On the Elaborate Network of Thioredoxins in Higher Plants

  • Ina ThormählenEmail author
  • Belén Naranjo
  • José Abraham Trujillo-Hernandez
  • Jean-Philippe Reichheld
  • Francisco Javier Cejudo
  • Peter Geigenberger
Part of the Progress in Botany book series (BOTANY, volume 80)


Thioredoxins represent ubiquitous small proteins acting as redox regulators of diverse metabolic and developmental processes in almost all organisms. These proteins contain highly conserved cysteines in their redox-active sites, which enable the modification of target enzyme conformation and activity by reversible thiol-disulfide exchanges. Since their discovery in plants around 40 years ago, the number of thioredoxin family members as well as the knowledge about their distinct functions are still increasing and under investigation. Originally, the first plant thioredoxin was found in chloroplasts, while further analyses demonstrated additional cytosolic, nuclear, mitochondrial, endomembrane, and non-photosynthetic plastid locations. This chapter provides an overview on the complexity of the thioredoxin family in higher plants and discusses its role in integrating metabolism, stress responses, development, and gene expression. This will help to understand why plants harbor the most versatile thioredoxin system among all organisms.



Atypical cysteine/histidine-rich thioredoxin


Adenosine diphosphate


ADP-glucose pyrophosphorylase


Adenosine monophosphate


Alternative oxidase


AGPase small subunit


Adenosine triphosphate


ATP synthase


Calvin-Benson cycle


Complementary DNA


Chloroplastic drought-induced stress protein


Mg-protoporphyrin methyl transferase


Atypical thioredoxin h with cysteine-x-x-serine active site



Cyt b6f

Cytochrome b6f complex


Deoxyribonucleic acid


Endoplasmic reticulum


Flavin adenine dinucleotide


Fructose 1,6-bisphosphatase




Ferredoxin NADP+ reductase


Ferredoxin thioredoxin reductase




Gossypium barbadense


Green fluorescent protein


Glycine-glycine-leucine-cysteine motif








High-chlorophyll-fluorescence-mutant protein


Histidine-cysteine-glycine-proline-cysteine motif




Locus orchestrating victorin effects protein




Methionine sulfoxide reductase


Nicotinamide adenine dinucleotide phosphate


NADP+-dependent malate dehydrogenase


Non-photochemical quenching


Non-pathogenesis-related protein expressor




NADPH-dependent thioredoxin reductase










Proliferating cell nuclear antigen


Proton gradient regulation complex


Inorganic phosphate


Inorganic pyrophosphate












Pisum sativum


Photosystem II subunit S


Energy- or ΔpH-dependent quenching


Gene of the Rubisco small subunit




Ribonucleic acid


Reactive oxygen species


Ribulose 1,5-bisphosphate carboxylase/oxygenase


Systemic acquired resistance


Sedoheptulose 1,7-bisphosphatase


Succinate dehydrogenase


Peroxidatic cysteine residue


Resolving cysteine residue




Single-stranded DNA binding protein


Tricarboxylic acid




h-type thioredoxins in Brassica napus




Tryptophan-cysteine-glutamic acid-valine-cysteine motif


Tryptophan-cysteine-glycine-proline-cysteine motif


Atypical thioredoxin with tryptophan-cysteine-arginine-lysine-cysteine active site


