Skip to main content

Redox Protein Thioredoxins: Function Under Salinity, Drought and Extreme Temperature Conditions

  • Chapter
  • First Online:
Antioxidants and Antioxidant Enzymes in Higher Plants

Abstract

Salinity, drought and extreme temperatures are environmental constraints that seriously alter plant growth and productivity. Oxidative and nitrosative stress are associated with these conditions and redox regulation is emerging as a key factor in the response of plants to such adverse environments. Thioredoxins (Trxs) are ubiquitous proteins present in the different cell compartments that control the structure and function of target proteins by reducing disulfide bridges in their redox active sites. The involvement of Trxs in the response of plants to abiotic stress is a subject of increasing interest due to the diverse target proteins that they regulate. In this chapter, we will first analyze the importance of salinity, drought and extreme temperatures as abiotic stress conditions in plant physiology. Furthermore, we provide information about the transcriptomic, genomic and enzymatic changes related to Trxs taking place under these adverse conditions, together with those observed in their protein targets. In this chapter we seek to unravel the specific roles of Trxs as redox sensors and their involvement in the ROS/RNS-mediated signal transduction.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 99.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 129.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aalen RB (1999) Peroxiredoxin antioxidants in seed physiology. Seed Sci Res 9:285–295

    Article  CAS  Google Scholar 

  • Abid G, Muhovski Y, Mingeot D, Watillon B, Toussaint A, Mergeai G, M’hamdi M, Sassi K, Jebara M (2015) Identification and characterization of drought stress responsive genes in faba bean (Vicia faba L.) by suppression subtractive hybridization. Plant Cell Tissue Organ Cult 121:367–379

    Article  CAS  Google Scholar 

  • Acosta-Motos JR, Diaz-Vivancos P, Álvarez S, Fernández-García N, Sanchez-Blanco MJ, Hernández JA (2015) Physiological and biochemical mechanisms of the ornamental Eugenia myrtifolia L. plants for coping with NaCl stress and recovery. Planta 242:829–846

    Article  CAS  PubMed  Google Scholar 

  • Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295

    Article  CAS  PubMed  Google Scholar 

  • Alkhalfioui F, Renard M, Vensel WH, Wong J, Tanaka CK, Hurkman WJ, Buchanan BB, Montrichard F (2007) Thioredoxin-linked proteins are reduced during germination of Medicago truncatula seeds. Plant Physiol 44:1559–1579

    Article  CAS  Google Scholar 

  • Alkhalfioui F, Renard M, Frendo P, Keichinger C, Meyer Y, Gelhaye E, Hirasawa M, Knaff DB, Ritzenthaler C, Montrichard FX (2008) A novel type of thioredoxin dedicated to symbiosis in legumes. Plant Physiol 148:424–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399

    Article  CAS  Google Scholar 

  • Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Kubiś J (2009) Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Sci 77:682–690

    Article  CAS  Google Scholar 

  • Arsova B, Hoja U, Wimmelbacher M, Greiner E, Ustun S, Melzer M, Petersen K, Lein W, Bornke F (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 Online 22:1498–1515

    Article  CAS  Google Scholar 

  • Asada K (1999) The WATER-WATER CYCLE IN CHLOROPLASTS: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  CAS  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 41:391–396

    Article  CAS  Google Scholar 

  • Atkin OK, Macherel D (2009) The crucial role of plant mitochondria in orchestrating drought tolerance. Annl Bot 103:581–597

    Article  CAS  Google Scholar 

  • Balsera M, Goetze TA, Kovács-Bogdán E, Schürmann P, Wagner R, Buchanan BB, Soll J, Bölter B (2009) Characterization of Tic110, a channel-forming protein at the inner envelope membrane of chloroplasts, unveils a response to Ca2+ and a stromal regulatory disulfide bridge. J Biol Chem 284:2603–2616

    Article  CAS  PubMed  Google Scholar 

  • Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barranco-Medina S, Krell T, Finkemeier I, Sevilla F, Lázaro JJ, Dietz KJ (2007) Biochemical and molecular characterization of the mitochondrial peroxiredoxin PsPrxIIF from Pisum sativum. Plant Physiol Biochem 45:729–739

    Article  CAS  PubMed  Google Scholar 

  • Barranco-Medina S, Krell T, Bernier-Villamor L, Sevilla F, Lázaro JJ, Dietz KJ (2008) Hexameric oligomerization of mitochondrial peroxiredoxin PrxIIF and formation of an ultrahigh affinity complex with its electron donor thioredoxin Trx-o. J Exp Bot 9:3259–3269

