en   ru   uk  
 
 
Fiziol. rast. genet. 2019, vol. 51, no. 3, 187-206, doi: https://doi.org/10.15407/frg2019.03.187

Phytohormonal regulation of seed germination

Kosakivska I.V., Voytenko L.V., Vasyuk V.A., Vedenichova N.P., Babenko L.M., Shcherbatyuk M.M.

  • M.G. Kholodny Institute of Botany National Academy of Sciences of Ukraine 2 Tereshchenkivska St., Kyiv, 01601, Ukraine

The review focuses on the analysis of new information concerning the role of phytohormones in the regulation of dormancy and seed germination. It is noted that abscisic acid (ABA) and gibberellins (GA) belong to key endogenous factors, which determine the state of seeds. High endogenous ABA and low GA levels result in deep seed dormancy, while low ABA and high GA levels induce the beginning of germination. Changes in accumulation of key hormones and expression of key regulators during seed maturation and germination were discussed. In addition to ABA and GA all other phytohormones are also involved in modulation of seed dormancy and germination, including auxin, cytokinins, ethylene, brassinosteroids, jasmonic acid, salicylic acid, and strigolactones. The two major aspects of the ABA/GA balance regulation — the balance of hormone levels and the balance of the signaling cascades were analyzed. The accumulation of plant hormones can positively or adversely affect seed germination, while interacting with each other. While the activity of plant hormones is controlled by the expression of genes at different levels, there are plant genes that activated in the presence of specific plant hormones. We presented the scheme of auxin, cytokinins, ethylene, brassinosteroids, jasmonic acid, salicylic acid, and strigolactones involvement into regulation of seed germination processes through an integrated network of interaction with ABA and gibberellins. The influence of external factors on the hormonal system during germination of seeds and the participation of phytohormones in the formation of protective reactions for the effects of abiotic stresses are discussed. The state of the study of the role of the phytohormonal system in the regulation of germination processes of cereal grains was characterized. The possibilities and perspectives of the use of exogenous phytohormones for presowing priming of seeds are analyzed in order to regulate the intensity of physiological and metabolic processes and increase the stress resistance.

Keywords: phytohormone, abscisic acid, gibberellins, seeds, dormancy, germination, priming

Fiziol. rast. genet.
2019, vol. 51, no. 3, 187-206

Full text and suplimented materials

Free full text: PDF  

References

1. Bewley, J.D. & Black, M. (1994). Seeds: Physiology of Development and Germination. Berlin: Springer https://doi.org/10.1007/978-1-4899-1002-8

2. Liu, A., Gao, F., Kanno, Y., Jordan, M., Kamiya, Y., Seo, M. & Ayele, B. (2013). Regulation of wheat seed dormancy by after-ripening is mediated by specific transcriptional switches that induce changes in seed hormone metabolism and signaling. PloS One, 8, e56570. https://doi.org/10.1371/journal.pone.0056570

3. Chitnis, V.R., Gao, F., Yao, Z., Jordan, M.C., Park, S. & Ayele, B.T. (2014). After ripening induced transcriptional changes of hormonal genes in wheat seeds: the cases of brassinosteroids, ethylene, cytokinin and salicylic acid. PLoS One, 9:e87543. https://doi.org/10.1371/journal.pone.0087543

4. Shu, K., Liu, X., Xie, Q. & He, Z. (2016). Two Faces of One Seed: Hormonal Regulation of Dormancy and Germination. Mol. Plant., 69, pp. 34-45. https://doi.org/10.1016/j.molp.2015.08.010

5. Santner, A., Calderon-Villalobos, L. & Estelle, M. (2009). Plant hormones are versatile chemical regulators of plant growth. Nature Chem. Biol., 5, pp. 301-307. https://doi.org/10.1038/nchembio.165

6. Miransari, M. & Smith, D.L. (2014). Plant hormones and seed germination. Environ. Exp. Bot., 99, pp. 111-123. https://doi.org/10.1016/j.envexpbot.2013.11.005

7. Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G. & Soppe, W. (2012). Molecular mechanisms of seed dormancy. Plant Cell Environ., 35 (10), pp. 1769-1786. https://doi.org/10.1111/j.1365-3040.2012.02542.x

8. Kucera, B., Cohn, M.A. & Leubner-Metzger, G. (2005). Plant hormone interactions during seed dormancy release and germination. Seed Sci Res., 15, pp. 281-307. https://doi.org/10.1079/SSR2005218

9. Finkelstein, R.R., Reeves, W., Ariizumi, T. & Steber, C. (2008). Molecular aspects of seed dormancy. Ann. Rev. Plant Biol., 59, pp. 387-415. https://doi.org/10.1146/annurev.arplant.59.032607.092740

10. Finch-Savage, W.E. & Footitt, S. (2017). Seed dormancy cycling and the regulation of dormancy mechanisms to time germination in variable field environments. J. Exp. Bot., 68, pp. 843-856. https://doi.org/10.1093/jxb/erw477

11. Olds, C.L., Glennon, E.K.K. & Luckhart, S. (2018). Abscisic acid: new perspectives on an ancient universal stress signaling molecule. Microbes Infection., 20 (9-10), pp. 484-492. https://doi.org/10.1016/j.micinf.2018.01.009

