Arabidopsis and maize RidA Proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids

Plant Cell

Volumn 26, Issue 7, 2014, Pages 3010-3022

  Niehaus, Thomas D ^a   Nguyen, Thuy N D ^b   Gidda, Satinder K ^b   ElBadawi Sidhu, Mona ^c   Lambrecht, Jennifer A ^d,f   McCarty, Donald R ^a   Downs, Diana M ^d   Cooper, Arthur J L ^e   Fiehn, Oliver ^c   Mullen, Robert T ^b   Hanson, Andrew D ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF GUELPH   (Canada)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF GEORGIA   (United States)

^e NEW YORK MEDICAL COLLEGE   (United States)

^f WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA-KETOBUTYRIC ACID; AMINOTRANSFERASE; ARABIDOPSIS PROTEIN; BRANCHED CHAIN AMINO ACID; BRANCHED-CHAIN AMINOTRANSFERASE-3, ARABIDOPSIS; BUTYRIC ACID DERIVATIVE; HYDROLASE; IMINE; PLANT PROTEIN; RIDA PROTEIN, ARABIDOPSIS; SERINE DEHYDRATASE; THREONINE AMMONIA LYASE;

AMINO ACID SEQUENCE; ANIMAL; ARABIDOPSIS; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; GENETICS; HYDROLYSIS; MAIZE; METABOLISM; METABOLOMICS; MOLECULAR GENETICS; PLANT ROOT; PLASTID; SEQUENCE ALIGNMENT; SHOOT;

AMINO ACID SEQUENCE; AMINO ACIDS, BRANCHED-CHAIN; AMINOHYDROLASES; ANIMALS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BUTYRATES; HYDROLYSIS; IMINES; L-SERINE DEHYDRATASE; METABOLOMICS; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PLANT ROOTS; PLANT SHOOTS; PLASTIDS; SEQUENCE ALIGNMENT; THREONINE DEHYDRATASE; TRANSAMINASES; ZEA MAYS;

EID: 84907324191     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.126854     Document Type: Article

References (63)

