Nitric Oxide Involvement in Regulation of the Growth Activity of Nonmorphogenic Tartary Buckwheat Callus
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Nitric Oxide Involvement in Regulation of the Growth Activity of Nonmorphogenic Tartary Buckwheat Callus

G.V. Sibgatullina*, A.N. Akulov**, O.V. Gorshkov***, N.I. Rumyantseva****

Kazan Institute of Biochemistry and Biophysics, Kazan Scientific Center,

Russian Academy of Sciences, Kazan, 420111 Russia

E-mail: *kam-guz@yandex.ru, **akulov_anton@mail.ru , ***o_gorshkov@mail.ru, ****nat_rumyantseva@mail.ru

Received January 25, 2017

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Abstract

The research presented in this paper is aimed to determine the role of nitric oxide (NO) in the regulation of cyclin D3;1 (CYCD3;1) and cyclin-dependent kinase A1;1 (CDKA1;1) expression. The nonmorphogenic callus of Tartary buckwheat (Fagopyrum tataricum (L.) Gaertn.) with high growth activity has been taken as the object of study. The methods of spectrophotometry and real-time PCR have been used.

In the first stage of the research, the dynamics of intracellular NO content and mitotic activity of callus cells have been compared. It has been noted that the peak of NO content precedes the peak of mitotic activity of the callus. It has been revealed that the maximum level of CYCD3;1 expression observed the day after the callus transfer to a new medium coincides with the peak of NO content and precedes the peak of mitotic activity. The addition of NO donor sodium nitroprusside to the culture medium has caused an increase in the mitotic index and CYCD3;1 expression, while the NO scavenger – 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) – has decreased CYCD3;1 expression and the mitotic index. In both cases, a decrease in CDKA1;1 expression has been found. Both sodium nitroprusside and cPTIO has had no strict specificity and influenced not only NO, but also H2O2 content. The possible mechanisms of interaction between reactive oxygen and nitrogen species signalling pathways have been discussed in this paper.

Based on the results of the study it has been concluded about the possibility of NO involvement in the regulation of not only CYCD3;1 expression, but also CDKA1;1 expression. It has been suggested that the regulatory effect of NO on CDKA1;1 expression may be mediated by cellular redox state changes.

Keywords: nitric oxide, cyclin D3;1, cyclin-dependent kinase А1;1, sodium nitroprusside, NO scavenger (cPTIO), proliferation, callus

Figure Captions

Fig. 1. The dynamics of intracellular NO content (a) and mitotic activity (b) of nonmorphogenic callus cells of Tartary buckwheat during the cultural cycle.

Fig. 2. Changes in the level of CDKA1;1 (a) and CYCD3;1 (b) expression during the cultural cycle of Tartary buckwheat callus.

Fig. 3. The influence of the intracellular NO content modulators (sodium nitroprusside (SNP) and cPTIO) on the intracellular NO content (a), mitotic index (b), level of CYCD3;1 and CDK1;1 expression (c). Cultivation length – one day.

Fig. 4. The effects of endogenous NO content modulators on the content of nonmorphogenic callus of Tartary buckwheat.