    Article  CAS  Google Scholar 

  • 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 105:4933–4938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D, Buchanan BB (2009) Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci U S A 106:3615–3620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biehler K, Fock H (1996) Evidence for the contribution of the Mehler-Peroxidase reaction in dissipating excess electrons indDrought-stressed wheat. Plant Physiol 11:265–272

    Article  Google Scholar 

  • Bogeat-Triboulot MB, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Altman A (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 143:876–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boo YC, Jung J (1999) Water deficit-induced oxidative stress and antioxidative defenses in rice plants. J Plant Physiol 155:255–261

    Article  CAS  Google Scholar 

  • Broin M, Rey P (2003) Potato plants lacking the CDSP32 plastidic thioredoxin exhibit overoxidation of the BAS1 2-Cysteine peroxiredoxin and increased lipid peroxidation in thylakoids under photooxidative stress. Plant Physiol 132:1335–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broin M, Cuiné S, Eymery F, Rey P (2002) The Plastidic 2-Cysteine peroxiredoxin is a target for a thioredoxin involved in the protection of the photosynthetic apparatus against oxidative damage. Plant Cell 14:1417–1432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buchanan BB (1980) Role of light in the regulation of chloroplast enzyme. Anu Rev Plant Physiol 198:341–374

    Article  Google Scholar 

  • Calderón A, Lázaro-Payo A, Iglesias-Baena I, Camejo D, Lázaro JJ, Sevilla F, Jiménez A (2017a) Glutathionylation of pea chloroplast 2-Cys Prx and mitochondrial PrxIIF affects their structure and peroxidase activity and sulfiredoxin deglutathionylates only the 2-Cys Prx. Front Plant Sci 8:118

    Article  PubMed  PubMed Central  Google Scholar 

  • Calderón A, Ortiz-Espín A, Iglesias-Fernández R, Carbonero P, Pallardó FV, Sevilla F, Jiménez A (2017b) Thioredoxin (Trxo1) interacts with proliferating cell nuclear antigen (PCNA) and its overexpression affects the growth of tobacco cell culture. Redox Biol 11:688–700

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Camejo D, Romero-Puertas MDC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteom 79:87–99

    Google Scholar 

  • Camejo D, Ortiz-Espín A, Lázaro JJ, Romero-Puertas MC, Lázaro-Payo A, Sevilla F, Jiménez A (2015) Functional and structural changes in plant mitochondrial PrxIIF caused by NO. J Proteom 119:112–125

    Article  CAS  Google Scholar 

  • Cantrel C, Vazquez T, Puyaubert J, Rezé N, Lesch M, Kaiser WM, Dutilleul C, Guillas I, Zachowski A, Baudouin E (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytol 189:415–427

    Article  CAS  PubMed  Google Scholar 

  • Cazalis R, Pulido P, Aussenac T, Pérez-Ruiz JM, Cejudo FJ (2006) Cloning and characterization of three thioredoxin h isoforms from wheat showing differential expression in seeds. J Exp Bot 57:2165–2172

    Article  CAS  PubMed  Google Scholar 

  • Cejudo FJ, Meyer AJ, Reichheld J-P, Rouhier N, Traverso JA, Huber SC (2014) Thiol-based redox homeostasis and signaling. Front Plant Sci 5:266

    Article  PubMed  PubMed Central  Google Scholar 

  • Cha JY, Kim JY, Jung IJ, Kim MR, Melencion A, Alam SS, Yun DJ, Lee SY, Kim MG, Kim WY (2014) NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiol Biochem 80:184–191

    Article  CAS  PubMed  Google Scholar 

  • Chae HB, Moon JC, Shin MR, Chi YH, Jung YJ, Lee SY, Kang CH (2013) Thioredoxin reductase type C (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function. Mol Plant 6:323–336

    Article  CAS  PubMed  Google Scholar 

  • Chattopadhyay A, Subba P, Pandey A, Bhushan D, Kumar R, Datta A, Chakraborty S, Chakraborty N (2011) Analysis of the grasspea proteome and identification of stress-responsive proteins upon exposure to high salinity, low temperature, and abscisic acid treatment. Phytochemistry 72:1293–1307

    Article  CAS  PubMed  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: Regulation mechanisms from whole plant to cell. Annl Bot 103:551–560

