Skip to main content
SpringerLink
Log in

Catalase associated with antagonistic changes of abscisic acid and gibberellin response, biosynthesis and catabolism is involved in eugenol-inhibited seed germination in rice

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

The inhibitory effect of eugenol on rice germination is mediated by a two-step modulatory process: Eugenol first regulates the antagonism of GA and ABA, followed by activation of catalase activity.

Abstract

The natural monoterpene eugenol has been reported to inhibit preharvest sprouting in rice. However, the inhibitory mechanism remains obscure. In this study, simultaneous monitoring of GA and ABA responses by the in vivo GA and ABA-responsive dual-luciferase reporter system showed that eugenol strongly inhibited the GA response after 6 h of imbibition, whereas eugenol significantly enhanced the ABA response after 12 h of imbibition. Gene expression analysis revealed that eugenol significantly induced the ABA biosynthetic genes OsNCED2, OsNCED3, and OsNCED5, but notably suppressed the ABA catabolic genes OsABA8ox1 and OsABA8ox2. Conversely, eugenol inhibited the GA biosynthetic genes OsGA3ox2 and OsGA20ox4 but significantly induced the GA catabolic genes OsGA2ox1 and OsGA2ox3 during imbibition. OsABI4, the key signaling regulator of ABA and GA antagonism, was notably induced before 12 h and suppressed after 24 h by eugenol. Moreover, eugenol markedly reduced the accumulation of H2O2 in seeds after 36 h of imbibition. Further analysis showed that eugenol strongly induced catalase activity, protein accumulation, and the expression of three catalase genes. Most importantly, mitigation of eugenol-inhibited seed germination was found in the catc mutant. These findings indicate that catalase associated with antagonistic changes of ABA and GA is involved in the sequential regulation of eugenol-inhibited seed germination in rice.

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
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

All data supporting the findings of this study are available within the paper and within its supplementary data published online.

References

  • Ahuja N, Singh HP, Batish DR, Kohli RK (2015) Eugenol-inhibited root growth in Avena fatua involves ROS-mediated oxidative damage. Pestic Biochem Physiol 118:64–70

    Article  CAS  PubMed  Google Scholar 

  • Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. CR Biol 331:806–814

    Article  CAS  Google Scholar 

  • Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York

    Book  Google Scholar 

  • Bi C, Ma Y, Wu Z, Yu YT, Liang S, Lu K, Wang XF (2017) Arabidopsis ABI5 plays a role in regulating ROS homeostasis by activating CATALASE 1 transcription in seed germination. Plant Mol Biol 94:197–213. https://doi.org/10.1007/s11103-017-0603-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bossi F, Cordoba E, Dupré P, Mendoza MS, Román CS, León P (2009) The arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2. 2 genes during sugar signaling. Plant J 59:359–374

    Article  CAS  PubMed  Google Scholar 

  • Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17:427–431

    Article  CAS  PubMed  Google Scholar 

  • Chen BX, Peng YX, Gao JD, Zhang Q, Liu QJ, Fu H, Liu J (2019) Coumarin-induced delay of rice seed germination is mediated by suppression of abscisic acid catabolism and reactive oxygen species production. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00828

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Xiang Z, Liu M, Wang S, Zhang L, Cai D (2023) ABA biosynthesis gene OsNCED3 contributes to pre-harvest sprouting resistance and grain development in rice. Plant Cell Environ. https://doi.org/10.1111/pce.14480

    Article  PubMed  PubMed Central  Google Scholar 

  • Darabi HR, Mohandessi S, Balavar Y, Moghaddam MM, Aghapoor K, Mohsenzadeh F, Nourinia AA (2011) Clove bud oil: an efficient, economical and widely available oil for the inhibition of wheat seed germination. Environ Chem Lett 9:519–524

    Article  CAS  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523

    Article  CAS  PubMed  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 

  • Guan LM, Scandalios JG (2002) Catalase gene expression in response to auxin-mediated developmental signals. Physiol Plant 114:288–295

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Hou X, Fang J, Wei P, Xu B, Chen M, Chu C (2013) The rice germination defective 1, encoding a B3 domain transcriptional repressor, regulates seed germination and seedling development by integrating GA and carbohydrate metabolism. Plant J 75:403–416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54

    Article  CAS  PubMed  Google Scholar 

  • Hsing Y-I, Chern CG, Fan MJ, Lu PC, Chen KT, Lo SF, Sun YuSM (2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol Biol 63:351–364

