The enzyme-like domain of Arabidopsis nuclear β-amylases is critical for DNA sequence recognition and transcriptional activation

Plant Cell

Volumn 26, Issue 4, 2014, Pages 1746-1763

  Soyk, Sebastian ^a   Simková, Klára ^a,d   Zürcher, Evelyne ^a,e   Luginbühl, Leonie ^a,f   Brand, Luise H ^b   Vaughan, Cara K ^c   Wanke, Dierk ^b   Zeeman, Samuel C ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d PSI (Photon Systems Instruments)   (Czech Republic)

^e UNIVERSITY OF ZURICH   (Switzerland)

^f NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84901428040     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.123703     Document Type: Article

References (49)

1. Atanassov, I.I., Atanassov, I.I., Etchells, J.P., and Turner, S.R. (2009). A simple, flexible and efficient PCR-fusion/Gateway cloning procedure for gene fusion, site-directed mutagenesis, short sequence insertion and domain deletions and swaps. Plant Methods 5: 14.
2. Barth, C., and Conklin, P.L. (2003). The lower cell density of leaf parenchyma in the Arabidopsis thaliana mutant lcd1-1 is associated with increased sensitivity to ozone and virulent Pseudomonas syringae. Plant J. 35: 206-218.
3. Berendzen, K.W., Stüber, K., Harter, K., and Wanke, D. (2006). Cis-motifs upstream of the transcription and translation initiation sites are effectively revealed by their positional disequilibrium in eukaryote genomes using frequency distribution curves. BMC Bioinformatics 7: 522.
4. Biggin, M.D. (2011). Animal transcription networks as highly connected, quantitative continua. Dev. Cell 21: 611-626.
5. Brand, L.H., Fischer, N.M., Harter, K., Kohlbacher, O., and Wanke, D. (2013). Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res. 41: 9764-9778.
6. Brand, L.H., Kirchler, T., Hummel, S., Chaban, C., and Wanke, D. (2010). DPI-ELISA: a fast and versatile method to specify the binding of plant transcription factors to DNA in vitro. Plant Methods 6: 25.
7. Casal, J.J. (2013). Photoreceptor signaling networks in plant responses to shade. Annu. Rev. Plant Biol. 64: 403-427.
8. Chanvivattana, Y., Bishopp, A., Schubert, D., Stock, C., Moon, Y.-H., Sung, Z.R., and Goodrich, J. (2004). Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263-5276.
9. Cho, Y.H., and Yoo, S.D. (2011). Signaling role of fructose mediated by FINS1/FBP in Arabidopsis thaliana. PLoS Genet. 7: e1001263.
10. Christianson, J.A., Wilson, I.W., Llewellyn, D.J., and Dennis, E.S. (2009). The low-oxygen-induced NAC domain transcription factor ANAC102 affects viability of Arabidopsis seeds following low-oxygen treatment. Plant Physiol. 149: 1724-1738.
11. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
12. DeLano, W. (2002). The PyMOL Molecular Graphics System. (San Carlos, CA: DeLano Scientific).
13. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K., and Pikaard, C.S. (2006). Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45: 616-629.
14. Eswar, N., Webb, B., Marti-Renom, M.A., Madhusudhan, M.S., Eramian, D., Shen, M.-Y., Pieper, U., and Sali, A. (2007). Comparative protein structure modeling using MODELLER. Curr. Protoc. Protein Sci. 2: 9.
15. Fisher, F., and Goding, C.R. (1992). Single amino acid substitutions alter helix-loop-helix protein specificity for bases flanking the core CANNTG motif. EMBO J. 11: 4103-4109.
16. Fulton, D.C., et al. (2008). Beta-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active beta-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058.
17. González-Bayón, R., Kinsman, E.A., Quesada, V., Vera, A., Robles, P., Ponce, M.R., Pyke, K.A., and Micol, J.L. (2006). Mutations in the RETICULATA gene dramatically alter internal architecture but have little effect on overall organ shape in Arabidopsis leaves. J. Exp. Bot. 57: 3019-3031.
18. Hanson, J., and Smeekens, S. (2009). Sugar perception and signaling-an update. Curr. Opin. Plant Biol. 12: 562-567.
19. Hornitschek, P., Lorrain, S., Zoete, V., Michielin, O., and Fankhauser, C. (2009). Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J. 28: 3893-3902.
20. Kang, Y.-N., Adachi, M., Utsumi, S., and Mikami, B. (2004). The roles of Glu186 and Glu380 in the catalytic reaction of soybean beta-amylase. J. Mol. Biol. 339: 1129-1140.
21. Kang, Y.-N., Tanabe, A., Adachi, M., Utsumi, S., and Mikami, B. (2005). Structural analysis of threonine 342 mutants of soybean beta-amylase: role of a conformational change of the inner loop in the catalytic mechanism. Biochemistry 44: 5106-5116.
22. Karimi, M., Inzé, D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7: 193-195.
