Glutaredoxin S15 is involved in Fe-S cluster transfer in mitochondria influencing lipoic acid-dependent enzymes, plant growth, and arsenic tolerance in Arabidopsis

Plant Physiology

Volumn 170, Issue 3, 2016, Pages 1284-1299

  Stroher, Elke ^a   Grassl, Julia ^a   Carrie, Chris ^a,c   Fenske, Ricarda ^a   Whelan, James ^b   Millar, A Harvey ^a  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ARSENIC; GLUTAREDOXIN; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; PROTEOME; THIOCTIC ACID;

ARABIDOPSIS; DRUG EFFECTS; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOCHONDRION; MUTATION; PLANT GENE; PLANT ROOT; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARSENIC; GENE KNOCKDOWN TECHNIQUES; GENES, PLANT; GLUTAREDOXINS; IRON-SULFUR PROTEINS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUTATION; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; PROTEOME; THIOCTIC ACID;

EID: 84959291973     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01308     Document Type: Article

References (103)

1. Abercrombie JM, Halfhill MD, Ranjan P, Rao MR, Saxton AM, Yuan JS, Stewart CN, Jr. (2008) Transcriptional responses of Arabidopsis thaliana plants to As (V) stress. BMC Plant Biol 8: 87
2. Aebersold R, Burlingame AL, Bradshaw RA (2013) Western blots versus selected reaction monitoring assays: time to turn the tables? Mol Cell Proteomics 12: 2381-2382
3. Andersen SU, Buechel S, Zhao Z, Ljung K, Novak O, Busch W, Schuster C, Lohmann JU (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. Plant Cell 20:88-100
4. Baerenfaller K, Grossmann J, Grobei MA, Hull R, Hirsch-Hoffmann M, Yalovsky S, Zimmermann P, Grossniklaus U, Gruissem W, Baginsky S (2008) Genome-scale proteomics reveals Arabidopsis thaliana gene models and proteome dynamics. Science 320: 938-941
5. Baker II PR, Friederich MW, Swanson MA, Shaikh T, Bhattacharya K, Scharer GH, Aicher J, Creadon-Swindell G, Geiger E, MacLean KN, Lee WT, Deshpande C, et al (2014) Variant nonketotic hyperglycinemia is caused by mutations in LIAS, BOLA3 and the novel gene GLRX5. Brain 137: 366-379
6. Balk J, Pilon M (2011) Ancient and essential: the assembly of iron-sulfur clusters in plants. Trends Plant Sci 16: 218-226 Balk J, Schaedler TA (2014) Iron cofactor assembly in plants. Annu Rev Plant Biol 65: 125-153
7. Balmer Y, Vensel WH, Tanaka CK, Hurkman WJ, Gelhaye E, Rouhier N, Jacquot JP, Manieri W, Schiirmann P, Droux M, Buchanan BB (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci USA 101: 2642-2647
8. Bandyopadhyay S, Gama F, Molina-Navarro MM, Gualberto JM, Claxton R, Naik SG, Huynh BH, Herrero E, Jacquot JP, Johnson MK, Rouhier N (2008) Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe-2S] clusters. EMBO J 27: 1122-1133
9. Bergquist ER, Fischer RJ, Sugden KD, Martin BD (2009) Inhibition by methylated organo-arsenicals of the respiratory 2-oxo-acid dehydrogenases. J Organomet Chem 694: 973-980
10. Bernard DG, Cheng Y, Zhao Y, Balk J (2009) An allelic mutant series of ATM3 reveals its key role in the biogenesis of cytosolic iron-sulfur proteins in Arabidopsis. Plant Physiol 151: 590-602
11. Bernard DG, Netz DJ, Lagny TJ, Pierik AJ, Balk J (2013) Requirements of the cytosolic iron-sulfur cluster assembly pathway in Arabidopsis. Philos Trans R Soc Lond B Biol Sci 368: 20120259
12. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806
13. Cameron JM, Janer A, Levandovskiy V, Mackay N, Rouault TA, Tong WH, Ogilvie I, Shoubridge EA, Robinson BH (2011) Mutations iniron sulfur cluster scaffold genes NFU1 and BOLA3 cause a fatal deficiency of multiple respiratory chain and 2-oxoacid dehydrogenase enzymes. Am J Hum Genet 89: 486-495
