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Вестник Томского государственного университета. Биология. 2017; : 144-160

Роль мелатонина в регуляции ИУК-зависимых реакций растений в разных условиях освещения

Головацкая И. Ф., Бойко Е. В., Карначук Р. А.

https://doi.org/10.17223/19988591/37/8

Аннотация

Показаны способность мелатонина (Мел) регулировать ИУК-зависимые ростовые реакции 7-дневных проростков Arabidopsis thaliana (L.) Heynh. экотипа Columbia дикого типа Col и его мутантной линии axr1-3 с нарушенной трансдукцией сигнала ауксина, а также возможность совместного действия Мел и ИУК на растяжение сегментов колеоптилей пшеницы Triticum aestivum L. сорта Иргина. Направление и величина действия Мел зависели от условий освещения (темнота, свет разного спектрального состава: синий, красный и белый свет), уровня ИУК и трансдукции ее сигнала. Поскольку Мел только частично компенсировал нарушения трансдукции сигнала ИУК и усиливал эффективность регуляции ростовых процессов только в присутствии ИУК, то нами высказано предположение, что действие Мел не связано с активацией им Н+-АТФазы плазмалеммы, но изменяет эффективность действия ИУК.
Список литературы

1. Hattori A., Migitaka H., Iigo M., Itoh M., Yamamoto K., Ohtani-Kaneko R., Hara M., Suzuki T., Reiter R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates // Biochem. Mol. Biol. 1995. Vol. 35. PP. 627-634.

2. Chen G., Huo Y., Tan D.X., Liang Z., Zhang W., Zhang Y. Melatonin in Chinese medicinal herbs // Life Sci. 2003. Vol. 73. PP. 19-26.

3. Kolar J., Machackova I. Melatonin in higher plants : occurrence and possible functions // Pineal Res. 2005. № 39. PR 333-341.

4. Reiter R.J., Tan D.X., Manchester L.C., Simopoulos A.P., Maldonado M.D., Flores L.J., Terron M.P. Melatonin in edible plants (phytomelatonin) : Identification, concentrations, bioavailability and proposed functions // World Rev Nutr Diet. 2007. Vol. 97. PP. 211-230.

5. Caniato R., Filippini R., Piovan A., Puricelli L., Borsarini A., Cappelletti E.M. Melatonin in plants In: Developments in Tryptophan and Serotonin Metabolism 7. Melatonin / cds. Allegri G., Costa C.V.L., Ragazzi E., Steinhart H., Laresio L. // Advances in Experimental Medicine and Biology. 2003. Vol. 527. PP. 593-597. Springer Science+Business Media, LLC.

6. Afreen F., Zobayed S.M.A., Kozai T. Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation // J. Pineal Research. 2006. Vol. 41. PP. 108-115.

7. Hardeland R, Pandi-Perumal S.R., Poeggeler B. Melatonin in plants: focus on a vertebrate night hormone with cytoprotective properties // FPSB. 2007. Vol. 1. PP. 32-45.

8. Kolar J., Johnson C.H., Machackova I. Exogenously applied melatonin (N-acetyl-5-methoxytryptamine) affects flowering of the short-day plant Chenopodium rubrum // Physiol. Plant. 2003. Vol. 118. PP. 605-612.

9. Lei X.Y., Zhu R.Y., Zhang G.Y., Dai Y.R. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: The possible involvement of polyamines // J. Pineal Res. 2004. Vol. 36. PP. 126-131.

10. Tan D.X., Manchester L.C., Mascio P., Martinez G.R., Prado F.M., Reiter R.J. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation // J. FASEB. 2007. Vol. 21. PP. 17241729.

11. Murch S.J., Krishna Raj S., Saxena P.K. Tryptophan is a precursor for melatonin and serotonin biosynthesis in vitro regenerated St John's wort (Hypericum perforatum L. cv. Anthos) plants // Plant Cell Reports. 2000. Vol. 19. PP. 698-704.

12. Arnao M.B., Hernandez-Ruiz J. The physiological function of melatonin in plants // Plant Signal. Behav. 2006. Vol. 1. PP. 89-95.

13. Manchester L.C., Tan D.X., Reiter R.J., Park W., Monis K., Qi W. High levels of melatonin in the seeds of edible plants: possible function in germ tissue protection // Life Sci. 2000. Vol. 67. PP. 3023-3029.

