Abstract
Sucrose nonfermenting-related kinase 1 (SnRK1) function as a key regulator in sensing sucrose-Tre6P (trehalose 6-phosphate) signalling and negatively regulating sucrose homeostasis and content in plants. To clarify the potential functions of SnRK1 in sugarcane, we isolated a SnRK1 catalytic α subunit gene ShSnRK1α from sugarcane. The structure conservation, intracellular localisation and gene expression of ShSnRK1α were analysed. Results showed that ShSnRK1α had a 1527 bp open reading frame encoding 509 amino acids. The protein sequence of ShSnRK1α contained three conserved domains, including an N-terminal catalytic protein-kinase domain, a middle-plant-specific ubiquitin associated (UBA) domain and a C-terminal regulatory (αCTD) domain. The N-terminal protein-kinase domain of ShSnRK1α was highly conserved in SnRK1αs from monocot and dicot plant species. The UBA and αCTD domains of ShSnRK1α had sugarcane specificity. ShSnRK1α shared high identity with SnRK1αs from sorghum, maize and rice. Intracellular localisation analysis showed that ShSnRK1α localised in the nucleus and cytoplasm regions of rice mesophyll protoplasts. Expression analysis showed that ShSnRK1α was constitutively expressed in sugarcane leaves and stem internodes. ShSnRK1α was more highly expressed in sucrose rapid-accumulation maturing internodes than in immature and mature internodes. Meanwhile, ShSnRK1α was expressed lower in leaves and sucrose accumulating internodes of high-sugar-content sugarcane plants than that of low-sugar-content sugarcane plants. Thus, ShSnRK1α may play an important role on regulating sucrose homeostasis and accumulation in sugarcane. This study provided a target to clarify the sugar-accumulation regulating mechanism of sugarcane and improve its sugar content.
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Abbreviations
- AMPK:
-
AMP-activated kinase
- CBM:
-
Carbohydrate binding module
- CBS:
-
Cystathione β-synthase
- CTD:
-
C-terminal regulatory domain
- ER:
-
Endoplasmic reticulum
- ORF:
-
Open reading frame
- pI:
-
Isoelectric point
- qPCR:
-
Quantitative real-time PCR
- SNF-1:
-
Sucrose non-fermenting 1
- SnRK1:
-
Sucrose non-fermenting 1-related kinase 1
- Tre6P:
-
Trehalose 6-phosphate
- UBA:
-
Ubiquitin-associated domain
References
Baena-Gonzalez, E., and J. Hanson. 2017. Shaping plant development through the SnRK1-TOR metabolic regulators. Current Opinion in Plant Biology 35: 152–157. https://doi.org/10.1016/j.pbi.2016.12.004.
Baena-Gonzalez, E., and J.E. Lunn. 2020. SnRK1 and trehalose 6-phosphate: Two ancient pathways converge to regulate plant metabolism and growth. Current Opinion in Plant Biology 55: 52–59. https://doi.org/10.1016/j.pbi.2020.01.010.
Baena-González, E., F. Rolland, J.M. Thevelein, and J. Sheen. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature 448 (7156): 938–942. https://doi.org/10.1038/nature06069.
Bitrian, M., F. Roodbarkelari, M. Horvath, and C. Koncz. 2011. BAC-recombineering for studying plant gene regulation: Developmental control and cellular localization of SnRK1 kinase subunits. Plant Journal 65 (5): 829–842. https://doi.org/10.1111/j.1365-313X.2010.04462.x.
Blanco, N.E., D. Liebsch, M.G. Diaz, A. Strand, and J. Whelan. 2019. Dual and dynamic intracellular localization of Arabidopsis thaliana SnRK1.1. Journal of Experimental Botany 70 (8): 2325–2338. https://doi.org/10.1093/jxb/erz023.
Broeckx, T., S. Hulsmans, and F. Rolland. 2016. The plant energy sensor: Evolutionary conservation and divergence of SnRK1 structure, regulation, and function. Journal of Experimental Botany 67 (22): 6215–6252. https://doi.org/10.1093/jxb/erw416.
