The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice

Plant Cell

Volumn 19, Issue 8, 2007, Pages 2484-2499

  Lu, Chung An ^a   Lin, Chih Cheng ^b   Lee, Kuo Wei ^b   Chen, Jyh Long ^b   Huang, Li Fen ^b   Ho, Shin Lon ^c   Liu, Hsin Ju ^b   Hsing, Yue Ie ^d   Yu, Su May ^b  

^a NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c NATIONAL CHIAYI UNIVERSITY   (Taiwan)

^d INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOASSAY; CELL CULTURE; SIGNAL TRANSDUCTION; SUGAR (SUCROSE); TRANSCRIPTION FACTORS; YEAST;

GENE PROMOTERS; GERMINATION; GLUCOSE-REPRESSIBLE GENES; SUGAR RESPONSE COMPLEX (SRC);

ENZYMES;

ORYZA SATIVA;

EID: 35348855772     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.105.037887     Document Type: Article

References (71)

1. Alderson, A., Sabelli, P.A., Dickinson, J.R., Cole, D., Richardson, M., Kreis, M., Shewry, P.R., and Halford, N.G. (1991). Complementation of snf1, a mutation affecting global regulation of carbon metabolism in yeast, by a plant protein kinase cDNA. Proc. Natl. Acad. Sci. USA 88: 8602-8605.
2. Bhalerao, R.P., Salchert, K., Bako, L., Okresz, L., Szabados, L., Muranaka, T., Machida, Y., Schell, J., and Koncz, C. (1999). Regulatory interaction of PRL1 WD protein with Arabidopsis SNF1-like protein kinases. Proc. Natl. Acad. Sci. USA 96: 5322-5327.
3. Boudsocq, M., Barbier-Brygoo, H., and Lauriere, C. (2004). Identification of nine sucrose nonfermenting 1-related protein kinases 2 activated by hyperosmotic and saline stresses in Arabidopsis thaliana. J. Biol. Chem. 279: 41758-41766.
4. Bruce, W.B., Christensen, A.H., Klein, T., Fromm, M., and Quail, P.H. (1989). Photoregulation of a phytochrome gene promoter from oat transferred into rice by particle bombardment. Proc. Natl. Acad. Sci. USA 86: 9692-9696.
5. Carlson, M. (1987). Regulation of sugar utilization in Saccharomyces species. J. Bacteriol. 169: 4873-4877.
6. Celenza, J.L., and Carlson, M. (1984). Structure and expression of the SNF1 gene of Saccharomyces cerevisiae. Mol. Cell. Biol. 4: 54-60.
7. Celenza, J.L., and Carlson, M. (1986). A yeast gene that is essential for release from glucose repression encodes a protein kinase. Science 233: 1175-1180.
8. Celenza, J.L., and Carlson, M. (1989). Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol. Cell. Biol. 9: 5034-5044.
9. Chan, M.T., Chao, Y.C., and Yu, S.M. (1994). Novel gene expression system for plant cells based on induction of alpha-amylase promoter by carbohydrate starvation. J. Biol. Chem. 269: 17635-17641.
10. Chan, M.T., and Yu, S.M. (1998a). The 3′ untranslated region of a rice alpha-amylase gene mediates sugar-dependent abundance of mRNA. Plant J. 15: 685-695.
11. Chan, M.T., and Yu, S.M. (1998b). The 3′ untranslated region of a rice alpha-amylase gene functions as a sugar-dependent mRNA stability determinant. Proc. Natl. Acad. Sci. USA 95: 6543-6547.
12. Chen, M.H., Liu, L.F., Chen, Y.R., Wu, H.K., and Yu, S.M. (1994). Expression of alpha-amylases, carbohydrate metabolism, and autophagy in cultured rice cells are coordinately regulated by sugar nutrient. Plant J. 6: 625-636.
13. Chen, P.W., Chiang, C.M., Tseng, T.H., and Yu, S.M. (2006). Interaction between rice MYBGA and the gibberellin response element controls tissue-specific sugar sensitivity of alpha-amylase genes. Plant Cell 18: 2326-2340.