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

13. Chandrasekaran, U. & Liu, A. (2014). Endogenous abscisic acid signaling towards storage reserve filling in developing seed tissues of castor bean (Ricinus communis L.). Plant Growth Regul., 72, pp. 203-207. https://doi.org/10.1007/s10725-013-9846-z

14. Finkelstein, R.R. & Rock, C.D. (2002). Abscisic acid biosynthesis and response. The Arabidopsis Book/Eds. C.R. Somerville, E.M. Meyerowitz. Amer. Soc. Plant Biologists: Rockville, MD, pp. 137-155. https://doi.org/10.1199/tab.0058

15. Graeber, K., Linkies, A., Muller, K., Wunchova, A., Rott, A. & Leubner-Metzger, G. (2010). Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol. Biol., 73, pp. 67-87. https://doi.org/10.1007/s11103-009-9583-x

16. Xiong, L. & Zhu, J.-K. (2003). Regulation of Abscisic acid Biosynthesis. Plant Physiol., 133 (1), pp. 29-36. https://doi.org/10.1104/pp.103.025395

17. Tooro, P.E., Van Aelst, A.C. & Hilhors, H.W.M. (2000). The Second Step of the Biphasic Endosperm Cap Weakening that Mediates Tomato (Lycopersicon esculentum) Seed Germination is Under Control of ABA. J. Exp. Bot., 51 (349), pp. 1371-1379. https://doi.org/10.1093/jxb/51.349.1371

18. Humplik, J.F., Bergougnoux, V. & Van Volkenburgh, E. (2017). To Stimulate or Inhibit? That Is the Question for the Function of Abscisic Acid. Trends in Plant Science, 22 (10), pp. 830-841. https://doi.org/10.1016/j.tplants.2017.07.009

19. Lorrai, R., Boccaccini, A., Ruta, V., Possenti, M., Costantino, P. & Vittorioso, P. (2017). Abscisic acid inhibits hypocotyl elongation acting on gibberellins, DELLA proteins and auxin. AoB PLANTS, 10: ply061. https://doi.org/10.1093/aobpla/ply061

20. Lee, Y.-I., Chung, M.-C., Yeung, E.C. & Lee, N. (2015). Dynamic distribution and the role of abscisic acid during seed development of a lady's slipper orchid, Cypripedium formosanum. Annals of Botany, 116 (3), pp. 403-411. https://doi.org/10.1093/aob/mcv079

21. Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L. & Zhu, J.K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature, 462, pp. 660-664. https://doi.org/10.1038/nature08599

22. Ren, C. & Bewley, J.D. (1999). Developmental and Germinative Events can Occure Concurrently in Precociously Germinating Chinese Cabbage (Brassica rapa ssp. Pekinensis) Seeds. J. Exp. Bot., 50 (341), pp. 1751-1761. https://doi.org/10.1093/jxb/50.341.1751

23. Muller, K., Tintelnot, S. & Leubner-Metzger, G. (2006). Endosperm limited Brassicaceae seed germination: abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol., 47, pp. 864-877. https://doi.org/10.1093/pcp/pcj059

24. Kosakivska, I.V., Vasyuk, V.A. & Voytenko, L.V. (2019). Effects of exogenous abscisic acid on seed germination and morphological characteristics of two related wheats Triticum aestivum L. and Triticum spelta L. Fiziol. rast. genet., 51, No. 1, pp. 55-66 [in Ukrainian]. https://doi.org/10.15407/frg2019.01.055

25. Nambara, E. & Marion-Poll, A. (2005). Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol., 56, pp. 165-185. https://doi.org/10.1146/annurev.arplant.56.032604.144046

26. Martinez-Andujar, C., Ordiz, M.I., Huang, Z., Nonogaki, M., Beachy, R.N. & Nonogaki, H. (2011). Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proc. Natl. Acad. Sci. USA, 108, pp. 17225-17229. https://doi.org/10.1073/pnas.1112151108

27. Behnam, B., Iuchi, S., Fujita, M., Fujita, Y., Takasaki, H., Osakabe, Y., Yamaguchi-Shinozaki, K., Kobayashi, M. & Shinozaki, K. (2013). Characterization of the promoter region of an arabidopsis gene for 9-cis-epoxycarotenoid dioxygenase involved in dehydration-inducible transcription. DNA Res., 20, pp. 315-324. https://doi.org/10.1093/dnares/dst012

28. Park, S., Fung, P., Nishimura, N., Jensen, D., Fujii, H., Zhao, Y., Lumb, S., Santiago, J., Rodrigues, A., Chow, T., Alfred, S., Bonetta, D., Finkelstein, R., Provart, N., Desveaux, D., Rodriguez, P., McCourt, P., Zhu, J., Schroeder, J., Volkman, B. & Cutler, S. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science, 324, pp. 1068-1071. https://doi.org/10.1126/science.1173041

29. Liu, X., Yue, Y., Li, B., Nie, Y., Li, W., Wu, W.H. & Ma, L. (2007). A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science, 315, pp. 1712-1716. https://doi.org/10.1126/science.1135882

30. Pandey, S., Nelson, D. & Assmann, S. (2009). Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell, 136 (1), pp. 136-148. https://doi.org/10.1016/j.cell.2008.12.026

