Structural determinants allowing transferase activity in sensitive to freezing 2, classified as a family i lycosyl hydrolase

Journal of Biological Chemistry

Volumn 289, Issue 38, 2014, Pages 26089-26106

  Roston, Rebecca L ^a   Wang, Kun ^a   Kuhn, Leslie A ^a,b   Benning, Christoph ^a  

^a Michigan State University   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FREEZING; LIPIDS;

CATALYTIC SITES; FREEZE TOLERANCE; GLYCOSYL HYDROLASES; GLYCOSYLTRANSFERASE ACTIVITY; LOOP REGIONS; MEMBRANE LIPIDS; STRUCTURAL DETERMINANTS; STRUCTURE-FUNCTION RELATIONSHIP;

HYDROLASES;

GLYCOSIDASE; SENSITIVE TO FREEZING 2; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; BETA GLUCOSIDASE; INTRINSICALLY DISORDERED PROTEIN; PROTEIN BINDING; SFR2 PROTEIN, ARABIDOPSIS;

ARABIDOPSIS THALIANA; ARTICLE; BIOASSAY; BIOCATALYSIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ENGINEERING; ENZYME MODIFICATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE COMPLEX; FREEZING; HYDROPHOBICITY; LIPID MEMBRANE; MOLECULAR MECHANICS; MOLECULAR MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; MOLECULAR GENETICS; PH; PROTEIN MOTIF; SEQUENCE HOMOLOGY; STRUCTURAL HOMOLOGY;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BETA-GLUCOSIDASE; CATALYTIC DOMAIN; CONSERVED SEQUENCE; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; INTRINSICALLY DISORDERED PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURAL HOMOLOGY, PROTEIN;

EID: 84907190359     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.576694     Document Type: Article

References (99)