1. Bessman, M.J., Frick, D.N., and O'Handley, S.F. (1996). The MutT proteins or "Nudix" hydrolases, a family of versatile, widely distributed, "housecleaning" enzymes. J. Biol. Chem. 271: 25059-25062.
2. Burman, J.D., Stevenson, C.E., Sawers, R.G., and Lawson, D.M. (2007). The crystal structure of Escherichia coli TdcF, a member of the highly conserved YjgF/YER057c/UK114 family. BMC Struct. Biol. 7: 30.
3. Chargaff, E., and Sprinson, D.B. (1943). Studies on the mechanism of deamination of serine and threonine in biological systems. J. Biol. Chem. 151: 273-280.
4. Chatr-Aryamontri, A., et al. (2013). The BioGRID interaction database: 2013 update. Nucleic Acids Res. 41: D816-D823.
5. Christopherson, M.R., Lambrecht, J.A., Downs, D., and Downs, D.M. (2012). Suppressor analyses identify threonine as a modulator of ridA mutant phenotypes in Salmonella enterica. PLoS ONE 7: e43082.
6. Christopherson, M.R., Schmitz, G.E., and Downs, D.M. (2008). YjgF is required for isoleucine biosynthesis when Salmonella enterica is grown on pyruvate medium. J. Bacteriol. 190: 3057-3062.
7. 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.
8. Colabroy, K.L., and Begley, T.P. (2005). Tryptophan catabolism: identification and characterization of a new degradative pathway. J. Bacteriol. 187: 7866-7869.
9. Costanzo, M., et al. (2010). The genetic landscape of a cell. Science 327: 425-431.
10. D'Ari, R., and Casadesús, J. (1998). Underground metabolism. BioEssays 20: 181-186.
11. Datta, P., and Bhadra, R. (1978). Biodegradative threonine dehydratase. Reduction of ferricyanide by an intermediate of the enzyme-catalyzed reaction. Eur. J. Biochem. 91: 527-532.
12. Davidson, R.M., Hansey, C.N., Gowda, M., Childs, K.L., Lin, H., Vaillancourt, B., Sekhon, R.S., de Leon, N., Kaeppler, S.M., Jiang, N., and Buell, C.R. (2011). Utility of RNA sequencing for analysis of maize reproductive transcriptomes. Plant Genome 4: 191-203.
13. Diebold, R., Schuster, J., Däschner, K., and Binder, S. (2002). The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol. 129: 540-550.
14. Enos-Berlage, J.L., Langendorf, M.J., and Downs, D.M. (1998). Complex metabolic phenotypes caused by a mutation in yjgF, encoding a member of the highly conserved YER057c/YjgF family of proteins. J. Bacteriol. 180: 6519-6528.
15. Farré, E.M., Tiessen, A., Roessner, U., Geigenberger, P., Trethewey, R.N., and Willmitzer, L. (2001). Analysis of the compartmentation of glycolytic intermediates, nucleotides, sugars, organic acids, amino acids, and sugar alcohols in potato tubers using a nonaqueous fractionation method. Plant Physiol. 127: 685-700.
16. Flynn, J.M., Christopherson, M.R., and Downs, D.M. (2013). Decreased coenzyme A levels in ridA mutant strains of Salmonella enterica result from inactivated serine hydroxymethyltransferase. Mol. Microbiol. 89: 751-759.
17. Flynn, J.M., and Downs, D.M. (2013). In the absence of RidA, endogenous 2-aminoacrylate inactivates alanine racemases by modifying the pyridoxal 59-phosphate cofactor. J. Bacteriol. 195: 3603-3609.
18. Franceschini, A., Szklarczyk, D., Frankild, S., Kuhn, M., Simonovic, M., Roth, A., Lin, J., Minguez, P., Bork, P., von Mering, C., and Jensen, L.J. (2013). STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acids Res. 41: D808-D815.
19. Frelin, O., Agrimi, G., Laera, V.L., Castegna, A., Richardson, L.G., Mullen, R.T., Lerma-Ortiz, C., Palmieri, F., and Hanson, A.D. (2012). Identification of mitochondrial thiamin diphosphate carriers from Arabidopsis and maize. Funct. Integr. Genomics 12: 317-326.
20. Galperin, M.Y., Moroz, O.V., Wilson, K.S., and Murzin, A.G. (2006). House cleaning, a part of good housekeeping. Mol. Microbiol. 59: 5-19.
21. Golubev, A.G. (1996). The other side of metabolism: a review. Biochemistry (Mosc.) 61: 2018-2039.
22. Hafner, E.W., and Wellner, D. (1979). Reactivity of the imino acids formed in the amino acid oxidase reaction. Biochemistry 18: 411-417.