23. Kim, T.-W., and Wang, Z.-Y. (2010). Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu. Rev. Plant Biol. 61: 681-704.
24. Lafos, M., Kroll, P., Hohenstatt, M.L., Thorpe, F.L., Clarenz, O., and Schubert, D. (2011). Dynamic regulation of H3K27 trimethylation during Arabidopsis differentiation. PLoS Genet. 7: e1002040.
25. Leivar, P., and Quail, P.H. (2011). PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16: 19-28.
26. Mikami, B., Degano, M., Hehre, E.J., and Sacchettini, J.C. (1994). Crystal structures of soybean b-amylase reacted with b-maltose and maltal: active site components and their apparent roles in catalysis. Biochemistry 33: 7779-7787.
27. Mikami, B., Hehre, E.J., Sato, M., Katsube, Y., Hirose, M., Morita, Y., and Sacchettini, J.C. (1993). The 2.0-A resolution structure of soybean beta-amylase complexed with alpha-cyclodextrin. Biochemistry 32: 6836-6845.
28. Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.-H., Liu, Y.-X., Hwang, I., Jones, T., and Sheen, J. (2003). Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300: 332-336.
29. Oh, E., Zhu, J.-Y., and Wang, Z.-Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14: 802-809.
30. Reinhold, H., Soyk, S., Simková, K., Hostettler, C., Marafino, J., Mainiero, S., Vaughan, C.K., Monroe, J.D., and Zeeman, S.C. (2011). β-Amylase-like proteins function as transcription factors in Arabidopsis, controlling shoot growth and development. Plant Cell 23: 1391-1403.
31. 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.
32. Sambrook, J., and Russel, D.W. (2001). Molecular Cloning: A Laboratory Manual. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
33. Schluepmann, H., Berke, L., and Sanchez-Perez, G.F. (2012). Metabolism control over growth: a case for trehalose-6-phosphate in plants. J. Exp. Bot. 63: 3379-3390.
34. Schütze, K., Harter, K., and Chaban, C. (2009). Bimolecular Fluorescence Complementation (BiFC) to study protein-protein interactions in living plant cells. In Plant Signal Transduction, T. Pfannschmidt, ed (Totowa, NJ: Humana Press), pp. 189-202.
35. Smeekens, S., Ma, J., Hanson, J., and Rolland, F. (2010). Sugar signals and molecular networks controlling plant growth. Curr. Opin. Plant Biol. 13: 274-279.
36. Spillane, C., Schmid, K.J., Laoueillé-Duprat, S., Pien, S., Escobar-Restrepo, J.-M., Baroux, C., Gagliardini, V., Page, D.R., Wolfe, K.H., and Grossniklaus, U. (2007). Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448: 349-352.
37. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
38. Thomas-Chollier, M., Defrance, M., Medina-Rivera, A., Sand, O., Herrmann, C., Thieffry, D., and van Helden, J. (2011). RSAT 2011: regulatory sequence analysis tools. Nucleic Acids Res. 39: W86-W91.
39. Toledo-Ortiz, G., Huq, E., and Quail, P.H. (2003). The Arabidopsis basic/ helix-loop-helix transcription factor family. Plant Cell 15: 1749-1770.
40. Torres Acosta, J.A., de Almeida Engler, J., Raes, J., Magyar, Z., De Groodt, R., Inzé, D., and De Veylder, L. (2004). Molecular characterization of Arabidopsis PHO80-like proteins, a novel class of CDKA;1-interacting cyclins. Cell. Mol. Life Sci. 61: 1485-1497.
41. Voinnet, O., Rivas, S., Mestre, P., and Baulcombe, D. (2003). An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J. 33: 949-956.
42. Wahl, V., Ponnu, J., Schlereth, A., Arrivault, S., Langenecker, T., Franke, A., Feil, R., Lunn, J.E., Stitt, M., and Schmid, M. (2013). Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339: 704-707.
43. Wang, Z.Y., Nakano, T., Gendron, J., He, J., Chen, M., Vafeados, D., Yang, Y., Fujioka, S., Yoshida, S., Asami, T., and Chory, J. (2002). Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev. Cell 2: 505-513.
44. Wenke, K., Wanke, D., Kilian, J., Berendzen, K., Harter, K., and Piechulla, B. (2012). Volatiles of two growth-inhibiting rhizobacteria commonly engage AtWRKY18 function. Plant J. 70: 445-459.
45. Yin, Y., Vafeados, D., Tao, Y., Yoshida, S., Asami, T., and Chory, J. (2005). A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120: 249-259.
46. Yin, Y., Wang, Z.Y., Mora-Garcia, S., Li, J., Yoshida, S., Asami, T., and Chory, J. (2002). BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109: 181-191.
47. Yoo, S.-D., Cho, Y.-H., and Sheen, J. (2007). Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.
48. Zeeman, S.C., Kossmann, J., and Smith, A.M. (2010). Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61: 209-234.
49. Zhang, L.-Y., et al. (2009). Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell 21: 3767-3780.