    Article  CAS  Google Scholar 

  • Chen Y, Cai J, Murphy TJ, Jones DP (2002) Overexpressed human mitochondrial thioredoxin confers resistance to oxidant-induced apoptosis in human osteosarcoma cells. J Biol Chem 277:33242–33248

    Article  CAS  PubMed  Google Scholar 

  • Chi YH, Moon JC, Park JH, Kim H-S, Zulfugarov IS, Fanata WI, Jang HH, Lee JR, Lee YM, Kim ST, Chung YY, Lim CO, Kim JY, Yun DJ, Lee CH, Lee KO, Lee SY (2008) Abnormal chloroplast development and growth inhibition in rice Thioredoxin m knock-down plants. Plant Physiol 48:808–817

    Article  CAS  Google Scholar 

  • Chibani K, Wingsle G, Jacquot JP, Gelhaye E, Rouhier N (2009) Comparative fenomic study of the thioredoxin family in photosynthetic organisms with emphasis on Populus trichocarpa. Mol Plant 2:308–322

    Article  CAS  PubMed  Google Scholar 

  • Cho EK, Choi YJ (2009) A nuclear-localized HSP70 confers thermoprotective activity and drought-stress tolerance on plants. Biotechnol Lett 1:597–606

    Article  CAS  Google Scholar 

  • Collin V, Issakidis-Bourguet E, Marchand C, Hirasawa M, Lancelin JM, Knaff DB, Miginiac-Maslow M (2003) The Arabidopsis plastidial thioredoxins. New functions and new insights into specificity. J Biol Chem 278:23747–23752

    Article  CAS  PubMed  Google Scholar 

  • Collin V, Lamkemeyer P, Miginiac-Maslow M, Hirasawa M, Knaff DB, Dietz KJ, Issakidis-Bourguet E (2004) Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y type. Plant Physiol 136:4088–4095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colville L, Kranner I (2010) Desiccation tolerant plants as model systems to study redox regulation of protein thiols. Plant Growth Regul 62:241–255

    Article  CAS  Google Scholar 

  • Corpas FJ, Barroso JB, del Río LA (2001) Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trend Plant Sci 6:145–150

    Article  CAS  Google Scholar 

  • Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126

    PubMed  PubMed Central  Google Scholar 

  • Courteille A, Vesa S, Sanz-Barrio R, Cazale AC, Becuwe-Linka N, Farran I, Havaux M, Rey P, Rumeau D (2013) Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol 61:508–520

    Article  CAS  Google Scholar 

  • Cushman JC (1993) Molecular cloning and expression of chloroplast NADP-malate dehydrogenase during Crassulacean acid metabolism induction by salt stress. Photosynth Res 35:15–27

    Article  CAS  PubMed  Google Scholar 

  • Dalle-Donne I, Giustarini D, Colombo R, Milzani A, Rossi R (2005) S-glutathionylation in human platelets by a thiol-disulfide exchange-independent mechanism. Free Rad Biol Med 38:1501–1510

    Article  CAS  PubMed  Google Scholar 

  • Daloso DM, Müller K, Obata T, Florian A, Tohge T, Bottcher A, Riondet C, Bariat L, Carrari F, Nunes-Nesi A, Buchanan BB, Reichheld JP, Araújo WL, Fernie AR, Miginiac-Maslow M, Møller IM (2015) Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria. Proc Natl Acad Sci U S A 112:E1392–E1400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Day DA, Krab K, Lambers H, Moore AL, Siedow JN, Wagner AM, Wiskich JT (1996) The cyanide-resistant oxidase: to inhibit or not to inhibit, that is the question. Plant Physiol 110:1–2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Pinto MC, Locato V, Sgobba A, Romero-Puertas MC, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco bright yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837

    Article  PubMed  CAS  Google Scholar 

  • del Río LA, López-Huertas E (2016) ROS generation in peroxisomes and its role in cell signalling. Plant Cell Physiol 57:1364–1376

    PubMed  Google Scholar 

  • del Río LA, Sandalio LM, Palma JM, Bueno P, Corpas FJ (1992) Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Rad Biol Med 13:557–580

    Article  PubMed  Google Scholar 

  • del Río LA, Palma JM, Sandalio LM, Corpas FJ, Pastori GM, Bueno P, López-Huertas P (1996) Peroxisomes as a source of superoxide and hydrogen peroxide in stressed plants. Biochem Societ Trans 24:434–438

    Article  Google Scholar 

  • del Río LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81

    Article  PubMed  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Google Scholar 