14. Chen, P.-W., Lu, C.-A., Yu, T.-S., Tseng, T.-H., Wang, C.-S., and Yu, S.-M. (2002). Rice alpha-amylase transcriptional enhancers direct multiple mode regulation of promoters in transgenic rice. J. Biol. Chem. 277: 13641-13649.
15. Coruzzi, G.M., and Zhou, L. (2001). Carbon and nitrogen sensing and signaling in plants: Emerging 'matrix effects.' Curr. Opin. Plant Biol. 4: 247-253.
16. Crute, B.E., Seefeld, K., Gamble, J., Kemp, B.E., and Witters, L.A. (1998). Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. J. Biol. Chem. 273: 35347-35354.
17. Dyck, J.R., Gao, G., Widmer, J., Stapleton, D., Fernandez, C.S., Kemp, B.E., and Witters, L.A. (1996). Regulation of 5′-AMP-activated protein kinase activity by the noncatalytic beta and gamma subunits. J. Biol. Chem. 271: 17798-17803.
18. Estruch, F., Treitel, M.A., Yang, X., and Carlson, M. (1992). N-terminal mutations modulate yeast SNF1 protein kinase function. Genetics 132: 639-650.
19. Fu, S.F., Chou, W.C., Huang, D.D., and Huang, H.J. (2002). Transcriptional regulation of a rice mitogen-activated protein kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol. 43: 958-963.
20. Gancedo, J.M. (1998). Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 62: 334-361.
21. Gazzarrini, S., and McCourt, P. (2001). Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr. Opin. Plant Biol. 4: 387-391.
22. Gibson, S.I. (2000). Plant sugar-response pathways. Part of a complex regulatory web. Plant Physiol. 124: 1532-1539.
23. Graham, I.A. (1996). Carbohydrate control of gene expression in higher plants. Res. Microbiol. 147: 572-580.
24. Halford, N.G., and Hardie, D.G. (1998). SNF1-related protein kinases: Global regulators of carbon metabolism in plants? Plant Mol. Biol. 37: 735-748.
25. Halford, N.G., Hey, S., Jhurreea, D., Laurie, S., McKibbin, R.S., Paul, M., and Zhang, Y. (2003). Metabolic signalling and carbon partitioning: Role of Snf1-related (SnRK1) protein kinase. J. Exp. Bot. 54: 467-475.
26. Halford, N.G., and Paul, M.J. (2003). Carbon metabolite sensing and signalling. Plant Biotechnol. J. 1: 381-398.
27. Hardie, D.G., Carling, D., and Carlson, M. (1998). The AMP-activated/SNF1 protein kinase subfamily: Metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67: 821-855.
28. Hardie, D.G., and Sakamoto, K. (2006). AMPK: A key sensor of fuel and energy status in skeletal muscle. Physiology (Bethesda) 21: 48-60.
29. Hey, S., Mayerhofer, H., Halford, N.G., and Dickinson, J.R. (2007). DNA sequences from Arabidopsis, which encode protein kinases and function as upstream regulators of Snf1 in yeast. J. Biol. Chem. 282: 10472-10479.
30. Ho, S., Chao, Y., Tong, W., and Yu, S. (2001). Sugar coordinately and differentially regulates growth- and stress- related gene expression via a complex signal transduction network and multiple control mechanisms. Plant Physiol. 125: 877-890.
31. Ho, S.L., Tong, W.F., and Yu, S.M. (2000). Multiple mode regulation of a cysteine proteinase gene expression in rice. Plant Physiol. 122: 57-66.
32. Hong, S.P., Leiper, F.C., Woods, A., Carling, D., and Carlson, M. (2003). Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc. Natl. Acad. Sci. USA 100: 8839-8843.
33. 2+/calmodulin-dependent protein kinase kinase alpha as Snf1-activating kinases in yeast. J. Biol. Chem. 280: 21804-21809.
34. Hsing, Y.I., et al. (2007). A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Mol. Biol. 63: 351-364.
