4157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sergiev I, Alexieva V, Karanov E (1997) Effect of spermine, atrazine and combination between them on some endogenous protective systems and stress markers in plants. Comptes Rendus de I’ Académie Bulgare Sciences 51:121–124

    Google Scholar 

  • Sheteiwy M, Fu Y, Hu Q, Nawaz A, Guan Y, Li Z, Huang Y, Hu J (2016) Seed priming with polyethylene glycol induces antioxidative defense and metabolic regulation of rice under nano-ZnO stress. Environ Sci Pollut R 23:19989–20002

    Article  CAS  Google Scholar 

  • Sheteiwy M, Shen H, Xu J, Guan Y, Song W, Hu J (2017) Seed polyamines metabolism induced by seed priming with spermidine and 5-aminolevulinic acid for chilling tolerance improvement in rice (Oryza sativa L.) seedlings. Environ Exp Bot 137:58–72

    Article  CAS  Google Scholar 

  • Song T, Xu F, Yuan W, Chen M, Hu Q, Tian Y, Zhang J, Xu W (2019) Combining alternate wetting and drying irrigation with reduced phosphorus fertilizer application reduces water use and promotes phosphorus use efficiency without yield loss in rice plants. Agric Water Manage 223:105686

    Article  Google Scholar 

  • Sung JM, Chiu CC (1995) Lipid peroxidation and peroxide-scavenging enzymes of naturally aged soybean seed. Plant Sci 110:45–52

    Article  CAS  Google Scholar 

  • Wang Y, Li B, Du M, Eneji AE, Wang B, Duan L, Li Z, Tian X (2012) Mechanism of phytohormone involvement in feedback regulation of cotton leaf senescence induced by potassium deficiency. J Exp Bot 63:5887–5901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waterworth WM, Masnavi G, Bhardwaj RM, Jiang Q, Bray CM, West CE (2010) A plant DNA ligase is an important determinant of seed longevity. Plant J 63:848–860

    Article  CAS  PubMed  Google Scholar 

  • Waypa GB, Smith KA, Schumacker PT (2016) O2 sensing, mitochondria and ROS signaling: the fog is lifting. Mol Aspects Med 47–48:76–89

    Article  PubMed  CAS  Google Scholar 

  • Weiler EW, Jourdan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571

    Article  CAS  PubMed  Google Scholar 

  • Wen XP, Ban Y, Inoue H, Matsuda N, Moriguchi T (2009) Aluminum tolerance in a spermidine synthase-overexpressing transgenic European pear is correlated with the enhanced level of spermidine via alleviating oxidative status. Environ Exp Bot 66:471–478

    Article  CAS  Google Scholar 

  • Willekens H, Inzé D, Montagu MV, Camp WV (1995) Catalases in plants. Mol Breeding 1:207–228

    Article  CAS  Google Scholar 

  • Wu Q, Du M, Wu J, Wang N, Wang B, Li F, Tian X, Li Z (2019) Mepiquat chloride promotes cotton lateral root formation by modulating plant hormone homeostasis. BMC Plant Biol 19:573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xin SQ, Gao Y, Zhao JM, Liu XM (2010) Effect of seed soaking in spermidine (Spd) under salt stress on rice seed germination. North Rice 40(6):23–30

    CAS  Google Scholar 

  • Xu H, Wei Y, Zhu Y, Lian L, Xie H, Cai Q, Chen Q, Lin Z, Wang Z, Xie H, Zhang J (2015) Antisense suppression of LOX3 gene expression in rice endosperm enhances seed longevity. Plant Biotechnol J 13:526–539

    Article  CAS  PubMed  Google Scholar 

  • Yang S, Jianchun X, Quanfa L (2012) Oxidative response and antioxidative mechanism in germinating soybean seeds exposed to cadmium. Int J Environ Res Public Health 9:2827–2838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang JF, Chen MX, Zhang JH, Hao GF, Yang GF (2020) Genome-wide phylogenetic and structural analysis reveals the molecular evolutionary mechanisms of ABA receptor gene family. J Exp Bot 71:1322–1336