1. Warren, G., McKown, R., Marin, A. L., and Teutonico, R. (1996) Isolation of mutations affecting the development of freezing tolerance in Arabidopsis thaliana (L) Heynh. Plant Physiol. 111, 1011-1019
2. Thorlby, G., Fourrier, N., and Warren, G. (2004) The SENSITIVE TO FREEZING2 gene, required for freezing tolerance in Arabidopsis thaliana, encodes a β-glucosidase. Plant Cell 16, 2192-2203
3. Moellering, E. R., Muthan, B., and Benning, C. (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228
4. Moellering, E. R., and Benning, C. (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci. 16, 98-107
5. Xu, Z., Escamilla-Treviño, L., Zeng, L., Lalgondar, M., Bevan, D., Winkel, B., Mohamed, A., Cheng, C. L., Shih, M. C., Poulton, J., and Esen, A. (2004) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 1. Plant Mol. Biol. 55, 343-367
6. Tribolo, S., Berrin, J. G., Kroon, P. A., Czjzek, M., and Juge, N. (2007) The crystal structure of human cytosolic β-glucosidase unravels the substrate aglycone specificity of a family 1 glycoside hydrolase. J. Mol. Biol. 370, 964-975
7. Luang, S., Cho, J. I., Mahong, B., Opassiri, R., Akiyama, T., Phasai, K., Komvongsa, J., Sasaki, N., Hua, Y. L., Matsuba, Y., Ozeki, Y., Jeon, J. S., and Cairns, J. R. (2013) RiceOs9BGlu31 is a transglucosidase with the capacity to equilibrate phenylpropanoid, flavonoid, and phytohormone glycocon-jugates. J. Biol. Chem. 288, 10111-10123
8. Matsuba, Y., Sasaki, N., Tera, M., Okamura, M., Abe, Y., Okamoto, E., Nakamura, H., Funabashi, H., Takatsu, M., Saito, M., Matsuoka, H., Na-gasawa, K., and Ozeki, Y. (2010) A novel glucosylation reaction on antho-cyanins catalyzed by acyl-glucose-dependent glucosyltransferase in the petals of carnation and delphinium. Plant Cell 22, 3374-3389
9. R. Ketudat Cairns, J., Pengthaisong, S., Luang, S., Sansenya, S., Tank-rathok, A., and Svasti, J. (2012) Protein-carbohydrate interactions leading to hydrolysis and transglycosylation in plant glycoside hydrolase family 1 enzymes. J. Appl. Glycosci. 59, 51-62
10. Withers, S. G. (2001) Mechanisms of glycosyl transferases and hydrolases. Carbohydr. Polym. 44, 325-337
11. Snyder, R. L., Melo-Abreu, J. P., and de Melo-Abreu, J. P. (2005) Frost Protection: Fundamentals, Practice and Economics, Vol. 1, Food and Agriculture Organization of the United Nations (FAO), Rome
12. Fourrier, N, Bédard, J., Lopez-Juez, E., Barbrook, A., Bowyer, J., Jarvis, P., Warren, G., and Thorlby, G. (2008) A role for SENSITIVE TO FREEZING2 in protecting chloroplasts against freeze-induced damage in Arabidopsis. Plant J. 55, 734-745
13. Camacho, C, Coulouris, G., Avagyan, V., Ma, N, Papadopoulos, J., Bealer, K., and Madden, T. L. (2009) BLAST plus: architecture and applications. BMC Bioinformatics 10, 421
14. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201
15. Braberg, H., Webb, B. M., Tjioe, E., Pieper, U., Sali, A., and Madhusudhan, M. S. (2012) SALIGN: a web server for alignment of multiple protein sequences and structures. Bioinformatics 28, 2072-2073
16. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N, Weissig, H., Shindyalov, I. N, and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242
17. Gloster, T. M., Roberts, S., Ducros, V. M., Perugino, G., Rossi, M., Hoos, R., Moracci, M., Vasella, A., and Davies, G. J. (2004) Structural studies of the β-glycosidase from Sulfolobus solfataricus in complex with covalently and noncovalently bound inhibitors. Biochemistry 43, 6101-6109
18. Xia, L., Ruppert, M., Wang, M., Panjikar, S., Lin, H., Rajendran, C, Barle-ben, L., and Stöckigt, J. (2012) Structures of alkaloid biosynthetic glucosi-dases decode substrate specificity. ACS Chem. Biol. 7, 226-234