14. Hernandez-Ruiz J., Cano A., Arnao M.B. Melatonin: a growth-stimulating compound present in lupin tissues // Planta. 2004. Vol. 220. PP. 140-144.

15. Hernandez-Ruiz J., Cano A., Arnao M.B. Melatonin acts as a growth-stimulating compound in some monocot species // J. Pineal Research. 2005. Vol. 39. PP. 137-142.

16. Li C., Tan D.X., Liang D., Chang C., Jia D., Ma F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress // J. Exp Bot. 2015. Vol. 66. PP. 669-680.

17. Weeda S., Zhang N., Zhao X. Ndip G., Guo Y., Buck G.A., Fu C., Ren S. Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems // PLоS ONE. 2014. Vol. 9 : e93462.

18. Murch S.J., Campbell S.S.B., Saxena P.K. The role of serotonin and melatonin in plant morphogenesis: regulation of auxin-induced root organogenesis in vitro cultured explants of St. John's wort (Hypericum perforatum L.) // In Vitro Cell. Dev. Biol. Plant. 2001. Vol. 37. PP. 786-793.

19. Lichtenthaler H.K. Chlorophylls and carotenoides: pigments of photosynthetic biomembranes // Methods Enzymol. 1987. Vol. 148. PP. 350-382.

20. Lincoln C., Britton J.H., Estelle M. Growth and development of the axrl mutants of Arabidopsis // Plant Cell. 1990. Vol. 2. PP. 1071-1080.

21. Estelle M.A., Sommerville C. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology // Mol. Gen. Genet. 1987. Vol. 206. PP. 200-206.

22. Song Y.J., Joo J.H., Ryu H.Y., Lee J.S., Bae Y.S., Nam K.H. Reactive oxygen species mediate IAA-induced ethylene production in mungbean (Vigna radiata L.) hypocotyls // J. Plant Biol. 2007. Vol. 50. PP. 18-23.

23. Новикова Г.В., Носов А.В., Степанченко Н.С., Фоменков А.А., Мамаева А.С., Мошков И.Е. Пролиферация клеток растений и ее регуляторы // Физиология растений. 2013. Т. 60, № 4. С. 529-537.

24. Schwechheimer C., Serino G., Deng X.-W. Multiple ubiquitin ligase-mediated processes require COP9 signalosome and AXR1 function // Plant Cell. 2002. Vol. 14. PP. 2553-2563.

25. Карначук Р.А., Большакова М.А., Ефимова М.В., Головацкая И.Ф. Интеграция сигналов синего света и жасмоновой кислоты в морфогенезе Arabidopsis thaliana (L.) Heynh // Физиология растений. 2008. Т. 55, № 5. С. 534-538.

26. Головацкая И.Ф., Дорофеев В.Ю., Медведева Ю.В., Никифоров П.Е., Карначук Р.А. Оптимизация условий освещения при культивировании микроклонов Solanum tuberosum L. сорта Луговской in vitro // Вестник Томского государственного университета. Биология. 2013. № 4 (24). С. 133-144.

27. Hughes R.M., Vrana J.D., Song J., Tucker C.L. Light-dependent, dark-promoted interaction between Arabidopsis cryptochrome 1 and phytochrome B proteins // J. Biol. Chem. 2012. Vol. 287. PP. 22165-22172.

28. Головацкая И.Ф., Карначук Р.А. Роль зеленого света в жизнедеятельности растений // Физиология растений. 2015. Т. 62, № 6. С. 776-791.

29. Dunand C., Crevecoeur M., Penel C. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development : possible interaction with peroxidases // New Phytologist. 2007. Vol. 174. PP. 332-341.

30. Guerrero J.M., Reiter R.J. Melatonin-immune system relationships // Curr. Top. Med. Chem. 2002. Vol. 2. PP. 167-179.

31. Adamczyk-Sowa M., Sowa P., Zwirska-Korczala K., Pierzchala K., Bartosz G., Sadowska-Bartosz I. Role of melatonin receptor MT2 and quinone reductase II in the regulation of the redox status of 3T3-L1 preadipocytes in vitro // Cell Biol. Int. 2013. Vol. 37. PP. 835-842.