Tyrosine-phenylalanine motif


  1. Arscott LD, Gromer S, Schirmer RH et al (1997) The mechanism of thioredoxin reductase from human placenta is similar to the mechanisms of lipoamide dehydrogenase and glutathione reductase and is distinct from the mechanism of thioredoxin reductase from Escherichia coli. Proc Natl Acad Sci U S A 94:3621–3626PubMedPubMedCentralCrossRefGoogle Scholar
  2. Arsova B, Hoja U, Wimmelbacher M et al (2010) Plastidial thioredoxin z interacts with two fructokinase-like proteins in a thiol-dependent manner: evidence for an essential role in chloroplast development in Arabidopsis and Nicotiana benthamiana. Plant Cell 22:1498–1515PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ballicora MA, Frueauf JB, Fu Y et al (2000) Activation of the potato tuber ADP-glucose pyrophosphorylase by thioredoxin. J Biol Chem 275:1315–1320PubMedCrossRefGoogle Scholar
  4. Balmer Y, Vensel WH, Tanaka CK et al (2004) Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria. Proc Natl Acad Sci U S A 101:2642–2647PubMedPubMedCentralCrossRefGoogle Scholar
  5. Banze M, Follmann H (2000) Organelle-specific NADPH thioredoxin reductase in plant mitochondria. J Plant Physiol 156:126–129CrossRefGoogle Scholar
  6. Barranco-Medina S, Krell T, Bernier-Villamor L et al (2008) Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF and formation of an ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J Exp Bot 59:3259–3269PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bartsch S, Monnet J, Selbach K, Quigley F, Gray J, von Wettstein D, Reinbothe S, Reinbothe C (2008) Three thioredoxin targets in the inner envelope membrane of chloroplasts function in protein import and chlorophyll metabolism. Proc Natl Acad Sci U S A 105:4933–4938PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bashandy T, Taconnat L, Renou J-P et al (2009) Accumulation of flavonoids in an ntra ntrb mutant leads to tolerance to UV-C. Mol Plant 2:249–258PubMedCrossRefGoogle Scholar
  9. Bashandy T, Guilleminot J, Vernoux T et al (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391PubMedPubMedCentralCrossRefGoogle Scholar
  10. Belin C, Bashandy T, Cela J et al (2015) A comprehensive study of thiol reduction gene expression under stress conditions in Arabidopsis thaliana. Plant Cell Environ 38:299–314PubMedCrossRefGoogle Scholar
  11. Benitez-Alfonso Y, Cilia M, San Roman A et al (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 106:3615–3620PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bernal-Bayard P, Hervas M, Cejudo FJ et al (2012) Electron transfer pathways and dynamics of chloroplast NADPH-dependent thioredoxin reductase C (NTRC). J Biol Chem 287:33865–33872PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bernal-Bayard P, Ojeda V, Hervas M et al (2014) Molecular recognition in the interaction of chloroplast 2-Cys peroxiredoxin with NADPH-thioredoxin reductase C (NTRC) and thioredoxin x. FEBS Lett 588:4342–4347PubMedCrossRefGoogle Scholar
  14. Biteau B, Labarre J, Toledano MB (2003) ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxin. Nature 425:980–984PubMedCrossRefGoogle Scholar
  15. Bohrer A-S, Massot V, Innocenti G et al (2012) New insights into the reduction systems of plastidial thioredoxins point out the unique properties of thioredoxin z from Arabidopsis. J Exp Bot 63:6315–6323PubMedCrossRefGoogle Scholar
  16. Bower MS, Matias DD, Fernandes-Carvalho E (1996) Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 8:1641–1650PubMedPubMedCentralGoogle Scholar
  17. Breazale VD, Buchanan BB, Wolosiuk RA (1978) Chloroplast sedoheptulose 1,7-bisphosphatase: evidence for regulation by the ferredoxin/thioredoxin system. Z Naturforsch 33c:521–528CrossRefGoogle Scholar
  18. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341–374CrossRefGoogle Scholar
  19. Cabrillac D, Cock JM, Dumas C et al (2001) The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410:220–223PubMedCrossRefGoogle Scholar
  20. Calderón A, Ortiz-Espín A, Iglesias-Fernández R et al (2017) Thioredoxin (Trxo1) interacts with proliferating cell nuclear antigen (PCNA) and its overexpression affects the growth of tobacco cell culture. Redox Biol 11:688–700PubMedPubMedCentralCrossRefGoogle Scholar
  21. Carrillo LR, Froehlich JE, Cruz JA et al (2016) Multi-level regulation of the chloroplast ATP synthase: the chloroplast NADPH thioredoxin reductase C (NTRC) is required for redox modulation specifically under low irradiance. Plant J 87:654–663PubMedCrossRefGoogle Scholar