Cho, H.Y., T.N. Wen, Y.T. Wang, and M.C. Shih. 2016. Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence. Journal of Experimental Botany 67 (9): 2745–2760. https://doi.org/10.1093/jxb/erw107.
Cho, Y.H., J.W. Hong, E.C. Kim, and S.D. Yoo. 2012. Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiology 158 (4): 1955–1964. https://doi.org/10.1104/pp.111.189829.
Crepin, N., and F. Rolland. 2019. SnRK1 activation, signaling, and networking for energy homeostasis. Current Opinion in Plant Biology 51: 29–36. https://doi.org/10.1016/j.pbi.2019.03.006.
Debast, S., A. Nunes-Nesi, M.R. Hajirezaei, J. Hofmann, U. Sonnewald, A.R. Fernie, and F. Bornke. 2011. Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiology 156 (4): 1754–1771. https://doi.org/10.1104/pp.111.179903.
Emanuelle, S., M.S. Doblin, P.R. Gooley, and M.S. Gentry. 2018. The UBA domain of SnRK1 promotes activation and maintains catalytic activity. Biochemical and Biophysical Research Communications 497 (1): 127–132. https://doi.org/10.1016/j.bbrc.2018.02.039.
Emanuelle, S., M.S. Doblin, D.I. Stapleton, A. Bacic, and P.R. Gooley. 2016. Molecular insights into the enigmatic metabolic regulator, SnRK1. Trends in Plant Science 21 (4): 341–353. https://doi.org/10.1016/j.tplants.2015.11.001.
Ghillebert, R., E. Swinnen, J. Wen, L. Vandesteene, M. Ramon, K. Norga, F. Rolland, and J. Winderickx. 2011. The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: Structure, function and regulation. FEBS Journal 278 (21): 3978–3990. https://doi.org/10.1111/j.1742-4658.2011.08315.x.
Griffiths, C.A., R. Sagar, Y. Geng, L.F. Primavesi, M.K. Patel, M.K. Passarelli, I.S. Gilmore, et al. 2016. Chemical intervention in plant sugar signalling increases yield and resilience. Nature 540 (7634): 574. https://doi.org/10.1038/nature20591.
Hartt, Constance E., H.P. Kortschak, Ada J. Forbes, and G.O. Burr. 1963. Translocation of C in sugarcane. Plant Physiology 38 (3): 305.
Hwang, G., S. Kim, J.Y. Cho, I. Paik, J.I. Kim, and E. Oh. 2019. Trehalose-6-phosphate signaling regulates thermoresponsive hypocotyl growth in Arabidopsis thaliana. Embo Reports. https://doi.org/10.15252/embr.201947828.
Iskandar, H.M., R.S. Simpson, R.E. Casu, G.D. Bonnett, D.J. Maclean, and J.M. Manners. 2004. Comparison of reference genes for quantitative real-time polymerase chain reaction analysis of gene expression in sugarcane. Plant Molecular Biology Reporter 22 (4): 325–337. https://doi.org/10.1007/BF02772676.
Kumar, S., G. Stecher, M. Li, C. Knyaz, and K. Tamura. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547–1549. https://doi.org/10.1093/molbev/msy096.
Li, Y., W.Q. Wang, Y.P. Feng, M. Tu, P.E. Wittich, N.J. Bate, and J. Messing. 2019. Transcriptome and metabolome reveal distinct carbon allocation patterns during internode sugar accumulation in different sorghum genotypes. Plant Biotechnology Journal 17 (2): 472–487. https://doi.org/10.1111/pbi.12991.
Li, Z.Y., X.J. Wei, X.H. Tong, J. Zhao, X.X. Liu, H.M. Wang, L.Q. Tang, et al. 2022. The OsNAC23-Tre6P-SnRK1a feed-forward loop regulates sugar homeostasis and grain yield in rice. Molecular Plant 15 (4): 706–722. https://doi.org/10.1016/j.molp.2022.01.016.
