Skip to main content
Log in

ABA and GA4 dynamic modulates secondary dormancy and germination in Syngonanthus verticillatus seeds

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

Abstract

Main conclusion

ABA and GA metabolism during incubation rather than hormone contents in dry seeds is the key to understanding secondary dormancy and germination of Syngonanthus verticillatus seeds.

Abstract

The mechanism of seed dormancy cycle, although very important for preventing germination during unfavorable periods for seedling establishment, is poorly understood in tropical species. Here, we used a perennial tropical species of the Brazilian campo rupestre, Syngonanthus verticillatus (Eriocaulaceae), to investigate the involvement of ABA and GA in modulating secondary dormancy of seeds buried in situ over time and the dynamic of these hormones during the incubation of dormant and non-dormant seeds. Hormone analyses were carried out with freshly harvested seeds and on buried seeds exhumed after 3, 6 and 9 months. Dynamics of ABA and GAs in dormant and non-dormant seeds during incubation (0, 12, 24 and 36 h) under favorable conditions for germination (at 20 °C in the presence of light) were also investigated. In addition, the effects of GA4 and fluridone were evaluated for overcoming secondary dormancy. Our results showed that changes in the contents of both ABA and GA4 occurred after burial, suggesting they may be related to the modulation of secondary dormancy/germination of S. verticillatus seeds. The application of fluridone was more effective than GA4 at overcoming secondary dormancy. We conclude that during incubation, de novo ABA synthesis and its consequent maintenance at high contents regulate the inhibition of germination in dormant seeds, while GA4 synthesis and ABA catabolism modulate the germination of non-dormant seeds. ABA and GA metabolism during incubation of both dormant and non-dormant seeds rather than hormone contents of dry seeds in the field is thought to be the key to understanding secondary dormancy and germination.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ali-Rachedi S, Bouinot D, Wagner M-H et al (2004) Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219:479–488

    Article  CAS  PubMed  Google Scholar 

  • Alves RJV, Silva N, Oliveira J, Medeiros D (2014) Circumscribing campo rupestre–megadiverse Brazilian rocky montane savanas. Braz J Biol 74:355–362

    Article  CAS  PubMed  Google Scholar 

  • Baskin J, Baskin C (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16

    Article  Google Scholar 

  • Benech-Arnold R, Sánchez R (2000) Environmental control of dormancy in weed seed banks in soil. Field Crop Res 67:105–122

    Article  Google Scholar 

  • Bentsink L, Koornneef M (2008) Seed dormancy and germination. Arabidopsis Book 6:e0119

    Article  PubMed  PubMed Central  Google Scholar 

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

    Book  Google Scholar 

  • Chen S-Y, Kuo S-R, Chien C-T (2008) Roles of gibberellins and abscisic acid in dormancy and germination of red bayberry (Myrica rubra) seeds. Tree Physiol 28:1431–1439

    Article  PubMed  Google Scholar 

  • Duarte D, Garcia Q (2015) Interactions between substrate temperature and humidity in signalling cyclical dormancy in seeds of two perennial tropical species. Seed Sci Res 25:170–178

    Article  Google Scholar 

  • Fenner M, Thompson K (2005) The ecology of seeds. Oxford University Press, Cambridge University Press, Cambridge

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

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415

    Article  CAS  PubMed  Google Scholar 

  • Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc Natl Acad Sci USA 108:20236–20241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia QS, Giorni VT, Müller M, Munné-Bosch S (2012) Common and distinct responses in phytohormone and vitamin E changes during seed burial and dormancy in Xyris bialata and X. peregrina. Plant Biol 14:347–353

    Article  CAS  PubMed  Google Scholar 

  • Garcia QS, Oliveira PG, Duarte DM (2014) Seasonal changes in germination and dormancy of buried seeds of endemic Brazilian Eriocaulaceae. Seed Sci Res 24:113–117

    Article  Google Scholar 

  • Giulietti A, Harley R, Queiroz L et al (2005) Biodiversity and conservation of plants in Brazil. Conserv Biol 19:632–639

    Article  Google Scholar 

  • Goggin DE, Steadman KJ, Emery RJN et al (2009) ABA inhibits germination but not dormancy release in mature imbibed seeds of Lolium rigidum Gaud. J Exp Bot 60:3387–3396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graeber K, Nakabayashi K, Miatton E et al (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35:1769–1786

    Article  CAS  PubMed  Google Scholar 

  • Grappin P, Bouinot D, Sotta B et al (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 

  • Hedden P, Kamiya Y (1997) Gibberelin biosynthesis: enzymes, genes and their regulation. Annu Rev Plant Physiol Plant Mol Biol 48:431–460

    Article  CAS  PubMed  Google Scholar 

  • Hermann K, Meinhard J, Dobrev P et al (2007) 1-Aminocyclopropane-1-carboxylic acid and abscisic acid during the germination of sugar beet (Beta vulgaris L.): a comparative study of fruits and seeds. J Exp Bot 58:3047–3060

    Article  CAS  PubMed  Google Scholar 

  • Hilhorst HWM (2007) Definitions and hypotheses of seed dormancy. In: Bradford K, Nonogaki H (eds) Seed development, dormancy and germination. Blackwell Publishing, Oxford, pp 50–71

    Chapter  Google Scholar 

  • Hilhorst HWM (1998) The regulation of secondary dormancy. The membrane hypothesis revisite. Seed Sci Res 8:77–90

    Article  CAS  Google Scholar 

  • Hilhorst HWM, Karssen CM (1992) Seed dormancy and germination: the role of abscisic acid and gibberellins and the importance of hormone mutants. Plant Growth Regul 11:225–238