  22. Cejudo FJ, Ferrandez J, Cano B et al (2012) The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signalling. FEBS Lett 586:2974–2980PubMedCrossRefGoogle Scholar
  23. Chae HB, Moon JC, Shin MR et al (2013) Thioredoxin reductase type C (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function. Mol Plant 6:323–336PubMedCrossRefGoogle Scholar
  24. Chibani K, Tarrago L, Schürmann P et al (2011) Biochemical properties of poplar thioredoxin z. FEBS Lett 585:1077–1081PubMedCrossRefGoogle Scholar
  25. Collin V, Issakidis-Bourguet E, Marchand C et al (2003) The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity. J Biol Chem 278:23747–23752PubMedCrossRefGoogle Scholar
  26. Collin V, Lamkemeyer P, Miginiac-Maslow M et al (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type. Plant Physiol 136:4088–4095PubMedPubMedCentralCrossRefGoogle Scholar
  27. Courteille A, Vesa S, Sanz-Barrio R et al (2013) Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol 161:508–520PubMedCrossRefGoogle Scholar
  28. Da Q, Wang P, Wang M et al (2017) Thioredoxin and NADPH-dependent thioredoxin reductase C regulation of tetrapyrrole biosynthesis. Plant Physiol 175:652–666PubMedPubMedCentralGoogle Scholar
  29. Daloso DM, Müller K, Obata T et al (2015) Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Natl Acad Sci U S A 112:E1392–E1400PubMedPubMedCentralCrossRefGoogle Scholar
  30. Dangoor I, Peled-Zehavi H, Levitan A et al (2009) A small family of chloroplast atypical thioredoxins. Plant Physiol 149:1240–1250PubMedPubMedCentralCrossRefGoogle Scholar
  31. Eliyahu E, Rog I, Inbal D et al (2015) ACHT4-driven oxidation of APS1 attenuates starch synthesis under low light intensity in Arabidopsis plants. Proc Natl Acad Sci U S A 112:12876–12881PubMedPubMedCentralCrossRefGoogle Scholar
  32. Entus R, Poling M, Herrmann KM (2002) Redox regulation of Arabidopsis 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase. Plant Physiol 129:1866–1871PubMedPubMedCentralCrossRefGoogle Scholar
  33. Geigenberger P, Fernie A (2014) Metabolic control of redox and redox control of metabolism in plants. Antioxid Redox Signal 21:1389–1421PubMedPubMedCentralCrossRefGoogle Scholar
  34. Geigenberger P, Kolbe A, Tiessen A (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 56:1469–1479PubMedCrossRefGoogle Scholar
  35. Geigenberger P, Thormählen I, Daloso DM et al (2017) The unprecedented versatility of the plant thioredoxin system. Trends Plant Sci 22:249–262PubMedCrossRefGoogle Scholar
  36. Gelhaye E, Rouhier N, Jacquot JP (2003) Evidence for a subgroup of thioredoxin h that requires GSH/Grx for its reduction. FEBS Lett 555:443–448PubMedCrossRefGoogle Scholar
  37. Gelhaye E, Rouhier N, Gérard J et al (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci U S A 101:14545–14550PubMedPubMedCentralCrossRefGoogle Scholar
  38. Gould SB, Waller RF, McFadden GI (2008) Plastid evolution. Annu Rev Plant Biol 59:491–517PubMedCrossRefGoogle Scholar
  39. Hertle AP, Blunder T, Wunder T et al (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49:511–523PubMedCrossRefGoogle Scholar
  40. Huang J, Niazi AK, Young D et al (2017) Self-protection of Arabidopsis cytosolic malate dehydrogenase against oxidative stress. J Exp Bot.
  41. Ikegami A, Yoshimura N, Motohashi K et al (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 282:19282–19291PubMedCrossRefGoogle Scholar
  42. Ishiga Y, Ishiga T, Wangdi T et al (2012) NTRC and chloroplast-generated reactive oxygen species regulate Pseudomonas syringae pv. tomato disease development in tomato and Arabidopsis. Mol Plant-Microbe Interact 25:294–306PubMedCrossRefGoogle Scholar
  43. Ishiga Y, Ishiga T, Ikeda Y et al (2016) NADPH-dependent thioredoxin reductase C plays a role in nonhost disease resistance against Pseudomonas syringae pathogens by regulating chloroplast-generated reactive oxygen species. Peer J 4:e1938PubMedCrossRefGoogle Scholar
  44. Ivanov R, Gaude T (2009) Endocytosis and endosomal regulation of the S-receptor kinase during the self-incompatibility response in Brassica oleracea. Plant Cell 21:2107–2117PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jacquot JP, Rivera-Madrid R, Marinho P et al (1994) Arabidopsis thaliana NAPHP thioredoxin reductase. cDNA characterization and expression of the recombinant protein in Escherichia coli. J Mol Biol 235:1357–1363PubMedCrossRefGoogle Scholar
