Skip to main content
Log in

Endogenous Phytohormones of Fern Polystichum aculeatum (L.) Roth Gametophytes at Different Stages of Morphogenesis in vitro Culture

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

The content of indole-3-acetic (IAA), gibberellic (GA3), abscisic acids (ABA), and cytokinins—zeatin (Z), zeatin glucoside (ZG), zeatin riboside (ZP), isopentenyladenin (iР), and isopentenyladenosine (iРА)—was determined using the method of high-performance liquid chromatography in fern Polystichum aculeatum gametophytes at different stages of morphogenesis in vitro culture. It was shown that, at the stage of spatulate prothallium development, gametophytes contained significant amounts of GA3 and IAA, while the content of ABA and cytokinins was low. The inactive ZG and active iP were dominant. At the stage of cordiform thallus formation, the level of GA3 increased by 1.6, IAA by 2.4, and ABA by 1.7 times. The content of inactive iPA increased twice, significantly increased the level of active ZR and iP. At the development stage of sporophyte on the surface of gametophyte thallus, the levels of IAA, ABA, and GA3 decreased. The accumulation of inactive ZG and decrease in the content of active zeatin and zeatin riboside were documented. At all stages of gametophytes’ morphogenesis, GA3 was dominant, and its highest content was detected during the development of archegonia and antheridia. The pattern of gibberellic acid and zeatin riboside accumulation has shown the key role of these hormones in the regulation of growth processes and the development of reproductive structures of P. aculeatum gametophytes.

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.

Similar content being viewed by others

REFERENCES

  1. Raghavan, V., Developmental Biology of Fern Gametophytes, Cambridge: University Press, 1989.

    Book  Google Scholar 

  2. Menéndez, V., Arbesu, R., Somer, M., Revilla, A., and Fernández, H., From spore to sporophyte: how to proceed in vitro, in Working with Ferns: Issues and Applications, Fernandez, H., Kumar, A., and Revilla, A., Eds., New York: Springer, 2011, pp. 97–110. https://doi.org/10.1007/978-1-4419-7162-3_7

    Google Scholar 

  3. Banks, J.A., Gametophyte development in ferns, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1999, vol. 50, pp. 163–186. https://doi.org/10.1146/annurev.arplant.50.1.163

    Article  CAS  PubMed  Google Scholar 

  4. Kosakivska, I.V., Babenko, L.M., Shcherbatiuk, M.M., Vedenicheva, N.P., Voytenko, L.V., and Vasyuk, V.A., Phytohormones during growth and development of Polypodiophyta, Adv.Biol. Earth Sci., 2016, vol. 1, no. 1, pp. 26–44.

    Google Scholar 

  5. Cheng, Y. and Zhao, Y., A role for auxin in flower development, J. Integr. Plant Biol., 2007, vol. 49, pp. 99–104. https://doi.org/10.1111/j.1672-9072.2007.00412.x

    Article  CAS  Google Scholar 

  6. Korasick, D.A., Enders, T.A., and Strader, L.C., Auxin biosynthesis and storage forms, J. Exp. Bot., 2013, vol. 64, no. 9, pp. 2541–2555. https://doi.org/10.1093/jxb/ert080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ludwig-Muller, J., Auxin conjugates: their role for plant development and in the evolution of land plants, J. Exp. Bot., 2011, vol. 62, no. 6, pp. 1757–1773. https://doi.org/10.1093/jxb/erq412

    Article  CAS  PubMed  Google Scholar 

  8. Mano, Y. and Nemoto, K., The pathway of auxin bio synthesis in plants, J. Exp. Bot., 2012, vol. 63, no. 8, pp. 2853–2872. https://doi.org/10.1093/jxb/ers091

    Article  CAS  PubMed  Google Scholar 

  9. Teale, W.D., Paponov, I.A., and Palme, K., Auxin in action: signalling, transport and the control of plant growth and development, Nat. Rev. Mol. Cell Biol., 2006, vol. 7, no. 11, pp. 847–859. https://doi.org/10.1038/nrm2020

