TSitologiya i Genetika 2019, vol. 53, no. 3, 3-11
Cytology and Genetics 2019, vol. 53, no. 3, 185–191, doi: https://www.doi.org/10.3103/S0095452719030022

Potential role of protein kinases SnRK1 in regulation of cell division of Arabidopsis thaliana

Krasnoperova E.E., Buy D.D., Goriunova I.I., Isayenkov S.V., Karpov P.A., Blume Ya.B., Yemets A.I.

SUMMARY. It is well known that the SNF1-related protein kinase-1 (SnRK1) subfamily is involved in the regulation of carbohydrate metabolism and energy balance. These enzymes are multifunctional and can participate in many other important cellular processes. In this work, the role of protein kinases SnRK1 (KIN10 and KIN11) in the regulation of the cell division of Arabidopsis tha-liana was studied. For this purpose, A. thaliana kin10 and kin11 knockout lines (http://arabidopsis.info/) were used. The cells of these mutant lines exhibited the low mitotic index. The expression level of the cell pro-liferation markers – CYCB1, 1 (cyclin B) and plant BRCA1 homolog (Breast Cancer Suppressor Protein) was reduced too. A significantly smaller mitotic index and expression level of CYCB1, 1 and BRCA1 genes were found in the mutants that were grown under energy starvation conditions. High level of expression of CYCB1, 1/BRCA1 and KIN10/KIN11 genes in A. thaliana cell suspension culture was also revealed in comparison to Arabidopsis seedlings. Obtained data may indicate the possible role of protein kinases KIN10/KIN11 in regulation of cell proliferative activity.

Keywords: protein kinases, Arabidopsis thaliana, SnRK1, KIN10, KIN11, gene expression, mitotic markers, cell division

TSitologiya i Genetika
2019, vol. 53, no. 3, 3-11

Current Issue
Cytology and Genetics
2019, vol. 53, no. 3, 185–191,
doi: 10.3103/S0095452719030022

Full text and supplemented materials

Free full text: PDF  

References

1. Wang, L., Hu, W., Sun, J., Liang, X., Yang, X., We, S., Wang, X., Zhou, Y., Xiao, Q., Yang, G., and He, G., Genome-wide analysis of SnRK gene family in Brachypodium distachyon and functional characterization of BdSnRK2.9, Plant Sci., 2015, vol. 237, pp. 35–45. https://doi.org/10.1016/j.plantsci.2015.05.008

2. Wang, Y., Berkowitz, O., Selinski, J., Xu, Y., Hartmann, A., and Whelan, J., Stress responsive mitochondrial proteins in Arabidopsis thaliana, Free Radic. Biol. Med., 2018, vol. 122, pp. 28–39. https://doi.org/10.1016/j.freeradbiomed.2018.03.031

3. Wang, X., Wang, L., Wang, Y., Liu, H., Hu, D., Zhang, N., Zhang, S., Cao, H., Cao, Q., Zhang, Z., Tang, S., Song, D., and Wang, C., Arabidopsis PCaP2 plays an important role in chilling tolerance and ABA response by activating CBF- and SnRK2-mediated transcriptional regulatory network, Front. Plant Sci., 2018, vol. 9, no. 215. https://doi.org/10.3389/fpls.2018.00215

4. Halford, N.G. and Hey, S.J., Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants, Biochem. J., 2009, vol. 419, no. 2, pp. 247–259. https://doi.org/10.1042/BJ20082408

5. Polge, C. and Thomas, M., SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control?, Trends Plant Sci., 2007, vol. 21, no. 1, pp. 20–28. https://doi.org/10.1016/j.tplants.2006.11.005

6. Lumbreras, V., Alba, M.M., Kleinow, T., Koncz, C., and Pages, M., Domain fusion between SNF1-related kinase subunits during plant evolution, EMBO Rep., 2001, vol. 2, no. 1, pp. 55–60. https://doi.org/10.1093/emboreports/kve001

7. Karpov, P.A., Rayevsky, A.V., Krasnoperova, E.E., Isayenkov, S.V., Yemets, A.I., and Blume, Ya.B., Protein kinase KIN10 from Arabidopsis thaliana as a potential regulator of primary microtubule nucleation centers in plants, Cytol. Genet., 2017, vol. 51, no. 6, pp. 415–421. https://doi.org/10.3103/S0095452717060056

