TSitologiya i Genetika 2019, vol. 53, no. 3, 12-24
Cytology and Genetics 2019, vol. 53, no. 3, 192–201, doi: https://www.doi.org/10.3103/S0095452719030034

Effects of exogenous cytokinins on spore germination and gametophyte morphogenesis of Dryopteris filix­mas (L.) Schott in vitro culture

Romanenko K.O., Kosakivska I.V., Babenko L.M., Vasheka O.V., Romanenko P.O., Negretsky V.A., Minarchenko V.M.

SUMMARY. The effects of exogenous cytokinin phytohormones: kinetin, zeatin, 6-benzylaminopurine, N6-2-isopenteny-ladenine on the pattern of spore germination as well as gametophyte morphology and growth features of Dryopteris filix-mas (L.) Schott in vitro culture have been studied. It was established that at the concentration of 10–5 М all studied cytokinins significantly retarded spore germination, inhibited gametophyte growth, caused deformations and changes in the thallus size, suppressed the development of reproductive structures and sporophyte growth. The reduction of the hormone concentration to 10–8 М stimulated the gametophyte development, induced cell divisions, particularly in the apical zone, due to which some of thalli were deformed, promoted the production of rhizoids, affected the formation of antheridia and archegonia and slowed the sporophyte development.

Keywords: Dryopteris filix-mas, gametophyte, spores, prothallium, thallus, cytokinins, kinetin, zeatin, 6-benzylaminopurine, ​N6-isopentenyladenine

TSitologiya i Genetika
2019, vol. 53, no. 3, 12-24

Current Issue
Cytology and Genetics
2019, vol. 53, no. 3, 192–201,
doi: 10.3103/S0095452719030034

Full text and supplemented materials

Free full text: PDF  

References

1. 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. Eearth Sci., 2016, vol. 1, pp. 26–44.

2. Plant Hormones: Biosynthesis, Signal Transduction, Action, Davies, P.J., Ed., Netherlands: Springer, 2010. 3rd ed. https://doi.org/10.1007/978-1-4020-2686-7

3. Fonseca, S., Rosado, A., Vaughan-Hirsch, J., Bishopp, A., and Chini, A., Molecular locks and keys: the role of small molecules in phytohormone research, Front. Plant Sci., 2014, vol. 5, art. 709, pp. 1–16. https://doi.org/10.3389/fpls.2014.00709

4. Wang, Y.H. and Irving, H.R., Developing a model of plant hormone interactions, Plant Signal. Behav., 2011, vol. 6, pp. 494–500. https://doi.org/10.4161/psb.6.4.14558

5. Wells, D.M., Laplaze, L., Bennett, M.J., and Vernoux, T., Biosensors for phytohormone quantification: challenges, solutions, and opportunities, Trends Plant Sci., 2013, vol. 18, pp. 244–249. https://doi.org/10.1016/j.tplants.2012.12.005

6. Borghi, L., Kang, J., Ko, D., Lee, Y., and Martinoia, E., The role of ABCG-type ABC transporters in phytohormone transport, Biochem. Soc. Trans., 2015, vol. 43, pp. 924–930. https://doi.org/10.1042/BST20150106

7. Raghavan, V., Developmental Biology of Fern Gametophytes, Cambridge University Press, 1989. https://doi.org/10.1017/CBO9780511529757

8. Du, H., Li, Y., Li, D., Dai, S., Jiang, C., and Shi, L., Effects of light, temperature and pH on spore germination and early gametophytic development of Alsophila metteniana, Biodiv. Sci., 2009, vol. 17, pp. 182–187. https://doi.org/10.3724/SP.J.1003.2009.08262

9. Juárez-Orozco, S., Orozco-Segovia, A., Mendoza-Ruiz, A., and Pérez-García, B., Spore germination of eight homosporous ferns in a temperature gradient, S. Afr. J. Bot., 2013, vol. 87, pp. 112–117. https://doi.org/10.1016/j.sajb.2013.04.005

10. Edwards, E.S. and Roux, S.J., Influence of gravity and light on the developmental polarity of Ceratopteris richardii fern spores, Planta, 1998, vol. 205, pp. 553–560. https://doi.org/10.1007/s004250050355

11. Wu, H., Liu, X.-Q., Ji, H., and Chen, L.-Q., Effects of light, macronutrients, and sucrose on germination and development of the endangered fern Adiantum reniforme var. sinense (Adiantaceae), Sci. Hortic., 2010, vol. 125, pp. 417–421. https://doi.org/10.1016/j.scienta.2010.03.004

12. Suo, J., Chen, S., Zhao, Q., Shi, L., and Dai, S., Fern spore germination in response to environmental factors, Front. Biol., 2015, vol. 10, pp. 358–376. https://doi.org/10.1007/s11515-015-1342-6

13. Edwards, M.E., Carbon dioxide and ethylene control of spore germination in Onoclea sensibilis L., Plant Physiol., 1977, vol. 59, pp. 756–758. https://doi.org/10.1104/pp.59.4.756

14. Camloh, M., Ravnikar, M., and Zel, J., Jasmonic acid promotes division of fern protoplasts, elongation of rhizoids and early development of gametophytes, Physiol. Plant, 1996, vol. 97, pp. 659–664. https://doi.org/10.1111/j.1399-3054.1996.tb00529.x

15. 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.