19. Heger, A., Mallick, S., Wilton, C, and Holm, L. (2007) The global trace graph, a novel paradigm for searching protein sequence databases. Bioinformatics 23, 2361-2367
20. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
21. Chi, Y. I., Martinez-Cruz, L. A., Jancarik, J., Swanson, R. V., Robertson, D. E., and Kim, S. H. (1999) Crystal structure of the β-glycosidase from the hyperthermophile Thermosphaera aggregans: insights into its activity and thermostability. FEBS Lett. 445, 375-383
22. Isorna, P., Polaina, J., Latorre-García, L., Cañada, F. J., González, B., and Sanz-Aparicio, J. (2007) Crystal structures of Paenibacillus polymyxa β-glucosidase B complexes reveal the molecular basis of substrate specificity and give new insights into the catalytic machinery of family I glyco-sidases. J. Mol. Biol. 371, 1204-1218
23. Sue, M., Yamazaki, K., Yajima, S., Nomura, T., Matsukawa, T., Iwamura, H, and Miyamoto, T. (2006) Molecular and structural characterization of hexameric β-D-glucosidases in wheat and rye. Plant Physiol. 141, 1237-1247
24. Eswar, N, Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chapter 5, Unit 5.6
25. Eswar, N, Eramian, D., Webb, B., Shen, M. Y., and Sali, A. (2008) Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145-159
26. Kuntal, B. K., Aparoy, P., and Reddanna, P. (2010) EasyModeller: A graphical interface to MODELLER. BMC Res. Notes 3, 226
27. Fiser, A., Do, R. K., and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci. 9, 1753-1773
28. Fiser, A., and Sali, A. (2003) ModLoop: automated modeling of loops in protein structures. Bioinformatics 19, 2500-2501
29. Schrödinger, L. (2010) The PyMOL Molecular Graphics System, Version 1.4, Schrödinger, LLC, New York
30. Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., Tyka, M., Baker, D., and Karplus, K. (2009) Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins 77, 114-122
31. Melo, F., Sánchez, R., and Sali, A. (2002) Statistical potentials for fold assessment. Protein Sci. 11, 430-448
32. Benkert, P., Künzli, M., and Schwede, T. (2009) QMEAN server for protein model quality estimation. Nucleic Acids Res. 37, W510-W514
33. Benkert, P., Tosatto, S. C, and Schomburg, D. (2008) QMEAN: A comprehensive scoring function for model quality assessment. Proteins 71, 261-277
34. Laskowski, R. A., Macarthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck-a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
35. Chen, V. B., Arendall, W. B., 3rd., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
36. Celniker, G., Nimrod, G., Ashkenazy, H., Glaser, F., Martz, E., Mayrose, I., Pupko, T., and Ben-Tal, N. (2013) ConSurf: using evolutionary data to raise testable hypotheses about protein function. Isr. J. Chem. 53, 199-206
37. Ashkenazy, H, Erez, E., Martz, E., Pupko, T., and Ben-Tal, N. (2010) Con-Surf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529-W533
38. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T., and Ben-Tal, N. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302
39. Ferron, F., Longhi, S., Canard, B., and Karlin, D. (2006) A practical overview of protein disorder prediction methods. Proteins 65, 1-14
40. Schlessinger, A., Punta, M., Yachdav, G., Kajan, L., and Rost, B. (2009) Improved disorder prediction by combination of orthogonal approaches. PLOS ONE 4, e4433
41. Schlessinger, A., Liu, J. F., and Rost, B. (2007) Natively unstructured loops differ from other loops. PLoS Comput. Biol. 3, 1335-1346
42. Ward, J. J., Sodhi, J. S., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J. Mol. Biol. 337, 635-645
43. Schlessinger, A., Yachdav, G., and Rost, B. (2006) PROFbval: predict flexible and rigid residues in proteins. Bioinformatics 22, 891-893