References

  1. Neill S.J., Desikan R., Hancock J.T. Nitric oxide signalling in plants. New Phytol., 2003, vol. 159, no. 1, pp. 11–35. doi: 10.1046/j.1469-8137.2003.00804.x.
  2. Molassiotis A., Fotopoulos V. Oxidative and nitrosative signaling in plants: Two branches in the same tree?. Plant Signaling Behav., 2011, vol. 6, no. 2, pp. 210–214. doi: 10.4161/psb.6.2.14878.
  3. Livanos P., Apostolakos P., Galatis B. Plant cell division: ROS homeostasis is required. Plant Signaling Behav., 2012, vol. 7, no. 7, pp. 771–778. doi: 10.4161/psb.20530.
  4. Delledonne M., Xia Y., Dixon R.A., Lamb C. Nitric oxide functions as a signal in plant disease Resistance. Nature, 1998, vol. 394, no. 6693, pp. 585–588.
  5. Durner J., Wendehenne D., Klessig D.F. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, no. 17, pp. 10328–10333.
  6. Tanou G., Molassiotis A., Diamantidis G. Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ. Exp. Bot., 2009, vol. 65, nos. 2–3, pp. 270–281. doi: 10.1016/j.envexpbot.2008.09.005.
  7. Ötvös K., Pasternak T., Miskolczi P., Domoki M., Dorjgotov D., Bottka S., Dudits D., Fehér A. Nitric oxide is required for, and promotes auxin-mediated activation of, cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures: NO in cell division. Plant J., 2005, vol. 43, no. 6, pp. 849–860. doi: 10.1111/j.1365-313X.2005.02494.x.
  8. Correa-Aragunde N., Graziano M., Chevalier C., Lamattina L. Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J. Exp. Bot., 2006, vol. 57, no. 3, pp. 581–588.
  9. Shen Q., Wang Y-T., Tian H., Guo F-Q. Nitric oxide mediates cytokinin functions in cell proliferation and meristem maintenance in Arabidopsis. Mol. Plant, 2013, vol. 6, no. 4, pp. 1214–1225. doi: 10.1093/mp/sss148.
  10. Feher A., Ötvös K., Pasternak T., Pettkó-Szandtner A. The involvement of reactive oxygen species (ROS) in the cell cycle activation (G0-to-G1 transition) of plant cells. Plant Signaling Behav., 2008, vol. 3, no. 10, pp. 823–826. doi: 10.1007/s10725-006-9152-0.
  11. Inzé D., De Veylder L. Cell cycle regulation in plant development. Annu. Rev. Genet., 2006, vol. 40, no. 1, pp. 77–105. doi: 10.1146/annurev.genet.40.110405.090431.
  12. Pasternak T., Potters G., Caubergs R., Jansen M.A. Complementary interactions between oxidative stress and auxins control plant growth responses at plant, organ, and cellular level. J. Exp. Bot., 2005, vol. 56, no. 418, pp. 1991–2001. doi: 10.1093/jxb/eri196.
  13. Pasternak T.P., Ötvös K., Domoki M., Fehér A. Linked activation of cell division and oxidative stress defense in alfalfa leaf protoplast-derived cells is dependent on exogenous auxin. Plant Growth Regul., 2007, vol. 51, no. 2, pp. 109–117. doi: 10.1007/s10725-006-9152-0.
  14. Correa-Aragunde N., Graziano M., Lamattina L. Nitric oxide plays a central role in determining lateral root development in tomato. Planta, 2004, vol. 218, no. 6, pp. 900–905. doi: 10.1007/s00425-003-1172-7.
  15. Pagnussat G.C., Simontacchi M., Puntarulo S., Lamattina L. Nitric oxide is required for root organogenesis. Plant Physiol., 2002, vol. 129, no. 3, pp. 954–956. doi: 10.1104/pp.004036.
  16. Tun N.N., Holk A., Scherer G.F. Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Lett., 2001, vol. 509, no. 2, pp. 174–176. doi: 10.1016/S0014-5793(01)03164-7.
  17. Zhou B., Guo Z., Xing J., Huang B. Nitric oxide is involved in abscisic acid-induced antioxidant activities in Stylosanthes guianensis. J. Exp. Bot., 2005, vol. 56, no. 422, pp. 3223–3228. doi: 10.1093/jxb/eri319.
  18. Pagnussat G.C., Lanteri M.L., Lombardo M.C., Lamattina L. Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol., 2004, vol. 135, no. 1, pp. 279–286. doi: 10.1104/pp.103.038554.
  19. del Rio L.A. ROS and RNS in plant physiology: An overview. J. Exp. Bot., 2015, vol. 66, no. 10, pp. 2827–2837. doi: 10.1093/jxb/erv099.
  20. Sibgatullina G.V., Rumyantseva N.I., Khaertdinova L.R., Akulov A.N., Tarasova N.B., Gumerova E.A. Esteblishment and characterization of the line of Fagopyrum tataricum morphogenic callus tolerant to aminotriazole. Russ. J. Plant Physiol., 2012, vol. 59, no 5, pp. 662–669. doi: 10.1134/S1021443712050172.
  21. Kamalova G.V., Akulov A.N., Rumyantseva N.I. Comparison of redox state of cells of tatar buckwheat morphogenic calluses and non-morphogenic calluses obtained from them. Biochemistry (Moscow), 2009, vol. 74, no. 6, pp. 686–694. doi: 10.1134/S0006297909060145.