14. Carrie C, Kuhn K, Murcha MW, Duncan O, Small ID, O'Toole N, Whelan J (2009) Approaches to defining dual-targeted proteins in Arabidopsis. Plant J 57: 1128-1139
15. Cheng NH (2008) AtGRX4, an Arabidopsis chloroplastic monothiol gluta-redoxin, is able to suppress yeast grx5 mutant phenotypes and respond to oxidative stress. FEBS Lett 582: 848-854
16. Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278: 46869-46877
17. Couturier J, Wu HC, Dhalleine T, Pegeot H, Sudre D, Gualberto JM, Jacquot JP, Gaymard F, Vignols F, Rouhier N (2014) Monothiol glutaredoxin-BolA interactions: redox control of Arabidopsis thaliana BolA2 and SufE1. Mol Plant 7: 187-205
18. Couturier J, Stroher E, Albetel AN, Roret T, Muthuramalingam M, Tarrago L, Seidel T, Tsan P, Jacquot JP, Johnson MK, Dietz KJ, Di-dierjean C, et al (2011) Arabidopsis chloroplastic glutaredoxin C5 as a model to explore molecular determinants for iron-sulfur cluster binding into glutaredoxins. J Biol Chem 286: 27515-27527
19. Couturier J, Jacquot JP, Rouhier N (2009) Evolution and diversity of glutaredoxins in photosynthetic organisms. Cell Mol Life Sci 66:2539-2557
20. Cronan JE (2014) Biotin and Lipoic Acid: Synthesis, Attachment and Regulation. Ecosal Plus 6: 10.1128/ecosalplus.ESP-0001-2012
21. Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462-469
22. Dailey HA, Finnegan MG, Johnson MK (1994) Humanferrochelatase is an iron-sulfur protein. Biochemistry 33: 403-407
23. De Vylder J, Vandenbussche F, Hu Y, Philips W, Van Der Straeten D (2012) Rosette tracker: an open source image analysis tool for automatic quantification of genotype effects. Plant Physiol 160: 1149-1159
24. Dhalleine T, Rouhier N, Couturier J (2014) Putative roles of glutaredoxin- BolA holo-heterodimers in plants. Plant Signal Behav 9: e28564
25. Dixon DP, Skipsey M, Grundy NM, Edwards R (2005) Stress-induced protein S-glutathionylation in Arabidopsis. Plant Physiol 138: 2233-2244
26. Douce R, Bourguignon J, Neuburger M, Rebeille F (2001) The glycine decarboxylase system: a fascinating complex. Trends Plant Sci 6: 167-176
27. Duan GL, Zhou Y, Tong YP, Mukhopadhyay R, Rosen BP, Zhu YG (2007) A CDC25 homologue from rice functions as an arsenate reductase. New Phytol 174: 311-321
28. Ellis DR, Gumaelius L, Indriolo E, Pickering IJ, Banks JA, Salt DE (2006) A novel arsenate reductase from the arsenic hyperaccumulating fern Pteris vittata. Plant Physiol 141: 1544-1554
29. Estavillo GM, Verhertbruggen Y, Scheller HV, Pogson BJ, Heazlewood JL, Ito J (2014) Isolation of the plant cytosolic fraction for proteomic analysis. Methods Mol Biol 1072: 453-467
30. Eubel H, Braun HP, Millar AH (2005) Blue-native PAGE in plants: a tool in analysis of protein-protein interactions. Plant Methods 1: 11
31. Eubel H, Lee CP, Kuo J, Meyer EH, Taylor NL, Millar AH (2007) Free-flow electrophoresis for purification of plant mitochondria by surface charge. Plant J 52: 583-594
32. Ewald R, Kolukisaoglu U, Bauwe U, Mikkat S, Bauwe H (2007) Mitochondrial protein lipoylation does not exclusively depend on the mtKAS pathway of de novo fatty acid synthesis in Arabidopsis. Plant Physiol 145: 41-48
33. Ferro M, Brugiere S, Salvi D, Seigneurin-Berny D, Court M, Moyet L, Ramus C, Miras S, Mellal M, Le Gall S, Kieffer-Jaquinod S, Bruley C, et al (2010) AT_CHLORO, a comprehensive chloroplast proteome database with subplastidial localization and curated information on envelope proteins. Mol Cell Proteomics 9: 1063-1084
34. Finkemeier I, Goodman M, Lamkemeyer P, Kandlbinder A, Sweetlove LJ, Dietz KJ (2005) The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress. J Biol Chem 280: 12168-12180
