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Potential Involvement of KIN10 and KIN11 Catalytic Subunits of the SnRK1 Protein Kinase Complexes in the Regulation of Arabidopsis γ-Tubulin

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Abstract

SnRK1 protein kinases are integral components of cell signaling involved in stress response, regulation of energy metabolism, seed germination and maturation, autophagy, and other processes. Nevertheless, many functions of these protein kinases remain unknown. In order to study the intracellular localization of KIN10 (catalytic subunit of the SnRK1 protein kinase complexes), protoplasts of the wild A. thaliana ecotype (Col-0) were transformed with a construct that included the KIN10-RFP fusion gene. It was established that the chimeric KIN10-RFP protein was diffusely distributed in the cytoplasm; however, it was mainly localized on the cell periphery, in the region adjacent to the plasma membrane. The diffuse distribution of KIN10 and γ-tubulin in the cytoplasm of A. thaliana root cells was demonstrated by immunofluorescence microscopy. The patterns of γ-tubulin intracellular localization in the root cells of the kin10 and kin11 knockout mutants and wild type A. thaliana were shown to be different. The intensity of γ-tubulin fluorescence in both mutants was lower than in the wild type-plants: this may be indicative of certain impairments in the formation of γ-tubulin complexes in the mutants. A lower intensity of γ-tubulin fluorescence was also recorded in cells of all lines cultivated under the conditions of energy shortage. In particular, the lowest level of fluorescence was recorded in the kin10 and kin11 mutants exposed to this type of stress, and this may be indicative of the synergistic influence of simultaneous dysfunction of one of these genes and energy deficiency on the formation of γ-tubulin complexes (γTuSC and γTuRC). The results obtained demonstrate the possible involvement of SnRK1 (KIN10 and KIN11) in the physiological response of plants to energy stress. With the data on the possible phosphorylation of the Ser131 residue in plant γ-tubulin by KIN10 taken into account, it can be assumed that SnRK1 protein kinases are involved in the regulation of microtubule polymerization in plants.

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REFERENCES

  1. 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 

  2. 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 

  3. Cho, H.Y., Wen, T.N., Wang, Y.T., and Shih, M.C., Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence, J. Exp. Bot., 2016, vol. 67, no. 9, pp. 2745–2760. https://doi.org/10.1093/jxb/erw107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Crozet, P., Margalha, L., Confraria, A., Rodrigues, A., Martinho, C., Adamo, M., Elias, C.A., and Baena-González, E., Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases, Front. Plant Sci., 2014, no. 5. https://doi.org/10.3389/fpls.2014.00190

  5. Hardie, D.G., AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy, Nat. Rev. Mol. Cell Biol., 2007, vol. 8, no. 10, pp. 774–785. https://doi.org/10.1038/nrm2249

    Article  CAS  PubMed  Google Scholar 

  6. Broeckx, T., Hulsmans, S., and Rolland, F., The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure, regulation, and function, J. Exp Bot., 2016, vol. 67, no. 22, pp. 6215–6252. https://doi.org/10.1093/jxb/erw416

    Article  CAS  PubMed  Google Scholar 

  7. Baena-González, E., Rolland, F., Thevelein, J.M., and Sheen, J., A central integrator of transcription networks in plant stress and energy signalling, Nature, 2007, vol. 448, no. 7156, pp. 938–942. https://doi.org/10.1038/nature06069

    Article  CAS  PubMed  Google Scholar 

  8. Zhang, Y., Primavesi, L.F., Jhurreea, D., Andralojc, P.J., Mitchell, R.A., Powers, S.J., Schluepmann, H., Delatte, T., Wingler, A., and Paul, M.J., Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate, Plant Physiol., 2009, vol. 149, no. 4, pp. 1860–1871. https://doi.org/10.1104/pp.108.133934

    Article  PubMed  PubMed Central  Google Scholar 

  9. Nagele, T. and Weckwerth, W., Mathematical modeling reveals that metabolic feedback regulation of SnRK1 and hexokinase is sufficient to control sugar homeostasis from energy depletion to full recovery, Front. Plant Sci., 2014, vol. 5, no. 365, https://doi.org/10.3389/fpls.2014.00365

  10. 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 

  11. Mair, A., Pedrotti, L., Wurzinger, B., Anrather, D., Simeunovic, A., Weiste, C., Valerio, C., Dietrich, K., Kirchler, T., Nägele, 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 lowenergy response in plants, eLife, 2015. https://doi.org/10.7554/eLife.05828

  12. Nukarinen, E., Nägele, T., Pedrotti, L., Wurzinger, B., Mair, A., Landgraf, R., Börnke, F., Hanson, J., Teige, M., Baena-González, E., Dröge-Laser, W., and Weckwerth, W., Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation, Sci. Rep., 2016, vol. 6. https://doi.org/10.1038/13.srep31697

  13. Soto-Burgos, J. and Bassham, D.C., SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana, PLoS One, 2017, vol. 12, no. 8, e0182591. https://doi.org/10.1371/journal.pone.0182591

    Article  PubMed  PubMed Central  Google Scholar 

  14. Krasnoperova, E.E., Buy, D.D., Goriunova, I.I., Isayenkov, S.V., Karpov, P.A., Blume, Ya.B., and Yemets, A.I., Potential role of protein kinases SNRK1 in regulation of cell division of Arabidopsis thaliana, Cytol. Genet., 2019. vol. 53, no. 3 (in press).

