The impact of the branched-chain ketoacid dehydrogenase complex on amino acid homeostasis in Arabidopsis

Plant Physiology

Volumn 169, Issue 3, 2015, Pages 1807-1820

  Peng, Cheng ^a   Uygun, Sahra ^a   Shiu, Shin Han ^a   Last, Robert L ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 OXOISOVALERATE DEHYDROGENASE (LIPOAMIDE); ARABIDOPSIS PROTEIN; BRANCHED CHAIN AMINO ACID;

ARABIDOPSIS; DARKNESS; ENERGY METABOLISM; ENZYMOLOGY; GENETICS; HOMEOSTASIS; LIGHT; METABOLISM; MUTATION; PHYSIOLOGY; PLANT SEED; RADIATION RESPONSE;

3-METHYL-2-OXOBUTANOATE DEHYDROGENASE (LIPOAMIDE); AMINO ACIDS, BRANCHED-CHAIN; ARABIDOPSIS; ARABIDOPSIS PROTEINS; DARKNESS; ENERGY METABOLISM; HOMEOSTASIS; LIGHT; METABOLIC NETWORKS AND PATHWAYS; MUTATION; SEEDS;

EID: 84946219219     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00461     Document Type: Article

References (79)

1. Anderson MD, Che P, Song J, Nikolau BJ, Wurtele ES (1998) 3-Methylcrotonyl-coenzyme A carboxylase is a component of the mitochondrial leucine catabolic pathway in plants. Plant Physiol 118: 1127–1138
2. Angelovici R, Fait A, Fernie AR, Galili G (2011) A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol 189: 148–159
3. Angelovici R, Lipka AE, Deason N, Gonzalez-Jorge S, Lin H, Cepela J, Buell R, Gore MA, Dellapenna D (2013) Genome-wide analysis of branched-chain amino acid levels in Arabidopsis seeds. Plant Cell 25: 4827–4843
4. Araújo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, et al. (2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22: 1549–1563
5. Ashmarina LI, Pshezhetsky AV, Branda SS, Isaya G, Mitchell GA (1999) 3-Hydroxy-3-methylglutaryl coenzyme A lyase: targeting and processing in peroxisomes and mitochondria. J Lipid Res 40: 70–75
6. Ashmarina LI, Rusnak N, Miziorko HM, Mitchell GA (1994) 3-Hydroxy- 3-methylglutaryl-CoA lyase is present in mouse and human liver peroxisomes. J Biol Chem 269: 31929–31932
7. Attaran E, Major IT, Cruz JA, Rosa BA, Koo AJ, Chen J, Kramer DM, He SY, Howe GA (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165: 1302–1314
8. Aubert S, Bligny R, Day DA, Whelan J, Douce R (1997) Induction of alternative oxidase synthesis by herbicides inhibiting branched-chain amino acid synthesis. Plant J 11: 649–657
9. Binder S (2010) Branched-chain amino acid metabolism in Arabidopsis thaliana. Arabidopsis Book 8: e0137, doi/10.1199/tab.0137
10. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30: 2114–2120
11. Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422: 433–438
12. Che P, Wurtele ES, Nikolau BJ (2002) Metabolic and environmental regulation of 3-methylcrotonyl-coenzyme A carboxylase expression in Arabidopsis. Plant Physiol 129: 625–637
13. Chen H, Saksa K, Zhao F, Qiu J, Xiong L (2010) Genetic analysis of pathway regulation for enhancing branched-chain amino acid biosynthesis in plants. Plant J 63: 573–583
14. Chen Y, McCarthy D, Robinson M, Smyth GK (2011) edgeR: differential expression analysis of digital gene expression data. User’s Guide. http://www.bioconductor.org/packages/release/bioc/vignettes/edgeR/inst/doc/edgeRUsersGuide.pdf (August 13, 2013)
15. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5–17
16. Däschner K, Couée I, Binder S (2001) The mitochondrial isovalerylcoenzyme A dehydrogenase of Arabidopsis oxidizes intermediates of leucine and valine catabolism. Plant Physiol 126: 601–612
17. Diebold R, Schuster J, Däschner K, Binder S (2002) The branched-chain amino acid transaminase gene family in Arabidopsis encodes plastid and mitochondrial proteins. Plant Physiol 129: 540–550
18. Ding G, Che P, Ilarslan H, Wurtele ES, Nikolau BJ (2012) Genetic dissection of methylcrotonyl CoA carboxylase indicates a complex role for mitochondrial leucine catabolism during seed development and germination. Plant J 70: 562–577
19. Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23: 469–478
20. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616–629
21. Espinoza C, Degenkolbe T, Caldana C, Zuther E, Leisse A, Willmitzer L, Hincha DK, Hannah MA (2010) Interaction with diurnal and circadian regulation results in dynamic metabolic and transcriptional changes during cold acclimation in Arabidopsis. PLoS ONE 5: e14101
22. Fujiki Y, Ito M, Nishida I, Watanabe A (2001) Leucine and its keto acid enhance the coordinated expression of genes for branched-chain amino acid catabolism in Arabidopsis under sugar starvation. FEBS Lett 499: 161–165
23. Fujiki Y, Sato T, Ito M, Watanabe A (2000) Isolation and characterization of cDNA clones for the e1b and E2 subunits of the branched-chain a-ketoacid dehydrogenase complex in Arabidopsis. J Biol Chem 275: 6007–6013
