Regulation of Sucrose non-Fermenting Related Kinase 1 genes in Arabidopsis thaliana

Frontiers in Plant Science

Volumn 5, Issue JUL, 2014, Pages

  Williams, Sarah P ^a   Rangarajan, Padma ^a   Donahue, Janet L ^a   Hess, Jenna E ^b   Gillaspy, Glenda E ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b Alliance Biosciences   (United States)

Author keywords

Energy; Gene expression; SnRK1; Sugar sensing; Trehalose

Indexed keywords

EID: 84979768746     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00324     Document Type: Article

References (58)

1. Aghdasi, M., Schluepmann, H., and Smeekens, S. (2010). Characterization of Arabidopsis seedlings growth and development under trehalose feeding. J. Cell Mol. Res. 1, 1-9.
2. Alderson, A., Sabelli, P. A., Dickinson, J. R., Cole, D., Richardson, M., Kreis, M., et al. (1991). Complementation of snf1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc. Natl. Acad. Sci. U.S.A. 88, 8602-8605. doi: 10.1073/pnas.88.19.8602
3. Ananieva, E. A., Gillaspy, G. E., Ely, A., Burnette, R. N., and Erickson, F. L. (2008). Interaction of the WD40 domain of a myoinositol polyphosphate 5-phosphatase with SnRK1 links inositol, sugar, and stress signaling. Plant Physiol. 148, 1868-1882. doi: 10.1104/pp.108.130575
4. Baena-Gonzalez, 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
5. Barker, L., Kuhn, C., Weise, A., Schulz, A., Gebhardt, C., Hirner, B., et al. (2000). SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12, 1153-1164. doi: 10.1105/tpc.12.7.1153
6. Bechtold, N., Ellis, J., and Pelletier, G. (1993). In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C. R. Acad. Sci. Ser. III Sci. Vie 316, 1194-1199.
7. Bitrian, M., Roodbarkelari, F., Horvath, M., and Koncz, C. (2011). BAC-recombineering for studying plant gene regulation: developmental control and cellular localization of SnRK1 kinase subunits. Plant J. 65, 829-842. doi: 10.1111/j.1365-313X.2010.04462.x
8. Bradford, K. J., Downie, A. B., Gee, O. H., Alvarado, V., Yang, H., and Dahal, P. (2003). Abscisic acid and gibberellin differentially regulate expression of genes of the SNF1-related kinase complex in tomato seeds. Plant Physiol. 132, 1560-1576. doi: 10.1104/pp.102.019141
9. Burnette, R. N., Gunesekera, B. M., and Gillaspy, G. E. (2003). An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling. Plant Physiol. 132, 1011-1019. doi: 10.1104/pp.019000
10. 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
11. Chock, P. B., Rhee, S. G., and Stadtman, E. R. (1980). Interconvertible enzyme cascades in cellular regulation. Ann. Rev. Biochem. 49, 813-843. doi: 10.1146/annurev.bi.49.070180.004121
12. 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
13. Confraria, A., Martinho, C., Elias, A., Rubio-Somoza, I., and Baena-Gonzalez, E. (2014). miRNAs mediate SnRK1-dependent energy signaling in Arabidopsis. Front. Plant Sci. 4:197. doi: 10.3389/fpls.2013.00197
14. Delatte, T. L., Sedijani, P., Kondou, Y., Matsui, M., De Jong, G. J., Somsen, G. W., et al. (2011). Growth arrest by trehalose-6-phosphate: an astonishing case of primary metabolite control over growth by way of the SnRK1 signaling pathway. Plant Physiol. 157, 160-174. doi: 10.1104/pp.111.180422
15. Donahue, J. L., Alford, S. R., Torabinejad, J., Kerwin, R. E., Nourbakhsh, A., Ray, W. K., et al. (2010). The Arabidopsis thaliana Myo-inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22, 888-903. doi: 10.1105/tpc.109.071779
16. Ercetin, M. E., Ananieva, E. A., Safaee, N. M., Torabinejad, J., Robinson, J. Y., and Gillaspy, G. E. (2008). A phosphatidylinositol phosphate-specific myo-inositol polyphosphate 5-phosphatase required for seedling growth. Plant Mol. Biol. 67, 375-388. doi: 10.1007/s11103-008-9327-3
17. Fragoso, S., Espindola, L., Paez-Valencia, J., Gamboa, A., Camacho, Y., Martinez-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
18. Gazzarrini, S., Tsuchiya, Y., Lumba, S., Okamoto, M., and McCourt, P. (2004). The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev. Cell 7, 373-385. doi: 10.1016/j.devcel.2004.06.017