  • Ding M, Hou P, Shen X, Wang M, Deng S, Sun J, Xiao F, Wang R, Zhou X, Lu C, Zhang D, Zheng X, Hu Z, Chen S (2010) Salt-induced expression of genes related to Na+/K+ and ROS homeostasis in leaves of salt-resistant and salt-sensitive poplar species. Plant Mol Biol 73:251–269

    Article  CAS  PubMed  Google Scholar 

  • Dos Santos CV, Rey P (2006) Plant thioredoxins are key actors in the oxidative stress response. Trend Plant Sci 11:329–334

    Article  CAS  Google Scholar 

  • Dubey RS (1999) Protein synthesis by plants under stressful conditions. Handbook Plant Crop Stress 2:365–397

    Article  Google Scholar 

  • Epron D, Toussaint ML, Badot PM (1999) Effects of sodium chloride salinity on root growth and respiration in oak seedlings. Annl Forest Sci 56:41–47

    Article  Google Scholar 

  • Fernández-Trijueque J, Barajas-López JD, Chueca A, Cazalis R, Sahrawy M, Serrato AJ (2012) Plastid thioredoxins f and m are related to the developing and salinity response of post-germinating seeds of Pisum sativum. Plant Sci 188:82–88

    Google Scholar 

  • Ferreira S, Hjernø K, Larsen M, Wingsle G, Larsen P, Fey S, Roepstorff P, Salomé Pais M (2006) Proteome profiling of Populus euphratica Oliv. upon heat stress. Annl Bot 98:361–377

    Article  CAS  Google Scholar 

  • Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 71:501–523

    Article  CAS  Google Scholar 

  • Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biolo 6:269–279

    Article  CAS  Google Scholar 

  • Florencio FJ, Yee BC, Johnson TC, Buchanan BB (1988) An NADP/thioredoxin system in leaves: purification and characterization of NADP-thioredoxin reductase and thioredoxin h from spinach. Arch Biochem Biophy 266:496–507

    Article  CAS  Google Scholar 

  • Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179:945–963

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    Article  CAS  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 46:359–388

    Article  Google Scholar 

  • Foyer CH, Noctor G (2016) Stress-triggered redox signalling: what’s in pROSpect? Plant Cell Environ 39:951–964

    Article  CAS  PubMed  Google Scholar 

  • Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009) Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. J Exp Bot 60:3891–3908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 81:401–404

    Article  CAS  Google Scholar 

  • Funato Y, Miki H (2010) Redox regulation of Wnt signalling via nucleoredoxin. Free Rad Res 44:379–388

    Article  CAS  Google Scholar 

  • Gama F, Bréhélin C, Gelhaye E, Meyer Y, Jacquot JP, Rey P, Rouhier N (2008) Functional analysis and expression characteristics of chloroplastic Prx IIE. Physiol Plant 33:599–610

    Article  CAS  Google Scholar 

  • Gelhaye E, Rouhier N, Gérard J, Jolivet Y, Gualberto J, Navrot N, Ohlsson PI, Wingsle G, Hirasawa M, Knaff DB, Wang H, Dizengremel P, Meyer Y, Jac JP, Gelhaye E, Gérard J, Hirasawa M, Jacquot JP (2004) A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase. Proc Natl Acad Sci U S A 101:14545–14550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Go YM, Jones DP (2010) Redox control systems in the nucleus: mechanisms and functions. Antioxid Redox Signa 13:489–509

    Article  CAS  Google Scholar 

  • Gómez JM, Hernández JA, Jiménez A, del Río LA, Sevilla F (1999) Differential response of antioxidative enzymes of chloroplasts and mitochondria to long-term NaCl stress of pea plants. Free Rad Res 31(sup1):11–18

    Article  Google Scholar 

  • Gómez JM, Jiménez A, Olmos E, Sevilla F (2004) Location and effects of long-term NaCl stress on superoxide dismutase and ascorbate peroxidase isoenzymes of pea (Pisum sativum cv. Puget) chloroplasts. J Exp Bot 55:119–130

    Article  PubMed  CAS  Google Scholar 

  • Gorantla M, Babu PR, Reddy Lachagari VB, Reddy AMM, Wusirika R, Bennetzen JL, Reddy AR (2007) Identification of stress-responsive genes in an indica rice (Oryza sativa L.) using ESTs generated from drought-stressed seedlings. J Exp Bot 58:253–265

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Kaiser WM (2010) Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol 51:576–584

