Skip to main content
SpringerLink
Log in

Antagonistic Interrelation Between Abscisic Acid and Gibberellic Acid in the Regulation of Senescence in Ray Florets of Calendula officinalis L.

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

Abstract

Petal senescence represents an extraordinary phase of flower development, involving precisely regulated biochemical and physiological reprogramming. Plant growth regulators (PGRs) stand as the chief regulatory switches to elicit such reprogramming causing programmed cell death (PCD) of petals. Ethylene is recognized as the key hormone that regulates senescence in ethylene-sensitive flowers. In contrast, there has been a constant pursuit to dispense the same role to a hormone other than ethylene in the ethylene-independent class of flowers. Pertinently, abscisic acid (ABA) is presumed to play a decisive role in the petal senescence of ethylene-insensitive flowers. Additionally, oxidative stress characterized by the accumulation of reactive oxygen species (ROS) is assumed to be the hallmark of PCD and senescence in petals. Consistent with this idea, the current investigation ascertains the role of PGRs viz., ethylene, ABA, and gibberellic acid (GA), besides ROS in regulating the senescence in ray florets of Calendula officinalis; a least documented ornamental of Asteraceae. The ray florets were analyzed for the transient biochemical changes from juvenility through maturity to senescence. Based on the current findings, it was ascertained that ABA plays a significant role in instigating senescence in ray florets of C. officinalis. Furthermore, postharvest treatment with ABA antagonists such as GA and sodium tungstate (ST) combatively delayed the senescence of this flower. GA and ST significantly reduced the hydrogen peroxide (H2O2) accretion and protein degradation, besides accentuating the cell membrane integrity and antioxidant system in the detached flowers of C. officinalis.

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
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Aftab T, Roychoudhury A (2021) Crosstalk among plant growth regulators and signaling molecules during biotic and abiotic stresses: molecular responses and signaling pathways. Plant Cell Rep 40(11):2017–2019

    Article  CAS  PubMed  Google Scholar 

  • Ahmad SS, Tahir I (2018) Putrescine and jasmonates outplay conventional growth regulators in improving postharvest performance of Iris germanica L. cut scapes. PNAS India Sect B Biol Sci 88(1):391–402

    CAS  Google Scholar 

  • Ahmad P, Raja V, Ashraf M, Wijaya L, Bajguz A, Alyemeni MN (2021) Jasmonic acid (JA) and gibberellic acid (GA3) mitigated Cd-toxicity in chickpea plants through restricted cd uptake and oxidative stress management. Sci Rep 11(1):19768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24(12):1337–1344

    Article  CAS  Google Scholar 

  • Almeida Trapp M, De Souza GD, Rodrigues-Filho E, Boland W, Mithöfer A (2014) Validated method for phytohormone quantification in plants. Front Plant Sci 5:417

    Article  PubMed  PubMed Central  Google Scholar 

  • Arrom L, Munné-Bosch S (2012a) Sucrose accelerates flower opening and delays senescence through a hormonal effect in cut lily flowers. Plant Sci 188:41–47

    Article  PubMed  Google Scholar 

  • Arrom L, Munné-Bosch S (2012b) Hormonal changes during flower development in floral tissues of Lilium. Planta 236:343–354

    Article  CAS  PubMed  Google Scholar 

  • Axelrod B, Cheesbrough TM, Laakso S (1981) Lipoxygenase from soybeans: EC 1.13. 11.12 Linoleate: oxygen oxidoreductase. In: Methods in enzymology, vol 71. Academic Press, New York, pp 441–451

  • Aziz S, Younis A, Jaskani MJ, Ahmad R (2020) Effect of PGRs on antioxidant activity and phytochemical in delay senescence of lily cut flowers. Agronomy 10(11):1704

    Article  CAS  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG et al (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42(4):567–585

    Article  CAS  PubMed  Google Scholar 

  • Chakrabarty D, Chatterjee J, Datta SK (2007) Oxidative stress and antioxidant activity as the basis of senescence in chrysanthemum florets. Plant Growth Regul 53:107–115