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Li H, Huang S, Wang C, Sun WJ, Mo HZ, Chen J (2018) Eugenol confers cadmium tolerance via intensifying endogenous hydrogen sulfide signaling in Brassica rapa. J Agric Food Chem 66:9914–9922

    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 7:5295. https://doi.org/10.1038/s41598-017-04104-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Jiao Y, Xie N, Guo Y, Zhang F, Xiang Z (2019) OsNCED5, a 9-cis-epoxycarotenoid dioxygenase gene, regulates salt and water stress tolerance and leaf senescence in rice. Plant Sci 287:110188

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Bao Y, Qin S, Ning M, Lyu J, Zhang S, Huang G, Zhang J, Wang W, Fu B, Hu F (2020) An ABA synthesis enzyme allele OsNCED2 promotes the aerobic adaption in upland rice. BioRxiv. https://doi.org/10.1101/2020.06.11.146092

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishibashi Y, Aoki N, Kasa S, Sakamoto M, Kai K, Tomokiyo R, Iwaya-Inoue M (2017) The interrelationship between abscisic acid and reactive oxygen species plays a key role in barley seed dormancy and germination. Front Plant Sci 8:275. https://doi.org/10.3389/fpls.2017.00275

    Article  PubMed  PubMed Central  Google Scholar 

  • Jana S, Choudhuri MA (1981) Glycolate metabolism of three submerged aquatic angiosperms during aging. Aquat Bot 12:345–354

    Article  Google Scholar 

  • Khalil AA, ur Rahman U, Khan MR, Sahar A, Mehmood T, Khan M (2017) Essential oil eugenol: sources, extraction techniques and nutraceutical perspectives. RSC Adv 7:32669–32681

    Article  CAS  Google Scholar 

  • Kobayashi Y, Nabeta K, Matsuura H (2010) Chemical inhibitors of viviparous germination in the fruit of watermelon. Plant Cell Physiol 51:1594–1598

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Liu X, Li J, Yang Y (2014) Advances in pharmacological research of eugenol. Curr Opin Complement Altern Med 1:8–11

    Google Scholar 

  • Lee S, Cheng H, King KE, Wang W, He Y, Hussain A, Peng J (2002) Gibberellin regulates Arabidopsis seed germination via RGL2, a GAI/RGA-like gene whose expression is up-regulated following imbibition. Genes Dev 16:646–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JS, Chebotarov D, McNally KL, Pede V, Setiyono TD, Raquid R, Hyun WJ, Jeung JU, Kohli A, Mo Y (2021) Novel sources of pre-harvest sprouting resistance for Japonica rice improvement. Plants 10:1709. https://doi.org/10.3390/plants10081709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Cui L, Xie Z, Zhang Z, Liu E, Peng X (2019) Two NCA1 isoforms interact with catalase in a mutually exclusive manner to redundantly regulate its activity in rice. BMC Plant Biol 19:1–10

    Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068. https://doi.org/10.1126/science.1172408

    Article  CAS  PubMed  Google Scholar 

  • Marchese A, Barbieri R, Coppo E, Orhan IE, Daglia M, Nabavi SF, Ajami M (2017) Antimicrobial activity of eugenol and essential oils containing eugenol: a mechanistic viewpoint. Cri Rev Microbiol 43:668–689

    Article  CAS  Google Scholar 

  • Marin E, Nussaume L, Quesada A, Gonneau M, Sotta B, Hugueney P, Marion-Poll A (1996) Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. EMBO J 15:2331–2342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nonogaki H, Barrero JM, Li C (2018) Seed dormancy, germination and pre-harvest sprouting. Front Plant Sci 9:1783. https://doi.org/10.3389/fpls.2018.01783

    Article  PubMed  PubMed Central  Google Scholar 

  • Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez MV, Barrero JM, Corbineau F, Gubler F, Benech-Arnold RL (2015) Dormancy in cereals (not too much, not so little): about the mechanisms behind this trait. Seed Sci Res 25:99–119. https://doi.org/10.1017/S0960258515000021

    Article  CAS  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, Luis A (2008) Imaging of reactive oxygen species and nitric oxide in vivo in plant tissues. Methods Enzymol 440:397–409

    Article  CAS  PubMed  Google Scholar 

  • Shkolnik-Inbar D, Bar-Zvi D (2010) ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. Plant Cell 22:3560–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shu K, Chen Q, Wu YR, Liu RJ, Zhang HW, Wang PF et al (2016) ABI4 mediates antagonistic effects of abscisic acid and gibberellins at transcript and protein levels. Plant J 85:348–361. https://doi.org/10.1111/tpj.13109