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trend Plant Sci 6:160–168

    Article  CAS  Google Scholar 

  • Habib SH, Kausar H, Saud HM (2016) Plant growth-promoting Rhizobacteria enhance salinity stress tolerance in Okra through ROS-scavenging enzymes. BioMed Res Int Article ID:6284547

    Google Scholar 

  • Haddad R, Japelaghi HR (2014) Abiotic and oxidative stress-dependent regulation of expression of the thioredoxin h multigenic family in grape Vitis vinifera. Biologia 69:152–162

    Article  CAS  Google Scholar 

  • Hägglund P, Finnie C, Yano H, Shahpiri A, Buchanan BB, Henriksen A, Svensson B (2016) Seed thioredoxin h. Biochim Biophy Acta Prot Proteom 864:974–982

    Article  CAS  Google Scholar 

  • Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J Proteom Res 6:1451–1460

    Article  CAS  Google Scholar 

  • Halliwell B, Gutteridge JM (2015) Free radicals in biology and medicine. Oxford University Press, USA.

    Google Scholar 

  • Hao GP, Xing Y, Zhang JH (2008) Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. J Integrat Plant Biol 50:435–442

    Article  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499

    Google Scholar 

  • Hernández JA, Corpas FJ, del Río LA, Sevilla F (1993) Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiol Plant 89:103–110

    Article  Google Scholar 

  • Hernández JA, Olmos E, Corpas FJ, Sevilla F, del Río LA (1995) Salt-induced oxidative stress in chloroplasts of pea plants. Plant Sci 105:151–167

    Article  Google Scholar 

  • Hernández A, Campillo A, Jiménez A, Alarcón JJ, Sevilla F (1999) Response of antioxidant systems and leaf water relations to NaCl stress in pea plants. New Phytol 141:241–251

    Article  Google Scholar 

  • Hernández JA, Jiménez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862

    Article  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Barcelo AR, Sevilla F (2001) Antioxidant systems and O 2 /H2O2 production in the apoplast of pea leaves. It’s relation with salt-induced necrotic lesions in minor veins. Plant Physiol 27:817–831

    Article  Google Scholar 

  • Hisabori T, Sunamura EI, Kim Y, Konno H (2013) The chloroplast ATP synthase features the characteristic redox regulation machinery. Antioxid Redox Signal 19:1846–1854

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmgren A (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254:9627–9632

    CAS  PubMed  Google Scholar 

  • Holmgren A (1985) Thioredoxin. Annl Rev Biochem 54:237–271

    Article  CAS  Google Scholar 

  • Holmgren A (1995) Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide. Structure 3:239–243

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev AU, Ratcliffe RG, Gupta KJ (2014) Plant mitochondria: source and target for nitric oxide. Mitochondrion 19:329–333

    Article  CAS  PubMed  Google Scholar 

  • Iglesias-Baena I, Barranco-Medina S, Lázaro-Payo A, López-Jaramillo FJ, Sevilla F, Lázaro JJ (2010) Characterization of plant sulfiredoxin and role of sulphinic form of 2-Cys peroxiredoxin. J Exp Bot 61:1509–1521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikegami A, Yoshimura N, Motohashi K, Takahashi S, Romano PGN, Hisabori T, Takamiya KI, Masuda T (2007) The CHLI1 subunit of Arabidopsis thaliana magnesium chelatase is a target protein of the chloroplast thioredoxin. J Biol Chem 82:19282–19291

    Article  Google Scholar 

  • Imin N, Nizamidin M, Daniher D, Nolan KE, Rose RJ, Rolfe BG (2005) Proteomic analysis of somatic embryogenesis in Medicago truncatula. Explant cultures grown under 6-benzylaminopurine and 1-naphthaleneacetic acid treatments. Plant Physiol 137:1250–1260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishiga Y, Ishiga T, Wangdi T, Mysore KS, Uppalapati SR (2012) NTRC and chloroplast-generated reactive oxygen species regulate Pseudomonas syringae pv. tomato disease development in tomato and Arabidopsis. Mol Plant Microb Interact 294:294–306

    Article  CAS  Google Scholar 

  • Ishiga Y, Ishiga T, Ikeda Y, Matsuura T, Mysore KS (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:e1938

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishiwatari Y, Honda C, Kawashima I, Nakamura S, Hirano H, Mori S, Fujiwara T, Hayashi H, Chino M (1995) Thioredoxin h is one of the major proteins in rice phloem. Planta 95:456–463

