Skip to main content
SpringerLink
Log in

Seed Priming with Spermidine and Trehalose Enhances Chilling Tolerance of Rice via Different Mechanisms

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Chilling stress is an important limiting factor for rice growth and development. To examine the effect of spermidine (Spd) and trehalose (TH) priming in response to chilling stress of rice seed, we investigated the effects of seed priming with Spd, TH, and a mixture of Spd + TH on response and resilience of rice plants to chilling stress. Priming with Spd, TH and Spd + TH resulted in better seed vigor and seedling growth than hydro-priming and non-priming under low temperature (15 °C). In addition, Spd-, TH-, and Spd + TH-priming notably decreased malondialdehyde content but increased the proline and soluble sugar contents and antioxidant enzymes activities. Interestingly, spermine content and the expression of spermine-synthase (SPMS) gene were improved by Spd-priming. However, lower spermine content and SPMS expression was observed in the TH-primed plants. Moreover, expressions of trehalose-6-phosphate–phosphatase (TPP) genes was upregulated by TH-priming but downregulated by Spd-priming. It could be concluded from our results that (1) both Spd- and TH-priming could increase the contents of proline and soluble sugar, which were involved in osmotic adjustment, and antioxidant enzymes activities; (2) Spd-priming promoted the accumulation of endogenous spermine by upregulating SPMS1 and SPMS2, but inhibiting the expressions of TPP1 and TPP2; and (3) TH-priming increased the expressions of TPP1 and TPP2 but downregulated the expressions of SPMS1 and SPMS2. These findings suggested that seed priming with Spd and TH might enhance the chilling tolerance of rice seedling via different mechanisms.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Reference

  • Akiyama T, Pillai MA, Sentoku N (2004) Cloning, characterization and expression of OsGLN2, a rice endo-1, 3-β-glucanase gene regulated developmentally in flowers and hormonally in germinating seeds. Planta 220(1):129–139

    Article  CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Chen WP, Li PH (2010) Membrane stabilization by abscisic acid under cold aids proline in alleviating chilling injury in maize (Zea mays L.) cultured cells. Plant Cell Environ 25(8):955–962

    Article  Google Scholar 

  • Cruz RPD, Sperotto RA, Cargnelutti D, Adamski JM, Freitasterra TD, Fett JP (2013) Avoiding damage and achieving cold tolerance in rice plants. Food Energy Secur 2(2):96–119

    Article  Google Scholar 

  • Cuevas JC, Lópezcobollo R, Alcázar R (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol 148(2):1094–1105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diao Q, Song Y, Qi H (2015) Exogenous spermidine enhances chilling tolerance of tomato (Solanum lycopersicum L.) seedlings via involvement in polyamines metabolism and physiological parameter levels. Acta Physiol Plant 37(11):1–15

    Article  CAS  Google Scholar 

  • Diao Q, Song Y, Shi D, Qi H (2016) Nitric oxide induced by polyamines involves antioxidant systems against chilling stress in tomato (Lycopersicon esculentum mill.) seedling. J Zhejiang Univ Sci B 17(12):916–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13(4):17R–27R

    Article  CAS  PubMed  Google Scholar 

  • Elena BG, Rolland F, Sheen J, Thevelein JM (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448(7156):938–942

    Article  CAS  Google Scholar 

  • Ge LF, Chao DY, Shi M, Zhu MZ, Gao JP, Lin HX (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228(1):191–201

    Article  CAS  PubMed  Google Scholar 

  • Gondor OK, Szalai G, Kovács V, Janda T, Pál M (2016) Relationship between polyamines and other cold-induced response mechanisms in different cereal species. J Agron Crop Sci 202(3):217–230

    Article  CAS  Google Scholar 

  • Howarth CJ, Ougham HJ (2010) Gene expression under temperature stress. New Phytol 125(1):1–26

    Article  Google Scholar 

  • Hu Q, Fu Y, Guan Y, Lin C, Cao D, Hu W (2016) Inhibitory effect of chemical combinations on seed germination and pre-harvest sprouting in hybrid rice. Plant Growth Regul 80:281–289

