Skip to main content
SpringerLink
Log in

High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

Seed germination is one of the most important biological processes in the life cycle of plants, and temperature and water are the two most critical environmental factors that influence seed germination. In the present study, we investigated the roles of the plant hormone abscisic acid (ABA) and reactive oxygen species (ROS) in high temperature (HT) and drought-induced inhibition of rice seed germination. HT and drought stress caused ABA accumulation in seeds and inhibited seed germination and seedling establishment. Quantitative real-time polymerase chain reaction analysis revealed that HT and drought stress induced the expression of OsNCED3, a key gene in ABA synthesis in rice seeds. In addition, ROS (O2•- and H2O2) and malondialdehyde contents were increased in germinating seeds under HT and drought stress. Moreover, we adopted the non-invasive micro-test technique to detect H2O2 and Ca2+ fluxes at the site of coleoptile emergence. HT and drought stress resulted in a H2O2 efflux, but only drought stress significantly induced Ca2+ influx. Antioxidant enzyme assays revealed that superoxide dismutase (SOD), peroxidase, catalase (CAT), and ascorbate peroxidase (APX) activity were reduced by HT and drought stress, consistent with the expression of OsCu/ZnSOD, OsCATc, and OsAPX2 during seed germination. Altogether, these results suggest that ABA and ROS accumulation under HT and drought conditions can inhibit rice seed germination and growth.

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

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

HT:

High temperature

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NMT:

Non-invasive Micro-test Technique

POD:

Glyoxylate reductase

qRT-PCR:

Quantitative real-time polymerase chain reaction

ROS:

Reactive Oxygen Species

SOD:

Superoxide dismutase

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2013) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240

    Article  CAS  PubMed  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bin W, Dinkova TD (2015) Effects of high temperature and water stress on seed germination of the invasive species mexican sunflower. PLoS One 10:e0141567

    Article  CAS  Google Scholar 

  • Bradford KJ (1990) A water relations analysis of seed germination rates. Plant Physiol 94:840–849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiu RS, Nahal H, Provart NJ, Gazzarrini S (2012) The role of the Arabidopsis FUSCA3 transcription factor during inhibition of seed germination at high temperature. BMC Plant Biol 12:15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867

    Article  CAS  PubMed  Google Scholar 

  • Dhindsa RS, Matowe W (1981) Drought tolerance in two mosses: correlated with enzymatic defence against lipid peroxidation. J Exp Bot 32:79–91

    Article  CAS  Google Scholar 

  • Donohue K, de Casas RR, Burghardt L, Kovach K, Willis CG (2010) Germination, post-germinationadaptation, and species ecological ranges. Annu Rev Ecol Evol Syst 41:293–319

    Article  Google Scholar 

  • Evans CE, Etherington JR (1990) The effect of soil water potential on seed germination of some British plants. New Phytol 115:539–548

    Article  PubMed  Google Scholar 

  • Feurtado JA, Ambrose SJ, Cutler AJ, Ross ARS, Abrams SR, Kermode AR (2004) Dormancy termination of western white pine (Pinus monticola Dougl. Ex D. Don) seeds is associated with changes in abscisic acid metabolism. Planta 218:630–639

    Article  CAS  PubMed  Google Scholar 

  • Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North H, Marion-Poll A (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70:501–512

    Article  CAS  PubMed  Google Scholar 

  • Gao HB, Zhang SJ, Shen YB (2012) Regurgitant from Orgyia ericae Germar induces calcium influx and accumulation of hydrogen peroxide in Ammopiptanthus mongolicus (Maximex Kom) Cheng f. cells. Acta Ecol Sin 32:6520–6526

    Article  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  CAS  PubMed  Google Scholar 

  • Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and preharvest sprouting. Curr Opin Plant Biol 8:183–187

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, da Silva JAT, Fujita M (2012) Plant response and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. In: Crop stress and its management: perspectives and strategies. Springer, New York, pp 261–315

    Chapter  Google Scholar 

  • Hasanuzzaman M, Oku H, Nahar K, Bhuyan MB, Al Mahmud J, Baluska F, Fujita M (2018) Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. Plant Biotechnol Rep 12:1–16

    Article  Google Scholar 

  • Hendry GAF (1993) Oxygen free radical process and seed longevity. Seed Sci Res 3:141–153

    Article  CAS  Google Scholar 

  • Hou X, Xie K, Yao J, Qi Z, Xiong L (2009) A homolog of human skiinteracting protein in rice positively regulates cell viability and stress tolerance. Proc Natl Acad Sci U S A 106:6410–6415

    Article  PubMed  PubMed Central  Google Scholar 

  • Kebreab E, Murdoch AJ (2000) The effect of water stress on the temperature range for germination of Orobanche aegyptiaca seeds. Seed Sci Res 10:127–133