16. 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, pp. 117–126. https://doi.org/10.3103/S0095452718020032

17. Gómez-Garay, A., Galán, J.M.G., Cabezuelo, A., Pintos, B., Prada, C., and Martín, L., Ecological significance of brassinosteroids in three temperate ferns, in Current Advances in Fern Research, Cham: Springer, 2018, pp. 453–466. https://doi.org/10.1007/978-3-319-75103-0_21

18. Takeno, K. and Furuya, M., Inhibitory effect of gibberellins on archegonial differentiation in Lygodium japonicum, Physiol. Plant., 1977, vol. 39, pp. 135–138. https://doi.org/10.1111/j.1399-3054.1977.tb04024.x

19. Swami, P. and Raghavan, V., Control of morphogenesis in the gametophyte of a fern by light and growth hormones, Can. J. Bot., 1980, vol. 58, pp. 1464–1473. https://doi.org/10.1139/b80-179

20. Kazmierczak, A., Induction of cell division and cell expansion at the beginning of gibberellin A3-induced precocious antheridia formation in Anemia phyllitidis gametophytes, Plant Sci., 2003, vol. 165, pp. 933–939. https://doi.org/10.1016/S0168-9452(03)00217-6

21. Castilho, C.V.V., Neto, J.F.F., Leitao, S.G., Bar-reto, S.C.P., and Silva, N.C.B., Anemia tomentosa var. anthriscifolia in vitro culture: sporophyte development and volatile compound profile of an aromatic fern, Plant Cell Tiss. Organ Cult., 2018, pp. 1–13. https://doi.org/10.1007/s11240-018-1383-z

22. Miller, J.H., Fern gametophytes as experimental material, Bot. Rev., 1968, vol. 34, pp. 361–440. https://doi.org/10.1007/BF02859133

23. Korpelainen, H., Growth, sex determination and reproduction of Dryopteris filix-mas (L.) Schott gametophytes under varying nutritional conditions, Bot. J. Linn. Soc., 1994, vol. 114, pp. 357–366. https://doi.org/10.1006/bojl.1994.1022

24. Atallah, N.M. and Banks, J.A., Reproduction and the pheromonal regulation of sex type in fern gametophytes, Front. Plant Sci., 2015, vol. 6, art. 100, pp. 1–6. https://doi.org/10.3389/fpls.2015.00100

25. Hollingsworth, S., Andres, E., and Greery, G., Pheromonal interactions among gametophytes of Osmundastrum cinnamomeum and the origins of antheridiogen systems in leptosporangiate ferns, Int. J. Plant Sci., 2012, vol. 173, pp. 382–390. https://doi.org/10.1086/664717

26. Menéndez, V., Revilla, M.A., Bernard, P., Gotor, V., and Fernández, 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

27. Kwa, S.H., Wee, Y.C., Lim, T.M., and Kumar, P.P., IAA-induced apogamy in Platycerium coronarium (Koenig) Desv. gametophytes cultured in vitro, Plant Cell Rep., 1995, vol. 14, pp. 598–602. https://doi.org/10.1007/BF00231946

28. Higuchi, H., Amaki, W., and Suzuki, S., In vitro propagation of Nephrolepis cordifolia Prsel., Sci. Hortic., 1987, vol. 32, pp. 105–113. https://doi.org/10.1016/0304-4238(87)90021-5

29. Fernández, H. and Revilla, M.A., In vitro culture of ornamental ferns, Plant Cell Tissue Organ Cult., 2003, vol. 73, pp. 1–13. https://doi.org/10.1023/A:1022650701341

30. Bharati, S.K., Manabendra, D.C., and Mazumder, P.B., In vitro propagation in Pteridophytes, Int. J. Res. Ayurveda Pharm., 2013, vol. 4, pp. 297–303. https://doi.org/10.7897/2277-4343.04245

31. Somer, M., Arbesū, R., Menéndez, V., Revilla, M.A., and Fernández, H., Sporophyte induction studies in ferns in vitro, Euphytica, 2010, vol. 171, p. 203. https://doi.org/10.1007/s10681-009-0018-1

32. Chen, S.Y. and Read, P.E., Micropropagation of leatherleaf fern (Rumohra adiantiformis), Proc. Fla. State Hort. Soc., 1983, vol. 96, pp. 266–269.