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Imai R, Ali A, Pramanik HR, Nakaminami K, Sentoku N, Kato H (2004) A distinctive class of spermidine synthase is involved in chilling response in rice. J Plant Physiol 161(7):883–886

    Article  CAS  PubMed  Google Scholar 

  • Jang IC, Oh SJ, Seo JS, Choi WB, Song IS, Kim CH, Kim YS, Seo HS, Choi WD, Nahm BH, Kim JK (2003) Expression of a bifunctional fusion of the escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131(2):516–524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji SL, Jiang L, Wang YH, Zhang WW, Liu X, Liu SJ (2010) Quantitative trait loci mapping and stability for low temperature germination ability of rice. Plant Breeding 128(4):387–392

    Article  Google Scholar 

  • Jing C, Siqi P, Xiulan Z (2016) Effects of exogenous auxins on growth and antioxidation system in maize seedlings under cadmium stress. Plant Physiol J 29:45–59

    Google Scholar 

  • Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45(6):712–722

    Article  CAS  PubMed  Google Scholar 

  • Kasukabe Y, He L, Watakabe Y, Otani M, Shimada T, Tachibana S (2006) Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase. Plant Biotechnol 23:75–83

    Article  CAS  Google Scholar 

  • Kosar F, Akram NA, Ashraf M, Sadiq M, Al-Qurainy F (2018) Trehalose-induced improvement in growth, photosynthetic characteristics and levels of some key osmoprotectants in sunflower (Helianthus annuus L.) under drought stress. Pak J Bot 50(3):955–961

    CAS  Google Scholar 

  • Kushad MM, Yelenosky G (1987) Evaluation of polyamine and proline levels during low temperature acclimation of citrus. Plant Physiol 84(3):692–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Z, Xu JG, Gao Y, Wang C, Guo GY, Guan YJ, Hu J (2017) The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Front Plant Sci 8:1153

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo Y, Li WM, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress. Environ Exp Bot 63(1–3):378–384

    Article  CAS  Google Scholar 

  • Mo H, Pua EC (2010) Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Physiol Plant 114(3):439–449

    Article  Google Scholar 

  • Moustakas M, Sperdouli I, Kouna T, Antonopoulou CI, Therios I (2011) Exogenous proline induces soluble sugar accumulation and alleviates drought stress effects on photosystem ii functioning of Arabidopsis thaliana leaves. Plant Growth Regul 65(2):315–325

    Article  CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiate L.) seedlings by modulating ascorbate-glutathione and glyoxalase pathway. Int J Mol Sci 16(12):30117–30132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190(5):355–365

    Article  CAS  Google Scholar 

  • Nayyar H, Kaur S, Kumar S, Singh KJ, Dhir KK (2005) Involvement of polyamines in the contrasting sensitivity of chickpea (Cicer arietinum L.) and soybean (Glycine max (L.) merrill.) to water deficit stress. Bot Bull Acad Sin 46(4):333–338

    CAS  Google Scholar 

  • Oscar G, María B, María T, María I, Merodio C (2010) The effects of high co 2 levels on anthocyanin composition, antioxidant activity and soluble sugar content of strawberries stored at low non-freezing temperature. Food Chem 122(3):673–678

    Article  CAS  Google Scholar 

  • Pramanik MH, Imai R (2005) Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58(6):751–762

    Article  CAS  Google Scholar 

  • Saddam H, Fahad K, Hussain HA, Lixiao N (2016) Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Front Plant Sci 7:116

    Google Scholar 

  • Shen W, Nada K, Tachibana S (2000) Involvement of polyamines in the chilling tolerance of cucumber cultivars. Plant Physiol 124(1):431–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urano K, Yoshiba Y, Nanjo T, Igarashi Y, Seki M, Sekiguchi F, Yamaguchi-Shinozaki K, Shinozaki K (2003) Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ 26:1917–1926

    Article  CAS  Google Scholar 

  • Wan YY, Zhang Y, Zhang L, Zhou ZQ, Li X, Shi Q (2015) Caffeic acid protects cucumber against chilling stress by regulating antioxidant enzyme activity and proline and soluble sugar contents. Acta Physiol Plant 37(1):1706