8. Tsai, A.Y.L. and Gazzarrini, S., Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture, Front. Plant Sci., 2014. https://doi.org/10.3389/fpls.2014.00119

9. Zhai, Z., Liu, H., and Shanklin, J., Phosphorylation of WRINKLED1 by KIN10 results in its proteasomal degradation, providing a link between energy homeostasis and lipid biosynthesis, Plant Cell, 2017, vol. 29, no. 4, pp. 871–889. https://doi.org/10.1105/tpc.17.00019

10. Shen, W., Reyes, M.I., and Hanley-Bowdoin, L., Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop, Plant Physiol., 2009, vol. 150, no. 2, pp. 996–1005. https://doi.org/10.1104/pp.108.132787

11. Mohannath, G., Jackel, J.N., Lee, Y.H., Buchmann, R.C., Wang, H., Patil, V., Adams, A.K., and Bisaro, D.M., A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis, PLoS One, 2014, vol. 149, no. 4, e87592. https://doi.org/10.1371/journal.pone.0087592

12. Wang, F., Ye, Y., Chen, X., Wang, J., Chen, Z., and Zhou, Q., A sucrose non-fermenting-1-related protein kinase 1 gene from potato, StSnRK1, regulates carbohydrate metabolism in transgenic tobacco, Physiol. Mol. Biol. Plants, 2017, vol. 23, no. 4, pp. 933–943. https://doi.org/10.1007/s12298-017-0473-4

13. Simon, N.M., Kusakina, J., Fernández-López, A., Chembath, A., Belbin, F.E., and Dodd, A.N., The energy-signalling hub SnRK1 is important for sucrose-induced hypocotyl elongation, Plant Physiol., 2018, vol. 176, pp. 1299–1310. https://doi.org/10.1104/pp.17.01395

14. Mair, A., Pedrotti, L., Wurzinger, B., Anrather, D., Simeunovic, A., Weiste, C., Valerio, C., Dietrich, K., Kirchler, T., Nagele, T., Carbajosa, J.V., Hanson, J., Baena-González, E., Chaban, C., Weckwerth, W., Dröge-Laser, W., and Teige, M., SnRK1-triggered switch of bZIP63 dimerization mediates the low energy response in plants, Elife, 2015. https://doi.org/10.7554/eLife.05828

15. Chen, L., Su, Z., Huang, L., Xia, F., Qi, H., Xie, L., Xiao, S., and Chen, Q.-F., The AMP-activated protein kinase KIN10 is involved in the regulation of autophagy in Arabidopsis, Front. Plant Sci., 2017, vol. 8. https://doi.org/10.3389/fpls.2017.01201

16. Nunes, C., O’Hara, L.E., Primavesi, L.F., Delatte, T.L., Schluepmann, H., Somsen, G.W., Silva, A.B., Fevereiro, P.S., Wingler, A., and Paul, M.J., The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation, Plant Physiol., 2013, vol. 162, no. 3, pp. 1720–1732. https://doi.org/10.1104/pp.113.220657

17. Martínez-Barajas, E., Delatte, T., Schluepmann, H., de Jong, G.J., Somsen, G.W., Nunes, C., Primavesi, L.F., Coello, P., Mitchell, R.A.C., and Paul, M.J., Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity, Plant Physiol., 2011, vol. 156, no. 1, pp. 373–381. https://doi.org/10.1104/pp.111.174524

18. Jeong, E.-Y., Seo, P.J., Woo, J.C., and Park, C.-M., AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis, BMC Plant Biol., 2015, vol. 15, no. 110. https://doi.org/10.1186/s12870-015-0503-8

19. Im, J.H., Cho, Y.H., Kim, G.D., Kang, G.H., Hong, J.W., and Yoo, S.D., Inverse modulation of the energy sensor Snf1-related protein kinase 1 on hypoxia adaptation and salt stress tolerance in Arabidopsis thaliana, Plant Cell Environ., 2014, vol. 10, pp. 2303–2312. https://doi.org/10.1111/pce.12375