  22. Rumyantseva N.I., Valieva A.I., Samokhvalova N.A., Mukhitov A.R., Ageeva M.V., Lozovaya V.V. Peculiarities of lignification of cell walls of buckwheat calli with different morphogenetic ability. Tsitologiya, 1998, vol. 40, no. 10, pp. 835–843. (In Russian)
  23. Gamborg O.L., Miller, R.A., Ojima R. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res., 1968, vol. 50, no. 1, pp. 151–158. doi: 10.1016/0014-4827(68)90403-5.
  24. Pfeiffer S., Leopold E., Hemmens B., Schmidt K., Werner E.R., Mayer B. Interference of carboxy-PTIO with nitric oxide-and peroxynitrite-mediated reactions. Free Radicals Biol. Med., 1997, vol. 22, no. 5, pp. 787–794. doi: 10.1016/S0891-5849(96)00407-8.
  25. Kumari A., Sheokand S., Swaraj K. Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in Chickpea. Braz. J. Plant Physiol., 2010, vol. 22, no. 4, pp. 271–284. doi: 10.1590/S1677-04202010000400007.
  26. Raldugina G.N., Kuznetsov V.V. Molecular Genetic and Biochemical Methods in Modern Plant Biology. Moscow, Izd. Binom Lab. Znanii, 2012. 487 p. (In Russian)
  27. Bellincampi D., Dipierro, N., Salvi, G., Cervone F., De Lorenzo G. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants. Plant Physiol., 2000, vol. 122, no. 4, pp. 1379–1386.
  28. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 2001, vol. 29, no. 9, pp. 2002–2007.
  29. Koroleva O.A., Tomlinson M., Parinyapong P., Sakvarelidze L., Leader D., Shaw P., Doonan J.H. CycD1, a putative g1 cyclin from Antirrhinum majus, accelerates the cell cycle in cultured tobacco BY-2 cells by enhancing both G1/S entry and progression through S and G2 PHASEs. Plant Cell, 2004, vol. 16, no. 9, pp. 2364–2379. doi: 10.1105/tpc.104.023754.
  30. Oakenfull E.A., Riou-Khamlichi C., Murray J.A.H. Plant D–type cyclins and the control of G1 progression. Philos. Trans. R. Soc., B., 2002, vol. 357, no. 1422, pp. 749–760. doi: 10.1098/rstb.2002.1085.
  31. Riou-Khamlichi C., Huntley R., Jacqmard A., Murray J.A.H. Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science, 1999, vol. 283, pp. 1541–1544. doi: 10.1126/science.283.5407.1541.
  32. Dewitte W., Murray J.A.H. The plant cell cycle. Annu. Rev. Plant Biol., 2003, vol. 54, no. 1, pp. 235–264. doi: 10.1146/annurev.arplant.54.031902.134836.
  33. Dewitte W., Scofield S., Alcasabas A.A., Maughan S. C., Menges M., Braun N., Collins C., Nieuwland J., Prinsen E., Sundaresan V., Murray J.A.H. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc. Natl. Acad. Sci. U. S. A., 2007, vol. 104, no. 36, pp. 14537–14542. doi: 10.1073/pnas.0704166104.
  34. Doerner P., Celenza J. Plant Hormone Research. How Are Plant Growth Regulators Involved in Cell Cycle Control?. Palme K., Schell J. (Eds.). Berlin, Springer, 2000, pp. 1–27.
  35. Harashima H., Kato K., Shinmyo A., Sekine M. Auxin is required for the assembly of A-type cyclin-dependent kinase complexes in tobacco cell suspension culture. J. Plant Physiol., 2007, vol. 164, no. 9, pp. 1103–1112. doi: 10.1016/j.jplph.2007.01.005.
  36. Zhang K., Letham D.S., John P.C. Cytokinin controls the cell cycle at mitosis by stimulating the tyrosine dephosphorylation and activation of p34cdc2-like H1 histone kinase. Planta, 1996, vol. 200, no. 1, pp. 2–12.
  37. Erdei L., Kolbert Z. Nitric oxide as a potent signalling molecule in plants. Acta Biol. Szeged., 2008, vol. 52, no. 1, pp. 1–5.
  38. Wang P., Du Y., Li Y., Ren D., Song C-P. Hydrogen peroxide–mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell, 2010, vol. 22, no. 9, pp. 2981–2998. doi: 10.1105/tpc.109.072959.
  39. Lum H.K., Butt Y.K.C., Lo S.C.L. Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide, 2002, vol. 6, no. 2, pp. 205–213. doi: 10.1006/niox.2001.0395.
  40. Navarre D.A., Wendehenne D., Durner J., Noad R., Klessig D.F. Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol., 2000, vol. 122, no. 2, pp. 573–582. doi: 10.1104/pp.122.2.573.

For citation: Sibgatullina G.V., Akulov A.N., Gorshkov O.V., Rumyantseva N.I. Nitric oxide involvement in regulation of the growth activity of nonmorphogenic Tartary buckwheat callus. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2017, vol. 159, no. 2, pp. 306–320. (In Russian)


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