Structural and functional basis for starch binding in the SnRK1 subunits AKINβ2 and AKINβγ

Frontiers in Plant Science

Volumn 5, Issue MAY, 2014, Pages

  Ávila Castañeda, Alejandra ^a   Gutiérrez Granados, Natalia ^a   Ruiz Gayosso, Ana ^a   Sosa Peinado, Alejandro ^a   Martínez Barajas, Eleazar ^a   Coello, Patricia ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

AKIN 2; AKIN ; Chloroplast proteins; SnRK1; Starch Binding Domain (SBD)

Indexed keywords

EID: 84901029449     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00199     Document Type: Article

References (35)

1. Amodeo, G. A., Rudolph, M. J., and Tong, L. (2007). Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1. Nature 449, 492-495. doi: 10.1038/nature06127
2. Baena-González, E., Rolland, F., Thevelein, J. M., and Sheen, J. (2007). A central integrator of transcription networks in plant stress and energy signalling. Nature 448, 938-942. doi: 10.1038/nature06069
3. Baena-González, E., and Sheen, J. (2008). Convergent energy and stress signaling. Trends Plant Sci. 13, 474-482. doi: 10.1016/j.tplants.2008.06.006
4. Ball, S., and Morell, M. K. (2003). From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Ann. Rev. Plant Biol. 54, 207-233. doi: 10.1146/annurev.arplant.54.031902.134927
5. Cenci, U., Nitschke, F., Steup, M., Minassian, B. A., Colleoni, C., and Ball, S. G. (2014). Transition from glycogen to starch metabolism in Archaeplastida. Trends Plant Sci. 19, 18-28. doi: 10.1016/j.tplants.2013.08.004
6. Chia, T., Thorneycroft, D., Chapple, A., Messerli, G., Chen, J., Zeeman, S. C., et al. (2004). A cytosolic glucosyltransferase is required for conversion of starch to sucrose in Arabidopsis leaves at night. Plant J. 37, 853-863. doi: 10.1111/j.1365-313X.2003.02012.x
7. Cho, Y. H., Hong, J. W., Kim, E. C., and Yoo, S. D. (2012). Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol. 158, 1955-1964. doi: 10.1104/pp.111.189829
8. Coello, P., Hey, S. J., and Halford, N. G. (2011). The sucrose non-fermenting-1-related (SnRK) family of protein kinases: potential for manipulation to improve stress tolerance and increase yield. J. Exp. Bot. 62, 883-893. doi: 10.1093/jxb/erq331
9. Fettke, J., Eckermann, N., Poeste, S., Pauly, M., Tiessen, A., Geigenberger, P., et al. (2005b). Analysis of cytosolic heteroglycans from leaves of transgenic potato (Solanum tuberosum L.) plants that under-or overexpress the Pho 2 phosphorylase isozyme. Plant Cell Physiol. 46, 1987-2004. doi: 10.1093/pcp/pci214
10. Fettke, J., Eckermann, N., Tiessen, A., Geigenberger, P., and Steup, M. (2005a). Identification, subcellular localisation and characterisation of soluble heteroglycans (SHG) in leaves of Arabidopsis thaliana L.: distinct SHG reside in the cytosol and in the apoplast. Plant J. 43, 568-585. doi: 10.1111/j.1365-313X.2005.02475.x
11. Fragoso, S., Espíndola, L., Páez-Valencia, J., Gamboa, A., Camacho, Y., Martínez-Barajas, E., et al. (2009). SnRK1 isoforms AKIN10 and AKIN11 are differentially regulated in Arabidopsis plants under phosphate starvation. Plant Physiol. 149, 1906-1916. doi: 10.1104/pp.108.133298
12. Ghillebert, R., Swinnen, E., Wen, J., Vandesteene, L., Ramon, M., Norga, K., et al. (2011). The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBC J. 278, 3978-3990. doi: 10.1111/j.1742-4658.2011.08315.x
13. Gissot, L., Polge, C., Bouly, J. P., Lemaitre, T., Kreis, M., and Thomas, M. (2004). AKINβ3, a plant specific SnRK1 protein, is lacking domains present in yeast and mammals non-catalytic beta-subunits. Plant Mol. Biol. 56, 747-759. doi: 10.1007/s11103-004-5111-1
14. Gissot, L., Polge, C., Jossier, M., Girin, T., Bouly, J. P., Kreis, M., et al. (2006). AKINβγ contributes to SnRK1 heterotrimeric complexes and interacts with two proteins implicated in plant pathogen resistance through its KIS/GBD sequence. Plant Physiol. 142, 931-944. doi: 10.1104/pp.106.087718
15. Hudson, E. R., Pan, D. A., James, J., Lucocq, J. M., Hawley, S. A., Green, K. A., et al. (2003). A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr. Biol. 13, 861-866. doi: 10.1016/S0960-9822(03)00249-5
16. Janecek, S., Svensson, B., and MacGregor, E. A. (2011). Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzyme Microb. Technol. 49, 429-440. doi: 10.1016/j.enzmictec.2011.07.002