    Article  CAS  Google Scholar 

  • Chen GX, Asada K (1989) Ascorbate peroxidase in tea leaves: occurrence of two isozymes and the differences in their enzymatic and molecular properties. Plant Cell Physiol 30(7):987–998

    CAS  Google Scholar 

  • Costa LCD, Araujo FFD, Lima PCC, Pereira AM, Finger FL (2016) Action of abscisic and gibberellic acids on senescence of cut gladiolus flowers. Bragantia 75:377–385. https://doi.org/10.1590/1678-4499.361

    Article  CAS  Google Scholar 

  • Cowan AK, Richardson GR (1993) 1′, 4′-Trans-[14C]-Abscisic acid diol: a major product of R-[2-14C]-mevalonic acid metabolism in extracts of Citrus sinensis exocarp. J Plant Physiol 142(6):730–734

    Article  CAS  Google Scholar 

  • Dar RA, Nisar S, Tahir I (2021) Ethylene: a key player in ethylene sensitive flower senescence: a review. Sci Hortic 290:110491

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa PAMELA, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32(1):93–101

    Article  CAS  Google Scholar 

  • do Nascimento Simões A, Diniz NB, da Silva Vieira MR, Ferreira-Silva SL, da Silva MB, Minatel IO, Lima GPP (2018) Impact of GA3 and spermine on postharvest quality of anthurium cut flowers (Anthurium andraeanum) cv. Arizona. Sci Horticult 241:178–186

    Article  Google Scholar 

  • Dwivedi SK, Arora A, Singh VP, Sairam R, Bhattacharya RC (2016) Effect of sodium nitroprusside on differential activity of antioxidants and expression of SAGs in relation to vase life of gladiolus cut flowers. Sci Hortic 210:158–165

    Article  CAS  Google Scholar 

  • Emamverdian A, Ding Y, Mokhberdoran F (2020) The role of salicylic acid and gibberellin signaling in plant responses to abiotic stress with an emphasis on heavy metals. Plant Signal Behav 15(7):1777372

    Article  PubMed  PubMed Central  Google Scholar 

  • Emongor VE (2004) Effects of gibberellic acid on postharvest quality and vaselife life of gerbera cut flowers (Gerbera jamesonii). J Agron (Pak) 3(3):191–195

    Article  Google Scholar 

  • Fan ZQ, Wei W, Tan XL, Shan W, Kuang JF, Lu WJ et al (2021) A NAC transcription factor BrNAC087 is involved in gibberellin-delayed leaf senescence in Chinese flowering cabbage. Postharvest Biol Technol 181:111673

    Article  CAS  Google Scholar 

  • Fukuchi-Mizutani M, Ishiguro K, Nakayama T, Utsunomiya Y, Tanaka Y, Kusumi T, Ueda T (2000) Molecular and functional characterization of a rose lipoxygenase cDNA related to flower senescence. Plant Sci 160(1):129–137

    Article  CAS  PubMed  Google Scholar 

  • Ge Y, Lai Q, Luo P, Liu X, Chen W (2019) Transcriptome profiling of Gerbera hybrida reveals that stem bending is caused by water stress and regulation of abscisic acid. BMC Genomics 20(1):1–22

    Article  CAS  Google Scholar 

  • Hemati E, Daneshvar MH, Heidari M (2019) The roles of sodium nitroprusside, salicylic acid and methyl jasmonate as hold solutions on vase life of Gerbera jamesonii ‘Sun Spot.’ Adv Horticult Sci 33(2):187–195

    Google Scholar 

  • Hossain Z, Mandal AKA, Datta SK, Biswas AK (2006) Decline in ascorbate peroxidase activity—a prerequisite factor for tepal senescence in gladiolus. J Plant Physiol 163(2):186–194. https://doi.org/10.1016/j.jplph.2005.03.004