31. Shen, Y.Y., Wang, X.F., Wu, F.Q., Du, S.Y., Cao, Z., Shang, Y., Wang, X.L., Peng, C.C., Yu, X.C., Zhu, S.Y., Fan, R.C., Xu, Y.H. & Zhang, D.P. (2006). The Mg-chelatase H subunit is an abscisic acid receptor. Nature, 443, pp. 823-826. https://doi.org/10.1038/nature05176

32. 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, pp. 1064-1068. https://doi.org/10.1126/science.1172408

33. Sponsel, V.M. & Hedden, P. (2010). Gibberellin Biosynthesis and Inactivation. Plant Hormones. Biosynthesis, Signal Transduction, Action/Ed. Davies P.J. Dordrecht: Springer, pp. 63-94. https://doi.org/10.1007/978-1-4020-2686-7_4

34. Daviere, J.M. & Achard, P. (2013). Gibberellin signaling in plants. Development, 140 (6), pp. 1147-1151. https://doi.org/10.1242/dev.087650

35. Gupta, R. & Chakrabarty, S. (2013). Gibberellic acid in plant. Plant Signal Behav., 8 (9): e25504. Published online 2013 Jun 28. https://doi.org/10.4161/psb.25504

36. Tuan, P.A., Kumar, R., Rehal, P.K., Toora, P.K. & Ayele, B.T. (2018). Molecular Mechanisms Underlying Abscisic Acid/Gibberellin Balance in the Control of Seed Dormancy and Germination in Cereals. Frontiers in Plant Science, 9, pp. 1-14. https://doi.org/10.3389/fpls.2018.00668

37. Gallardo, K., Job, C., Groot, P.C., Puype, M., Demol, H., Vandekerckhove J. & Job, D. (2002). Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin deficient seeds. Plant Physiol., 129, pp. 823-837. https://doi.org/10.1104/pp.002816

38. Yamaguchi, S. (2008). Gibberellin metabolism and its regulation. Ann Rev Plant Biol., 59, pp. 225-251. https://doi.org/10.1146/annurev.arplant.59.032607.092804

39. Gubler, F., Kalla, R., Roberts, J.K. & Jacobsen, J.V. (1995). Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI alpha-amylase gene promoter. Plant Cell., 7 (11), pp. 1879-1891. https://doi.org/10.2307/3870195

40. Ogawa, M., Hanada, A., Yamauchi, Y., Kuwahara, A., Kamiya, Y. & Yamaguchi, S. (2003). Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell, 15, pp. 1591-1604. https://doi.org/10.1105/tpc.011650

41. Fincher, G.B. (1989). Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu. Rev. Plant Physiol. Plant Mol. Biol., 40, pp. 305-346. https://doi.org/10.1146/annurev.pp.40.060189.001513

42. Kaneko, M., Itoh, H., Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M. & Ashikari, M. (2003). Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? Plant J., 35, pp. 104-115. https://doi.org/10.1046/j.1365-313X.2003.01780.x

43. Gubler, F., Chandler, P.M., White, R.G., Llewellyn, D.J. & Jacobsen, J.V. (2002). Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol., 129, pp. 191-200. https://doi.org/10.1104/pp.010918

44. Voegele, A., Linkies, A., Muller, K. & Leubner-Metzger, G. (2011). Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp. Bot., 62 (14), pp. 5131-5147. https://doi.org/10.1093/jxb/err214

45. Shu, K., Zhang, H., Wang, S., Chen, M., Wu, Y., Tang, S., Liu, C., Feng, Y., Cao, X. & Xie, Q. (2013). ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genet., 9 (6), e1003577. https://doi.org/10.1371/journal.pgen.1003577

46. Yamauchi, Y., Takeda-Kamiya, N., Hanada, A., Ogawa, M., Kuwahara, A., Seo, M., Kamiya, Y. & Yamaguchi, S. (2007). Contribution of gibberellin deactivation by AtGA2ox2 to the suppression of germination of dark-imbibed Arabidopsis thaliana seeds. Plant Cell Physiol., 48, pp. 555-561. https://doi.org/10.1093/pcp/pcm023

47. Lee, S., Cheng, H., King, K.E., Wang, W., He, Y., Hussain, A., Lo, J., Harberd, N.P. & 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, pp. 646-658. https://doi.org/10.1101/gad.969002

48. Seo, M., Hanada, A., Kuwahara, A., Endo, A., Okamoto, M., Yamauchi, Y., North, H., Marion-Poll, A., Sun, T.P. & Koshiba, T. (2006). Regulation of hormone metabolism in Arabidopsis seeds phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. Plant J., 48, pp. 354-366. https://doi.org/10.1111/j.1365-313X.2006.02881.x

49. Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y. & Lopez-Molina, L. (2008). The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell, 20, pp. 2729-2745. https://doi.org/10.1105/tpc.108.061515

50. Izydorczyk, C., Nguyen, T.-N., Jo, S., Son, S., Tuan, P.A. & Ayele, B.T. (2017). Spatiotemporal modulation of abscisic acid and gibberellin metabolism and signaling mediates the effects of suboptimal and supraoptimal temperatures on seed germination in wheat (Triticum aestivum L.). Plant Cell Environ., 41, pp. 1022-1037. https://doi.org/10.1111/pce.12949