44. Schlessinger, A., Punta, M., and Rost, B. (2007) Natively unstructured regions in proteins identified from contact predictions. Bioinformatics 23, 2376-2384
45. Peng, K., Vucetic, S., Radivojac, P., Brown, C. J., Dunker, A. K., and Obra-dovic, Z. (2005) Optimizing long intrinsic disorder predictors with protein evolutionary information. J. Bioinform. Comput. Biol. 3, 35-60
46. Obradovic, Z., Peng, K., Vucetic, S., Radivojac, P., and Dunker, A. K. (2005) Exploiting heterogeneous sequence properties improves prediction of protein disorder. Proteins 61, 176-182
47. Peng, K., Radivojac, P., Vucetic, S., Dunker, A. K., and Obradovic, Z. (2006) Length-dependent prediction of protein intrinsic disorder. BMC Bioinformatics 7, 208
48. Ho, B. K., and Gruswitz, F. (2008) HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49
49. Offredi, F., Dubail, F., Kischel, P., Sarinski, K., Stern, A. S., Van de Weerdt, C., Hoch, J. C, Prosperi, C, François, J. M., Mayo, S. L., and Martial, J. A. (2003) De novo backbone and sequence design of an idealized α/β-barrel protein: evidence of stable tertiary structure. J. Mol. Biol. 325, 163-174
50. Deckert, K., Budiardjo, S. J., Brunner, L. C, Lovell, S., and Karanicolas, J. (2012) Designing allosteric control into enzymes by chemical rescue of structure. J.Am. Chem. Soc. 134, 10055-10060
51. Heilmann, I., Pidkowich, M. S., Girke, T., and Shanklin, J. (2004) Switching desaturase enzyme specificity by alternate subcellular targeting. Proc. Natl. Acad. Sci. U.S.A. 101, 10266-10271
52. Geiler-Samerotte, K. A., Dion, M. F., Budnik, B. A., Wang, S. M., Hartl, D. L., and Drummond, D. A. (2011) Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast. Proc. Natl. Acad. Sci. U.S.A. 108, 680-685
53. Dahlqvist, A., Stahl, U., Lenman, M., Banas, A., Lee, M., Sandager, L., Ronne, H., and Stymne, S. (2000) Phospholipid:diacylglycerol acyltrans-ferase: an enzyme that catalyzes the acyl-CoA-independent formation of triacylglycerol in yeast and plants. Proc. Natl. Acad. Sci. U.S.A. 97, 6487-6492
54. Blakeney, A. B., Harris, P. J., Henry, R. J., and Stone, B. A. (1983) A simple and rapid preparation of alditol acetates for monosaccharide analysis. Carbohydr. Res. 113, 291-299
55. Li, X., Moellering, E. R., Liu, B., Johnny, C., Fedewa, M., Sears, B. B., Kuo, M. H., and Benning, C. (2012) A galactoglycerolipid lipase is required for triacylglycerol accumulation and survival following nitrogen deprivation in Chlamydomonas reinhardtii. Plant Cell 24, 4670-4686
56. Kikuchi, S., Hirohashi, T., and Nakai, M. (2006) Characterization of the preprotein translocon at the outer envelope membrane of chloroplasts by blue native PAGE. Plant Cell Physiol. 47, 363-371
57. Bodennec, J., Pelled, D., and Futerman, A. H. (2003) Aminopropyl solid phase extraction and 2D TLC of neutral glycosphingolipids and neutral lysoglycosphingolipids. J. Lipid Res. 44, 218-226
58. Bruce, B. D., Perry, S., Froehlich, J., and Keegstra, K. (1994) in Plant Molecular Biology Manual (Gelvin, S. B., and Schilperoort, R. A., eds) pp. 1-15, Kluwer Academic Publishers, Boston
59. Schnell, D. J., and Blobel, G. (1993) Identification of intermediates in the pathway of protein import into chloroplasts and their localization to envelope contact sites. J. Cell Biol. 120, 103-115
60. TerBush, A. D., and Osteryoung, K. W. (2012) Distinct functions of chlo-roplast FtsZ1 and FtsZ2 in Z-ring structure and remodeling. J. Cell Biol. 199, 623-637
61. Roston, R. L., Gao, J., Murcha, M. W., Whelan, J., and Benning, C. (2012) TGD1,-2, and-3 proteins involved in lipid trafficking form ATP-binding cassette (ABC) transporter with multiple substrate-binding proteins. J. Biol. Chem. 287, 21406-21415