24. Ganko EW, Meyers BC, Vision TJ (2007) Divergence in expression between duplicated genes in Arabidopsis. Mol Biol Evol 24: 2298–2309
25. Gibon Y, Blaesing OE, Hannemann J, Carillo P, Höhne M, Hendriks JH, Palacios N, Cross J, Selbig J, Stitt M (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16: 3304–3325
26. Gibon Y, Usadel B, Blaesing OE, Kamlage B, Hoehne M, Trethewey R, Stitt M (2006) Integration of metabolite with transcript and enzyme activity profiling during diurnal cycles in Arabidopsis rosettes. Genome Biol 7: R76
27. Goff LA, Trapnell C, Kelley D (2012) CummeRbund: visualization and exploration of Cufflinks high-throughput sequencing data. R Package Version 2.2.0. http://www.bioconductor.org/packages/release/bioc/vignettes/cummeRbund/inst/doc/cummeRbund-manual.pdf (September 19, 2013)
28. Gu L, Jones AD, Last R (2012) Rapid LC–MS/MS profiling of protein amino acids and metabolically related compounds for large-scale assessment of metabolic phenotypes. In MA Alterman, P Hunziker, eds, Amino Acid Analysis, Vol 828. Humana Press, New York, pp 1-11
29. Gu L, Jones AD, Last RL (2007) LC-MS/MS assay for protein amino acids and metabolically related compounds for large-scale screening of metabolic phenotypes. Anal Chem 79: 8067–8075
30. Gu L, Jones AD, Last RL (2010) Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J 61: 579–590
31. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H, Shibata D, Tabata S, Ohsumi Y (2002) Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129: 1181–1193
32. Harper AE, Miller RH, Block KP (1984) Branched-chain amino acid metabolism. Annu Rev Nutr 4: 409–454
33. Ishizaki K, Larson TR, Schauer N, Fernie AR, Graham IA, Leaver CJ (2005) The critical role of Arabidopsis electron-transfer flavoprotein: ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 17: 2587–2600
34. Ishizaki K, Schauer N, Larson TR, Graham IA, Fernie AR, Leaver CJ (2006) The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J 47: 751–760
35. Izumi M, Wada S, Makino A, Ishida H (2010) The autophagic degradation of chloroplasts via Rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154: 1196–1209
36. Jander G, Norris SR, Joshi V, Fraga M, Rugg A, Yu S, Li L, Last RL (2004) Application of a high-throughput HPLC-MS/MS assay to Arabidopsis mutant screening; evidence that threonine aldolase plays a role in seed nutritional quality. Plant J 39: 465–475
37. Jones E, Oliphant T, Peterson P (2001) SciPy: Open source scientific tools for Python. http://www.scipy.org/ (April 2, 2014)
38. Joshi V, Laubengayer KM, Schauer N, Fernie AR, Jander G (2006) Two Arabidopsis threonine aldolases are nonredundant and compete with threonine deaminase for a common substrate pool. Plant Cell 18: 3564–3575
39. Karchi H, Shaul O, Galili G (1994) Lysine synthesis and catabolism are coordinately regulated during tobacco seed development. Proc Natl Acad Sci USA 91: 2577–2581
40. Keith B, Dong XN, Ausubel FM, Fink GR (1991) Differential induction of 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase genes in Arabidopsis thaliana by wounding and pathogenic attack. Proc Natl Acad Sci USA 88: 8821–8825
41. Kilian J, Whitehead D, Horak J, Wanke D, Weinl S, Batistic O, D’Angelo C, Bornberg-Bauer E, Kudla J, Harter K (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347–363
42. Kochevenko A, Araújo WL, Maloney GS, Tieman DM, Do PT, Taylor MG, Klee HJ, Fernie AR (2012) Catabolism of branched chain amino acids supports respiration but not volatile synthesis in tomato fruits. Mol Plant 5: 366–375
43. Kotewicz ML, D’Alessio JM, Driftmier KM, Blodgett KP, Gerard GF (1985) Cloning and overexpression of Moloney murine leukemia virus reverse transcriptase in Escherichia coli. Gene 35: 249–258
44. Lee M, Huang T, Toro-Ramos T, Fraga M, Last RL, Jander G (2008) Reduced activity of Arabidopsis thaliana HMT2, a methionine biosynthetic enzyme, increases seed methionine content. Plant J 54: 310–320
45. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079
46. Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63: 215–237
47. Lu Y, Savage LJ, Ajjawi I, Imre KM, Yoder DW, Benning C, Dellapenna D, Ohlrogge JB, Osteryoung KW, Weber AP, (2008) New connections across pathways and cellular processes: industrialized mutant screening reveals novel associations between diverse phenotypes in Arabidopsis. Plant Physiol 146: 1482–1500
48. Lu Y, Savage LJ, Larson MD, Wilkerson CG, Last RL (2011) Chloroplast 2010: a database for large-scale phenotypic screening of Arabidopsis mutants. Plant Physiol 155: 1589–1600