Tomsk State University Journal of Biology. 2017; : 144-160

Role of melatonin in the regulation of IAA-dependent plant reaction in different lighting conditions

Golovatskaya I. F., Boyko E. V., Karnachuk R. A.

https://doi.org/10.17223/19988591/37/8

Abstract

Currently, expansion of melatonin (Mel) in the plant kingdom has been established. Mel has an impact on many processes in a plant. The existence of contradictory data about the Mel hormonal function in a plant is the basis for further research. Moreover, in the regulation of plant growth processes an interrelation of Mel and indole-3-acetic acid (plant hormone IAA) (as metabolic products of tryptophan) has not been found. In this regard, the aim of this research was to determine the role of Mel in auxin-dependent growth reactions and possible interaction of Mel and IAA in the regulation of plant processes in the dark and in the light. Our studied objects were 7-day-long seedlings of Arabidopsis thaliana (L.) Heynh. Columbia ecotype Col wild type and its mutant line axr1-3 with impaired transduction of auxin signal. They were grown in hormone-free Murashige and Skoog medium in the dark, under blue, red and white light (control) and with an addition of Mel (an experience) under long-day conditions (16 h light: 8 h dark) at PAR photon flux density about 120 ^mol / (m2 s), at a temperature 22-25oC. The light source was white TL-D 36W / 54-765, blue TL-D 36W / 18 and red TL-D 36W / 15 fluorescent lamps (Fig. 1). Also, we studied wheat coleoptile segments Triticum aestivum L. of Irgina variety. These segments were cultured in the darkness using 2% sucrose (control) with an addition of IAA or Mel, or Mel + IAA (experience). The range of the studied concentrations of Mel and IAA varied from 0.1pM to 1 ^M. In the experiment, we measured growth parameters and determined the content of photosynthetic pigments. The optical density of the extract of pigments in 96%-ethanol was registered using the spectrophotometer at a wavelength of 470, 648 and 664 nm. Our experiments showed that direction and magnitude of 1 ^M Mel influence depended on the lighting conditions and IAA signal transduction (Fig. 4). In the darkness Mel inhibited the elongation of mutant axial organs, whereas it increased the size of the cotyledon wild type under the white light. Mel reduced the size of the root and the cotyledons under the white light in both lines, but increased the size of the root under the red light. Furthermore, the efficiency of Mel during axr1-3 growth regulation was higher than Col. The experience has shown that the exogenous Mel under the white light has a stimulating effect on the growth of seedlings of A. thaliana in lower concentrations (0.1 pM) than IAA (1 nM). Mel was restoring axr1-3 mutant axial organs growth and the content of photosynthetic pigments to the wild-type levels, probably by compensating violations of IAA signal transduction (Fig. 2, 3). In the absence of the IAA Mel did not affect the coleoptile segments of T. aestivum elongation, but during their coeffect Mel intensified its effectiveness in the regulation of the growth processes (Fig. 5). It appears from this that the action of Mel was not associated with the activation of plasma membrane H+-ATPase, but changed the efficiency of IAA action. The article contains 5 Figures, 31 References. Currently, expansion of melatonin (Mel) in the plant kingdom has been established. Mel has an impact on many processes in a plant. The existence of contradictory data about the Mel hormonal function in a plant is the basis for further research. Moreover, in the regulation of plant growth processes an interrelation of Mel and indole-3-acetic acid (plant hormone IAA) (as metabolic products of tryptophan) has not been found. In this regard, the aim of this research was to determine the role of Mel in auxin-dependent growth reactions and possible interaction of Mel and IAA in the regulation of plant processes in the dark and in the light. Our studied objects were 7-day-long seedlings of Arabidopsis thaliana (L.) Heynh. Columbia ecotype Col wild type and its mutant line axr1-3 with impaired transduction of auxin signal. They were grown in hormone-free Murashige and Skoog medium in the dark, under blue, red and white light (control) and with an addition of Mel (an experience) under long-day conditions (16 h light: 8 h dark) at PAR photon flux density about 120 ^mol / (m2 s), at a temperature 22-25oC. The light source was white TL-D 36W / 54-765, blue TL-D 36W / 18 and red TL-D 36W / 15 fluorescent lamps (Fig. 1). Also, we studied wheat coleoptile segments Triticum aestivum L. of Irgina variety. These segments were cultured in the darkness using 2% sucrose (control) with an addition of IAA or Mel, or Mel + IAA (experience). The range of the studied concentrations of Mel and IAA varied from 0.1pM to 1 ^M. In the experiment, we measured growth parameters and determined the content of photosynthetic pigments. The optical density of the extract of pigments in 96%-ethanol was registered using the spectrophotometer at a wavelength of 470, 648 and 664 nm. Our experiments showed that direction and magnitude of 1 ^M Mel influence depended on the lighting conditions and IAA signal transduction (Fig. 4). In the darkness Mel inhibited the elongation of mutant axial organs, whereas it increased the size of the cotyledon wild type under the white light. Mel reduced the size of the root and the cotyledons under the white light in both lines, but increased the size of the root under the red light. Furthermore, the efficiency of Mel during axr1-3 growth regulation was higher than Col. The experience has shown that the exogenous Mel under the white light has a stimulating effect on the growth of seedlings of A. thaliana in lower concentrations (0.1 pM) than IAA (1 nM). Mel was restoring axr1-3 mutant axial organs growth and the content of photosynthetic pigments to the wild-type levels, probably by compensating violations of IAA signal transduction (Fig. 2, 3). In the absence of the IAA Mel did not affect the coleoptile segments of T. aestivum elongation, but during their coeffect Mel intensified its effectiveness in the regulation of the growth processes (Fig. 5). It appears from this that the action of Mel was not associated with the activation of plasma membrane H+-ATPase, but changed the efficiency of IAA action. The article contains 5 Figures, 31 References.
References