62. Sinnott, M. L. (1990) Catalytic mechanisms of enzymatic glycosyl transfer. Chem. Rev. 90, 1171-1202
63. Monsan, P., and Paul, F. (1995) Enzymatic-synthesis of oligosaccharides. FEMS Microbiol. Rev. 16, 187-192
64. Heemskerk, J. W., Bogemann, G., and Wintermans, J. F. (1983) Turnover of galactolipids incorporated into chloroplast envelopes an assay for ga-lactolipid-galactolipid galactosyltransferase. Biochim. Biophys. Acta 754, 181-189
65. Reiter, W. D., Chapple, C. C., and Somerville, C R. (1993) Altered growth and cell-walls in a fucose-deficient mutant of Arabidopsis. Science 261, 1032-1035
66. Xu, C, Fan, J., Riekhof, W., Froehlich, J. E., and Benning, C. (2003) A permease-like protein involved in ER to thylakoid lipid transfer in Arabidopsis. EMBOJ. 22, 2370-2379
67. Gasulla, F., Vom Dorp, K., Dombrink, I., Zähringer, U., Gisch, N., Dör-mann, P., and Bartels, D. (2013) The role of lipid metabolism in the acquisition of desiccation tolerance in Craterostigma plantagineum: a comparative approach. Plant J. 75, 726-741
68. Sander, C, and Schneider, R. (1991) Database of homology-derived protein structures and the structural meaning of sequence alignment. Proteins 9, 56-68
69. Nagano, N., Orengo, C. A., and Thornton, J. M. (2002) One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 321, 741-765
70. Greer, J. (1981) Comparative model-building of the mammalian serine proteases. J. Mol. Biol. 153, 1027-1042
71. Larsson, P., Wallner, B., Lindahl, E., and Elofsson, A. (2008) Using multiple templates to improve quality of homology models in automated homology modeling. Protein Sci. 17, 990-1002
72. Benkert, P., Schwede, T., and Tosatto, S. C. (2009) QMEANclust: estimation of protein model quality by combining a composite scoring function with structural density information. BMC Struct. Biol. 9, 35
73. Dunker, A. K., Babu, M. M., Barbar, E., Blackledge, M., Bondos, S. E., Dosztányi, Z., Dyson, H. J., Forman-Kay, J., Fuxreiter, M., Gsponer, J., Han, K.-H, Jones, D. T., Longhi, S., Metallo, S. J., Nishikawa, K., Nussinov, R., Obradovic, Z., Pappu, R. V., Rost, B., Selenko, P., Subramaniam, V., Suss-man, J. L., Tompa, P., and Uversky, V. N. (2013) What's in a name? Why these proteins are intrinsically disordered. Intrinsically Disord. Proteins 1, 0-4 10.4161/idp. 24157
74. Kuhn, L. A., Swanson, C. A., Pique, M. E., Tainer, J. A., and Getzoff, E. D. (1995) Atomic and residue hydrophilicity in the context of folded protein structures. Proteins 23, 536-547
75. Cline, K., Werner-Washburne, M., Andrews, J., and Keegstra, K. (1984) Thermolysin is a suitable protease for probing the surface of intact pea chloroplasts. Plant Physiol. 75, 675-678
76. 2+and a stromal regulatory disulfide bridge. J. Biol. Chem. 284, 2603-2616
77. Smith, M. D., Hiltbrunner, A., Kessler, F., and Schnell, D. J. (2002) The targeting of the atToc159 preprotein receptor to the chloroplast outer membrane is mediated by its GTPase domain and is regulated by GTP. J. Cell Biol. 159, 833-843
78. Muckel, E., and Soll, J. (1996) A protein import receptor of chloroplasts is inserted into the outer envelope membrane by a novel pathway. J. Biol. Chem. 271, 23846-23852
79. Lung, S. C, and Chuong, S. D. (2012) A transit peptide-like sorting signal at the C terminus directs the Bienertia sinuspersici preprotein receptor Toc159 to the chloroplast outer membrane. Plant Cell 24, 1560-1578
80. Barrett, T., Suresh, C. G., Tolley, S. P., Dodson, E. J., and Hughes, M. A. (1995) The crystal-structure of a cyanogenic β-glucosidase from white clover, a family-1-glycosyl-hydrolase (Vol. 3, p. 951, 1995). Structure 3, 1126-1126