51. Gubler, F., Hughes, T., Waterhouse, P. & Jacobsen, J. (2008). Regulation of dormancy in barley by blue light and after-ripening: effects on abscisic acid and gibberellin metabolism. Plant Physiol., 147, pp. 886-896. https://doi.org/10.1104/pp.107.115469

52. Ishibashi, Y., Kasa, S., Sakamoto, M., Aoki, N., Kai, K. & Yuasa, T. (2015). A role for reactive oxygen species produced by NADPH oxidases in the embryo and aleurone cells in barley seed germination. PLoS One, 10, e0143173. https://doi.org/10.1371/journal.pone.0143173

53. Bassel, G.W., Lan, H., Glaab, E., Gibbs, D.J., Gerjets, T., Krasnogor, N., Bonner, A.J., Holdsworth, M.J. & Provart, N.J. (2011). Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl. Acad. Sci. USA, 108 (23), pp. 9709-9714. https://doi.org/10.1073/pnas.1100958108

54. Vishal, B. & Kumar, P.P. (2018). Regulation of Seed Germination and Abiotic Stresses by Gibberellins and Abscisic Acid. Frontiers in Plant Science, 9, pp. 1-15. https://doi.org/10.3389/fpls.2018.00838

55. Enders, T.A. & Strader, L.C. (2015). Auxin activity: past, present, and future. Amer. J. Botany, 102 (2), pp. 180-196. https://doi.org/10.3732/ajb.1400285

56. Wang, L., Hua, D., He, J., Duan, Y., Chen, Z., Hong, X. & Gong, Z. (2011). Auxin Response Factor 2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet., 7 (7), e1002172. https://doi.org/10.1371/journal.pgen.1002172

57. Belin, C., Megies, C., Hauserova, E. & Lopez-Molina, L. (2009). Abscisic acid represses growth of the Arabidopsis embryonic axis after germination by enhancing auxin signaling. Plant Cell, 21 (8), pp. 2253-2268. https://doi.org/10.1105/tpc.109.067702

58. Pieruzzi, F.P., Dias, L.L.C., Balbuena, T.S., Santa-Catarina, C., dos Santos, A.L.W. & Floh, E.I.S. (2011). Polyamines, IAA and ABA during germination in two recalcitrant seeds: Araucaria angustifolia (Gymnosperm) and Ocotea odorifera (Angiosperm). Ann. Bot., 108, pp. 337-345. https://doi.org/10.1093/aob/mcr133

59. Dias, L.L.C., Santa-Catarina, C., Silveira, V., Pieruzzi, F.P. & Floh, E.I.S. (2009). Polyamines, amino acids, IAA and ABA contents during Ocotea catharinensis seed germination. Seed Science and Technology, 37 (1), pp. 42-51. https://doi.org/10.15258/sst.2009.37.1.06

60. Santa-Catarina, C., Silveira, V., Balbuena, T.S., Maranhao, M.E.E., Handro, W. & Floh, E.I.S. (2006). IAA, ABA, polyamines and free amino acids associated with zygotic embryo development of Ocotea catharinensis. Plant Growth Regul., 49, pp. 237-247. https://doi.org/10.1007/s10725-006-9129-z

61. Park, J., Kim, Y.S., Kim, S.G., Jung, J.H., Wo, J.C. & Park, C.M. (2011). Integration of auxin and salt signals by the NAC transcription factor NTM2 during seed germination in Arabidopsis. Plant Physiol., 156, pp. 537-549. https://doi.org/10.1104/pp.111.177071

62. Ramaih, S., Guedira, M. & Paulsen, G.M. (2003). Relationship of indoleacetic acid and tryptophan to dormancy and preharvest sprouting of wheat. Funct. Plant Biol., 30, pp. 939-945. https://doi.org/10.1071/FP03113

63. Liu, X., Zhang, H., Zhao, Y., Feng, Z., Li, Q., Yang, H.Q., Luan, S., Li, J. & He, Z.H. (2013). Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc. Natl. Acad. Sci. USA, 110, pp. 15485-15490. https://doi.org/10.1073/pnas.1304651110

64. Hentrich, M., Boettcher, C. & Duchting, P. (2013). The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. Plant J., 74, pp. 626-637. https://doi.org/10.1111/tpj.12152

65. Friml, J., Wisniewska, J., Benkova, E., Mendgen, K. & Palme, K. (2002). Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature, 415, pp. 806-809. https://doi.org/10.1038/415806a

66. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz H., Hamann, T., Offringa, R. & Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 426 (6363), pp. 147-153. https://doi.org/10.1038/nature02085

67. Friml, J., Yang, X., Michniewicz, M., Weijers, D., Quint, A., Tietz, O., Benjamins, R., Ouwerkerk, P.B., Ljung, K., Sandberg, G., Hooykaas, P.J., Palme, K. & Offringa, R. (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306 (5697), pp. 862-865. https://doi.org/10.1126/science.1100618

68. Michniewicz, M., Zago, M.K., Abas, L., Weijers, D., Schweighofer, A., Meskiene, I., Heisler, M.G., Ohno, C., Zhang, J., Huang, F., Schwab, R., Weigel, D., Meyerowitz, E.M., Luschnig, C., Offringa, R. & Friml, J. (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell., 130, pp. 1044-1056. https://doi.org/10.1016/j.cell.2007.07.033

69. Dhonukshe, P., Tanaka, H., Goh, T., Ebine, K., Mahonen, A.P., Prasad, K., Blilou, I., Geldner, N., Xu, J., Uemura, T., Chory, J., Ueda, T., Nakano, A., Scheres, B. & Friml, J. (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature, 456 (7224), pp. 962-966. https://doi.org/10.1038/nature07409

70. Vedenicheva, N.P. & Kosakivska, I.V. (2017). Cytokinins as regulators of plant ontogenesis under different growth conditions. Kyiv: Nash Format [in Ukrainian].