19. 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. FEBS J. 278, 3978-3990. doi: 10.1111/j.1742-4658.2011.08315.x
20. Gissot, L., Polge, C., Jossier, M., Girin, T., Bouly, J. P., Kreis, M., et al. (2006). AKINbetagamma 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
21. Halford, N. G., Hey, S., Jhurreea, D., Laurie, S., McKibbin, R. S., Paul, M., et al. (2003). Metabolic signalling and carbon partitioning: role of Snf1-related (SnRK1) protein kinase. J. Exp. Bot. 54, 467-475. doi: 10.1093/jxb/erg038
22. Halford, N. G., and Hey, S. J. (2009). Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochem. J. 419, 247-259. doi: 10.1042/BJ20082408
23. Halford, N. G., and Paul, M. J. (2003). Carbon metabolite sensing and signalling. Plant Biotechnol. J. 1, 381-398. doi: 10.1046/j.1467-7652.2003.00046.x
24. Harlow, E., and Lane, D. (1988). Antibodies a Laboratory Manual. New York, NY: Cold Spring Harbor Laboratory.
25. Hey, S. J., Byrne, E., and Halford, N. G. (2010). The interface between metabolic and stress signalling. Ann. Bot. 105, 197-203. doi: 10.1093/aob/mcp285
26. Higo, K., Ugawa, Y., Iwamoto, M., and Korenaga, T. (1999). Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27, 297-300. doi: 10.1093/nar/27.1.297
27. Jossier, M., Bouly, J. P., Meimoun, P., Arjmand, A., Lessard, P., Hawley, S., et al. (2009). SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J. 59, 316-328. doi: 10.1111/j.1365-313X.2009.03871.x
28. Kapila, J., Derycke, R., Van Montagu, M., and Angenon, G. (1997). An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci. 122, 101-108. doi: 10.1016/S0168-9452(96)04541-4
29. Karimi, M., Inze, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195. doi: 10.1016/S1360-1385(02)02251-3
30. Kleinow, T., Bhalerao, R., Breuer, F., Umeda, M., Salchert, K., and Koncz, C. (2000). Functional identification of an Arabidopsis snf4 ortholog by screening for heterologous multicopy suppressors of snf4 deficiency in yeast. Plant J. 23, 115-122. doi: 10.1046/j.1365-313x.2000.00809.x
31. Lastdrager, J., Hanson, J., and Smeekens, S. (2014). Sugar signals and the control of plant growth and development. J. Exp. Bot. 65, 799-807. doi: 10.1093/jxb/ert474
32. Lin, C. R., Lee, K. W., Chen, C. Y., Hong, Y. F., Chen, J. L., Lu, C. A., et al. (2014). SnRK1A-interacting negative regulators modulate the nutrient starvation signaling sensor SnRK1 in source-sink communication in cereal seedlings under abiotic stress. Plant Cell 26, 808-827. doi: 10.1105/tpc.113.121939
33. Lopez-Paz, C., Vilela, B., Riera, M., Pages, M., and Lumbreras, V. (2009). Maize AKINbetagamma dimerizes through the KIS/CBM domain and assembles into SnRK1 complexes. FEBS Lett. 583, 1887-1894. doi: 10.1016/j.febslet.2009.05.022
34. Lumbreras, V., Alba, M. M., Kleinow, T., Koncz, C., and Pages, M. (2001). Domain fusion between SNF1-related kinase subunits during plant evolution. EMBO Rep. 2, 55-60. doi: 10.1093/embo-reports/kve001
35. Matsoukas, I. G., Massiah, A. J., and Thomas, B. (2013). Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. Plant Cell Environ. 36, 1802-1811. doi: 10.1111/pce.12088
36. 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. J. 4, 409-418. doi: 10.1111/j.1467-7652.2006.00190.x
37. Mohannath, G., Jackel, J. N., Lee, Y. H., Buchmann, R. C., Wang, H., Patil, V., et al. (2014). A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis. PLoS ONE 9:e87592. doi: 10.1371/journal.pone.0087592
38. Nelson, B. K., Cai, X., and Nebenfuhr, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126-1136. doi: 10.1111/j.1365-313X.2007.03212.x
39. Ng, S., Giraud, E., Duncan, O., Law, S. R., Wang, Y., Xu, L., et al. (2013). Cyclin-dependent kinase E1 (CDKE1) provides a cellular switch in plants between growth and stress responses. J. Biol. Chem. 288, 3449-3459. doi: 10.1074/jbc.M112.416727
40. O'Hara, L. E., Paul, M. J., and Wingler, A. (2013). How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol. Plant 6, 261-274. doi: 10.1093/mp/sss120