  46. Juárez-Díaz JA, McClure B, Vázquez-Santana S et al (2006) A novel thioredoxin h is secreted in Nicotiana alata and reduces S-RNase in vitro. J Biol Chem 281:3418–3424PubMedCrossRefGoogle Scholar
  47. Kirchsteiger K, Pulido P, Gonzalez M et al (2009) NADPH thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in Arabidopsis thaliana. Mol Plant 2:298–307PubMedCrossRefGoogle Scholar
  48. Kirchsteiger K, Ferrandez J, Pascual MB et al (2012) NADPH thioredoxin reductase C is localized in plastids of photosynthetic and nonphotosynthetic tissues and is involved in lateral root formation in Arabidopsis. Plant Cell 24:1534–1548PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kneeshaw S, Gelineau S, Tada Y et al (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162PubMedCrossRefGoogle Scholar
  50. Kneeshaw S, Keyani R, Delorme-Hinoux V et al (2017) Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes. Proc Natl Acad Sci U S A 114:8414–8419PubMedCentralCrossRefGoogle Scholar
  51. Koh CS, Navrot N, Didierjean C et al (2008) An atypical catalytic mechanism involving three cysteines of thioredoxin. J Biol Chem 283:23062–23072PubMedCrossRefGoogle Scholar
  52. Konrad A, Banze M, Follmann H (1996) Mitochondria of plant leaves contain two thioredoxins. Completion of the thioredoxin profile of higher plants. J Plant Physiol 149:317–321CrossRefGoogle Scholar
  53. Laloi C, Rayapuram N, Chartier Y et al (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci U S A 98:14144–14149PubMedPubMedCentralCrossRefGoogle Scholar
  54. Laloi C, Mestres-ortega D, Marco Y et al (2004) The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-box-mediated response to pathogen elicitor. Plant Physiol 134:1006–1016PubMedPubMedCentralCrossRefGoogle Scholar
  55. Laughner BJ, Sehnke PC, Ferl RJ (1998) A novel nuclear member of the thioredoxin superfamily. Plant Physiol 118:987–996PubMedPubMedCentralCrossRefGoogle Scholar
  56. Laugier E, Tarrago L, Courteille A et al (2013) Involvement of thioredoxin y2 in the preservation of leaf methionine sulfoxide reductase capacity and growth under high light. Plant Cell Environ 36:670–682PubMedCrossRefGoogle Scholar
  57. Lee JR, Lee SS, Jang HH et al (2009) Heat-shock dependent oligomeric status alters the function of a plant-specific thioredoxin-like protein, AtTDX. Proc Natl Acad Sci U S A 106:5978–5983PubMedPubMedCentralCrossRefGoogle Scholar
  58. Lemaire SD, Michelet L, Zaffagnini M et al (2007) Thioredoxins in chloroplasts. Curr Genet 51:343–365PubMedCrossRefGoogle Scholar
  59. Lennartz K, Plücken H, Seidler A et al (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b6f complex in Arabidopsis. Plant Cell 13:2539–2551PubMedPubMedCentralGoogle Scholar
  60. Lepistö A, Kangasjarvi S, Luomala EM et al (2009) Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 149:1261–1276PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lepistö A, Pakula E, Toivola J et al (2013) Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods. J Exp Bot 64:3843–3854PubMedPubMedCentralCrossRefGoogle Scholar
  62. Li X, Nield J, Hayman D et al (1996) A self-fertile mutant of Phalaris produces an S protein with reduced thioredoxin activity. Plant J 10:505–513PubMedCrossRefGoogle Scholar
  63. Li YB, Han LB, Wang HY et al (2016) The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiol 170:2392–2406PubMedPubMedCentralCrossRefGoogle Scholar
  64. Lichter A, Häberlein I (1998) A light-dependent redox signal participates in the regulation of ammonia fixation in chloroplasts of higher plants – ferredoxin: glutamate synthase is a thioredoxin-dependent enzyme. J Plant Physiol 153:83–90CrossRefGoogle Scholar
  65. Lorang J, Kidarsa T, Bradford CS et al (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science 338:659–662PubMedPubMedCentralCrossRefGoogle Scholar
  66. Luo T, Fan T, Liu Y et al (2012) Thioredoxin redox regulates ATPase activity of magnesium chelatase CHLI subunit and modulates redox-mediated signaling in tetrapyrrole biosynthesis and homeostasis of reactive oxygen species in pea plants. Plant Physiol 159:118–130PubMedPubMedCentralCrossRefGoogle Scholar
  67. Machida T, Ishibashi A, Kirino A et al (2012) Chloroplast NADPH-dependent thioredoxin reductase from Chlorella vulgaris alleviates environmental stresses in yeast together with 2-Cys peroxiredoxin. PLoS One 7:e45988PubMedPubMedCentralCrossRefGoogle Scholar