71. Nonogaki, H. (2018). Seed germination and dormancy - the classic story, new puzzles, and evolution. J. of Integrative. Plant Biology, 40, pp. 1-23. https://doi.org/ 10.1111/jipb.12762

72. Stirk, W.A., Novak, O., Zizkova, E., Motyka, V., Strnad, M. & van Staden, J. (2012). Comparison of endogenous cytokinins and cytokinin oxidase/dehydrogenase activity in germinating and thermoinhibited Tagetes minuta achenes. J. Plant Physiol., 169 (7), pp. 696-703. https://doi.org/10.1016/j.jplph.2012.01.013

73. Stirk, W.A., Vaclavikova, K., Novak, O. & Gajdosova, S. (2012). Involvement of cis-zeatin, dihydrozeatin, and aromatic cytokinins in germination and seedling establishment of maize, oats, and lucerne. J. Plant Growth Regul., 31, pp. 392-405. https://doi.org/10.1007/s00344-011-9249-1

74. Wang, Y., Li, L., Ye, T., Zhao, S., Liu, Z., Feng, Y.Q. & Wu, Y. (2011). Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J., 68 (2), pp. 249-261. https://doi.org/10.1111/j.1365-313X.2011.04683.x

75. Guan, C., Wang, X., Feng, J., Hong, S., Liang, Y., Ren, B. & Zuo, J. (2014). Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of abscisic acid insensitive 5 protein in Arabidopsis. Plant Physiol., 164, pp. 1515-1526. https://doi.org/10.1104/pp.113.234740

76. Heyl, A., Riefler, M., Romanov, G. & Schmulling, T. (2012). Properties, functions and evolution of cytokinin receptors. Eur. J. Cell Biol., 91, pp. 246-256. https://doi.org/10.1016/j.ejcb.2011.02.009

77. Subbiah, V. & Reddy, K.J. (2010). Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J. Biosci., 35, pp. 451-458. https://doi.org/10.1007/s12038-010-0050-2

78. Liu, Y.Y. & Zang, D.K. (2016). Effects of hormone balance on Korean Hackberry seed germination. Africal Journal of Agricultural Research., 11 (29), pp. 2650-2657. https://doi.org/10.5897/AJAR2016.11170

79. Lopes, P.S., Munne-Bosch, S. & Garcia, Q.S. (2017). Hormonal profile and the role of cell expansion in the germination control of Cerrado biome palm seeds. Plant Physiol. and Biochem., 118, pp. 168-177. https://doi.org/10.1016/j.plaphy.2017.06.015

80. Bicalho, E.M., Pinto-Marijuan, M., Muller, M., Morales, M., Munne-Bosch, S. & Garcia, Q.S. (2015). Control of macaw palm seed germination by gibberellin/abscisic acid balance. Plant Biol., 17, pp. 990-996. https://doi.org/10.1111/plb.12332

81. Goggin, D.E., Emery, R.J., Kurepin, L.V. & Powles, S.B. (2014). A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds. Ann. Bot., 115 (2), pp. 293-301. https://doi.org/10.1093/aob/mcu231

82. Chiwocha, S.D., Cutler, A.J., Abrams, S.R., Ambrose, S.J. & Yang, J. (2005). The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. Plant J., 42 (1), pp. 35-48. https://doi.org/10.1111/j.1365-313X.2005.02359.x

83. Lotfi, N., Soleimani, A., Vahdati, K. & Cakmakci, R. (2019). Comprehensive biochemical insights into the seed germination of walnut under drought stress. Scientia Horticulturae, 250, pp. 329-343. https://doi.org/10.1016/j.scienta.2019.02.060

84. Arteca, R. & Arteca, J. (2008). Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants. J. Exp. Bot., 59 (11), pp. 3019-3026. https://doi.org/10.1093/jxb/ern159

85. Zapata, P.J., Serrano, M., Pretel, M.T., Amoros, A. & Botella, M.A. (2004). Polyamines and ethylene changes during germination of different plant species under salinity. Plant Sci., 167, pp. 781-788. https://doi.org/10.1016/j.plantsci.2004.05.014

86. Bleecker, A.B. & Kende, H. (2000). Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol., 16 (16), pp. 1-18. https://doi.org/10.1146/annurev.cellbio.16.1.1

87. Kendrick, M.D. & Chang, C. (2008). Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol., 11, pp. 479-485. https://doi.org/10.1016/j.pbi.2008.06.011