    Article  CAS  PubMed  Google Scholar 

  10. Gantait, S., Sinniah, U.R., Ali, M.N., and Sahu, N.C., Gibberellins —a multifaceted hormone in plant growth regulatory network, Curr. Protein Pept. Sci., 2015, vol. 16, no. 5, pp. 406–412. https://doi.org/10.2174/1389203716666150330125439

    Article  CAS  PubMed  Google Scholar 

  11. Wybouw, B. and De Rybel, B., Cytokinin, a developing story, Trends Plant Sci., 2019, vol. 24, no. 2, pp. 177–185. https://doi.org/10.1016/j.tplants.2018.10.012

    Article  CAS  PubMed  Google Scholar 

  12. Vishwakarma, K., Upadhyay, N., Kumar, N., Yadav, G., Singh, J., Mishra, R., Kumar, V., Verma, R., Upadhyay, R.G., Pandey, M., and Sharma, S., Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects, Front. Plant Sci., 2017, vol. 8, pp. 161–173. https://doi.org/10.3389/fpls.2017.00161

    Article  PubMed  PubMed Central  Google Scholar 

  13. Finkelstein, R., Reeves, W., Ariizumi, T., and Steber, C., Molecular aspects of seed dormancy, Annu. Rev. Plant Biol., 2008, vol. 59, pp. 387–415. https://doi.org/10.1146/annurev.arplant.59.032607.092740

    Article  CAS  PubMed  Google Scholar 

  14. Harris, J., Abscisic acid: hidden architect of root system structure, Plants, 2015, vol. 4, pp. 548–572. https://doi.org/10.3390/plants4030548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Rasool, R., Kamili, A., Masood, A., Ganai, B., and Akbar, S., Synergistic effect of auxins and cytokinins on propagation of Artemisia amygdalina (Asteraceae), a critically endangered plant of Kashmir, Pak. J. Bot., 2013, vol. 45, no. 2, pp. 629–634.

    Google Scholar 

  16. Zia, M., Riaz-ur-Rehman, and Chaudhary, M.F., Hormonal regulation for callogenesis and organogenesis of Artemisia absinthium L., Afr. J. Biotechnol., 2007, vol. 6, no. 16, pp. 1874–1878.

    Article  CAS  Google Scholar 

  17. Albaum, H.G., Inhibitions due to growth hormones in fern Prothallium,Am. J. Bot., 1938, vol. 25, pp. 124–133.

    Article  CAS  Google Scholar 

  18. Atallah, N.M. and Banks, J.A., Reproduction and the pheromonal regulation of sex type in fern gametophytes, Front. Plant Sci., 2015, vol. 6, pp. 100–107. https://doi.org/10.3389/fpls.2015.00100

    Article  PubMed  PubMed Central  Google Scholar 

  19. Yamane, H., Fern antheridiogens, Int. Rev. Cytol., 1998, vol. 184, pp. 1–32.https://doi.org/10.1016/S0074-7696

  20. Tanaka, J., Yano, K., Aya, K., Hirano, K., Takehara, S., Koketsu, E., Ordonio, R.L., Park, S.H., Nakajima, M., Ueguchi-Tanaka, M., and Matsuoka, M., Antheridiogen determines sex in ferns via a spatiotemporally split gibberellin synthesis pathway, Science, 2014, vol. 346, no. 6208, pp. 469–473. https://doi.org/10.1126/science.1259923

    Article  CAS  PubMed  Google Scholar 

  21. Chiou, W.L. and Farrar, D.R., Antheridiogen production and response in Polypodiaceae species, Am. J. Bot., 1997, vol. 84, no. 5, pp. 633–640.https://doi.org/10.2307/2445900