20. Krasnoperova, E.E., Isayenkov, S.V., Karpov, P.A., and Yemets, A.I., The cladistic analysis and characteristic of an expression of serine/threonine protein kinase KIN10 in different organs of Arabidopsis thaliana, Rep. Natl. Acad. Sci. Ukraine, 2016, no. 1, pp. 81–91. . https://doi.org/10.15407/dopovidi2016.01.081

21. Yemets, A.I., Lloyd, C., and Blume, Ya.B., Plant tubulin phosphorylation and its role in cell cycle progression, in The Plant Cytoskeleton: A Key Tool for Agro-Biotechnology, Netherlands: Springer, 2008, pp. 145–159. https://doi.org/10.1007/978-1-4020-8843-8

22. Crisanto, G., The Arabidopsis cell division cycle, Arabidopsis Book, 2009. no. 7, e0120. https://doi.org/10.1199/tab.0120

23. Trapp, O., Seeliger, K., and Puchta, H., Homologs of breast cancer genes in plants, Front Plant Sci., 2011, vol. 2, no. 19. https://doi.org/10.3389/fpls.2011.00019

24. Menges, M. and Murray, J.A., Murray synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity, Plant J., 2002, vol. 30, no. 2, pp. 203–212. https://doi.org/10.1046/j.1365-313X.2002.01274.x

25. Guzzo, F., Portaluppi, P., Grisi, R., Barone, S., Zampieri, S., Franssen, H., and Levi, M., Reduction of cell size induced by enod40 in Arabidopsis thaliana, J. Exp Bot., 2005, vol. 56, no. 412, pp. 507–513. https://doi.org/10.1093/jxb/eri028

26. Gamborg, O.L. and Eveleigh, D.E., Culture methods and detection of glucanases in cultures of wheat and barley, Can. J. Biochem., 1968, vol. 46, no. 5, pp. 417–421.

27. Livak, K.J. and Schmittgen, T.D., Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔC T method, Methods, 2001, vol. 25, no. 4, pp. 402–408. https://doi.org/10.1006/meth.2001.1262

28. Shevchenko, G.V., Talaliev, A.S., and Doonan, J., Arabidopsis thaliana seedlings from the Chernobyl NPP zone are tolerant to DNA-damaging agents, Rep. Natl. Acad. Sci. Ukraine, 2012, no. 12, pp. 157–162. https://doi.org/10.15407/dopovidi2017.04.084

29. Starita, L.M., Machida, Y., Sankaran, S., Elias, J.E., Griffin, K., Schlegel, B.P., Gygi, S.P., and Parvin, J.D., BRCA1-dependent ubiquitination of gamma-tubulin regulates centrosome number, Mol. Cell. Biol., 2004, vol. 24, no. 19, pp. 8457–8466. https://doi.org/10.1128/MCB.24.19.8457-8466.2004

30. Baena-González, E. and Sheen, J., Convergent energy and stress signaling, Trends Plant Sci., 2008, vol. 13, no. 9, pp. 474–482. https://doi.org/10.1016/j.tplants.2008.06.006

31. Sample, V., Ramamurthy, S., Gorshkov, K., Ronnett, G.V., and Zhang, J., Polarized activities of AMPK and BRSK in primary hippocampal neurons, Mol. Biol. Cell, 2015, vol. 26, no. 10, pp. 1935–1946. https://doi.org/10.1091/mbc.E14-02-0764

32. Alvarado-Kristensson, M., Rodríguez, M.J., Silio, V., Valpuesta, J.M., and Carrera, A.C., SADB phosphorylation of γ-tubulin regulates centrosome duplication, Nat. Cell Biol., 2009, vol. 11, no. 9, pp. 1081–1092. https://doi.org/10.1038/ncb1921

33. Dhumale, P., Menon, S., Chiang, J., and Püschel, A.W., The loss of the kinases SadA and SadB results in early neuronal apoptosis and a reduced number of progenitors, PLoS One, 2018, vol. 13, no. 4, e0196698. https://doi.org/10.1371/journal.pone.0196698

34. Eklund, G., Lang, S., Glindre, J., Ehlén, E., and Alvarado-Kristensson, M., The nuclear localization of γ‑tubulin is regulated by SadB-mediated phosphorylation, J. Biol. Chem., 2014, vol. 289, no. 31, pp. 21360–21373. https://doi.org/10.1074/jbc.M114.562389