81. Czjzek, M., Cicek, M., Zamboni, V., Burmeister, W. P., Bevan, D. R., Hen-rissat, B., and Esen, A. (2001) Crystal structure of a monocotyledon (maize ZMGlu1) β-glucosidase and a model of its complex with p-nitrophenyl β-D-thioglucoside. Biochem. J. 354, 37-46
82. Lu, B., Xu, C, Awai, K., Jones, A. D., and Benning, C. (2007) A small ATPase protein of Arabidopsis, TGD3, involved in chloroplast lipid import. J. Biol. Chem. 282, 35945-35953
83. Shafii, B. (2012) Profiling of Bioactive Lipids Using Ultrahigh Performance Liquid Chromatography and Mass Spectrometry. Ph.D. thesis, Michigan State University
84. Schmeing, T. M., Huang, K. S., Strobel, S. A., and Steitz, T. A. (2005) An induced-fit mechanism to promote peptide bond formation and exclude hydrolysis of peptidyl-tRNA. Nature 438, 520-524
85. Buschiazzo, A., Amaya, M. F., Cremona, M. L., Frasch, A. C., and Alzari, P. M. (2002) The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol. Cell 10, 757-768
86. Persson, K., Ly, H. D., Dieckelmann, M., Wakarchuk, W. W., Withers, S. G., and Strynadka, N. C. (2001) Crystal structure of the retaining galac-tosyltransferase LgtC from Neisseria meningitidis in complex with donor and acceptor sugar analogs. Nat. Struct. Biol. 8, 166-175
87. van der Veen, B. A., Leemhuis, H., Kralj, S., Uitdehaag, J. C., Dijkstra, B. W., and Dijkhuizen, L. (2001) Hydrophobic amino acid residues in the acceptor binding site are main determinants for reaction mechanism and specificity of cyclodextrin-glycosyltransferase. J. Biol. Chem. 276, 44557-44562
88. Britton, K. L., Abeysinghe, I. S., Baker, P. J., Barynin, V., Diehl, P., Lan-gridge, S. J., McFadden, B. A., Sedelnikova, S. E., Stillman, T. J., Weera-dechapon, K., and Rice, D. W. (2001) The structure and domain organization of Escherichia coli isocitrate lyase. Acta Crystallogr. D Biol. Crystallogr. 57, 1209-1218
89. Korndörfer, I. P., Fessner, W. D., and Matthews, B. W. (2000) The structure of rhamnose isomerase from Escherichia coli and its relation with xylose isomerase illustrates a change between inter and intra-subunit complementation during evolution. J. Mol. Biol. 300, 917-933
90. Joseph, D., Petsko, G. A., and Karplus, M. (1990) Anatomy of a conforma-tional change-hinged lid motion of the triosephosphate isomerase loop. Science 249, 1425-1428
91. Campbell, Z. T., and Baldwin, T. O. (2009) Two lysine residues in the bacterial luciferase mobile loop stabilize reaction intermediates. J. Biol. Chem. 284, 32827-32834
92. Teze, D., Hendrickx, J., Dion, M., Tellier, C, Woods, V.L., Jr., Tran, V., and Sanejouand, Y. H. (2013) Conserved water molecules in family 1 glycosi-dases: a DXMS and molecular dynamics study. Biochemistry 52, 5900-5910
93. Shaul, O. (2002) Magnesium transport and function in plants: the tip of the iceberg. Biometals 15, 309-323
94. Assunção, A. G., Persson, D. P., Husted, S., Schjørring, J. K., Alexander, R. D., and Aarts, M. G. (2013) Model of how plants sense zinc deficiency. Metallomics 5, 1110-1116
95. 2+follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiol. 147, 1690-1698
96. +in root hairs of Arabidopsis thaliana: in vivo measurements using the fluorescent dyes SBFI and PBFI.J. Exp. Bot. 54, 2035-2043
97. Babor, M., Gerzon, S., Raveh, B., Sobolev, V., and Edelman, M. (2008) Prediction of transition metal-binding sites from apo protein structures. Proteins 70, 208-217
98. Ebert, J. C., and Altman, R. B. (2008) Robust recognition of zinc binding sites in proteins. Protein Sci. 17, 54-65
99. Sodhi, J. S., Bryson, K., McGuffin, L. J., Ward, J. J., Wernisch, L., and Jones, D. T. (2004) Predicting metal-binding site residues in low-resolution structural models. J. Mol. Biol. 342, 307-320