    Google Scholar 

  • Jahan MS, Ogaw KI, Nakamura Y, Shimoishi Y, Mori IC, Murata Y (2008) Deficient glutathione in guard cells facilitates abscisic acid-induced stomatal closure but does not affect light-induced stomatal opening. Biosci Biotechnol Biochem 72:2795–2798

    Google Scholar 

  • Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 42:1246–1255

    Article  CAS  Google Scholar 

  • Jedmowski C, Ashoub A, Beckhaus T, Berberich T, Karas M, Brüggemann W (2014) Comparative analysis of Sorghum bicolor proteome in response to drought stress and following recovery. Int J Proteom, Article ID:395905

    Google Scholar 

  • Ji W, Koh J, Li S, Zhu N, Dufresne CP, Zhao X, Chen S, Li J (2016) Quantitative proteomics reveals an important role of GsCBRLK in salt stress response of soybean. Plant Soil 402:159–178

    Article  CAS  Google Scholar 

  • Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114:275–284

    Article  PubMed  PubMed Central  Google Scholar 

  • Jiménez A, Hernández JA, Pastori G, del Río LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327–1335

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang Y, Udvardi M (2012) Global regulation of reactive oxygen species scavenging genes in alfalfa root and shoot under gradual drought stress and recovery. Plant Signal Behav 7:539–543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khavari-Nejad RA, Chaparzadeh N (1998) The effects of NaCl and CaCl2 on photosynthesis and growth of alfalfa plants. Photosynthetica 35:461–466

    Article  CAS  Google Scholar 

  • Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: Winter and the timing of flowering in plants. Annul Rev Cell Develop Biol 25:277–299

    Article  CAS  Google Scholar 

  • Kim MR, Khaleda L, Jung IJ, Kim JY, Lee SY, Cha JY, Kim WY (2017) Overexpression of chloroplast-localized NADPH-dependent thioredoxin reductase C (NTRC) enhances tolerance to photo-oxidative and drought stresses in Arabidopsis thaliana. J Plant Biol 60:175–180

    Article  CAS  Google Scholar 

  • Kirchsteiger K, Ferrández J, Pascual MB, González M, Cejudo FJ (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 24:1534–1548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kneeshaw S, Gelineau S, Tada Y, Loake GJ, Spoel SH (2014) Selective protein denitrosylation activity of thioredoxin-h5 modulates plant immunity. Mol Cell 56:153–162

    Article  CAS  PubMed  Google Scholar 

  • Kneeshaw S, Keyani R, Delorme-Hinoux V, Imrie L, Loakea GJ, Le Bihan T, Reichheld JP, Spoel SH (2017) Nucleoredoxin guards against oxidative stress by protecting antioxidant enzymes. Proc Natl Acad Sci U S A 114:8414–8419

    Article  CAS  PubMed Central  Google Scholar 

  • Kocsy G, Kobrehel K, Szalai G, Duviau MP, Buzás Z, Galiba G (2004) Abiotic stress-induced changes in glutathione and thioredoxin h levels in maize. Environ Exp Bot 52:101–112

    Article  CAS  Google Scholar 

  • Kohzuma K, Froehlich JE, Davis GA, Temple JA, Minhas D, Dhingra A, Cruz JA, Kramer DM (2017) The role of light-dark regulation of the chloroplast ATP synthase. Front Plant Sci 8:1248

    Article  PubMed  PubMed Central  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017

    Article  CAS  Google Scholar 

  • Korn M, Gärtner T, Erban A, Kopka J, Selbig J, Hincha DK (2010) Predicting Arabidopsis freezing tolerance and heterosis in freezing tolerance from metabolite composition. Mol Plant 3:224–235

    Article  CAS  PubMed  Google Scholar 

  • Kosová K, Vítámvás P, Urban MO, Prášil IT (2013) Plant proteome responses to salinity stress-comparison of glycophytes and halophytes. Funct Plant Biol 40:775–786

    Google Scholar 

  • Koussevitzky S, Suzuki N, Huntington S, Armijo L, Sha W, Cortes D, Shulaev V, Mittler R (2008) Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J Biol Chem 283:34197–34203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyro HW (2006) Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte Plantago coronopus (L.). Environ Exp Bot 56:136–146

    Article  CAS  Google Scholar 

  • Kumar RG, Shah K, Dubey RS (2000) Salinity induced behavioural changes in malate dehydrogenase and glutamate dehydrogenase activities in rice seedlings of differing salt tolerance. Plant Sci 56:23–34