    Article  CAS  PubMed  Google Scholar 

  • Hunter DA, Ferrante A, Vernieri P, Reid MS (2004a) Role of abscisic acid in perianth senescence of daffodil (Narcissus pseudonarcissus “Dutch Master”). Physiol Plant 121(2):313–321

    Article  CAS  PubMed  Google Scholar 

  • Hunter DA, Lange NE, Reid MS (2004b) Physiology of flower senescence. In: Plant cell death processes. Academic Press, New York, pp 307–318

    Chapter  Google Scholar 

  • Iqbal N, Nazar R, Khan MIR, Masood A, Khan NA (2011) Role of gibberellins in regulation of source–sink relations under optimal and limiting environmental conditions. Curr Sci (Bangalore) 100(7):998–1007

    CAS  Google Scholar 

  • Jajic I, Sarna T, Strzalka K (2015) Senescence, stress, and reactive oxygen species. Plants 4(3):393–411

    Article  PubMed  PubMed Central  Google Scholar 

  • Jan S, Abbas N, Ashraf M, Ahmad P (2019) Roles of potential plant hormones and transcription factors in controlling leaf senescence and drought tolerance. Protoplasma 256:313–329

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Ni DA, Ruan YL (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21(7):2072–2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong X, Tian H, Yu Q, Zhang F, Wang R, Gao S et al (2018) PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep 22(5):1350–1363

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Singh VP, Arora A, Singh N (2014) The role of abscisic acid (ABA) in ethylene insensitive Gladiolus (Gladiolus grandiflora Hort.) flower senescence. Acta Physiol Plant 36:151–159

    Article  CAS  Google Scholar 

  • Li L, Zhang W, Zhang L, Li N, Peng J, Wang Y et al (2015) Transcriptomic insights into antagonistic effects of gibberellin and abscisic acid on petal growth in Gerbera hybrida. Front Plant Sci 6:168

    PubMed  PubMed Central  Google Scholar 

  • Li S, Liu S, Zhang Q, Cui M, Zhao M, Li N et al (2022) The interaction of ABA and ROS in plant growth and stress resistances. Front Plant Sci. https://doi.org/10.3389/fpls.2022.1050132

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao X, Li M, Liu B, Yan M, Yu X, Zi H et al (2018) Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proc Natl Acad Sci 115(49):E11542–E11550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Hou X (2018) Antagonistic regulation of ABA and GA in metabolism and signaling pathways. Front Plant Sci 9:251. https://doi.org/10.3389/fpls.2018.00251

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X (2016) The NF-YC–RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun 7(1):12768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lone ML, Haq AU, Farooq S, Altaf F, Tahir I (2021) Nitric oxide effectively curtails neck bending and mitigates senescence in isolated flowers of Calendula officinalis L. Physiol Mol Biol Plants 27:835–845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  PubMed  Google Scholar 

  • Ma N, Ma C, Liu Y, Shahid MO, Wang C, Gao J (2018) Petal senescence: a hormone view. J Exp Bot 69(4):719–732. https://doi.org/10.1093/jxb/ery009

    Article  CAS  PubMed  Google Scholar 

  • Mattoo AK, Sobieszczuk-Nowicka E (2019) Polyamine as signaling molecules and leaf senescence. In: Senescence signalling and control in plants. Elsevier, Amsterdam, pp 125–138

    Chapter  Google Scholar 

  • Naing AH, Lee K, Kim KO, Ai TN, Kim CK (2017) Involvement of sodium nitroprusside (SNP) in the mechanism that delays stem bending of different gerbera cultivars. Front Plant Sci 8:2045. https://doi.org/10.3389/fpls.2017.02045

    Article  PubMed  PubMed Central  Google Scholar 

  • Naing AH, Soe MT, Kyu SY, Kim CK (2021) Nano-silver controls transcriptional regulation of ethylene-and senescence-associated genes during senescence in cut carnations. Sci Hortic 287:110280