41. Pien, S., Wyrzykowska, J., and Fleming, A. J. (2001). Novel marker genes for early leaf development indicate spatial regulation of carbohydrate metabolism within the apical meristem. Plant J. 25, 663-674. doi: 10.1046/j.1365-313x.2001.01002.x
42. Pilot, G., Stransky, H., Bushey, D. F., Pratelli, R., Ludewig, U., Wingate, V. P., et al. (2004). Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from Hydathodes of Arabidopsis leaves. Plant Cell 16, 1827-1840. doi: 10.1105/tpc.021642
43. Polge, C., Jossier, M., Crozet, P., Gissot, L., and Thomas, M. (2008). Beta-subunits of the SnRK1 complexes share a common ancestral function together with expression and function specificities; physical interaction with nitrate reductase specifically occurs via AKINbeta1-subunit. Plant Physiol. 148, 1570-1582. doi: 10.1104/pp.108.123026
44. Ramon, M., Ruelens, P., Li, Y., Sheen, J., Geuten, K., and Rolland, F. (2013). The hybrid four-CBS-domain KINbetagamma subunit functions as the canonical gamma subunit of the plant energy sensor SnRK1. Plant J. Cell Mol. Biol. 75, 11-25. doi: 10.1111/tpj.12192
45. Rodrigues, A., Adamo, M., Crozet, P., Margalha, L., Confraria, A., Martinho, C., et al. (2013). ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signaling in Arabidopsis. Plant Cell 25, 3871-3884. doi: 10.1105/tpc.113.114066
46. Rolland, F., Baena-Gonzalez, E., and Sheen, J. (2006). Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675-709. doi: 10.1146/annurev.arplant.57.032905.105441
47. Schluepmann, H., Pellny, T., Van Dijken, A., Smeekens, S., and Paul, M. (2003). Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 100, 6849-6854. doi: 10.1073/pnas.1132018100
48. Schluepmann, H., Van Dijken, A., Aghdasi, M., Wobbes, B., Paul, M., and Smeekens, S. (2004). Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. Plant Physiol. 135, 879-890. doi: 10.1104/pp.104.039503
49. Singh, B., Cheek, H. D., and Haigler, C. H. (2009). A synthetic auxin (NAA) suppresses secondary wall cellulose synthesis and enhances elongation in cultured cotton fiber. Plant Cell Rep. 28, 1023-1032. doi: 10.1007/s00299-009-0714-2
50. Styer, J. C., Keddie, J., Spence, J., and Gillaspy, G. E. (2004). Genomic organization and regulation of the LeIMP-1 and LeIMP-2 genes encoding myo-inositol monophosphatase in tomato. Gene 326, 35-41. doi: 10.1016/j.gene.2003.09.048
51. Szklarczyk, D., Franceschini, A., Kuhn, M., Simonovic, M., Roth, A., Minguez, P., et al. (2011). The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39, D561-D568. doi: 10.1093/nar/gkq973
52. Takano, M., Kajiya-Kanegae, H., Funatsuki, H., and Kikuchi, S. (1998). Rice has two distinct classes of protein kinase genes related to SNF1 of Saccharomyces cerevisiae, which are differently regulated in early seed development. Mol. Gen. Genet. 260, 388-394. doi: 10.1007/s004380050908
53. Thelander, M., Olsson, T., and Ronne, H. (2004). Snf1-related protein kinase 1 is needed for growth in a normal day-night light cycle. EMBO J. 23, 1900-1910. doi: 10.1038/sj.emboj.7600182
54. Tsai, A. Y., and Gazzarrini, S. (2012a). AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. Plant J. 69, 809-821. doi: 10.1111/j.1365-313X.2011.04832.x
55. Tsai, A. Y., and Gazzarrini, S. (2012b). Overlapping and distinct roles of AKIN10 and FUSCA3 in ABA and sugar signaling during seed germination. Plant Signal. Behav. 7, 1238-1242. doi: 10.4161/psb.21549
56. Tsai, A. Y., and Gazzarrini, S. (2014). Trehalose-6-phosphate and SnRK1 kinases in plant development and signaling: the emerging picture. Front. Plant Sci. 5:119. doi: 10.3389/fpls.2014.00119
57. Wahl, V., Ponnu, J., Schlereth, A., Arrivault, S., Langenecker, T., Franke, A., et al. (2013). Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339, 704-707. doi: 10.1126/science.1230406
58. Zhang, Y., Primavesi, L. F., Jhurreea, D., Andralojc, P. J., Mitchell, R. A., Powers, S. J., et al. (2009). Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 149, 1860-1871. doi: 10.1104/pp.108.133934