35. Finnegan PM, Chen W (2012) Arsenic toxicity: the effects on plant metabolism. Front Physiol 3: 182
36. Fish WW (1988) Rapid colorimetric micromethod for the quantitation of complexed iron in biological samples. Methods Enzymol 158: 357-364
37. Gao H, Subramanian S, Couturier J, Naik SG, Kim SK, Leustek T, Knaff DB, Wu HC, Vignols F, Huynh BH, Rouhier N, Johnson MK (2013) Arabidopsis thaliana Nfu2 accommodates [2Fe-2S] or [4Fe-4S] clusters and is competent for in vitro maturation of chloroplast [2Fe-2S] and [4Fe-4S] cluster-containing proteins. Biochemistry 52: 6633-6645
38. Gao XH, Zaffagnini M, Bedhomme M, Michelet L, Cassier-Chauvat C, Decottignies P, Lemaire SD (2010) Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii: kinetics and specificity in deglutathionylation reactions. FEBS Lett 584: 2242-2248
39. Grassl J, Pruzinska A, Hortensteiner S, Taylor NL, Millar AH (2012) Early events in plastid protein degradation in stay-green Arabidopsis reveal differential regulation beyond the retention of LHCII and chlorophyll. J Proteome Res 11: 5443-5452
40. Grassl J, Scaife C, Polden J, Daly CN, Iacovella MG, Dunn MJ, Clyne RK (2010) Analysis of the budding yeast pH 4-7 proteome in meiosis. Proteomics 10: 506-519
41. Han L, Qin G, Kang D, Chen Z, Gu H, Qu LJ (2010) A nuclear-encoded mitochondrial gene AtCIB22 is essential for plant development in Arabidopsis. J Genet Genomics 37: 667-683
42. Herald VL, Heazlewood JL, Day DA, Millar AH (2003) Proteomic identification of divalent metal cation binding proteins in plant mitochondria. FEBS Lett 537: 96-100
43. Holmgren, A., and Lu, J. (2010). Glutaredoxin catalysis and function in redox regulation. Mary Ann Liebert, Inc. Publications, New York.
44. Huang M, Friso G, Nishimura K, Qu X, Olinares PD, Majeran W, Sun Q, van Wijk KJ (2013a) Construction of plastid reference proteomes for maize and Arabidopsis and evaluation of their orthologous relationships; the concept of orthoproteomics. J Proteome Res 12: 491-504
45. Huang S, Taylor NL, Stroher E, Fenske R, Millar AH (2013b) Succinate dehydrogenase assembly factor 2 is needed for assembly and activity of mitochondrial complex II and for normal root elongation in Arabidopsis. Plant J 73: 429-441
46. Ida T, Sawa T, Ihara H, Tsuchiya Y, Watanabe Y, Kumagai Y, Suematsu M, Motohashi H, Fujii S, Matsunaga T, Yamamoto M, Ono K, Devarie-Baez NO, Xian M, Fukuto JM, Akaike T (2014) Reactive cysteine persulfides and S-polythiolation regulate oxidative stress and redox signaling. Proc Natl Acad Sci USA 111: 7606-7611
47. Johansson C, Roos AK, Montano SJ, Sengupta R, Filippakopoulos P, Guo K, von Delft F, Holmgren A, Oppermann U, Kavanagh KL (2011) The crystal structure of human GLRX5: iron-sulfur cluster co-ordination, tetrameric assembly and monomer activity. Biochem J 433: 303-311
48. Kessler D, Papenbrock J (2005) Iron-sulfur cluster biosynthesis in photo-syntheticorganisms. Photosynth Res 86: 391-407
49. Klodmann J, Senkler M, Rode C, Braun HP (2011) Defining the protein complex proteome of plant mitochondria. Plant Physiol 157: 587-598
50. Klodmann J, Sunderhaus S, Nimtz M, Jansch L, Braun HP (2010) Internal architecture of mitochondrial complex I from Arabidopsis thaliana. Plant Cell 22: 797-810
51. Knuesting J, Riondet C, Maria C, Kruse I, Becuwe N, Konig N, Berndt C, Tourrette S, Guilleminot-Montoya J, Herrero E, Gaymard F, Balk J, et al (2015) Arabidopsis glutaredoxin S17 and its partner, the nuclear factor Y subunit C11/negative cofactor 2a, contribute to maintenance of the shoot apical meristem under long-day photoperiod. Plant Physiol 167: 1643-1658