23. Hagelstein, P., Sieve, B., Klein, M., Jans, H., and Schultz, G. (1997). Leucine synthesis in chloroplasts: Leucine/isoleucine aminotransferase and valine aminotransferase are different enzymes in spinach chloroplasts. J. Plant Physiol. 150: 23-30.
24. Heath, C., Posner, M.G., Aass, H.C., Upadhyay, A., Scott, D.J., Hough, D.W., and Danson, M.J. (2007). The 2-oxoacid dehydrogenase multienzyme complex of the archaeon Thermoplasma acidophilum-recombinant expression, assembly and characterization. FEBS J. 274: 5406-5415.
25. Hillebrand, G.G., Dye, J.L., and Suelter, C.H. (1979). Formation of an intermediate and its rate of conversion to pyruvate during the tryptophanase-catalyzed degradation of S-o-nitrophenyl-L-cysteine. Biochemistry 18: 1751-1755.
26. Jia, Y., Lisch, D.R., Ohtsu, K., Scanlon, M.J., Nettleton, D., and Schnable, P.S. (2009). Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet. 5: e1000737.
27. Kessler, F., and Schnell, D. (2009). Chloroplast biogenesis: diversity and regulation of the protein import apparatus. Curr. Opin. Cell Biol. 21: 494-500.
28. Kim, J.M., Yoshikawa, H., and Shirahige, K. (2001). A member of the YER057c/yjgf/Uk114 family links isoleucine biosynthesis and intact mitochondria maintenance in Saccharomyces cerevisiae. Genes Cells 6: 507-517.
29. Kim, K.S., Pelton, J.G., Inwood, W.B., Andersen, U., Kustu, S., and Wemmer, D.E. (2010). The Rut pathway for pyrimidine degradation: novel chemistry and toxicity problems. J. Bacteriol. 192: 4089-4102.
30. Knill, T., Schuster, J., Reichelt, M., Gershenzon, J., and Binder, S. (2008). Arabidopsis branched-chain aminotransferase 3 functions in both amino acid and glucosinolate biosynthesis. Plant Physiol. 146: 1028-1039.
31. Lambrecht, J.A., Browne, B.A., and Downs, D.M. (2010). Members of the YjgF/YER057c/UK114 family of proteins inhibit phosphoribosylamine synthesis in vitro. J. Biol. Chem. 285: 34401-34407.
32. Lambrecht, J.A., Flynn, J.M., and Downs, D.M. (2012). Conserved YjgF protein family deaminates reactive enamine/imine intermediates of pyridoxal 59-phosphate (PLP)-dependent enzyme reactions. J. Biol. Chem. 287: 3454-3461.
33. Lambrecht, J.A., Schmitz, G.E., and Downs, D.M. (2013). RidA proteins prevent metabolic damage inflicted by PLP-dependent dehydratases in all domains of life. MBio 4: e00033-e13.
34. Leitner-Dagan, Y., Ovadis, M., Zuker, A., Shklarman, E., Ohad, I., Tzfira, T., and Vainstein, A. (2006). CHRD, a plant member of the evolutionarily conserved YjgF family, influences photosynthesis and chromoplastogenesis. Planta 225: 89-102.
35. Li, P., et al. (2010). The developmental dynamics of the maize leaf transcriptome. Nat. Genet. 42: 1060-1067.
36. Libal-Weksler, Y., Vishnevetsky, M., Ovadis, M., and Vainstein, A. (1997). Isolation and regulation of accumulation of a minor chromoplastspecific protein from cucumber corollas. Plant Physiol. 113: 59-63.
37. Linster, C.L., Van Schaftingen, E., and Hanson, A.D. (2013). Metabolite damage and its repair or pre-emption. Nat. Chem. Biol. 9: 72-80.
38. Manjasetty, B.A., et al. (2004). Crystal structure of Homo sapiens protein hp14.5. Proteins 54: 797-800.
39. McCartney, A.W., Greenwood, J.S., Fabian, M.R., White, K.A., and Mullen, R.T. (2005). Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 17: 3513-3531.
40. Meister, A. (1950). Reduction of alpha gamma-diketo and alpha-keto acids catalyzed by muscle preparations and by crystalline lactic dehydrogenase. J. Biol. Chem. 184: 117-129.
41. Morishita, R., Kawagoshi, A., Sawasaki, T., Madin, K., Ogasawara, T., Oka, T., and Endo, Y. (1999). Ribonuclease activity of rat liver perchloric acid-soluble protein, a potent inhibitor of protein synthesis. J. Biol. Chem. 274: 20688-20692.
42. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37: D987-D991.
43. O'Brien, P.J., and Herschlag, D. (1999). Catalytic promiscuity and the evolution of new enzymatic activities. Chem. Biol. 6: R91-R105.