    Article  CAS  Google Scholar 

  • Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153(2):375–380

    Article  CAS  Google Scholar 

  • Oracz K, Karpiński S (2016) Phytohormones signaling pathways and ROS involvement in seed germination. Front Plant Sci 7:864

    Article  PubMed  PubMed Central  Google Scholar 

  • Panavas T, Rubinstein B (1998) Oxidative events during programmed cell death of daylily (Hemerocallis hybrid) petals. Plant Sci 133(2):125–138

    Article  CAS  Google Scholar 

  • Panavas T, Pikula A, Reid PD, Rubinstein B, Walker EL (1999) Identification of senescence-associated genes from daylily petals. Plant Mol Biol 40(2):237

    Article  CAS  PubMed  Google Scholar 

  • Qiu D, Hu W, Zhou Y, Xiao J, Hu R, Wei Q et al (2021) TaASR1-D confers abiotic stress resistance by affecting ROS accumulation and ABA signalling in transgenic wheat. Plant Biotechnol J 19(8):1588–1601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rahmani I, Ahmadi N, Ghanati F, Sadeghi M (2015) Effects of salicylic acid applied pre-or post-transport on post-harvest characteristics and antioxidant enzyme activity of gladiolus cut flower spikes. N Z J Crop Hortic Sci 43(4):294–305

    Article  CAS  Google Scholar 

  • Raza A, Charagh S, Zahid Z, Mubarik MS, Javed R, Siddiqui MH, Hasanuzzaman M (2020) Jasmonic acid: a key frontier in conferring abiotic stress tolerance in plants. Plant Cell Rep. https://doi.org/10.1007/s00299-020-02614-z

    Article  PubMed  Google Scholar 

  • Rogers HJ (2013) From models to ornamentals: how is flower senescence regulated? Plant Mol Biol 82:563–574

    Article  CAS  PubMed  Google Scholar 

  • Rogers H, Munné-Bosch S (2016) Production and scavenging of reactive oxygen species and redox signaling during leaf and flower senescence: similar but different. Plant Physiol 171(3):1560–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenwasser S, Belausov E, Riov J, Holdengreber V, Friedman H (2010) Gibberellic acid (GA 3) inhibits ROS increase in chloroplasts during dark-induced senescence of pelargonium cuttings. J Plant Growth Regul 29:375–384

    Article  CAS  Google Scholar 

  • Saeed T, Hassan I, Abbasi NA, Jilani G (2014) Effect of gibberellic acid on the vase life and oxidative activities in senescing cut gladiolus flowers. Plant Growth Regul 72:89–95

    Article  CAS  Google Scholar 

  • Sairam RK (1994) Effect of moisture-stress on physiological activities of two contrasting wheat genotypes. Indian J Exp Biol 32:594–594

    Google Scholar 

  • Sane AP, Khan S (2013) Metabolic shifts in sugars during floral senescence. Stewart Postharvest Rev 9(4):1–5

    Article  Google Scholar 

  • Shibuya K (2012) Molecular mechanisms of petal senescence in ornamental plants. J Jpn Soc Horticult Sci 81(2):140–149

    Article  CAS  Google Scholar 

  • Shu K, Zhou W, Chen F, Luo X, Yang W (2018) Abscisic acid and gibberellins antagonistically mediate plant development and abiotic stress responses. Front Plant Sci 9:416

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh A, Kumar J, Kumar P (2008) Effects of plant growth regulators and sucrose on post harvest physiology, membrane stability and vase life of cut spikes of gladiolus. Plant Growth Regul 55:221–229

    Article  CAS  Google Scholar 

  • Sun X, Qin M, Yu Q, Huang Z, Xiao Y, Li Y et al (2021) Molecular understanding of postharvest flower opening and senescence. Mol Horticult 1(1):7

    Article  CAS  Google Scholar 

  • Tahir I, Nisar S, Dar RA (2018) Gibberellin and cytokinins modulate flower senescence and longevity in Nicotiana plumbaginifolia. In: XXX International horticultural congress IHC2018: international symposium on ornamental horticulture and XI international 1263, pp 469–476