52. Kumanovics A, Chen OS, Li L, Bagley D, Adkins EM, Lin H, Dingra NN, Outten CE, Keller G, Winge D, Ward DM, Kaplan J (2008) Identification of FRA1 and FRA2 as genes involved in regulating the yeast iron regulon in response to decreased mitochondrial iron-sulfur cluster synthesis. J Biol Chem 283: 10276-10286
53. Law SR, Narsai R, Taylor NL, Delannoy E, Carrie C, Giraud E, Millar AH, Small I, Whelan J (2012) Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol 158: 1610-1627
54. Lee CP, Eubel H, O'Toole N, Millar AH (2008) Heterogeneity of the mi-tochondrial proteome for photosynthetic and non-photosynthetic Arabidopsis metabolism. Mol Cell Proteomics 7: 1297-1316
55. Leferink NGH, van Duijn E, Barendregt A, Heck AJR, van Berkel WJH (2009) Galactonolactone dehydrogenase requires a redox-sensitive thiol for optimal production of vitamin C. Plant Physiol 150: 596-605
56. Leon S, Touraine B, Ribot C, Briat JF, Lobreaux S (2003) Iron-sulphur cluster assembly in plants: distinct NFU proteins in mitochondria and plastids from Arabidopsis thaliana. Biochem J 371: 823-830
57. Lill R, Hoffmann B, Molik S, Pierik AJ, Rietzschel N, Stehling O, Uzarska MA,Webert H,Wilbrecht C,Muhlenhoff U(2012) The role of mitochondria in cellular iron-sulfur protein biogenesis and iron metabolism. Biochim Biophys Acta 1823: 1491-1508
58. Lillig CH, Berndt C, Vergnolle O, Lonn ME, Hudemann C, Bill E, Holmgren A (2005) Characterization of human glutaredoxin 2 as iron-sulfur protein: a possible role as redox sensor. Proc Natl Acad Sci USA 102: 8168-8173
59. Lundberg M, Johansson C, Chandra J, Enoksson M, Jacobsson G, Ljung J, Johansson M, Holmgren A (2001) Cloning and expression of a novel human glutaredoxin (Grx2) with mitochondrial and nuclear isoforms. J Biol Chem 276: 26269-26275
60. MacDougall AJ, ap Rees T (1991) Control of the Krebs Cycle in Arum Spadix. J Plant Phys 131: 683-690
61. Mapolelo DT, Zhang B, Randeniya S, Albetel AN, Li H, Couturier J, Outten CE, Rouhier N, Johnson MK (2013) Monothiol glutaredoxins and A-type proteins: partners in Fe-S cluster trafficking. Dalton Trans 42: 3107-3115
62. Martin P, DeMel S, Shi J, Gladysheva T, Gatti DL, Rosen BP, Edwards BFP (2001) Insights into the structure, solvation, and mechanism of ArsC arsenate reductase, a novel arsenic detoxification enzyme. Structure 9:1071-1081
63. Michelet L, Zaffagnini M, Marchand C, Collin V, Decottignies P, Tsan P, Lancelin JM, Trost P, Miginiac-Maslow M, Noctor G, Lemaire SD (2005) Glutathionylation of chloroplast thioredoxin f is a redox signaling mechanism in plants. Proc Natl Acad Sci USA 102: 16478-16483
64. Miller G, Suzuki N, Rizhsky L, Hegie A, Koussevitzky S, Mittler R (2007) Double mutants deficient in cytosolic and thylakoid ascorbate peroxi-dase reveal a complex mode of interaction between reactive oxygen species, plant development, and response to abiotic stresses. Plant Physiol 144: 1777-1785
65. Miller JR, Busby RW, Jordan SW, Cheek J, Henshaw TF, Ashley GW, Broderick JB, Cronan JE, Jr., Marletta MA (2000) Escherichia coli LipA is a lipoyl synthase: in vitro biosynthesis of lipoylated pyruvate dehy-drogenase complex from octanoyl-acyl carrier protein. Biochemistry 39: 15166-15178
66. Morgan MJ, Lehmann M, Schwarzlander M, Baxter CJ, Sienkiewicz-Porzucek A, Williams TC, Schauer N, Fernie AR, Fricker MD, Ratcliffe RG, Sweetlove LJ, Finkemeier I (2008) Decrease in manganese superoxide dismutase leads to reduced root growth and affects tricar-boxylic acid cycle flux and mitochondrial redox homeostasis. Plant Physiol 147: 101-114