44. Okumoto, S., and Pilot, G. (2011). Amino acid export in plants: a missing link in nitrogen cycling. Mol. Plant 4: 453-463.
45. Parsot, C. (1987). A common origin for enzymes involved in the terminal step of the threonine and tryptophan biosynthetic pathways. Proc. Natl. Acad. Sci. USA 84: 5207-5210.
46. Pu, Y.G., Jiang, Y.L., Ye, X.D., Ma, X.X., Guo, P.C., Lian, F.M., Teng, Y.B., Chen, Y., and Zhou, C.Z. (2011). Crystal structures and putative interface of Saccharomyces cerevisiae mitochondrial matrix proteins Mmf1 and Mam33. J. Struct. Biol. 175: 469-474.
47. Rudhe, C., Chew, O., Whelan, J., and Glaser, E. (2002). A novel in vitro system for simultaneous import of precursor proteins into mitochondria and chloroplasts. Plant J. 30: 213-220.
48. Schadewaldt, P., and Adelmeyer, F. (1996). Coupled enzymatic assay for estimation of branched-chain L-amino acid aminotransferase activity with 2-Oxo acid substrates. Anal. Biochem. 238: 65-71.
49. Shah, J. (2009). Plants under attack: systemic signals in defence. Curr. Opin. Plant Biol. 12: 459-464.
50. Skarstedt, M.T., and Greer, S.B. (1973). Threonine synthetase of Bacillus subtilis. The nature of an associated dehydratase activity. J. Biol. Chem. 248: 1032-1044.
51. Steinhauser, D., Usadel, B., Luedemann, A., Thimm, O., and Kopka, J. (2004). CSB. DB: a comprehensive systems-biology database. Bioinformatics 20: 3647-3651.
52. Sun, Q., Zybailov, B., Majeran, W., Friso, G., Olinares, P.D., and van Wijk, K.J. (2009). PPDB, the Plant Proteomics Database at Cornell. Nucleic Acids Res. 37: D969-D974.
53. Szamosi, I., Shaner, D.L., and Singh, B.K. (1993). Identification and characterization of a biodegradative form of threonine dehydratase in senescing tomato (Lycopersicon esculentum) leaf. Plant Physiol. 101: 999-1004.
54. Szecowka, M., Heise, R., Tohge, T., Nunes-Nesi, A., Vosloh, D., Huege, J., Feil, R., Lunn, J., Nikoloski, Z., Stitt, M., Fernie, A.R., and Arrivault, S. (2013). Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell 25: 694-714.
55. Takenaka, S., Murakami, S., Kim, Y.J., and Aoki, K. (2000). Complete nucleotide sequence and functional analysis of the genes for 2-aminophenol metabolism from Pseudomonas sp. AP-3. Arch. Microbiol. 174: 265-272.
56. Tawfik, D.S. (2010). Messy biology and the origins of evolutionary innovations. Nat. Chem. Biol. 6: 692-696.
57. Teng, Y.S., Chan, P.T., and Li, H.M. (2012). Differential agedependent import regulation by signal peptides. PLoS Biol. 10: e1001416.
58. Van Schaftingen, E., Rzem, R., Marbaix, A., Collard, F., Veiga-da-Cunha, M., and Linster, C.L. (2013). Metabolite proofreading, a neglected aspect of intermediary metabolism. J. Inherit. Metab. Dis. 36: 427-434.
59. Wang, X., Elling, A.A., Li, X., Li, N., Peng, Z., He, G., Sun, H., Qi, Y., Liu, X.S., and Deng, X.W. (2009). Genome-wide and organ-specific landscapes of epigenetic modifications and their relationships to mRNA and small RNA transcriptomes in maize. Plant Cell 21: 1053-1069.
60. Waters, A.J., Makarevitch, I., Eichten, S.R., Swanson-Wagner, R.A., Yeh, C.T., Xu, W., Schnable, P.S., Vaughn, M.W., Gehring, M., and Springer, N.M. (2011). Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23: 4221-4233.
61. Wessel, P.M., Graciet, E., Douce, R., and Dumas, R. (2000). Evidence for two distinct effector-binding sites in threonine deaminase by site-directed mutagenesis, kinetic, and binding experiments. Biochemistry 39: 15136-15143.
62. Yu, H., Zhang, F., Wang, G., Liu, Y., and Liu, D. (2013). Partial deficiency of isoleucine impairs root development and alters transcript levels of the genes involved in branched-chain amino acid and glucosinolate metabolism in Arabidopsis. J. Exp. Bot. 64: 599-612.
63. Zhou, L., Wang, J.Y., Wu, J., Wang, J., Poplawsky, A., Lin, S., Zhu, B., Chang, C., Zhou, T., Zhang, L.H., and He, Y.W. (2013). The diffusible factor synthase XanB2 is a bifunctional chorismatase that links the shikimate pathway to ubiquinone and xanthomonadins biosynthetic pathways. Mol. Microbiol. 87: 80-93.