    Article  CAS  Google Scholar 

  22. Furber, M., Kraft-Klaunzer, P., Mander, L.N., Pour, M., Yamane, H., Yamauchi, T., and Murofushi, N., Synthesis and structure determination of gibberellins derived antheridiogens from fern gametophytes of the Lygodium genus, Austr. J. Chem., 1995, vol. 48, pp. 427–444.https://doi.org/10.1071/CH9950427

    Article  CAS  Google Scholar 

  23. Furber, M., Lewis, N., and Graham, L.P., New synthesis pathways from gibberellins to antheridiogens isolated from tree fern genus, Anemia,J. Org. Chem., 1990, vol. 55, no. 16, pp. 4860–4870.

    Article  CAS  Google Scholar 

  24. Korpelainen, H., Labile sex expression in plants, Biol. Rev., 1998, vol. 73, pp. 157–180.https://doi.org/10.1111/j.1469-185X.1997.tb00028.x

    Article  Google Scholar 

  25. Menéndez, V., Abul, Y., Bohanec, B., Lafont, F., and Fernández, H., The effect of exogenous and endogenous phytohormones on the in vitro development of gametophyte and sporophyte in Asplenium nidus L., Acta Physiol. Plant., 2011, vol. 33, pp. 2493–2500. https://doi.org/10.1007/s11738-011-0794-9

    Article  CAS  Google Scholar 

  26. Menéndez, V., Villacorta, N.F., Revilla, M.A., Gotor, V., Bernard, P., and Fernandez, H., Exogenous and endogenous growth regulators on apogamy in Dryopteris affnis (Lowe) Frasser-Jenkins, Plant Cell Rep., 2006, vol. 25, no. 2, pp. 85–91. https://doi.org/10.1007/s00299-005-0041-1

    Article  CAS  PubMed  Google Scholar 

  27. Menéndez, V., Revilla, M.A., Bernard, P., Gotor, V., and Fernandez, H., Gibberellins and antheridiogen on sex in Blechnum spicant L., Plant Cell Rep., 2006, vol. 25, pp. 1104–1110. https://doi.org/10.1007/s00299-006-0149-y

    Article  CAS  PubMed  Google Scholar 

  28. Menéndez, V., Revilla, M.A., Fal, M.A., and Fernández, H., The effect of cytokinins on growth and sexual organ development in the gametophyte of Blechnum spicant L., Plant Cell Tiss. Organ. Cult., 2009, vol. 96, pp. 245–250. https://doi.org/10.1007/s11240-008-9481-y

    Article  CAS  Google Scholar 

  29. Cheng, C.Y. and Schraudolf, H., Nachweis von abscisinsaure in sporen und jungen Prothallien von Anemia phyllitidis L. Sw., Zeitschrift fur Pflanzenphysiologie, 1974, vol. 71, pp. 366–369. https://doi.org/10.1016/S0044-328

  30. Bürcky, K., Das Vorkommen von Abscisin saure in Anemia phyllitidis L. Sw. (Schizaeaceae) wahrencl cler Sporenreifung, Zeitschrift fur Pflanzenphysiologie, 1977, vol. 85, no. 2, pp. 181–183.https://doi.org/10.1016/S0044-328X(77)80294-8

    Article  Google Scholar 

  31. Hickok, L.G., Abscisic acid resistant mutants in the fern Ceratopteris: characterization and genetic analysis, Can. J. Bot., 1985, vol. 63, pp.1582–1585.https://doi.org/10.1139/b85-220

    Article  CAS  Google Scholar 

  32. Warne, T.R. and Hickok, L.G., Control of sexual development in gametophytes of Ceratopteris richardii: antheridiogen and abscisic acid, Bot. Gaz., 1991, vol. 152, pp. 148–153. https://doi.org/10.1086/337874

    Article  CAS  Google Scholar 

  33. Hickok, L.G., Abscisic acid blocks antheridiogen induced antheridium formation in gametophytes of the fern Ceratopteris, Can. J. Bot., 1983, vol. 61, pp. 888–892.https://doi.org/10.1139/b83-098