67. Moseler A, Aller I, Wagner S, Nietzel T, Przybyla-Toscano J, Muhlenhoff U, Lill R, Berndt C, Rouhier N, Schwarzlander M, Meyer AJ (2015) The mitochondrial monothiol glutaredoxin S15 is essential for iron-sulfur protein maturation in Arabidopsis thaliana. Proc Natl Acad Sci USA 112: 13735-13740
68. Muhlenhoff U, Molik S, Godoy JR, Uzarska MA, Richter N, Seubert A, Zhang Y, Stubbe J, Pierrel F, Herrero E, Lillig CH, Lill R (2010) Cytosolic monothiol glutaredoxins function in intracellular iron sensing and trafficking via their bound iron-sulfur cluster. Cell Metab 12: 373-385
69. Mukhopadhyay R, Shi J, Rosen BP (2000) Purification and characterization of ACR2p, the Saccharomyces cerevisiae arsenate reductase. J Biol Chem 275: 21149-21157
70. Nikolovski N, Rubtsov D, Segura MP, Miles GP, Stevens TJ, Dunkley TP, Munro S, Lilley KS, Dupree P (2012) Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol 160: 1037-1051
71. Ossowski S, Schwab R, Weigel D (2008) Gene silencing in plants using artificial microRNAs and other small RNAs. Plant J 53: 674-690
72. Palmieri MC, Lindermayr C, Bauwe H, Steinhauser C, Durner J (2010) Regulation of plant glycine decarboxylase by s-nitrosylation and glutathionylation. Plant Physiol 152:1514-1528
73. Pedrajas, J.R., Padilla, C.A., McDonagh, B. Barcena, J.A. (2010). Glutaredoxin participates in the reduction of peroxides by the mitochondrial 1-CYS peroxiredoxin in Saccharomyces cerevisiae. Antioxid Redox Signal 13, 249-258.
74. Peters RA, Sinclair HM, Thompson RHS (1946) An analysis of the inhibition of pyruvate oxidation by arsenicals in relation to the enzyme theory of vesication. Biochem J 40: 516-524
75. Picciocchi A, Saguez C, Boussac A, Cassier-Chauvat C, Chauvat F (2007) CGFS-type monothiol glutaredoxins from the cyanobacterium Syn-echocystis PCC6803 and other evolutionary distant model organisms possess a glutathione-ligated [2Fe-2S] cluster. Biochemistry 46: 1501815026
76. Poor CB, Wegner SV, Li H, Dlouhy AC, Schuermann JP, Sanishvili R, Hinshaw JR, Riggs-Gelasco PJ, Outten CE, He C (2014) Molecular mechanism and structure of the Saccharomyces cerevisiae iron regulator Aft2. Proc Natl Acad Sci USA 111: 4043-4048
77. Pracharoenwattana I, Cornah JE, Smith SM (2005) Arabidopsis peroxi-somal citrate synthase is required for fatty acid respiration and seed germination. Plant Cell 17: 2037-2048
78. Riondet C, Desouris JP, Montoya JG, Chartier Y, Meyer Y, Reichheld JP (2012) A dicotyledon-specific glutaredoxin GRXC1 family with dimer-dependent redox regulation is functionally redundant with GRXC2. Plant Cell Environ 35: 360-373
79. Rodriguez-Manzaneque MT, Tamarit J, Belli G, Ros J, Herrero E (2002) Grx5 is a mitochondrial glutaredoxin required for the activity of iron/sulfur enzymes. Mol Biol Cell 13: 1109-1121
80. Rouault TA (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease. Dis Model Mech 5: 155-164
81. Rouhier N, Gelhaye E, Jacquot JP (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61: 1266-1277
82. Sabar M, Balk J, Leaver CJ (2005) Histochemical staining and quantification of plant mitochondrial respiratory chain complexes using blue-native polyacrylamide gel electrophoresis. Plant J 44: 893-901
83. Schagger H (2006) Tricine-SDS-PAGE. Nat Protoc 1: 16-22 Schmidt-Bleek K, Heiser V, Thieck O, Brennicke A, Grohmann L (1997) The 28.5-kDa iron-sulfur protein of mitochondrial complex I is encoded in the nucleus in plants. Mol Gen Genet 253: 448-454
84. Solheim C, Li L, Hatzopoulos P, Millar AH (2012) Loss of Lon1 in Arabidopsis changes the mitochondrial proteome leading to altered metabolite profiles and growth retardation without an accumulation of oxidative damage. Plant Physiol 160: 1187-1203