    Article  Google Scholar 

  • Kermode AR (2005) Role of abscisic acid in seed dormancy. J Plant Growth Regul 24:319–344

    Article  CAS  Google Scholar 

  • Khoubnasabjafari M, Ansarin K, Jouyban A (2015) Reliability of malondialdehyde as a biomarker of oxidative stress in psychological disorders. BioImpacts 5:123–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307

    Article  CAS  Google Scholar 

  • Kundu P, Gill R, Ahlawat S, Anjum NA, Sharma KK, Ansari AA, Hasanuzaman M, Ramakrishna A, Chauhan N, Tuteja N, Gill SS (2018) Targeting the redox regulatory mechanisms for abiotic stress tolerance in crops. In: Wani SH (ed) Biochemical, physiological and molecular avenues for combating abiotic stress tolerance in plants. Academic Pres, New York. https://doi.org/10.1016/B978-0-12813066-7.00010-3

    Chapter  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 

  • Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126:1109–1120

    Article  CAS  PubMed  Google Scholar 

  • Li J, Wang Y, Pritchard HW, Wang X (2014) The fluxes of H2O2 and O2 can be used to evaluate seed germination and vigor of caragana korshinskii. Planta 239:1363–1373

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Ye N, Liu R, Chen M, Zhang J (2010) H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. J Exp Bot 61:2979–2990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu SJ, Xu HH, Wang WQ, Li N, Wang WP, Møller IM, Song SQ (2015) A proteomic analysis of rice seed germination as affected by high temperature and ABA treatment. Physiol Plant 154:142–161

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Wang Z, Xiao HM, Yang Y (2018) Characterization of tadreb1 in wheat genotypes with different seed germination under osmotic stress. Hereditas 155:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Lou DJ, Wang HP, Liang G, Yu DQ (2017) OsSAPK2 confers abscisic acid sensitivity and tolerance to drought stress in rice. Front Plant Sci 8:993

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma C, Wang ZQ, Kong BB, Lin TB (2013) Exogenous trehalose differentially modulate antioxidant defense system in wheat callus during water deficit and subsequent recovery. Plant Growth Regul 70:275–285

    Article  CAS  Google Scholar 

  • Mangrauthia SK, Agarwal S, Sailaja B, Sarla N, Voleti SR (2016) Transcriptome analysis of Oryza sativa (rice) seed germination at high temperature shows dynamics of genome expression associated with hormones signalling and abiotic stress pathways. Trop Plant Biol 9:215–228

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22:11–19

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Møller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annu Rev Plant Biol 52:561–591

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Annu Rev Plant Biol 56:165–185

    Article  CAS  PubMed  Google Scholar 

  • Nambara E, Okamoto M, Tatematsu K, Yano R, Seo M, Kamiya Y (2010) Abscisic acid and the control of seed dormancy and germination. Seed Sci Res 20:55–67

    Article  CAS  Google Scholar 

  • Nonogaki H, Bassel GW, Bewley JD (2010) Germination—still a mystery. Plant Sci 179:574–581

    Article  CAS  Google Scholar 

  • Ogawa M (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode ABA 80-hydroxylases, are indispensable for a proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Tatematsu K, Matsui A, Morosawa T, Ishida J, Tanaka ETA, Mochizuki Y, Toyoda T, Kamiya Y, Shinozaki K, Nambara E, Seki M (2010) Genome-wide analysis of endogenous abscisic acidmediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays. Plant J 62:39–51

    Article  CAS  PubMed  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klu¨sener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Penfield S, Josse EM, Kannangara R, Gilday AD, Halliday KJ, Graham IA (2005) Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol 15:1998–2006

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Lv Q, Zhang J, Li J, Du Y, Zhao Q (2011) Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sativa). J Exp Bot 62:4943–4954

    Article  CAS  PubMed  Google Scholar 

  • Piskurewicz U, Tureckova V, Lacombe E, Lopez-Molina L (2009) Farred light inhibits germination through DELLA-dependent stimulation of ABA synthesis and ABI3 activity. EMBO J 28:2259–2271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin XQ, Zeevaart JAD (2002) Overexpression of a 9-cisepoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Calcium supplementation improves Na+/k+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci 7:609

    PubMed  PubMed Central  Google Scholar 

  • Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of α-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134:1598–1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren G, Wang X, Chen D, Wang X, Liu X (2014) Effects of aphids Myzus persicae on the changes of Ca2+ and H2O2 flux and enzyme activities in tobacco. J Plant Interact 9:883–888

    Article  CAS  Google Scholar 

  • Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 134:1439–1449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samarah N, Alqudah (2011) Effects of late-terminal drought stress on seed germination and vigor of barley (Hordeum vulgare L.). Arch Agron Soil Sci 57:27–32