  68. Marchal C, Delorme-Hinoux V, Bariat L et al (2014) NTR/NRX define a new thioredoxin system in the nucleus of Arabidopsis thaliana cells. Mol Plant 7:30–44PubMedCrossRefGoogle Scholar
  69. Marchand CH, Vanacker H, Collin V et al (2010) Thioredoxin targets in Arabidopsis roots. Proteomics 10:2418–2428PubMedCrossRefGoogle Scholar
  70. Marri L, Zaffagnini M, Collin V et al (2009) Prompt and easy activation by specific thioredoxins of calvin cycle enzymes of Arabidopsis thaliana associated in the GAPDH/CP12/PRK supramolecular complex. Mol Plant 2:259–269PubMedCrossRefGoogle Scholar
  71. Martí MC, Olmos E, Calvete JJ et al (2009) Mitochondrial and nuclear localization of a novel pea thioredoxin: identification of its mitochondrial target proteins. Plant Physiol 150:646–657PubMedPubMedCentralCrossRefGoogle Scholar
  72. Marty L, Siala W, Schwarzländer M et al (2009) The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis. Proc Natl Acad Sci U S A 106:9109–9114PubMedPubMedCentralCrossRefGoogle Scholar
  73. McKinney DW, Buchanan BB, Wolosiuk RA (1978) Activation of chloroplast ATPase by reduced thioredoxin. Phytochemistry 17:794–795CrossRefGoogle Scholar
  74. Meng L, Wong JH, Feldman LJ et al (2010) A membrane-associated thioredoxin required for plant growth moves from cell to cell, suggestive of a role in intercellular communication. Proc Natl Acad Sci U S A 107:3900–3905PubMedPubMedCentralCrossRefGoogle Scholar
  75. Meyer Y, Reichheld J-P, Vignols F (2005) Thioredoxins in Arabidopsis and other plants. Photosynth Res 86:419–433PubMedCrossRefGoogle Scholar
  76. Meyer Y, Riondet C, Constans L et al (2006) Evolution of redoxin genes in the green lineage. Photosynth Res 89:179–192PubMedCrossRefGoogle Scholar
  77. Meyer Y, Belin C, Delorme-Hinoux V et al (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160PubMedCrossRefGoogle Scholar
  78. Michalska J, Zauber H, Buchanan BB et al (2009) NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci U S A 106:9908–9913PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mikkelsen R, Mutenda KE, Mant A et al (2005) α-Glucan, water dikinase (GWD): a plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci U S A 102:1785–1790PubMedPubMedCentralCrossRefGoogle Scholar
  80. Moon JC, Jang HH, Chae HB et al (2006) The C-type Arabidopsis thioredoxin reductase ANTR-C acts as an electron donor to 2-Cys peroxiredoxins in chloroplasts. Biochem Biophys Res Commun 348:478–484PubMedCrossRefGoogle Scholar
  81. Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281:35039–35047PubMedCrossRefGoogle Scholar
  82. Najera VA, Gonzalez MC, Perez-Ruiz JM et al (2017) An event of alternative splicing affects the expression of the NTRC gene, encoding NADPH-thioredoxin reductase C, in seed plants. Plant Sci 258:21–28PubMedCrossRefGoogle Scholar
  83. Naranjo B, Diaz-Espejo A, Lindahl M et al (2016a) Type-f thioredoxins have a role in the short-term activation of carbon metabolism and their loss affects growth under short-day conditions in Arabidopsis thaliana. J Exp Bot 67:1951–1964PubMedPubMedCentralCrossRefGoogle Scholar
  84. Naranjo B, Mignee C, Krieger-Liszkay A et al (2016b) The chloroplast NADPH thioredoxin reductase C, NTRC, controls non-photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis. Plant Cell Environ 39:804–822PubMedCrossRefGoogle Scholar
  85. Navrot N, Collin V, Gualberto J et al (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379PubMedPubMedCentralCrossRefGoogle Scholar
  86. Née G, Zaffagnini M, Trost P et al (2009) Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett 583:2827–2832PubMedCrossRefGoogle Scholar
  87. Nikkanen L, Toivola J, Rintamäki E (2016) Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis. Plant Cell Environ 39:804–822CrossRefGoogle Scholar
  88. Ojeda V, Perez-Ruiz JM, Gonzalez MC et al (2017) NADPH thioredoxin reductase C and thioredoxins act concertedly in seedling development. Plant Physiol 174:1436–1448PubMedPubMedCentralCrossRefGoogle Scholar
  89. Okegawa Y, Motohashi K (2015) Chloroplastic thioredoxin m functions as a major regulator of Calvin cycle enzymes during photosynthesis in vivo. Plant J 84:900–913PubMedCrossRefGoogle Scholar
  90. Park SK, Jung YJ, Lee JR et al (2009) Heat-shock and redox-dependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone. Plant Physiol 150:552–561PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pascual MB, Mata-Cabana A, Florencio FJ et al (2010) Overoxidation of 2-Cys peroxiredoxin in prokaryotes: cyanobacterial 2-Cys peroxiredoxins sensitive to oxidative stress. J Biol Chem 285:34485–34492PubMedPubMedCentralCrossRefGoogle Scholar