33. 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. 2493–500. https://doi.org/10.1007/s11738-011-0794-9

34. Higuchi, H. and Amaki, W., Effects of 6-benzylaminopurine on the organogenesis of Asplenium nidus L. through in vitro propagation, Sci. Hortic., 1989, vol. 37, pp. 351–359. https://doi.org/10.1016/0304-4238(89)90146-5

35. Vedenicheva, N.P. and Kosakivska, I.V., Modern aspects of cytokinins studies: evolution and crosstalk with other phytohormones, Fiziol. Rast. Genet., 2016, vol. 48, pp. 3–19.

36. Vedenicheva, N.P. and Kosakivska, I.V., Cytokinins As Regulators of Plant Ontogenesis Under Different Growth Conditions, Kyiv: Nash Format, 2017.

37. Veselov, D.S., Kudoyarova, G.R., Kudryakova, N.V., and Kusnetsov, V.V., Role of cytokinins in stress resistance of plants, Russ. J. Plant Physiol., 2017, vol. 64, pp. 15–27. https://doi.org/10.1134/S1021443717010162

38. Kudo, T., Makita, No., Kojima, M., Tokunaga, H., and Sakakibara, H., Cytokinin activity of cis-zeatin and phenotypic alterations induced by overexpression of putative cis-zeatin-o-glucosyltransferase in rice, Plant Physiol., 2012, vol. 160, pp. 319–331. https://doi.org/10.1104/pp.112.196733

39. Huang, S., Cerny, R.E., Qi, Y., Bhat, D., Aydt, C.M., Hanson, D.D., Malloy, K.P., and Ness, L.A., Transgenic studies on the involvement of cytokinin and gibberellin in male development, Plant Physiol., 2003, vol. 131, pp. 1270–1282. https://doi.org/10.1104/pp.102.018598

40. Gerashchenkov, G.A. and Rozhnova, N.A., The involvement of phytohormones in the plant sex regulation, Russ. J. Plant Physiol., 2013, vol. 60, pp. 597–610. https://doi.org/10.1134/S1021443713050063

41. Beck, M.J. and Caponetti, J.D., The effects of kinetin and naphthaleneacetic acid on in vitro shoot multiplication and rooting in the fishtail fern, Am. J. Bot, 1983, vol. 70, pp. 1–7.

42. Hicks, G. and Aderkas, P.V., A tissue culture of the Ostrich fern Matteuccia struthiopteris (L.) Todaro, Plant Cell Tiss. Organ Cult, 1986, vol. 5, pp. 199–204. https://doi.org/10.1007/BF00040130

43. Amaki, W. and Higuchi, H., A possible propagation system of Nephrolepis, Asplenium, Pteris, Adiantum and Rumora through tissue culture, Acta Hortic., 1991, vol. 300, pp. 237–243. https://doi.org/10.17660/ActaHortic.1992.300.33

44. Fernández, H., Bertrand, A.M., and Sánchez-Tamés, R., Micropropagation and phase change in Blechnum spicant and Pteris ensiformis, Plant Cell Tiss. Organ Cult., 1996, vol. 44, pp. 261–265. https://doi.org/10.1007/BF00048534

45. Fernández, H., Bertrand, A., and Sánchez-Tamés, R., Plantlet regeneration in Asplenium nidus L. and Pteris ensiformis L. by homogenization of BA treated rhizomes, Sci. Hortic., 1997, vol. 68, pp. 243–247. https://doi.org/10.1016/S0304-4238(96)00986-7

46. 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

47. 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 regalisgametophytes, Am. Fern J., 2012, vol. 102, pp. 32–46. https://doi.org/10.1640/0002-8444-102.1.32

48. 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.

49. 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

50. 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

51. Parajuli, J. and Joshi, S.D., In vitro study of effects of growth hormones on sporophyte development of Cyathea spinulosa, Int. J. Biodivers. Conserv., 2014, vol. 6, pp. 247–255. https://doi.org/10.5897/IJBC2014.0684

52. Grichuk, V.P. and Monoszon, M.H., The Determinant of Single-Beam Spores of the Ferns from the Family Polypodiaceae R. Br., Growing on the Territory of the USSR, Moscow: Nauka, 1971.

53. Nayar, B.K. and Kaur, S., Gametophytes of homosporous ferns, Bot. Rev., 1971, vol. 37, pp. 295–396. https://doi.org/10.1007/BF02859157

54. Tryon, A.F. and Lugardon, B., Dryopteridaceae Herter, in spores of the pteridophyta, springer, New York, 1991. https://doi.org/10.1007/978-1-4613-8991-0_25

55. Gaba, V., Plant growth regulators in plant tissue culture and development, in Plant Tissue Culture, Development, and Biotechnology, Trigiano, R.N. and Gray, D.J., Eds., CRC Press, 2005, pp. 87–99.