    Article  Google Scholar 

  • Seck PA, Diagne A, Mohanty S, Wopereis MCS (2012) Crops that feed the world 7: rice. Food Secur 4:7–24

    Article  Google Scholar 

  • Sekmen AH, Ozgur R, Uzilday B, Turkan I (2014) Reactive oxygen species scavenging capacities of cotton (Gossypium hirsutum) cultivars under combined drought and heat induced oxidative stress. Environ Exp Bot 99:141–149

    Article  CAS  Google Scholar 

  • Sewelam N, Kazan K, Schenk PM (2016) Global plant stress signaling: reactive oxygen species at the cross-road. Front Plant Sci 7:187

    Article  PubMed  PubMed Central  Google Scholar 

  • Tambussi EA, Bartoli CG, Beltrano J, Guiamet JJ, Arans JL (2000) Oxidative damage to thylakoid proteins in water stress leaves of wheat (Triticum aestivum). Physiol Plant 108:398–404

    Article  CAS  Google Scholar 

  • Thabet SG, Moursi YS, Karam MA, Graner A, Alqudah AM, Perovic D (2018) Genetic basis of drought tolerance during seed germination in barley. PLoS One 13:e0206682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toh S, Imamura A, Watanabe A, Nakabayashi K, Okamoto M, Jikumaru Y, Hanada A, Aso Y, Ishiyama K, Tamura N, Iuchi S, Kobayashi M, Yamaguchi S, Kamiya Y, Nambara E, Kawakami N (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146:1368–1385

    Article  CAS  PubMed  PubMed Central  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 

  • Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey NF, Leung J (2008) An update on abscisic acid signaling in plants and more …. Mol Plant 1:198–217

    Article  CAS  PubMed  Google Scholar 

  • Wen B (2015) Effects of high temperature and water stress on seed germination of the invasive species Mexican sunflower. PLoS One 10:e0141567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wen B, Liu M, Tan Y, Liu Q (2016) Sensitivity to high temperature and water stress in recalcitrant Baccaurea ramiflora seeds. J Plant Res 129:637–645

    Article  CAS  PubMed  Google Scholar 

  • Williams J, Shaykewich CF (1971) Influence of water matric potential and hydraulic conductivity on the germination of rape (Brassica napus L.). J Exp Bot 22:586–597

    Article  Google Scholar 

  • Yamauchi T, Yoshioka M, Fukazawa A, Mori H, Nishizawa NK, Tsutsumi N, Yoshioka H, Nakazono M (2017) An NADPH oxidase RBOH functions in rice roots during lysigenous aerenchyma formation under oxygen-deficient conditions. Plant Cell 29:775–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, Shi L, Jia L, Zhang J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J Exp Bot 63:1809–1822

    Article  CAS  PubMed  Google Scholar 

  • Ye N, Li H, Zhu G, Liu Y, Liu R, Xu W, Jing Y, Peng X, Zhang J (2014) Copper suppresses abscisic acid catabolism and catalase activity, and inhibits seed germination of rice. Plant Cell Physiol 55:2008–2016

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Piao S, Wang X, Huang Y, Ciais P, Elliott J, Huang M, Janssens I, Li T, Lian X, Liu Y, Müller C, Peng S, Wang T, Zeng Z, Peñuelas J (2017) Plausible rice yield losses under future climate warming. Nat Plants 3:16202

    Article  Google Scholar 

  • Zhu G, Ye N, Zhang J (2009) Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by Major Science and Technology Project of Henan Province (141100110600), Modern Agricultural Industry Technology System Projects of Henan Province (S2012-04-02), and the Support Plan of Science and Technology Innovation Team in Universities of Henan province (17IRTSTHN015).

Author information

Author notes

  1. Juan Liu and Mirza Hasanuzzaman contributed equally to this work.

Authors and Affiliations

  1. Collaborative Innovation Center of Henan Grain Crops, Henan Key Laboratory of Rice Biology, Henan Agricultural University, Zhengzhou, China

    Juan Liu, Huili Wen, Jing Zhang, Ting Peng, Huwei Sun & Quanzhi Zhao

  2. Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Dhaka, 1207, Bangladesh

    Mirza Hasanuzzaman

Authors
  1. Juan Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mirza Hasanuzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huili Wen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ting Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Huwei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Quanzhi Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Juan Liu, Mirza Hasanuzzaman, Huili Wen, and Quanzhi Zhao designed and performed the experiments, analyzed the data, and wrote the manuscript. Jing Zhang carried out data analysis. Ting Peng and Huwei Sun gave technical advice and contributed to the study design. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Quanzhi Zhao.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Handling Editor: Néstor Carrillo

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

Liu, J., Hasanuzzaman, M., Wen, H. et al. High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma 256, 1217–1227 (2019). https://doi.org/10.1007/s00709-019-01354-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01354-6

Keywords

Search

Navigation