    Article  Google Scholar 

  15. 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

  16. 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 

  17. 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 

  18. Jossier, M., Bouly, J.P., Meimoun, P., Arjmand, A., Lessard, P., Hawley, S., Grahame, HardieD., and Thomas, M., SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana, Plant J., 2009, vol. 59, no. 2, pp. 316–328. https://doi.org/10.1111/j.1365-313X.2009.03871.x

    Article  CAS  PubMed  Google Scholar 

  19. Yoo, S.-D., Cho, Y.-H., and Sheen, J., Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis, Nat. Protoc., 2007, vol. 2, no. 7, pp. 1565–1572. https://doi.org/10.1038/nprot.2007.199

    Article  CAS  Google Scholar 

  20. Krasnoperova, E.E., Novozhylov, D.O., Blume, Y.B., and Isayenkov, S.V., Creating of the plasmid construction protein kinase AtKIN10, conjoint with RFP to study the cellular localization of this enzyme, Proc. Uman NUH, 2014, vol. 84, no. 1, pp. 95–100. http://nbuv.gov.ua/UJRN/zhpumus_2014_84_15.

  21. Isayenkov, S.V., Isner, J.C., and Maathuis, F.J., Rice two-pore K+ channels are expressed in different types of vacuoles, Plant Cell, 2011, vol. 23, no. 2, pp. 756–768. https://doi.org/10.1105/tpc.110.081463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Szechyńska-Hebda, M., Wedzony, M., Dubas, E., Kieft, H., and van Lammeren, A., Visualisation of microtubules and actin filaments in fixed BY-2 suspension cells using an optimised whole mount immunolabelling protocol, Plant Cell Rep., 2006, vol. 25, no. 8, pp. 758–766. https://doi.org/10.1007/s00299-005-0089-y

    Article  CAS  PubMed  Google Scholar 

  23. Sheen, J., Master regulators in plant glucose signaling network, J. Plant Biol., 2014, vol. 57, no. 2, pp. 67–79. https://doi.org/10.1007/s12374-014-0902-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Fragoso, S., Espíndola, L., Páez-Valencia, J., Gamboa, A., Camacho, Y., Martínez-Barajas, E., and Coello, P., SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation, Plant Physiol., 2009, vol. 149, no. 4, pp. 1906–1916. https://doi.org/10.1104/pp.108.133298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hulsmans, S., Rodriguez, M., De Coninck, B., and Rolland, F., The SnRK1 energy sensor in plant biotic interactions, Trends Plant Sci., 2016, vol. 21, no. 8, pp. 648–661. https://doi.org/10.1016/j.tplants.2016.04.008

    Article  CAS  PubMed  Google Scholar 

  26. Eklund, G., Lang, S., Glindre, J., Ehlén, A., and Alvarado-Kristensson, M., The nuclear localization of -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 

  27. 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 

  28. 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, pp. 1081–1092. https://doi.org/10.1038/ncb1921

    Article  CAS  PubMed  Google Scholar 

  29. Dhumale, P., Menon, S., Chiang, J., and Puschel, 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 

  30. Eklund, G., Lang, S., Glindre, J., Ehlen, A., 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 

  31. Kollman, J.M., Merdes, A., Mourey, L., and Agard, D.A., Microtubule nucleation by γ-tubulin complexes, Nat. Rev. Mol. Cell Biol., 2011, vol. 12, pp. 709–721. https://doi.org/10.1038/nrm3209

    Article  CAS  PubMed  Google Scholar 

  32. Yemets, A., Stelmakh, O., and Blume, Y.B., Effects of the herbicide isopropyl-N-phenyl carbamate on microtubules and MTOCs in lines of Nicotiana sylvestris resistant and sensitive to its action, Cell Biol Int., 2008, vol. 32, no. 6, pp. 623–629. https://doi.org/10.1016/j.cellbi.2008.01.012

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, 04123, Kyiv, Ukraine

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

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  1. E. E. Krasnoperova
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  2. I. I. Goriunova
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  3. S. V. Isayenkov
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Correspondence to E. E. Krasnoperova, I. I. Goriunova, S. V. Isayenkov, P. A. Karpov, Ya. B. Blume or A. I. Yemets.

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Translated by S. Semenova

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Krasnoperova, E.E., Goriunova, I.I., Isayenkov, S.V. et al. Potential Involvement of KIN10 and KIN11 Catalytic Subunits of the SnRK1 Protein Kinase Complexes in the Regulation of Arabidopsis γ-Tubulin. Cytol. Genet. 53, 349–356 (2019). https://doi.org/10.3103/S0095452719050104

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