    Article  CAS  Google Scholar 

  34. Voytenko, L.V. and Kosakivska, I.V., Peculiarities of the accumulation and distribution of indole-3-acetic and abscisic acids in the organs of sporophyte of wild fern Polystichum aculeatum (L.) Roth. at different phenological phases of development, Dopov. Natl. Acad. Sci. Ukr., 2017, vol. 12, pp. 112–118. https://doi.org/10.15407/dopovidi2017.12.112

  35. Babenko, L.M., Romanenko, K.O., Shcherbatiuk, M.M., Vasheka, O.V., Romanenko, P.O., Negretsky, V.A., and Kosakivska, I.V., Effects of exogenous phytohormones on spore germination and morphogenesis of Polystichum aculeatum (L.) Roth gametophyte in vitro culture, Cytol. Genet., 2018, vol. 52, no. 2, pp. 117–126.https://doi.org/10.3103/S0095452718020032

    Article  Google Scholar 

  36. Dobrev, P.I. and Vankova, R., Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues, in Plant Salt Tolerance. Methods in Molecular Biology (Methods and Protocols), Shabala, S. and Cuin, T., Eds., Totowa, N.J.: Humana Press, 2012, vol. 913, pp. 2251–2261. https://doi.org/10.1007/978-1-61779-986-0_17

    Google Scholar 

  37. Kiran, N.S., Benkova, E., Rekova, A., Dubova, J., Malbeck, J., Palme, K., and Brzobohaty, B., Retargeting a maize -glucosidase to the vacuole-evidence from intact plants that zeatin-O-glucoside is stored in the vacuole, Phytochemistry, 2012, vol. 79, pp. 67–77. https://doi.org/10.1016/j.phytochem.2012.03.012

    Article  CAS  PubMed  Google Scholar 

  38. Sassi, M. and Vernoux, T., Auxin and self-organization at the shoot apical meristem, J. Exp. Bot., 2013, vol. 64, no. 9, pp. 2579–2592. https://doi.org/10.1093/jxb/ert101

    Article  CAS  PubMed  Google Scholar 

  39. Simm, S., Scharf, K.-D., Jegadeesan, S., Chiusano, M.L., Firon, N., and Schleiff, E., Survey of genes involved in biosynthesis, transport, and signaling of phytohormones with focus on Solanum lycopersicum,Bioinform. Biol. Insights, 2016, vol. 10, pp. 185–207. https://doi.org/10.4137/BBI.S38425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Valledor, L., Menendez, V., Canal, M.J., Revilla, A., and Fernandez, H., Proteomic approaches to sexual development mediated by antheridiogen in the fern Blechnum spicant L., Proteomics, 2014, vol. 14, nos. 17–18, pp. 2061–2071. https://doi.org/10.1002/pmic.201300166

    Article  CAS  PubMed  Google Scholar 

  41. Kazmerczak, A., Ethylene is a positive regulation for GA3-induced male sex in Anemia phyllitidis gametophytes, Plant Cell Rep., 2003, vol. 22, no. 5, pp. 295–302.https://doi.org/10.1007/s10535-007-0143-4

    Article  Google Scholar 

  42. Banks, J.A., Mutations affecting the sexual phenotype of the Ceratopteris richardii gametophyte, J. Cell Biochem., 1993, suppl. 17 B, pp. 13–26.

  43. Nakanishi, K., Endo, M., Naef, U., and Johnson, L.F., Structure of the antheridium-inducing factor of the fern Anemia phyllitidis, J. Am. Chem. Soc., 1971, vol. 93, no. 21, pp. 5579–5581.https://doi.org/10.1021/ja00750a047

    Article  CAS  Google Scholar 

  44. Schafer, M., Brutting, C., Meza-Canales, I.D., Grokinsky, D.K., Vankova, R., Baldwin, I.T., and Meldau, S., The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions, J. Exp. Bot., 2015, vol. 66, no. 16, pp. 4873–4884.https://doi.org/10.1093/jxb/erv214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schaller, G.E., Street, I.H., and Kieber, J.J., Cytokinin and the cell cycle, Curr. Opin. Plant Biol., 2014, vol. 21, pp. 7–15.