1. Hattori A., Migitaka H., Iigo M., Itoh M., Yamamoto K., Ohtani-Kaneko R., Hara M., Suzuki T., Reiter R.J. Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates // Biochem. Mol. Biol. 1995. Vol. 35. PP. 627-634.

2. Chen G., Huo Y., Tan D.X., Liang Z., Zhang W., Zhang Y. Melatonin in Chinese medicinal herbs // Life Sci. 2003. Vol. 73. PP. 19-26.

3. Kolar J., Machackova I. Melatonin in higher plants : occurrence and possible functions // Pineal Res. 2005. № 39. PR 333-341.

4. Reiter R.J., Tan D.X., Manchester L.C., Simopoulos A.P., Maldonado M.D., Flores L.J., Terron M.P. Melatonin in edible plants (phytomelatonin) : Identification, concentrations, bioavailability and proposed functions // World Rev Nutr Diet. 2007. Vol. 97. PP. 211-230.

5. Caniato R., Filippini R., Piovan A., Puricelli L., Borsarini A., Cappelletti E.M. Melatonin in plants In: Developments in Tryptophan and Serotonin Metabolism 7. Melatonin / cds. Allegri G., Costa C.V.L., Ragazzi E., Steinhart H., Laresio L. // Advances in Experimental Medicine and Biology. 2003. Vol. 527. PP. 593-597. Springer Science+Business Media, LLC.

6. Afreen F., Zobayed S.M.A., Kozai T. Melatonin in Glycyrrhiza uralensis: response of plant roots to spectral quality of light and UV-B radiation // J. Pineal Research. 2006. Vol. 41. PP. 108-115.

7. Hardeland R, Pandi-Perumal S.R., Poeggeler B. Melatonin in plants: focus on a vertebrate night hormone with cytoprotective properties // FPSB. 2007. Vol. 1. PP. 32-45.

8. Kolar J., Johnson C.H., Machackova I. Exogenously applied melatonin (N-acetyl-5-methoxytryptamine) affects flowering of the short-day plant Chenopodium rubrum // Physiol. Plant. 2003. Vol. 118. PP. 605-612.

9. Lei X.Y., Zhu R.Y., Zhang G.Y., Dai Y.R. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: The possible involvement of polyamines // J. Pineal Res. 2004. Vol. 36. PP. 126-131.

10. Tan D.X., Manchester L.C., Mascio P., Martinez G.R., Prado F.M., Reiter R.J. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation // J. FASEB. 2007. Vol. 21. PP. 17241729.

11. Murch S.J., Krishna Raj S., Saxena P.K. Tryptophan is a precursor for melatonin and serotonin biosynthesis in vitro regenerated St John's wort (Hypericum perforatum L. cv. Anthos) plants // Plant Cell Reports. 2000. Vol. 19. PP. 698-704.

12. Arnao M.B., Hernandez-Ruiz J. The physiological function of melatonin in plants // Plant Signal. Behav. 2006. Vol. 1. PP. 89-95.

13. Manchester L.C., Tan D.X., Reiter R.J., Park W., Monis K., Qi W. High levels of melatonin in the seeds of edible plants: possible function in germ tissue protection // Life Sci. 2000. Vol. 67. PP. 3023-3029.