88. Cheng, W.H., Chiang, M.H., Hwang, S.G. & Lin, P.C. (2009). Antagonism between abscisic acid and ethylene in Arabidopsis acts in parallel with the reciprocal regulation of their metabolism and signaling pathways. Plant Mol. Biol., 71 (1-2), pp. 61-80. https://doi.org/10.1007/s11103-009-9509-7

89. Linkies, A., Muller, K., Morris, K., Tureckova, V., Wenk, M., Cadman, C.S., Corbineau, F., Strnad, M., Lynn, J.R. & Finch-Savage, W.E. (2009). Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell, 21, pp. 3803-3822. https://doi.org/10.1105/tpc.109.070201

90. Wilson, R.L., Kim, H., Bakshi, A. & Binder, B.M. (2014). The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiol., 165, pp. 1353-1366. https://doi.org/10.1104/pp.114.241695

91. Arc, E., Sechet, J., Corbineau, F., Rajjou, L. & Marion-Poll, A. (2013). ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci., 4, pp. 1-19. https://doi.org/10.3389/fpls.2013.00063

92. Corbineau, F., Xia, Q., Bailly, C. & El-Maarouf-Bouteau, H. (2014). Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci., 5, pp. 539. https://doi.org/10.3389/fpls.2014.00539

93. Kepczynski, J. & Kepczynska, E. (1997). Ethylene in seed dormancy and germination. Physiol. plant., 101, pp. 720-726. https://doi.org/10.1034/j.1399-3054.1997.1010407.x

94. Arora, N., Bhardwaj, R., Sharma, P. & Arora, H. (2008). Effects of 28-homobrassinolide on growth, lipid peroxidation and antioxidative enzyme activities in seedlings of Zea mays L. under salinity stress. Acta Physiol Plant., 30, pp. 833-839. https://doi.org/10.1007/s11738-008-0188-9

95. Khripach, V., Zhabinskii, V. & Groot, A.D. (2000). Twenty years of brassinosteroids: steroidal plant hormones warrant better crops for XXI century. Ann Bot., 86, pp. 441-447. https://doi.org/10.1006/anbo.2000.1227

96. Zhang, S., Cai, Z. & Wang, X. (2009). The primary signaling outputs of brassinosteroids are regulated by abscisic acid signaling. Proc Nat Acad. Sci. USA, 1106, pp. 4543-4548. https://doi.org/10.1073/pnas

97. Hu, Y. & Yu, D. (2014). BRASSINOSTEROID INSENSITIVE2 interacts with ABSCISIC ACID INSENSITIVE5 to mediate the antagonism of brassinosteroids to abscisic acid during seed germination in Arabidopsis. Plant Cell, 26, pp. 4394-4408. https://doi.org/10.1105/tpc.114.130849

98. Steber, C.M. & McCourt, P. (2001). A role for brassinosteroids in germination in Arabidopsis. Plant Physiol., 125, pp. 763-769. https://doi.org/10.1104/pp.125.2.763

99. Finch-Savage, W. & Leubner-Metzger, G. (2006). Seed dormancy and the control of germination. New Phytol., 171, pp. 501-523. https://doi.org/10.1111/j.1469-8137.2006.01787.x

100. Leubner-Metzger, G. (2001). Brassinosteroids and gibberellins promote tobacco seed germination by distinct pathways. Planta, 213, pp. 758-763. https://doi.org/10.1007/s004250100542

101. Leubner-Metzger, G. (203). Brassinosteroids promote seed germination. Brassinosteroids. S.Hayat and A.Ahmad (eds.). Kluwer: Academic Publishers, pp. 119-128. https://doi.org/10.1007/978-94-017-0948-4_5

102. Kunes, I., Balas, M., Linda, R., Gallo, J. & Novbkovb, O. (2016). Effects of brassinosteroid application on seed germination of Norway spruce, Scots pine, Douglas fir and English oak. Forest., 10, pp. 121-127. https://doi.org/10.3832/ifor1578-009

103. Cukor, J., Rapbkov, N.M., Linda, R., Linhart, L., Gutsch, M.R. & Kunep, I. (2018). Effects of Brassinosteroid Application on Seed Germination of Scots Pine under Standard and Heat Stress Conditions. Baltic Forestry, 24 (1), pp. 60-67.

104. Karpets, Yu.V., Kolupaev, Yu.E. & Kosakivska, I.V. (2016). Nitric oxide and hydrogen peroxide as signal mediators at induction of heat resistance of wheat plantlets by exogenous jasmonic and salicylic acids. Fiziol. rast. genet., 48, No. 2, pp. 158-166 [in Ukrainian]. https://doi.org/10.15407/frg2016.02.158

105. Xie, Z., Zhang, Z.L., Hanzlik, S., Cook, E. & Shen, Q.J. (2007). Salicylic acid inhibits gibberellin-induced alpha-amylase expression and seed germination via a pathway involving an abscisic-acid inducible WRKY gene. Plant Mol. Biol., 64 (3), pp. 293-303. https://doi.org/10.1007/s11103-007-9152-0

106. Rajjou, L., Belghazi, M., Huguet, R., Robin, C., Moreau, A., Job, C. & Job, D. (2006). Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol., 141, pp. 910-923. https://doi.org/10.1104/pp.106.082057