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Xie Q (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet 9:e1003577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci 94:12235–12240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai WA, Weng SH, Chen MC, Lin JS, Tsai WS (2019) Priming of plant resistance to heat stress and tomato yellow leaf curl Thailand virus with plant-derived materials. Front Plant Sci 10:906

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Zhang Y, Jin XB, Wei Y, Zhu J (2008) The selection of inhibitors combination to inhibit pre-harvest sprouting in rice and study on eletrophoretic analysis. Seed 8:18–21

    Google Scholar 

  • Wang JY, Yao DD, Xu CX, Zhao GQ, Hua CL (2017) Effect of coumarin on Sorghum sudanense seed germination and seedling growth. Pratacult Sci 34:2279–2288

    Google Scholar 

  • Wind JJ, Peviani A, Snel B, Hanson J, Smeekens SC (2013) ABI4: versatile activator and repressor. Trends Plant Sci 18:125–132

    Article  CAS  PubMed  Google Scholar 

  • Wu CY, Hong CY (2021) An in vivo GA-and ABA-responsive dual-luciferase reporter system for simultaneous detection of GA and ABA responses, hormone crosstalk and heat stress response in rice. Plant Biotechnol J 19:1486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamauchi Y, Takeda-Kamiya N, Hanada A, Ogawa M, Kuwahara A, Seo M, Yamaguchi S (2007) Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol 48:555–561

    Article  CAS  PubMed  Google Scholar 

  • Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, 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, 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 

  • Ye Y, Zhao Y (2016) The pleiotropic effects of the seed germination inhibitor germostatin. Plant Signal Behav 11:e1144000

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Li M, He D, Wang K, Yang P (2020) Mutations on ent-kaurene oxidase 1 encoding gene attenuate its enzyme activity of catalyzing the reaction from ent-kaurene to ent-kaurenoic acid and lead to delayed germination in rice. PLoS Genet 16:e1008562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Wang Q, Wu X, Jiang M, Jin H, Tao K, Hou T (2021) Unraveling the polypharmacology of a natural antifungal product, eugenol, against Rhizoctonia solani. Pest Manag Sci 77:3469–3483

    Article  CAS  PubMed  Google Scholar 

  • Zhao M, Jin J, Wang J, Gao T, Luo Y, Jing T, Schwab W (2022) Eugenol functions as a signal mediating cold and drought tolerance via UGT71A59-mediated glucosylation in tea plants. Plant J 109:1489–1506

    Article  CAS  PubMed  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

Acknowledgements

We thank the staff at the phytotron at the College of Bioresources and Agriculture, National Taiwan University for providing the support with facilities.

Funding

This work was supported by the National Science and Technology Council of Taiwan (MOST 108-2313-B-002 -055 -MY3, MOST 111-2311-B-002-013, and MOST 111-2311-B-002-013 -) to CY Hong.

Author information

Authors and Affiliations

  1. Department of Agricultural Chemistry, College of Bioresources and Agriculture, National Taiwan University, Taipei, 10617, Taiwan

    Chi-Chieh Hu, Chin-Yu Wu, Min-Yu Yang & Chwan-Yang Hong

  2. Department of Plant Industry, National Pingtung University of Science and Technology, Neipu Township, Pingtung County, 91201, Taiwan

    Jian-Zhi Huang

  3. Kaohsiung District Agricultural Research and Extension Station, Changzhi Township, Pingtung County, 908126, Taiwan

    Chi-Chieh Hu & Chih-Wen Wu

Authors
  1. Chi-Chieh Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chin-Yu Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min-Yu Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian-Zhi Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chih-Wen Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chwan-Yang Hong
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CCH, CYW, CWW and CYH conceived and designed the experiments. CCH, CYW, MYY, and JZH performed the experiments. CCH, CYW, MYY, CWW and CYH wrote the paper.

Corresponding author

Correspondence to Chwan-Yang Hong.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Communicated by Hiroshi Ezura.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 284 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, CC., Wu, CY., Yang, MY. et al. Catalase associated with antagonistic changes of abscisic acid and gibberellin response, biosynthesis and catabolism is involved in eugenol-inhibited seed germination in rice. Plant Cell Rep 43, 10 (2024). https://doi.org/10.1007/s00299-023-03096-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00299-023-03096-5

Keywords

Search

Navigation