Skip to main content
Log in

The Potential Role of SnRK1 Protein Kinases in the Regulation of Cell Division in Arabidopsis thaliana

  • Published:
Cytology and Genetics Aims and scope Submit manuscript

Abstract

It is known that the sucrose nonfermenting-1 (SNF1)-related protein kinase (SnRK1) subfamily participates in the regulation of carbohydrate metabolism and energy balance. These enzymes are multifunctional and can participate in many other important cellular processes. The role of the SnRK1 protein kinases (KIN10 and KIN11) in the regulation of cell division in Arabidopsis thaliana has been studied in this work. The KIN10 and KIN11 gene knockout lines of A. thaliana were used for this purpose (http://arabidopsis.info/). A low mitotic index was recorded in cells of these mutant lines and a decreased expression level was shown in the cell proliferation markers—the CYCB1;1 gene (B1 type cyclin) and the plant homolog BRCA1 (Breast Cancer Suppressor Protein). The significantly lower mitotic index and expression level of CYCB1;1 and BRCA1 were observed in the mutants grown in the conditions of energy deficiency. The higher expression of CYCB1;1/BRCA1 and KIN10/KIN11 genes was also recorded in the suspension culture of A. thaliana compared with intact sprouts. These data may confirm a possible role of the KIN10/KIN11 protein kinases in the regulation of cell proliferative activity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.

Similar content being viewed by others

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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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.

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

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

Additional information

Translated by N. Tarasyuk

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krasnoperova, O.E., Buy, D.D., Goriunova, I.I. et al. The Potential Role of SnRK1 Protein Kinases in the Regulation of Cell Division in Arabidopsis thaliana. Cytol. Genet. 53, 185–191 (2019). https://doi.org/10.3103/S0095452719030022

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.3103/S0095452719030022

Keywords:

Navigation