107. Guan, L. & Scandalios, J.G. (1995). Developmentally related responses of maize catalase genes to salicylic acid. Proc. Natl. Acad. Sci. USA, 92, pp. 5930-5934. https://doi.org/10.1073/pnas.92.13.5930

108. Lee, S., Kim, S.G. & Park, C.M. (2010). Salicylic acid promotes seed germination under high salinity by modulating antioxidant activity in Arabidopsis. New Phytol., 188, pp. 626-637. https://doi.org/10.1111/j.1469-8137.2010.03378.x

109. Alonso-Ramirez, A., Rodriguez, D., Reyes, D., Jimenez, J.A., Nicolas, G., Lopez-Climent, M., Gomez-Cadenas, A. & Nicolas, C. (2009). Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol., 150, pp. 1335-1344. https://doi.org/10.1104/pp.109.139352

110. Rivas-San Vicente, M. & Plasencia, J. (2011). Salicylic Acid beyond Defence: Its Role in Plant Growth and Development. J. Exp. Bot., 62, pp. 3321-3338. https://doi.org/10.1093/jxb/err031

111. Dempsey, A.D. & Klessig, D.F. (2017). How does the multifaceted plant hormone salicylic acid combat disease in plants and are similar mechanisms utilized in humans? BMC Biology, 15 (23), pp. 1-11. https://doi.org/10.1186/s12915-017-0364-8

112. Babenko, L.M., Kosakivska, I.V. & Skaterna, T.D.(2015). Jasmonic acid: role in biotechnology and the regulation of plants biochemical processes. Biotechnologia Acta, 8 (2), pp. 35-51. https://doi.org/10.15407/ubj89.01.005

113. Babenko, L.M., Shcherbatiuk, M.M., Skaterna, T.D. & Kosakivska, I.V. (2017). Lipoxygenases and their metabolites in formation of plant stress tolerance. Ukr. Biochem. J., 89 (1), pp. 5-21. https://doi.org/10.15407/ubj89.01.005

114. Wasternack, C. (2007). Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot., 100, pp. 681-669. https://doi.org/10.1093/aob/mcm079

115. Chini, A., Gimenez-Ibanez, S., Goossens, A. & Solano, R. (2016). Redundancy and specificity in jasmonate signaling. Curr. Opin. Plant Biol., 33, pp. 147-156. https://doi.org/10.1016/j.pbi.2016.07.005

116. Wasternack, C. & Strnad, M. (2016). Jasmonate signaling in plant stress responses and development - active and inactive compounds. New Biotechnology, 33, pp. 604-613. https://doi.org/10.1016/j.nbt.2015.11.001

117. Nambara, E., Okamoto, M., Tatematsu, K., Yano, R., Seo, M. & Kamiya, Y. (2010). Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res., 20, pp. 55-67. https://doi.org/10.1017/S0960258510000012

118. Jacobsen, J.V., Barrero, J.M., Hughes, T., Julkowska, M., Taylor, J.M., Xu, Q. & Gubler, F. (2013). Roles for blue light, jasmonate and nitric oxide in the regulation of dormancy and germination in wheat grain (Triticum aestivum L.). Planta, 238, pp. 121-138. https://doi.org/10.1007/s00425-013-1878-0

119. Fernandez-Arbaizar, A., Regalado, J.J. & Lorenzo, O. (2012). Isolation and characterization of novel mutant loci suppressing the ABA hypersensitivity of the Arabidopsis coronatine insensitive 1-16 (coi1-16) mutant during germination and seedling growth. Plant Cell Physiol., 53, pp. 53-63. https://doi.org/10.1093/pcp/pcr174

120. Yildiz, K., Muradoglu, F. & Yilmaz, H. (2008). The effect of jasmonic acid on germination of dormant and nondormant pear (Pyrus communis L.) seeds. Seed Sci. Technol., 36, pp. 569-574. https://doi.org/10.15258/sst.2008.36.3.06

121. Norastehnia, A., Sajedi, R.H. & Nojavan-Asghari, M. (2007). Inhibitory effects of methyl jasmonate on seed germination in maize (Zea mays): effect on a-amylase activity and ethylene production. Gen. Appl. Plant. Physiol., 33 (1-2), pp. 13-23.

122. Hassini, I., Baenas, N., Moreno, D.A., Carvajal, M., Boughanmi, N. & Martinez Ballesta, M.D.C. (2017). Effects of seed priming, salinity and methyl jasmonate treatment on bioactive composition of Brassica oleracea var. capitata (white and red varieties) sprouts. J. Sci. Food Agric., 97, pp. 2291-2299. https://doi.org/10.1002/jsfa.8037

123. Mishra, S., Upadhyay, S. & Shukla, R.K. (2017). The Role of Strigolactones and Their Potential Cross-talk under Hostile Ecological Conditions in Plants. Front. Physiol., 7, pp. 691-720. https://doi.org/10.3389/fphys.2016.00691

124. Toh, S., Kamiya, Y., Kawakami, N., Nambara, E., McCourt, P. & Tsuchiya, Y. (2012). Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol., 53, pp. 107-117. https://doi.org/10.1093/pcp/pcr176