Lin, C.R., K.W. Lee, C.Y. Chen, Y.F. Hong, J.L. Chen, C.A. Lu, K.T. Chen, T.H.D. Ho, and S.M. Yu. 2014. SnRK1A-interacting negative regulators modulate the nutrient starvation signaling sensor SnRK1 in source-sink communication in cereal seedlings under abiotic stress. The Plant Cell 26 (2): 808–827. https://doi.org/10.1105/tpc.113.121939.
Livak, K.J., and T.D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 (4): 402–408. https://doi.org/10.1006/meth.2001.1262.
Mair, A., L. Pedrotti, B. Wurzinger, D. Anrather, A. Simeunovic, C. Weiste, C. Valerio, et al. 2015. SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife. https://doi.org/10.7554/eLife.05828.
Nietzsche, M., R. Landgraf, T. Tohge, and F. Brnke. 2015. A protein-protein interaction network linking the energy-sensor kinase SnRK1 to multiple signaling pathways in Arabidopsis thaliana. Current Plant Biology 5 (3): 36–44. https://doi.org/10.1016/j.cpb.2015.10.004.
O’Brien, M., R.N. Kaplan-Levy, T. Quon, P.G. Sappl, and D.R. Smyth. 2015. PETAL LOSS, a trihelix transcription factor that represses growth in Arabidopsis thaliana, binds the energy-sensing SnRK1 kinase AKIN10. Journal of Experimental Botany 66 (9): 2475–2485. https://doi.org/10.1093/jxb/erv032.
Peixoto, B., T.A. Moraes, V. Mengin, L. Margalha, R. Vicente, R. Feil, M. Hohne, et al. 2021. Impact of the SnRK1 protein kinase on sucrose homeostasis and the transcriptome during the diel cycle. Plant Physiology 187 (3): 1357–1373. https://doi.org/10.1093/plphys/kiab350.
Rae, A.L., J.M. Perroux, and C.P. Grof. 2005. Sucrose partitioning between vascular bundles and storage parenchyma in the sugarcane stem: A potential role for the ShSUT1 sucrose transporter. Planta 220 (6): 817–825. https://doi.org/10.1007/s00425-004-1399-y.
Robertlee, J., K. Kobayashi, M. Suzuki, and T. Muranaka. 2017. AKIN10, a representative Arabidopsis SNF1-related protein kinase 1 (SnRK1), phosphorylates and downregulates plant HMG-CoA reductase. FEBS Letters 591 (8): 1159–1166. https://doi.org/10.1002/1873-3468.12618.
Saitou, N., and M. Nei. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4 (4): 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454.
Williams, S.P., P. Rangarajan, J.L. Donahue, J.E. Hess, and G.E. Gillaspy. 2014. Regulation of sucrose non-fermenting related kinase 1 genes in Arabidopsis thaliana. Frontiers in Plant Science. https://doi.org/10.3389/fpls.2014.00324.
Yoo, S.D., Y.H. Cho, and J. Sheen. 2007. Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols 2 (7): 1565–1572. https://doi.org/10.1038/nprot.2007.199.
Acknowledgements
This research was supported by grants from the National Natural Science Foundation of China (31901593), National Key Research and Development Program of China (2018YFD1000503), Sugar Crop Research System (CARS-170301) and Hainan Provincial Natural Science Foundation of China (2019RC301).
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S-ZZ and TZ conceived and designed the experiments. JW and TZ performed the experiments, result analysis and manuscript drafting. WW, CF, XF and LS revised the manuscript. All authors have read and approved the final manuscript.
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Zhao, Tt., Wang, Jg., Wang, Wz. et al. Structure, Intracellular Localisation and Expression Analysis of Sucrose Nonfermenting-Related Kinase ShSnRK1α in Sugarcane. Sugar Tech 25, 69–76 (2023). https://doi.org/10.1007/s12355-022-01203-6
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DOI: https://doi.org/10.1007/s12355-022-01203-6