49. Lutziger I, Oliver DJ (2001) Characterization of two cDNAs encoding mitochondrial lipoamide dehydrogenase from Arabidopsis. Plant Physiol 127: 615–623
50. McCourt JA, Pang SS, King-Scott J, Guddat LW, Duggleby RG (2006) Herbicide-binding sites revealed in the structure of plant acetohydroxyacid synthase. Proc Natl Acad Sci USA 103: 569–573
51. Mentzen WI, Peng J, Ransom N, Nikolau BJ, Wurtele ES (2008) Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol 8: 76
52. Mikkelsen MD, Halkier BA (2003) Metabolic engineering of valine- and isoleucine-derived glucosinolates in Arabidopsis expressing CYP79D2 from Cassava. Plant Physiol 131: 773–779
53. Milo R, Last RL (2012) Achieving diversity in the face of constraints: lessons from metabolism. Science 336: 1663–1667
54. Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM, Givan SA, McEntee C, Kay SA, Chory J (2007) The DIURNAL project: DIURNAL and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harb Symp Quant Biol 72: 353–363
55. Mooney BP, Henzl MT, Miernyk JA, Randall DD (2000) The dihydrolipoyl acyltransferase (BCE2) subunit of the plant branched-chain a-ketoacid dehydrogenase complex forms a 24-mer core with octagonal symmetry. Protein Sci 9: 1334–1339
56. Mooney BP, Miernyk JA, Randall DD (2002) The complex fate of a-ketoacids. Annu Rev Plant Biol 53: 357–375
57. Oh SA, Park JH, Lee GI, Paek KH, Park SK, Nam HG (1997) Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J 12: 527–535
58. Oliver DJ (1994) The glycine decarboxylase complex from plant mitochondria. Annu Rev Plant Physiol Plant Mol Biol 45: 323–337
59. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
60. Sarkar D, Sarkar MD (2007) The lattice Package. http://cran.r-project.org/web/packages/lattice/lattice.pdf (May 14, 2014)
61. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, et al. (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24: 447–454
62. Schertl P, Braun HP (2014) Respiratory electron transfer pathways in plant mitochondria. Front Plant Sci 5: 163
63. Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Schölkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501–506
64. Schuster J, Binder S (2005) The mitochondrial branched-chain aminotransferase (AtBCAT-1) is capable to initiate degradation of leucine, isoleucine and valine in almost all tissues in Arabidopsis thaliana. Plant Mol Biol 57: 241–254
65. Shariati SA, De Strooper B (2013) Redundancy and divergence in the amyloid precursor protein family. FEBS Lett 587: 2036–2045
66. Singh BK (1999) Biosynthesis of valine, leucine, and isoleucine. In BK Singh, ed, Plant Amino Acids: Biochemistry and Biotechnology. Marcel Dekker, New York, pp 227-247
67. Singh BK, Shaner DL (1995) Biosynthesis of branched chain amino acids: from test tube to field. Plant Cell 7: 935–944
68. Slocombe SP, Schauvinhold I, McQuinn RP, Besser K, Welsby NA, Harper A, Aziz N, Li Y, Larson TR, Giovannoni J, et al. (2008) Transcriptomic and reverse genetic analyses of branched-chain fatty acid and acyl sugar production in Solanum pennellii and Nicotiana benthamiana. Plant Physiol 148: 1830–1846
69. Stern DL, Orgogozo V (2008) The loci of evolution: how predictable is genetic evolution? Evolution 62: 2155–2177
70. Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, et al. (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53: 11–28
71. Tan S, Evans R, Singh B (2006) Herbicidal inhibitors of amino acid biosynthesis and herbicide-tolerant crops. Amino Acids 30: 195–204
72. Taylor NL, Heazlewood JL, Day DA, Millar AH (2004) Lipoic acid-dependent oxidative catabolism of a-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabidopsis. Plant Physiol 134: 838–848
73. Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-seq. Nat Biotechnol 31: 46–53
74. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111
75. Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A (2009) Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149: 885–893
76. Yu Q, Han H, Vila-Aiub MM, Powles SB (2010) AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61: 3925–3934
77. Zhu X, Galili G (2003) Increased lysine synthesis coupled with a knockout of its catabolism synergistically boosts lysine content and also transregulates the metabolism of other amino acids in Arabidopsis seeds. Plant Cell 15: 845–853
78. Zhu X, Galili G (2004) Lysine metabolism is concurrently regulated by synthesis and catabolism in both reproductive and vegetative tissues. Plant Physiol 135: 129–136
79. Zou C, Lehti-Shiu MD, Thomashow M, Shiu SH (2009) Evolution of stress-regulated gene expression in duplicate genes of Arabidopsis thaliana. PLoS Genet 5: e1000581