125. Stanga, J.P., Smith, S.M., Briggs, W.R. & Nelson, D.C. (2013). SUPPRESSOR OF MORE AXILLARY GROWTH2 1 controls seed germination and seedling development in Arabidopsis. Plant Physiol., 163, pp. 318-330. https://doi.org/10.1104/pp.113.221259

126. Jiang, L., Liu, X., Xiong, G., Liu, H., Chen, F., Wang, L., Meng, X., Liu, G., Yu, H., Yuan, Y., Yi, W., Zhao, L., Ma, H., He, Y., Wu, Z., Melcher, K., Qian, Q., Xu, H., Wang, Y. & Li, J. (2013). DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature, 504, pp. 401-405. https://doi.org/10.1038/nature12870

127. Zhou, F., Lin, Q., Zhu, L., Ren, Y., Zhou, K., Shabek, N., Wu, F., Mao, H., Dong, W., Gan, L., Ma, W., Gao, H., Chen, J., Yang, C., Wang, D., Tan, J., Zhang X., Guo, X., Wang, J., Jiang, L., Liu, X., Chen, W., Chu, J., Yan, C., Ueno, K., Ito, S., Asami, T., Cheng, Z., Wang, J., Lei, C., Zhai, H., Wu, C., Wang, H., Zheng, N. & Wan, J. (2013). D14-SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature, 504, pp. 406-410. https://doi.org/10.1038/nature12878

128. Cho, J.N., Ryu, J.Y., Jeong, Y.M., Park, J., Song, J.J., Amasino, R.M., Noh, B. & Noh, Y.S. (2012). Control of seed germination by light-induced histone arginine demethylation activity. Dev. Cell., 22 (4), pp. 736-748. https://doi.org/10.1016/j.devcel.2012.01.024

129. Barrero, J.M., Downie, A.B., Xu, Q. & Gubler, F. (2014). A role for barley CRYPTOCHROME1 in light regulation of grain dormancy and germination. Plant Cell, 26 (3), pp. 1094-10104. https://doi.org/10.1105/tpc.113.121830

130. Footitt, S., Douterelo-Soler, I., Clay, H. & Finch-Savage, W.E. (2011). Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc. Natl. Acad. Sci. USA. 108, pp. 20236-20241. https://doi.org/10.1073/pnas.1116325108

131. Kendall, S.L., Hellwege, A., Marriot, P., Whalley, C., Graham, I.A. & Penfield, S. (2011). Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell., 23, pp. 2568-2580. https://doi.org/10.1105/tpc.111.087643

132. MacGregor, D.R., Kendall, S.L., Florance, H., Fedi, F., Moore, K., Paszkiewicz, K., Smirnoff, N. & Penfield, S. (2015). Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. New Phytol., 205, pp. 642-652. https://doi.org/10.1111/nph.13090

133. Xi, W., Liu, C., Hou, X. & Yu, H. (2010). Mother of FT and TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell, 22 (6), pp. 1733-1748. https://doi.org/10.1105/tpc.109.073072

134. Nakamura, S., Abe, F., Kawahigashi, H., Nakazono, K., Tagir, A., Matsumoto, T., Utsugi, S., Ogawa, T., Handa, H., Ishida, H., Mori M., Kawaura, K., Ogihara, Y. & Miura, H. (2011). A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell, 23, pp. 3215-3229. https://doi.org/10.1105/tpc.111.088492

135. Muhei, S.H. (2018). Seed Priming with Phytohormones to Improve Germination Under Dormant and Abiotic Stress Conditions. Adv. Crop Sci. Tech., 6 (6), pp. 403-409. https://doi.org/10.4172/2329-8863.1000403

136. Chauhan, J.S., Tomar, Y.K., Singh, I.N., Ali, S. & Debarati, A. (2009). Effect of growth hormones on seed germination and seedling growth of black gram and horse gram. J. Amer. Sci., 5 (5), pp. 79-84.

137. Iqbal, M. & Ashraf, M. (2013). Gibberellic acid mediated induction of salt tolerance in wheat plants: growth, ionic partitioning, photosynthesis, yield and hormonal homeostasis. Environ. Exp. Bot., 86, pp. 76-85. https://doi.org/10.1016/j.envexpbot.2010.06.002

138. Yang, L., Hong, X.U., Xiao-Xia, W.E.N., Yun-Cheng, L. Liu, Y., Wen, X., Xu, H. & Yun-Cheng, L. (2016). Effect of polyamine on seed germination of wheat under drought stress is related to changes in hormones and carbohydrates. J. Integr. Agr., 15 (12), pp. 2759-2774. https://doi.org/10.1016/S2095-3119(16)61366-7

139. Yuan, Z., Wang, C., Li, S., Li, X. & Tai, F. (2014). Effects of different plant hormones or PEG seed soaking on maize resistance to drought stress. Canad. J. Plant Sci., 94, pp. 1491-1499. https://doi.org/10.4141/cjps-2014-110

140. Sneideris, L.C., Gavassi, M.A., Campos, M.L., D'Amico-Damiao, V. & Carvalho, R.F. (2015). Effects of hormonal priming on seed germination of pigeon pea under cadmium stress. Anais da Academia Brasileira de Ciencias, 87 (3), pp. 1847-1852. https://doi.org/10.1590/0001-3765201520140332