17. Koay, A., Woodcroft, B., Petrie, E. J., Yue, H., Emanuelle, S., Bieri, M., et al. (2010). AMPK β subunits display isoform specific affinities for carbohydrates. FEBS Lett. 584, 3499-3503. doi: 10.1016/j.febslet.2010.07.015
18. López-Paz, C., Vilela, B., Riera, M., Pagès, M., and Lumbreras, V. (2009). Maize AKINβγ dimerizes through the KIS/CBM domain and assembles into SnRK1 complexes. FEBS Lett. 583, 1887-1894. doi: 10.1016/j.febslet.2009.05.022
19. Lumbreras, V., Alba, M. M., Kleinow, T., Koncz, C., and Pagès, M. (2001). Domain fusion between SNF1-related kinase subunits during plant evolution. EMBO Rep. 2, 55-60. doi: 10.1093/embo-reports/kve001
20. Mangat, S., Chandrashekarappa, D., McCartney, R. R., Elbing, K., and Schmidt, M. C. (2010). Differential roles of the glycogen-binding domains of β subunits in regulation of the Snf1 kinase complex. Eukaryot. Cell 9, 173-183. doi: 10.1128/EC.00267-09
21. Martínez-Barajas, E., Delatte, T., Schluepmann, H., de Jong, G. J., Somsen, G. W., Nunes, C., et al. (2011). Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregain filling: tissue distribution and relationship to SNF1-related protein kinase 1 activity. Plant Physiol. 156, 373-381. doi: 10.1104/pp.111.174524
22. McBride, A., Ghilagaber, S., Nikolaev, A., and Hardie, G. D. (2009). The glycogen-binding domain on the AMPK β subunit allows the kinase to act as a glycogen sensor. Cell 9, 23-34. doi: 10.1016/j.cmet.2008.11.008
23. McKibbin, R. S., Muttucumaru, N., Paul, M. J., Powers, S. J., Burrell, M. M., Coates, S., et al. (2006). Production of high-starch, low-glucose potatoes through over-expression of the metabolic regulator SnRK1. Plant Biotechnol. 4, 409-418. doi: 10.1111/j.1467-7652.2006.00190.x
24. Momcilovic, M., Iram, S. H., Liu, Y., and Carlson, M. (2008). Roles of the glycogen-binding domain and Snf4 in glucose inhibition of SNF1 protein kinase. J. Biol. Chem. 283, 19521-19529. doi: 10.1074/jbc.M803624200
25. Nunes, C., O'Hara, L. E., Primavesi, L. F., Delatte, T. L., Schluepmann, H., Somsen, G. W., et al. (2013a). The trehalose 6-phosphate/SnRK1 signaling pathway primes growth recovery following relief of sink limitation. Plant Physiol. 162, 1720-1732. doi: 10.1104/pp.113.220657
26. Nunes, C., Primavesi, L. F., Patel, M. K., Martínez-Barajas, E., Powers, S. J., Sagar, R., et al. (2013b). Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol. Biochem. 63, 89-98. doi: 10.1016/j.plaphy.2012.11.011
27. Polekhina, G., Gupta, A., Michell, B. J., van Denderen, B., Murthy, S., Feil, S. C., et al. (2003). AMPK β subunit targets metabolic stress sensing to glycogen. Curr. Biol. 13, 867-871. doi: 10.1016/S0960-9822(03)00292-6
28. Polekhina, G., Gupta, A., van Denderen, B. J. W., Feil, S. C., Kemp, B. E., Stapleton, D., et al. (2005). Structural basis for glycogen recognition by AMP-activated protein kinase. Structure 13, 1453-1462. doi: 10.1016/j.str.2005.07.008
29. Polge, C., Jossier, M., Crozet, P., Gissot, L., and Thomas, M. (2008). b-Subunits of the SnRK1 complexes share a common ancestral function together with expression and function specificities: physical interaction with nitrate reductase specifically occurs via AKINβ1-subunit. Plant Physiol. 148, 1570-1582. doi: 10.1104/pp.108.123026
30. Polge, C., and Thomas, M. (2007). SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci. 12, 20-28. doi: 10.1016/j.tplants.2006.11.005
31. Radchuk, R., Radchuk, V., Weschke, W., Borisjuk, L., and Weber, H. (2006). Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol. 140, 263-278. doi: 10.1104/pp.105.071167
32. Ramon, M., Ruelens, P., Li, Y., Sheen, J., Geuten, K., and Rolland, F. (2013). The hybrid four-CBS-domain KINβγ subunit functions as the canonical γ subunit of the plant energy sensor SnRK1. Plant J. 75, 11-25. doi: 10.1111/tpj.12192
33. Sanz, P., Rubio, T., and García-Gimeno, M. A. (2013). AMPKβ subunits: more than just a scaffold in the formation of AMPK complex. FEBS J. 280, 3723-3733. doi: 10.1111/febs.12364
34. Streb, S., and Zeeman, S. C. (2012). Starch metabolism in Arabidopsis. Arabidopsis Book 10:e0160. doi: 10.1199/tab.0160
35. Weigel, D., and Glazebrook, J. (2002). Arabidopsis: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.