14. Hernandez-Ruiz J., Cano A., Arnao M.B. Melatonin: a growth-stimulating compound present in lupin tissues // Planta. 2004. Vol. 220. PP. 140-144.

15. Hernandez-Ruiz J., Cano A., Arnao M.B. Melatonin acts as a growth-stimulating compound in some monocot species // J. Pineal Research. 2005. Vol. 39. PP. 137-142.

16. Li C., Tan D.X., Liang D., Chang C., Jia D., Ma F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress // J. Exp Bot. 2015. Vol. 66. PP. 669-680.

17. Weeda S., Zhang N., Zhao X. Ndip G., Guo Y., Buck G.A., Fu C., Ren S. Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems // PLoS ONE. 2014. Vol. 9 : e93462.

18. Murch S.J., Campbell S.S.B., Saxena P.K. The role of serotonin and melatonin in plant morphogenesis: regulation of auxin-induced root organogenesis in vitro cultured explants of St. John's wort (Hypericum perforatum L.) // In Vitro Cell. Dev. Biol. Plant. 2001. Vol. 37. PP. 786-793.

19. Lichtenthaler H.K. Chlorophylls and carotenoides: pigments of photosynthetic biomembranes // Methods Enzymol. 1987. Vol. 148. PP. 350-382.

20. Lincoln C., Britton J.H., Estelle M. Growth and development of the axrl mutants of Arabidopsis // Plant Cell. 1990. Vol. 2. PP. 1071-1080.

21. Estelle M.A., Sommerville C. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology // Mol. Gen. Genet. 1987. Vol. 206. PP. 200-206.

22. Song Y.J., Joo J.H., Ryu H.Y., Lee J.S., Bae Y.S., Nam K.H. Reactive oxygen species mediate IAA-induced ethylene production in mungbean (Vigna radiata L.) hypocotyls // J. Plant Biol. 2007. Vol. 50. PP. 18-23.

23. Novikova G.V., Nosov A.V., Stepanchenko N.S., Fomenkov A.A., Mamaeva A.S., Moshkov I.E. Proliferatsiya kletok rastenii i ee regulyatory // Fiziologiya rastenii. 2013. T. 60, № 4. S. 529-537.

24. Schwechheimer C., Serino G., Deng X.-W. Multiple ubiquitin ligase-mediated processes require COP9 signalosome and AXR1 function // Plant Cell. 2002. Vol. 14. PP. 2553-2563.

25. Karnachuk R.A., Bol'shakova M.A., Efimova M.V., Golovatskaya I.F. Integratsiya signalov sinego sveta i zhasmonovoi kisloty v morfogeneze Arabidopsis thaliana (L.) Heynh // Fiziologiya rastenii. 2008. T. 55, № 5. S. 534-538.

26. Golovatskaya I.F., Dorofeev V.Yu., Medvedeva Yu.V., Nikiforov P.E., Karnachuk R.A. Optimizatsiya uslovii osveshcheniya pri kul'tivirovanii mikroklonov Solanum tuberosum L. sorta Lugovskoi in vitro // Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya. 2013. № 4 (24). S. 133-144.

27. Hughes R.M., Vrana J.D., Song J., Tucker C.L. Light-dependent, dark-promoted interaction between Arabidopsis cryptochrome 1 and phytochrome B proteins // J. Biol. Chem. 2012. Vol. 287. PP. 22165-22172.

28. Golovatskaya I.F., Karnachuk R.A. Rol' zelenogo sveta v zhiznedeyatel'nosti rastenii // Fiziologiya rastenii. 2015. T. 62, № 6. S. 776-791.

29. Dunand C., Crevecoeur M., Penel C. Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development : possible interaction with peroxidases // New Phytologist. 2007. Vol. 174. PP. 332-341.

30. Guerrero J.M., Reiter R.J. Melatonin-immune system relationships // Curr. Top. Med. Chem. 2002. Vol. 2. PP. 167-179.

31. Adamczyk-Sowa M., Sowa P., Zwirska-Korczala K., Pierzchala K., Bartosz G., Sadowska-Bartosz I. Role of melatonin receptor MT2 and quinone reductase II in the regulation of the redox status of 3T3-L1 preadipocytes in vitro // Cell Biol. Int. 2013. Vol. 37. PP. 835-842.

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