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Xu CN, Wang BM, Jia JZ (2001) Effects of plant growth regulators on secondary wall thickening of cotton fibres. Plant Growth Regul 35:233–237

    Article  CAS  Google Scholar 

  • Yao Z, Liu L, Gao F, Rampitsch C, Reinecke DM, Ozga JA, Ayele BT (2012) Developmental and seed aging mediated regulation of antioxidative genes and differential expression of proteins during pre- and post-germinative phases in pea. J Plant Physiol 169:1477–1488

    Article  CAS  PubMed  Google Scholar 

  • Yi Z, Li Z, Hu XH (2014) Exogenous spermidine-induced changes at physiological and biochemical parameters levels in tomato seedling grown in saline-alkaline condition. Bot Stud 55:1–8

    Article  CAS  Google Scholar 

  • Yin G, Whelan J, Wu S, Zhou J, Chen B, Chen X, Zhang J, He J, Xin X, Lu X (2016) Comprehensive mitochondrial metabolic shift during the critical node of seed ageing in rice. PLoS ONE 11:e148013

    Google Scholar 

  • Yoshiyuki N, Kozi A (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    Google Scholar 

  • Zheng M, Tao Y, Hussain S, Jiang Q, Peng S, Huang J, Cui K, Nie L (2016) Seed priming in dry direct-seeded rice: consequences for emergence, seedling growth and associated metabolic events under drought stress. Plant Growth Regul 78:167–178

    Article  CAS  Google Scholar 

  • Zhou Y, Chu P, Chen H, Li Y, Liu J, Ding Y, Tsang EWT, Jiang L, Wu K, Huang S (2012) Overexpression of Nelumbo nucifera metallothioneins 2a and 3 enhances seed germination vigor in Arabidopsis. Planta 235:523–537

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Yan P, Li Z, Peng Y, Zhang XQ, Pan MH, Ma X, Huang LK, Yan YH (2014) Exogenous spermidine improves water stress tolerance of white clover (Trifolium repens L.) involved in antioxidant defence, gene expression and proline metabolism. Plant Omics 7:517–526

    Google Scholar 

  • Zhu GL, Zhong HW, Zhang AQ (1990) The experiments of plant physiology. The Peking University Press, Beijing

    Google Scholar 

  • Zhu LW, Cao DD, Hu QJ, Guan YJ, Hu WM, Nawaz A, Hu J (2016) Physiological changes and sHSPs genes relative transcription in relation to the acquisition of seed germination during maturation of hybrid rice seed. J Sci Food Agric 96:1764–1771

    Article  CAS  PubMed  Google Scholar 

  • Zhu FY, Chen MX, Ye NH, Shi L, Ma KL, Yang JF, Cao YY, Zhang YJ, Yoshida T, Fernie AR, Fan GY, Wen B, Zhou R, Liu TY, Fan T, Gao B, Zhang D, Hao GF, Xiao S, Liu YG, Zhang JH (2017) Proteogenomic analysis reveals alternative splicing and translation as part of the abscisic acid response in Arabidopsis seedlings. Plant J 91:518–533

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from Shenzhen Science Technology and Innovation Commission (International Collaborative Funding), the China Postdoctoral Science Foundation (2018M633162 and 2019M663122), the National Natural Science Foundation of China (Nos. 31201279, 31371708 and 31671774), and the Jiangsu Collaborative Innovation Center for Modern Crop Production, People's Republic of China.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jian-Hua Zhang.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, QJ., Chen, MX., Song, T. et al. Spermidine enhanced the antioxidant capacity of rice seeds during seed aging. Plant Growth Regul 91, 397–406 (2020). https://doi.org/10.1007/s10725-020-00613-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-020-00613-4

Keywords

Navigation