85. Stroher E, Millar AH (2012) The biological roles of glutaredoxins. Biochem J 446: 333-348
86. Sundaram S, Rathinasabapathi B, Ma LQ, Rosen BP (2008) An arsenate-activated glutaredoxin from the arsenic hyperaccumulator fern Pteris vittata L. regulates intracellular arsenite. J Biol Chem 283: 6095-6101
87. Sundaram S, Wu S, Ma LQ, Rathinasabapathi B (2009) Expression of a Pteris vittata glutaredoxin PvGRX5 in transgenic Arabidopsis thaliana increases plant arsenic tolerance and decreases arsenic accumulation in the leaves. Plant Cell Environ 32: 851-858
88. Tamarit J, Belli G, Cabiscol E, Herrero E, Ros J (2003) Biochemical characterization of yeast mitochondrial Grx5 monothiol glutaredoxin. J Biol Chem 278: 25745-25751
89. Taylor NL, Day DA, Millar AH (2002) Environmental stress causes oxi-dative damage to plant mitochondria leading to inhibition of glycine decarboxylase. J Biol Chem 277: 42663-42668
90. Taylor NL, Heazlewood JL, Millar AH (2011) The Arabidopsis thaliana 2-D gel mitochondrial proteome: Refining the value of reference maps for assessing protein abundance, contaminants and post-translational modifications. Proteomics 11: 1720-1733
91. Taylor NL, Stroher E, Millar AH (2014) Arabidopsis organelle isolation and characterization. Methods Mol Biol 1062: 551-572
92. Taylor NL, Heazlewood JL, Day DA, Millar AH (2004) Lipoic acid-dependent oxidative catabolism of alpha-keto acids in mitochondria provides evidence for branched-chain amino acid catabolism in Arabi dopsis. Plant Physiol 134: 838-848
93. van der Merwe MJ, Osorio S, Araujo WL, Balbo I, Nunes-Nesi A, Maximova E, Carrari F, Bunik VI, Persson S, Fernie AR (2010) Tri-carboxylic acid cycle activity regulates tomato root growth via effects on secondary cell wall production. Plant Physiol 153: 611-621
94. Winger AM, Taylor NL, Heazlewood JL, Day DA, Millar AH (2007) Identification of intra- and intermolecular disulphide bonding in the plant mitochondrial proteome by diagonal gel electrophoresis. Proteomics 7: 4158-4170
95. Yasuno R, Wada H (1998) Biosynthesis of lipoic acid in Arabidopsis: cloning and characterization of the cDNA for lipoic acid synthase. Plant Physiol 118: 935-943
96. Yasuno R, Wada H (2002) The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana. FEBS Lett 517: 110-114
97. Yoshida K, Noguchi K, Motohashi K, Hisabori T (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54: 875-892
98. Zaffagnini M, Bedhomme M, Lemaire SD, Trost P (2012) The emerging roles of protein glutathionylation in chloroplasts. Plant Sci 185-186: 86-96
99. Zaffagnini M, Michelet L, Massot V, Trost P, Lemaire SD (2008) Biochemical characterization of glutaredoxins from Chlamydomonas rein-hardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem 283: 8868-8876
100. Zaffagnini M, Michelet L, Marchand C, Sparla F, Decottignies P, Le Marechal P, Miginiac-Maslow M, Noctor G, Trost P, Lemaire SD (2007) The thioredoxin-independent isoform of chloroplastic glyceraldehyde-3-phosphate dehydrogenase is selectively regulated by glutathionylation. FEBS J 274: 212-226
101. Zhou X, Li Q, Chen X, Liu J, Zhang Q, Liu Y, Liu K, Xu J (2011) The Arabidopsis RETARDED ROOT GROWTH gene encodes a mitochondria-localized protein that is required for cell division in the root meristem. Plant Physiol 157: 1793-1804
102. Ziemann M, Bhave M, Zachgo S (2009) Origin and diversification of land plant CC-type glutaredoxins. Genome Biol Evol 1: 265-277
103. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q. van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3, e1994