    Article  CAS  Google Scholar 

  • Hu XW, Huang XH, Wang YR (2012) Hormonal and temperature regulation of seed dormancy and germination in Leymus chinensis. Plant Growth Regul 67:199–207

    Article  CAS  Google Scholar 

  • Ibarra SE, Tognacca RS, Dave A et al (2016) Molecular mechanisms underlying the entrance in secondary dormancy of Arabidopsis seeds. Plant Cell Environ 39:213–221

    Article  CAS  PubMed  Google Scholar 

  • Jacobsen J, Pearce D, Poole A et al (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 

  • Jacobsen JV, Barrero JM, Hughes T et al (2013) Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.). Planta 238:121–138

    Article  CAS  PubMed  Google Scholar 

  • Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36

    Article  CAS  PubMed  Google Scholar 

  • Kruk BC, Benech-Arnold RL (1998) Functional and quantitative analysis of seed thermal responses in prostrate knotweed (Polygonum aviculare) and common purslane (Portulaca oleracea). Weed Sci 46:83–90

    Article  CAS  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 

  • Leymarie J, Robayo-Romero ME, Gendreau E et al (2008) Involvement of ABA in induction of secondary dormancy in barley (Hordeum vulgare L.) seeds. Plant Cell Physiol 49:1830–1838

    Article  CAS  PubMed  Google Scholar 

  • Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Munné-Bosch S, Oñate M, Oliveira PG, Garcia QS (2011) Changes in phytohormones and oxidative stress markers in buried seeds of Vellozia alata. Flora 206:704–711

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ogawa M, Hanada A, Yamauchi Y et al (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 et al (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 

  • Oliveira PG, Garcia QS (2011) Germination characteristics of Syngonanthus seeds (Eriocaulaceae) in campos rupestres vegetation in south-eastern Brazil. Seed Sci Res 21:39–45

    Article  CAS  Google Scholar 

  • Oliveira TGS, Diamantino IP, Garcia QS (2017) Dormancy cycles in buried seeds of three perennial Xyris (Xyridaceae) species from the Brazilian campo rupestre. Plant Biol 19:818–823

    Article  CAS  PubMed  Google Scholar 

  • Oliveira TGS, Garcia QS (2019) Germination ecology of the perennial herb Xyris longiscapa: inter-annual variation in seed germination and seasonal dormancy cycles. Seed Sci Res 29:179–183

    Article  CAS  Google Scholar 

  • Seo M, Nambara E, Choi G, Yamaguchi S (2009) Interaction of light and hormone signals in germinating seeds. Plant Mol Biol 69:463–472

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45

    Article  CAS  PubMed  Google Scholar 

  • Silveira FAO, Negreiros D, Barbosa NPU et al (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152

    Article  CAS  Google Scholar 

  • Son S, Chitnis VR, Liu A et al (2016) Abscisic acid metabolic genes of wheat (Triticum aestivum L.): identification and insights into their functionality in seed dormancy and dehydration tolerance. Planta 244:429–447

    Article  CAS  PubMed  Google Scholar 

  • Thammina C, He M, Yu H et al (2011) Continuous biosynthesis of abscisic acid (ABA) may be required for maintaining dormancy of isolated embryos and intact seeds of Euonymus alatus. Plant Cell Tissue Organ Cult 108:493–500

    Article  CAS  Google Scholar 

  • Toh S, Imamura A, Watanabe A et al (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 

  • Toyomasu T, Tsuji H, Yamane H (1993) Light effects on endogenous levels of gibberellins in photoblastic lettuce seeds. J Plant Growth Regul 12:85

    Article  CAS  Google Scholar 

  • Tuan PA, Kumar R, Rehal PK et al (2018) Molecular mechanisms underlying abscisic acid/gibberellin balance in the control of seed dormancy and germination in cereals. Front Plant Sci 9:668

    Article  PubMed  PubMed Central  Google Scholar 

  • Vieira BC, Bicalho EM, Munné-Bosch S, Garcia QS (2017) Abscisic acid regulates seed germination of Vellozia species in response to temperature. Plant Biol 19:211–216

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S, Kamiya Y (2001) Gibberellins and light-stimulated seed germination. J Plant Growth Regul 20:369–376

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi S, Smith MW, Brown RG et al (1998) Phytochrome regulation and differential expression of gibberellin 3beta-hydroxylase genes in germinating Arabidopsis seeds. Plant Cell 10:2115–2126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshioka T, Endo T, Satoh S (1998) Restoration of seed germination at supraoptimal temperatures by fluridone, an inhibitor of abscisic acid biosynthesis. Plant Cell Physiol 39:307–312

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for financial support for the project, the Scientific and Technical Services of the University of Barcelona for technical assistance in hormone analyses, Maren Müller for help with hormone analyses and Jochen Dreixler (Joe) for help in preparing Fig. 5. We also thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and FAPEMIG for providing a scholarship for L.C.B.; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) and FAPEMIG for providing a scholarship for D.M.D.H; CAPES for providing a scholarship for B.M.R.S. Q.S.G. received a research productivity scholarship from CNPq.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Queila S. Garcia.

Ethics declarations

Conflict of interest

The authors declare that they have 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

Barreto, L.C., Herken, D.M.D., Silva, B.M.R. et al. ABA and GA4 dynamic modulates secondary dormancy and germination in Syngonanthus verticillatus seeds. Planta 251, 86 (2020). https://doi.org/10.1007/s00425-020-03378-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-020-03378-2

Keywords

Navigation