  92. Pascual MB, Mata-Cabana A, Florencio FJ et al (2011) A comparative analysis of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system from plants and cyanobacteria. Plant Physiol 155:1806–1816PubMedPubMedCentralCrossRefGoogle Scholar
  93. Perez-Ruiz JM, Cejudo FJ (2009) A proposed reaction mechanism for rice NADPH thioredoxin reductase C, an enzyme with protein disulfide reductase activity. FEBS Lett 583:1399–1402PubMedCrossRefGoogle Scholar
  94. Perez-Ruiz JM, Spinola MC, Kirchsteiger K et al (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18:2356–2368PubMedPubMedCentralCrossRefGoogle Scholar
  95. Perez-Ruiz JM, Guinea M, Puerto-Galan L et al (2014) NADPH thioredoxin reductase C is involved in redox regulation of the Mg-chelatase I subunit in Arabidopsis thaliana chloroplasts. Mol Plant 7:1252–1255PubMedCrossRefGoogle Scholar
  96. Perez-Ruiz JM, Naranjo B, Ojeda V et al (2017) NTRC-dependent redox balance of 2-Cys peroxiredoxins is needed for optimal function of the photosynthetic apparatus. Proc Natl Acad Sci U S A 114:12069–12074PubMedPubMedCentralCrossRefGoogle Scholar
  97. Perkins A, Nelson KJ, Parsonage D et al (2015) Peroxiredoxins: guardians against oxidative stress and modulators of peroxide signaling. Trends Biochem Sci 40:435–445PubMedPubMedCentralCrossRefGoogle Scholar
  98. Puerto-Galan L, Perez-Ruiz JM, Ferrandez J et al (2013) Overoxidation of chloroplast 2-Cys peroxiredoxins: balancing toxic and signaling activities of hydrogen peroxide. Front Plant Sci 4:310PubMedPubMedCentralCrossRefGoogle Scholar
  99. Puerto-Galan L, Perez-Ruiz JM, Guinea M et al (2015) The contribution of NADPH thioredoxin reductase C (NTRC) and sulfiredoxin to 2-Cys peroxiredoxin overoxidation in Arabidopsis thaliana chloroplasts. J Exp Bot 66:2957–2966PubMedPubMedCentralCrossRefGoogle Scholar
  100. Pulido P, Cazalis R, Cejudo FJ (2009) An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. Plant J 57:132–145PubMedCrossRefGoogle Scholar
  101. Pulido P, Spinola MC, Kirchsteiger K et al (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J Exp Bot 61:4043–4054PubMedPubMedCentralCrossRefGoogle Scholar
  102. Qin Y, Leydon AR, Manziello A et al (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 8:e1000621CrossRefGoogle Scholar
  103. Reichheld J-P, Mestres-Ortega D, Laloi C et al (2002) The multigenic family of thioredoxin h in Arabidopsis thaliana: specific expression and stress response. Plant Physiol Biochem 40:685–690CrossRefGoogle Scholar
  104. Reichheld J-P, Meyer E, Khafif M et al (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 579:337–342PubMedCrossRefGoogle Scholar
  105. Reichheld J-P, Khafif M, Riondet C et al (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19:1851–1865PubMedPubMedCentralCrossRefGoogle Scholar
  106. Rey P, Pruvot G, Becuwe N et al (1998) A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J 13:97–107PubMedCrossRefGoogle Scholar
  107. Rey P, Cuine S, Eymery F et al (2005) Analysis of the proteins targeted by CDSP32, a plastidic thioredoxin participating in oxidative stress responses. Plant J 41:31–42PubMedCrossRefGoogle Scholar
  108. Richter AS, Peter E, Rothbart M et al (2013) Posttranslational influence of NADPH-dependent thioredoxin reductase C on enzymes in tetrapyrrole synthesis. Plant Physiol 162:63–73PubMedPubMedCentralCrossRefGoogle Scholar
  109. Rivera-Madrid R, Mestres D, Marinho P et al (1995) Evidence for five divergent thioredoxin h sequences in Arabidopsis thaliana. Proc Natl Acad Sci U S A 92:5620–5624PubMedPubMedCentralCrossRefGoogle Scholar
  110. Sahrawy M, Hecht V, Lopez-Jaramillo J et al (1996) Intron position as an evolutionary marker of thioredoxins and thioredoxin domains. J Mol Evol 42:422–431PubMedCrossRefGoogle Scholar
  111. Sanchez-Riego AM, Mata-Cabana A, Galmozzi CV et al (2016) NADPH-thioredoxin reductase C mediates the response to oxidative stress and thermotolerance in the cyanobacterium Anabaena sp. PCC7120. Front Microbiol 7:1283PubMedPubMedCentralCrossRefGoogle Scholar
  112. Sanz-Barrio R, Corral-Martinez P, Ancin M et al (2013) Overexpression of plastidial thioredoxin f leads to enhanced starch accumulation in tobacco leaves. Plant Biotechnol J 11:618–627PubMedCrossRefGoogle Scholar