35. Hwang, Y.S., Karrer, E.E., Thomas, B.R., Chen, L., and Rodriguez, R.L. (1998). Three cis-elements required for rice alpha-amylase Amy3D expression during sugar starvation. Plant Mol. Biol. 36: 331-341.
36. Jiang, R., and Carlson, M. (1996). Glucose regulates protein interactions within the yeast SNF1 protein kinase complex. Genes Dev. 10: 3105-3115.
37. Jiang, R., and Carlson, M. (1997). The Snf1 protein kinase and its activating subunit, Snf4, interact with distinct domains of the Sip1/Sip2/Gal83 component in the kinase complex. Mol. Cell. Biol. 17: 2099-2106.
38. Kanegae, H., Miyoshi, K., Hirose, T., Tsuchimoto, S., Mori, M., Nagato, Y., and Takano, M. (2005). Expressions of rice sucrose nonfermenting-1 related protein kinase 1 genes are differently regulated during the caryopsis development. Plant Physiol. Biochem. 43: 669-679.
39. 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.
40. Kobayashi, Y., Yamamoto, S., Minami, H., Kagaya, Y., and Hattori, T. (2004). Differential activation of the rice sucrose nonfermenting1- related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16: 1163-1177.
41. Koch, K.E. (1996). Carbohydrate-modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 509-540.
42. Kuchin, S., Treich, I., and Carlson, M. (2000). A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. USA 97: 7916-7920.
43. Lakatos, L., Klein, M., Hofgen, R., and Banfalvi, Z. (1999). Potato StubSNF1 interacts with StubGAL83: A plant protein kinase complex with yeast and mammalian counterparts. Plant J. 17: 569-574.
44. Laurie, S., McKibbin, R.S., and Halford, N.G. (2003). Antisense SNF1-related (SnRK1) protein kinase gene represses transient activity of an alpha-amylase (alpha-Amy2) gene promoter in cultured wheat embryos. J. Exp. Bot. 54: 739-747.
45. Lee, Y.-C., Lu, C.-A., Chen, P.-W., Casaretto, J., and Yu, S.-M. (2003). An ABA-responsive bZIP protein, OsBZ8, mediates sugar repression of alpha-amylase gene expression. Physiol. Plant. 119: 78-86.
46. Lo, W.S., Gamache, E.R., Henry, K.W., Yang, D., Pillus, L., and Berger, S.L. (2005). Histone H3 phosphorylation can promote TBP recruitment through distinct promoter-specific mechanisms. EMBO J. 24: 997-1008.
47. Lovas, A., Sos-Hegedus, A., Bimbo, A., and Banfalvi, Z. (2003). Functional diversity of potato SNF1-related kinases tested in Saccharomyces cerevisiae. Gene 321: 123-129.
48. Lu, C.A., Ho, T.H., Ho, S.L., and Yu, S.M. (2002). Three novel MYB proteins with one DNA binding repeat mediate sugar and hormone regulation of alpha-amylase gene expression. Plant Cell 14: 1963-1980.
49. Lu, C.A., Lim, E.K., and Yu, S.M. (1998). Sugar response sequence in the promoter of a rice alpha-amylase gene serves as a transcriptional enhancer. J. Biol. Chem. 273: 10120-10131.
50. Man, A.L., Purcell, P.C., Hannappel, U., and Halford, N.G. (1997). Potato SNF1-related protein kinase: Molecular cloning, expression analysis and peptide kinase activity measurements. Plant Mol. Biol. 34: 31-43.
51. Muranaka, T., Banno, H., and Machida, Y. (1994). Characterization of tobacco protein kinase NPK5, a homolog of Saccharomyces cerevisiae SNF1 that constitutively activates expression of the glucose-repressible SUC2 gene for a secreted invertase of S. cerevisiae. Mol. Cell. Biol. 14: 2958-2965.