    Article  Google Scholar 

  • Kumar A, Li C, Portis AR (2009) Arabidopsis thaliana expressing a thermostable chimeric Rubisco activase exhibits enhanced growth and higher rates of photosynthesis at moderately high temperatures. Photosynt Res 100:143–153

    Article  CAS  Google Scholar 

  • Laloi C, Rayapuram N, Chartier Y, Grienenberger J-M, Raldine Bonnard G, Meyer Y, Buchanan BB (2001) Identification and characterization of a mitochondrial thioredoxin system in plants. Proc Natl Acad Sci U S A 98:14144–14149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lázaro JJ, Jiménez A, Camejo D, Iglesias-Baena I, Martí M del C, Lázaro-Payo A, Barranco-Medina S, Sevilla F (2013) Dissecting the integrative antioxidant and redox systems in plant mitochondria. Effect of stress and S-nitrosylation. Front Plant Sci 4:460

    Google Scholar 

  • Lee KO, Jang HH, Jung BG, Chi YH, Lee JY, Choi YO, Lee JR, Lim CO, Cho MJ, Lee SY (2000) Rice 1 Cys-peroxiredoxin over-expressed in transgenic tobacco does not maintain dormancy but enhances antioxidant activity. FEBS Lett 486:103–106

    Article  CAS  PubMed  Google Scholar 

  • Lee JR, Lee SS, Jang HH, Lee YM, Park JH, Park S-C, Moon JC, Park SK, Kim SY, Lee SY, Chae HB, Jung YJ, Kim WY, Shin MR, Cheong G-W, Kim MG, Kang KR, Lee KO, Lee SY (2009) Heat-shock dependent oligomeric status alters the function of a plant-specific thioredoxin-like protein, AtTDX. Proc Natl Acad Sci U S A 106:5978–5983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lillig CH, Holmgren A (2007) Thioredoxin and related molecules—from biology to health and disease. Antioxid Redox Signal 9:25–47

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr C, Saalbach G, Rg Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168:343–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333:616–620

    Article  CAS  PubMed  Google Scholar 

  • Loggini B, Scartazza A, Brugnoli E, Navari-Izzo F (1999) Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119:1091–1100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu C, Vonshak A (2002) Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol Plant 114:405–413

    Article  CAS  PubMed  Google Scholar 

  • Luo T, Fan T, Liu Y, Rothbart M, Yu J, Zhou S, Grimm B, Luo M (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 59:118–130

    Article  CAS  Google Scholar 

  • M’rah S, Ouerghi Z, Eymery F, Rey P, Hajji M, Grignon C, Lachaâl M (2007) Efficiency of biochemical protection against toxic effects of accumulated salt differentiates Thellungiella halophila from Arabidopsis thaliana. J Plant Physiol 164:375–384

    Google Scholar 

  • Maeda K, Tsugita A, Dalzoppo D, Vilbois F, Schurmann P (1986) Further characterization and amino acid sequence of m-type thioredoxins from spinach chloroplasts. FEBS J 154:197–203

    CAS  Google Scholar 

  • Mäkelä P, Kontturi M, Pehu E, Somersalo S (1999) Photosynthetic response of drought-and salt-stressed tomato and turnip rape plants to foliar-applied glycinebetaine. Physiol Plant 105:45–50

    Article  Google Scholar 

  • Manaa A, Ben Ahmed H, Valot B, Bouchet JP, Aschi-Smiti S, Causse M, Faurobert M (2011) Salt and genotype impact on plant physiology and root proteome variations in tomato. J Exp Bot 62:2797–2813

    Article  CAS  PubMed  Google Scholar 

  • Marchal C, Delorme-Hinoux V, Bariat L, Siala W, Belin C, Saez-Vasquez J, Riondet C, Reichheld JP (2014) NTR/NRX define a new thioredoxin system in the nucleus of Arabidopsis thaliana cells. Mol Plant 7:30–44

    Article  CAS  PubMed  Google Scholar 

  • Martí MC, Olmos E, Calvete JJ, Díaz I, Barranco-Medina S, Whelan J, Lázaro JJ, Sevilla F, Jiménez A (2009) Mitochondrial and nuclear localization of a novel pea thioredoxin: identification of its mitochondrial target proteins. Plant Physiol 150:646–657