  113. Sarkar N, Lemaire S, Wu-Scharf D et al (2005) Functional specialization of Chlamydomonas reinhardtii cytosolic thioredoxin h1 in the response to alkylation induced DNA damage. Eukaryot Cell 4:262–273PubMedPubMedCentralCrossRefGoogle Scholar
  114. Sasaki Y, Kozaki A, Hatano M (1997) Link between light and fatty acid synthesis: thioredoxin-linked reductive activation of plastidic acetyl-CoA carboxylase. Proc Natl Acad Sci U S A 94:11096–11101PubMedPubMedCentralCrossRefGoogle Scholar
  115. Scheibe R, Anderson LE (1981) Dark modulation of NADP-dependent malate dehydrogenase and glucose-6-phosphate dehydrogenase in the chloroplast. Biochim Biophys Acta 636:58–64PubMedCrossRefGoogle Scholar
  116. Schmidtmann E, König AC, Orwat A et al (2014) Redox regulation of Arabidopsis mitochondrial citrate synthase. Mol Plant 7:156–169PubMedCrossRefGoogle Scholar
  117. Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1274PubMedCrossRefGoogle Scholar
  118. Serrato AJ, Cejudo FJ (2003) Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217:392–399PubMedCrossRefGoogle Scholar
  119. Serrato AJ, Crespo JL, Florencio FJ et al (2001) Characterization of two thioredoxins h with predominant localization in the nucleus of aleurone and scutellum cells of germinating wheat seeds. Plant Mol Biol 46:361–371PubMedCrossRefGoogle Scholar
  120. Serrato AJ, Perez-Ruiz JM, Cejudo FJ (2002) Cloning of thioredoxin h reductase and characterization of the thioredoxin reductase-thioredoxin h system from wheat. Biochem J 367:491–497PubMedPubMedCentralCrossRefGoogle Scholar
  121. Serrato AJ, Perez-Ruiz JM, Spinola MC et al (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279:43821–43827PubMedCrossRefGoogle Scholar
  122. Serrato AJ, Guilleminot J, Meyer Y et al (2008) AtCXXS: atypical members of the Arabidopsis thaliana thioredoxin h family with a remarkably high disulfide isomerase activity. Physiol Plant 133:611–622PubMedCrossRefGoogle Scholar
  123. Seung D, Thalmann M, Sparla F et al (2013) Arabidopsis thaliana AMY3 is a unique redox-regulated chloroplastic α-amylase. J Biol Chem 288:33620–33633PubMedPubMedCentralCrossRefGoogle Scholar
  124. Silver DM, Silva LP, Issakidis-Bourguet E et al (2013) Insight into the redox regulation of the phosphoglucan phosphatase SEX4 involved in starch degradation. FEBS J 280:538–548PubMedCrossRefGoogle Scholar
  125. Skryhan K, Cuesta-Seijo JA, Nielsen MM et al (2015) The role of cysteine residues in redox regulation and protein stability of Arabidopsis thaliana starch synthase 1. PLoS One 10:e0136997PubMedPubMedCentralCrossRefGoogle Scholar
  126. Sparla F, Costa A, Lo Schiavo F et al (2006) Redox regulation of a novel plastid-targeted beta-amylase of Arabidopsis. Plant Physiol 141:840–850PubMedPubMedCentralCrossRefGoogle Scholar
  127. Sweat TA, Wolpert TJ (2007) Thioredoxin h5 is required for victorin sensitivity mediated by a CC-NBS-LRR gene in Arabidopsis. Plant Cell 19:673–687PubMedPubMedCentralCrossRefGoogle Scholar
  128. Tada Y, Spoel SH, Pajerowska-Mukhtar K et al (2008) Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–956PubMedCrossRefGoogle Scholar
  129. Tarrago L, Laugier E, Zaffagnini M et al (2010) Plant thioredoxin CDSP32 regenerates 1-Cys methionine sulfoxide reductase B activity through the direct reduction of sulfenic acid. J Biol Chem 285:14964–14972PubMedPubMedCentralCrossRefGoogle Scholar
  130. Thormählen I, Ruber J, von Roepenack-Lahaye E et al (2013) Inactivation of thioredoxin f1 leads to decreased light activation of ADP-glucose pyrophosphorylase and altered diurnal starch turnover in leaves of Arabidopsis thaliana. Plant Cell Environ 36:16–29PubMedCrossRefGoogle Scholar
  131. Thormählen I, Meitzel T, Groysman J et al (2015) Thioredoxin f1 and NADPH-dependent thioredoxin reductase C have overlapping functions in regulating photosynthetic metabolism and plant growth in response to varying light conditions. Plant Physiol 169:1766–1786PubMedPubMedCentralGoogle Scholar
  132. Thormählen I, Zupok A, Rescher J et al (2017) Thioredoxins play a crucial role in dynamic acclimation of photosynthesis in fluctuating light. Mol Plant 10:168–182PubMedCrossRefGoogle Scholar
  133. Toivola J, Nikkanen L, Dahlstrom KM et al (2013) Overexpression of chloroplast NADPH-dependent thioredoxin reductase in Arabidopsis enhances leaf growth and elucidates in vivo function of reductase and thioredoxin domains. Front Plant Sci 4:389PubMedPubMedCentralCrossRefGoogle Scholar