52. Perata, P., Matsukura, C., Vernieri, P., and Yamaguchi, J. (1997). Sugar repression of gibberellin-dependent signalling pathway in barley embryos. Plant Cell 9: 2197-2208.
53. Polge, C., and Thomas, M. (2007). SNF1/AMPK/SnRK1 kinases, global regulators at the heart of energy control? Trends Plant Sci. 12: 20-28.
54. Purcell, P.C., Smith, A.M., and Halford, N.G. (1998). Antisense expression of a sucrose non-fermenting-1-related protein kinase sequence in potato results in decreased expression of sucrose synthase in tubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves. Plant J. 14: 195-202.
55. 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.
56. Rolland, F., Moore, B., and Sheen, J. (2002). Sugar sensing and signaling in plants. Plant Cell 14 (suppl.): S185-S205.
57. Sheen, J., Zhou, L., and Jang, J.C. (1999). Sugars as signaling molecules. Curr. Opin. Plant Biol. 2: 410-418.
58. Shen, W., and Hanley-Bowdoin, L. (2006). Geminivirus infection upregulates the expression of two Arabidopsis protein kinases related to yeast SNF1- and mammalian AMPK-activating kinases. Plant Physiol. 142: 1642-1655.
59. Sheu, J.-J., Jan, S.-P., Lee, H.-T., and Yu, S.-M. (1994). Control of transcription and mRNA turnover as mechanisms of metabolic repression of alpha-amylase gene expression. Plant J. 5: 655-664.
60. Sheu, J.-J., Yu, T.-S., Tong, W.-F., and Yu, S.-M. (1996). Carbohydrate starvation stimulates differential expression of rice alpha-amylase genes that is modulated through complicated transcriptional and posttranscriptional processes. J. Biol. Chem. 271: 26998-27004.
61. Smeekens, S. (2000). Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51: 49-81.
62. 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.
63. Toyofuku, K., Umemura, T., and Yamaguchi, J. (1998). Promoter elements required for sugar-repression of the RAmy3D gene for alpha-amylase in rice. FEBS Lett. 428: 275-280.
64. Umemura, T., Perata, P., Futsuhara, Y., and Yamaguchi, J. (1998). Sugar sensing and alpha-amylase gene repression in rice embryos. Planta 204: 420-428.
65. Wilson, W.A., Hawley, S.A., and Hardie, D.G. (1996). Glucose repression/derepression in budding yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr. Biol. 6: 1426-1434.
66. Woods, A., Munday, M.R., Scott, J., Yang, X., Carlson, M., and Carling, D. (1994). Yeast SNF1 is functionally related to mammalian AMP-activated protein kinase and regulates acetyl-CoA carboxylase in vivo. J. Biol. Chem. 269: 19509-19515.
67. Yu, S.M. (1999). Cellular and genetic responses of plants to sugar starvation. Plant Physiol. 121: 687-693.
68. Yu, S.M., Kuo, Y.H., Sheu, G., Sheu, Y.J., and Liu, L.F. (1991). Metabolic derepression of alpha-amylase gene expression in suspension-cultured cells of rice. J. Biol. Chem. 266: 21131-21137.
69. Yu, S.M., Lee, Y.C., Fang, S.C., Chan, M.T., Hwa, S.F., and Liu, L.F. (1996). Sugars act as signal molecules and osmotica to regulate the expression of alpha-amylase genes and metabolic activities in germinating cereal grains. Plant Mol. Biol. 30: 1277-1289.
70. Yu, S.M., Tzou, W.S., Lo, W.S., Kuo, Y.H., Lee, H.T., and Wu, R. (1992). Regulation of alpha-amylase-encoding gene expression in germinating seeds and cultured cells of rice. Gene 122: 247-253.
71. Zhang, Y., Shewry, P.R., Jones, H., Barcelo, P., Lazzeri, P.A., and Halford, N.G. (2001). Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J. 28: 431-441.