  • Tayyab S, Qamar S (1992) A look into enzyme kinetics: some introductory experiments. Biochem Educ 20(2):116–118

    Article  CAS  Google Scholar 

  • Thomas H, Ougham H (2014) The stay-green trait. J Exp Bot 65(14):3889–3900

    Article  CAS  PubMed  Google Scholar 

  • Trivellini A, Ferrante A, Vernieri P, Mensuali-Sodi A, Serra G (2011) Effects of promoters and inhibitors of ethylene and ABA on flower senescence of Hibiscus rosasinensis L. J Plant Growth Regul 30:175–184

    Article  CAS  Google Scholar 

  • van Doorn WG, Woltering EJ (2008) Physiology and molecular biology of petal senescence. J Exp Bot 59(3):453–480. https://doi.org/10.1093/jxb/erm356

    Article  CAS  PubMed  Google Scholar 

  • Williams MH, Nell TA, Barrett JE (1995) Investigation of proteins in petals of potted chrysanthemum as a potential indicator of longevity. Postharvest Biol Technol 5(1–2):91–100

    Article  CAS  Google Scholar 

  • Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66(10):2839–2856

    Article  CAS  PubMed  Google Scholar 

  • Xie HT, Wan ZY, Li S, Zhang Y (2014) Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26(5):2007–2023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng J, Dong Z, Wu H, Tian Z, Zhao Z (2017) Redox regulation of plant stem cell fate. EMBO J 36(19):2844–2855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang K, Gan SS (2012) An abscisic acid-AtNAP transcription factor-SAG113 protein phosphatase 2C regulatory chain for controlling dehydration in senescing Arabidopsis leaves. Plant Physiol 158(2):961–969

    Article  CAS  PubMed  Google Scholar 

  • Zhong Y, Ciafré C (2011) Role of ABA in ethylene-independent Iris flower senescence. ICFEB 7–9(14):3543–3552

    Google Scholar 

  • Zhu G, Yin J, Guo X, Chen X, Zhi W, Liu J et al (2019) Gibberellic acid amended antioxidant enzyme and osmotic regulation to improve salt tolerance of okra at early growth stage. Int J Agric Biol 22(2):270–276

    CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Dr. Mohammad Arif Zargar, Assistant Professor, Department of Botany, University of Kashmir for his valuable suggestions throughout this investigation. The authors thank the DST (Govt. of India) for providing funds to the Department of Botany, University of Kashmir, under the FIST program [SR/FST/LS-II/2017 103 (c)] dated 05-02-2019. The authors also thank Mr. Mohd Masarat Dar, Department of Food Science and Technology, University of Kashmir, for his assistance in carrying out HPLC analysis.

Author information

Authors and Affiliations

  1. Plant Physiology and Biochemistry Research Laboratory, Department of Botany, University of Kashmir, Srinagar, 190006, India

    Mohammad Lateef Lone, Sumira Farooq, Aehsan ul Haq, Shazia Parveen, Foziya Altaf & Inayatullah Tahir

Authors
  1. Mohammad Lateef Lone
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sumira Farooq
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aehsan ul Haq
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shazia Parveen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Foziya Altaf
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Inayatullah Tahir
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MLL: Literature survey and drafting of the manuscript; SF, AUH, SP, and FA: literature survey and reviewing; IT: Editing and reviewing.

Corresponding author

Correspondence to Inayatullah Tahir.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Václav Motyka.

Publisher's Note

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

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

Lone, M.L., Farooq, S., Haq, A.u. et al. Antagonistic Interrelation Between Abscisic Acid and Gibberellic Acid in the Regulation of Senescence in Ray Florets of Calendula officinalis L.. J Plant Growth Regul (2024). https://doi.org/10.1007/s00344-024-11342-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00344-024-11342-7

Keywords

Search

Navigation