    Article  CAS  Google Scholar 

  • Wang Y, Wang P, Jiahai WU, Zhao L, Bentian MO, Jun LI (2012a) Effect of polyamine priming on chilling tolerance of lolium perenne during seed imbibition. Agric Sci Technol 13(9):1859–1863

    CAS  Google Scholar 

  • Wang Y, Wang P, Jiahai WU, Zhao L, Bentian MO, Jun LI (2012b) Effect of polyamine priming on chilling tolerance of lolium perenne during seed imbibition. Agric Sci Technol 13(9):1859–1863

    CAS  Google Scholar 

  • Williams B, Njaci I, Moghaddam L, Long H, Dickman MB, Zhang X (2015) Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet 11(12):1–17

    Article  CAS  Google Scholar 

  • Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60(5):437–440

    Article  CAS  PubMed  Google Scholar 

  • Xie DW, Wang XN, Fu LS, Sun J, Li ZF, Zheng W (2015) Effect of exogenous trehalose on germ length and seedling freeze resistance of winter wheat under cold stress. J Triticeae Crops 32(2):215–223

    Google Scholar 

  • Zeng YH, Zhang YP, Xiang J, Wu H, Chen HZ, Zhang YK, Zhu DF (2016) Effects of chilling tolerance induced by spermidine pretreatment on antioxidative activity, endogenous hormones and ultrastructure of indica-japonica hybrid rice seedlings. Agric Sci Technol 15(2):295–308

    CAS  Google Scholar 

  • Zhang YP, Zhang HM, Gu HF, Zhang WX, Fan HW, Diao QN (2018) Effect of spermidine on photosynthesis, antioxidant characteristics and related gene expression in melon under chilling stress. Northwest Bot J 38(04):671–681

    Google Scholar 

  • Zheng YY, Cao DD, Zhang S, Guan YJ, Hu J (2008) Effect of polyamines on chilling tolerance in seed imbibition and seed germination in maize. Acta Agron Sin 34(2):261–267

    Article  CAS  Google Scholar 

  • Zhu L, Cao D, Hu Q, Guan Y, Hu W, Nawaz A (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 

Download references

Acknowledgements

We greatly appreciate Zhejiang Agricultural Seed Industry co. LTD for providing the seed materials.

Funding

This research was supported by National Key R & D Program of China(No. 2018YFD0100806, 2018YFD0100902), Zhejiang Provincial Natural Science Foundation (LQ19C130004), Key Research and Development Project of Zhejiang Province (No. 2019C02011, 2019C02004), the Fundamental Research Funds for the Central Universities (No. 2019QNA6015), National Natural Science Foundation of China (No. 31671774), Science and Technology Program of Zhejiang Province SannongLiufang Cooperation (No. 2018SNLF004), Dabeinong Funds for Discipline Development and Talent Training in Zhejiang University and Jiangsu Collaborative Innovation Center for Modern Crop Production, P. R. China.

Author information

Authors and Affiliations

  1. Seed Science Center, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Yuying Fu, Zhihao Zhang, Jun Liu, Min Chen, Ronghui Pan, Weimin Hu, Yajing Guan & Jin Hu

Authors
  1. Yuying Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhihao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Min Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ronghui Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Weimin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yajing Guan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jin Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

YYF designed and performed most of the experiments; ZHZ, JL and MC assisted with the experiments; YYF analyzed the data and wrote the article with contributions from all of the authors; WMH provided the seed materials; RHP and JH polished the manuscript; YJG analyzed the data and revised the whole manuscript;

Corresponding author

Correspondence to Yajing Guan.

Ethics declarations

Conflict of interest

There is no conflict of interest.

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

Fu, Y., Zhang, Z., Liu, J. et al. Seed Priming with Spermidine and Trehalose Enhances Chilling Tolerance of Rice via Different Mechanisms. J Plant Growth Regul 39, 669–679 (2020). https://doi.org/10.1007/s00344-019-10009-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-019-10009-y

Keywords

Search

Navigation