    Article  CAS  Google Scholar 

  46. Letham, D.S., Cytokinins as phytohormones—sites of biosynthesis, translocation and function of translocated cytokinin, in Cytokinins: Chemistry, Activity and Function, Mok, D.W.S. and Mok, M.C., Eds., Boca Raton, Florida: CRC Press, 1994, pp. 57–80.

    Google Scholar 

  47. Nakazawa, S., Morphogenesis of the fern protonema. II. Modification of the apical differentiation in Dryopteris affected by IAA, Protoplasma, 1959, vol. 52, no. 1, pp. 1–4.https://doi.org/10.1007/BF02665680

    Article  Google Scholar 

  48. Kwa, S.H., Wee, Y.C., Lim, T.M., and Kumar, P.P., Morphogenetic plasticity of callus reinitiated from cell suspension cultures of the fern Platycerium coronarium, Plant Cell Tissue Organ. Cult., 1997, vol. 48, pp. 37–44.https://doi.org/10.1023/A:1005756822370

    Article  CAS  Google Scholar 

  49. Chia, S.G.E. and Raghavan, V., Abscisic acid effects on spore germination and protonemal growth in the fern Mohria caffrorum, New Phytol., 1982, vol. 92, pp. 31–37.https://doi.org/10.1111/j.1469-8137.1982.tb03360.x

    Article  CAS  Google Scholar 

  50. Bonomo, M.C., Martinez, O.G., Tanco, M.E., Cardozo, R., and Aviles, Z., Spores germination and gametophytes of Alsophila odonelliana (Cyatheaceae) in different sterile media, Phyton (Buenos Aires), 2013, vol. 82, pp. 119–126.

    Google Scholar 

  51. Greer, G.K., Dietrich, M.A., DeVol, J.A., and Rebert, A., The effects of exogenous cytokinin on the morphology and gender expression of Osmunda regalis gametophytes, Am. Fern J., 2012, vol. 102, pp. 32–46.https://doi.org/10.1640/0002-8444-102.1.32

    Article  Google Scholar 

  52. Spiro, M.D., Torabi, B., and Cornell, C.N., Cytokinins induce photomorphogenic development in dark grown gametophytes of Ceratopteris richardii,Plant Cell Physiol., 2004, vol. 45, pp. 1252–1260. https://doi.org/10.1093/pcp/pch146

    Article  CAS  PubMed  Google Scholar 

  53. Miller, P.M., Sweet, H.C., and Miller, J.H., Growth Regulation by Ethylene in Fern Gametophytes. I. Effects on protonemal and rhizoidal growth and interaction with auxin, Am. J. Bot., 1970, vol. 57, no. 2, pp. 212–217.

    Article  CAS  Google Scholar 

Download references

Funding

The publication contains the results of research performed within the framework of the project funded by the National Academy of Sciences of Ukraine no. III-71-14.431 “Hormonal Control of Growth and Development of Spore Plants (Various Taxonomic Affiliation).”

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to I. V. Kosakivska, V. A. Vasyuk, L. V. Voytenko, M. M. Shcherbatiuk, K. O. Romanenko or L. M. Babenko.

Ethics declarations

The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

Additional information

Translated by V. Mittova

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kosakivska, I.V., Vasyuk, V.A., Voytenko, L.V. et al. Endogenous Phytohormones of Fern Polystichum aculeatum (L.) Roth Gametophytes at Different Stages of Morphogenesis in vitro Culture. Cytol. Genet. 54, 23–30 (2020). https://doi.org/10.3103/S0095452720010089

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452720010089

Keywords:

Navigation