  134. Traverso JA, Micalella C, Martinez A et al (2013) Roles of N-terminal fatty acid acylations in membrane compartment partitioning: Arabidopsis h-type thioredoxins as a case study. Plant Cell 25:1056–1077PubMedPubMedCentralCrossRefGoogle Scholar
  135. Valerio C, Costa A, Marri L et al (2011) Thioredoxin-regulated β-amylase (BAM1) triggers diurnal starch degradation in guard cells, and in mesophyll cells under osmotic stress. J Exp Bot 62:545–555PubMedCrossRefGoogle Scholar
  136. Vieira Dos Santos C, Laugier E, Tarrago L et al (2007) Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett 581:4371–4376PubMedCrossRefGoogle Scholar
  137. Vignols F, Mouaheb N, Thomas D et al (2003) Redox control of Hsp70-Co-chaperone interaction revealed by expression of a thioredoxin-like Arabidopsis protein. J Biol Chem 278:4516–4523PubMedCrossRefGoogle Scholar
  138. Wang P, Liu J, Liu B et al (2013) Evidence for a role of chloroplastic m-type thioredoxins in the biogenesis of photosystem II in Arabidopsis. Plant Physiol 163:1710–1728PubMedPubMedCentralCrossRefGoogle Scholar
  139. Williams CH, Arscott LD, Muller S et al (2000) Thioredoxin reductase two modes of catalysis have evolved. Eur J Biochem 267:6110–6117PubMedCrossRefGoogle Scholar
  140. Wimmelbacher M, Börnke F (2014) Redox activity of thioredoxin z and fructokinase-like protein 1 is dispensable for autotrophic growth of Arabidopsis thaliana. J Exp Bot 65:2405–2413PubMedPubMedCentralCrossRefGoogle Scholar
  141. Wolosiuk RA, Buchanan BB (1977) Thioredoxin and glutathione regulate photosynthesis in chloroplasts. Nature 266:565–567CrossRefGoogle Scholar
  142. Wolosiuk RA, Buchanan BB, Crawford NA (1977) Regulation of NADP-malate dehydrogenase by the light-actuated ferredoxin/thioredoxin system of chloroplasts. FEBS Lett 81:253–258CrossRefGoogle Scholar
  143. Wood ZA, Poole LB, Karplus PA (2003) Peroxiredoxin evolution and the regulation of hydrogen peroxide signaling. Science 300:650–653PubMedCrossRefGoogle Scholar
  144. Wulff RP, Lundqvist J, Rutsdottir G et al (2011) The activity of barley NADPH-dependent thioredoxin reductase C is independent of the oligomeric state of the protein: tetrameric structure determined by cryo-electron microscopy. Biochemist 50:3713–3723CrossRefGoogle Scholar
  145. Yamamoto M, Nasrallah JB (2009) In planta assessment of the role of thioredoxin h proteins in the regulation of S-locus receptor kinase signaling in transgenic Arabidopsis. Plant Physiol 163:1387–1395CrossRefGoogle Scholar
  146. Yamaryo Y, Motohashi K, Takamiya K et al (2006) In vitro reconstitution of monogalactosyldiacylglycerol (MGDG) synthase regulation by thioredoxin. FEBS Lett 580:4086–4090PubMedCrossRefGoogle Scholar
  147. Yoshida K, Hisabori T (2014) Mitochondrial isocitrate dehydrogenase is inactivated upon oxidation and reactivated by thioredoxin-dependent reduction in Arabidopsis. Front Environ Sci 2:38CrossRefGoogle Scholar
  148. Yoshida K, Hisabori T (2016a) Adenine nucleotide-dependent and redox-independent control of mitochondrial malate dehydrogenase activity in Arabidopsis thaliana. Biochim Biophys Acta 1857:810–818PubMedCrossRefGoogle Scholar
  149. Yoshida K, Hisabori T (2016b) Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability. Proc Natl Acad Sci U S A 113:E3967–E3976PubMedPubMedCentralCrossRefGoogle Scholar
  150. Yoshida K, Noguchi K, Motohashi K et al (2013) Systematic exploration of thioredoxin target proteins in plant mitochondria. Plant Cell Physiol 54:875–892PubMedCrossRefGoogle Scholar
  151. Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts. J Biol Chem 290:14278–14288PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Ina Thormählen
    • 1
    Email author
  • Belén Naranjo
    • 2
  • José Abraham Trujillo-Hernandez
    • 3
    • 4
  • Jean-Philippe Reichheld
    • 3
    • 4
  • Francisco Javier Cejudo
    • 5
  • Peter Geigenberger
    • 1
  1. 1.Fakultät für Biologie – PflanzenmetabolismusLudwig-Maximilians-Universität MünchenMunichGermany
  2. 2.Fakultät für Biologie – Molekularbiologie der PflanzenLudwig-Maximilians-Universität MünchenMunichGermany
  3. 3.Laboratoire Génome et Développement des PlantesUniversité de Perpignan Via DomitiaPerpignanFrance
  4. 4.Laboratoire Génome et Développement des PlantesCentre National de la Recherche ScientifiqueParisFrance
  5. 5.Instituto de Bioquímica Vegetal y FotosíntesisUniversidad de Sevilla and CSICSevillaSpain

Personalised recommendations