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martí MC, Florez-Sarasa I, Camejo D, Ribas-Carbó M, Lázaro JJ, Sevilla F, Jiménez A (2011) Response of mitochondrial thioredoxin PsTrxo1, antioxidant enzymes, and respiration to salinity in pea (Pisum sativum L.) leaves. J Exp Bot 62:3863–3874

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Martí MC, Florez-Sarasa I, Camejo D, Pallol B, Ortiz A, Ribas-Carbó M, Jiménez A, Sevilla F (2013) Response of mitochondrial antioxidant system and respiratory pathways to reactive nitrogen species in pea leaves. Physiol Plant 147:194–206

    Article  PubMed  CAS  Google Scholar 

  • McKinney DW, Buchanan BB, Wolosiuk RA (1978) Activation of chloroplast ATPase by reduced thioredoxin. Phytochemistry 17:794–795

    Article  CAS  Google Scholar 

  • Meng L, Wong JH, Feldman LJ, Lemaux PG, Buchanan BB (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 107:3900–3905

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer Y, Belin C, Delorme-Hinoux V, Reichheld JP, Riondet C (2012) Thioredoxin and glutaredoxin systems in plants: molecular mechanisms, crosstalks, and functional significance. Antioxid Redox Signal 17:1124–1160

    Article  CAS  PubMed  Google Scholar 

  • Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci 4:470

    Article  PubMed  PubMed Central  Google Scholar 

  • Millar AH, Whelan J, Soole KL, Day DA (2011) Organization and regulation of mitochondrial respiration in plants. Annl Rev Plant Biol 62:79–104

    Article  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mishra SK, Subrahmanyam D, Singhal GS (1991) Interrelationship between salt and light stress on primary processes of photosynthesis. J Plant Physiol 38:92–96

    Article  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, van Breusegem F (2004) Reactive oxygen gene network of plants. Trend Plant Sci 9:490–498

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trend Plant Sci 16:300–309

    Article  CAS  Google Scholar 

  • Mittova V, Tal M, Volokita M, Guy M (2003) Up-regulation of the leaf mitochondrial and peroxisomal antioxidative systems in response to salt-induced oxidative stress in the wild salt-tolerant tomato species Lycopersicon pennellii. Plant Cell Environ 26:845–856

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Schreiber U, Hormann H, Sano S, Asada K (1998) The FAD-enzyme monodehydroascorbate radical reductase mediates photoproduction of superoxide radicals in spinach thylakoid membranes. Plant Cell Physiol 39:821–829

    Article  CAS  Google Scholar 

  • Møller IM, Sweetlove LJ (2010) ROS signalling—specificity is required. Trend Plant Sci 15:370–374

    Article  CAS  Google Scholar 

  • Møller IS, Tester M (2007) Salinity tolerance of Arabidopsis: a good model for cereals? Trend Plant Sci 12:534–540

    Article  CAS  Google Scholar 

  • Mor A, Koh E, Weiner L, Rosenwasser S, Sibony-Benyamini H, Fluhr R (2014) Singlet oxygen signatures are detected independent of light or chloroplasts in response to multiple stresses. Plant Physiol 165:249–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mowla SB, Thomson JA, Farrant JM, Mundree SG (2002) A novel stress-inducible antioxidant enzyme identified from the resurrection plant Xerophyta viscosa baker. Planta 215:716–726

    Article  CAS  PubMed  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annl Rev Plant Biol 59:651–681

    Article  CAS  Google Scholar 

  • Nájera VA, González MC, Pérez-Ruiz JM, Cejudo FJ (2017) An event of alternative splicing affects the expression of the NTRC gene, encoding NADPH-thioredoxin reductase C, in seed plants. Plant Sci 258:21–28

    Article  PubMed  CAS  Google Scholar 

  • Naranjo B, Mignée C, Krieger-Liszkay A, Hornero-Méndez D, Gallardo-Guerrero L, Cejudo FJ, Lindahl M (2016) The chloroplast NADPH thioredoxin reductase C, NTRC, controls non-photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis. Plant Cell Environ 39:804–822

    Article  CAS  PubMed  Google Scholar 

  • Nikitovic D, Holmgren A (1996) S-nitrosoglutathione is cleaved by the thioredoxin system with liberation of glutathione and redox regulating nitric oxide. J Biol Chem 271:19180–19185

    Article  CAS  PubMed  Google Scholar 

  • Nikkanen L, Toivola J, Rintamäki E (2016) Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis. Plant Cell Environ 39:1691–1705

    Article  CAS  PubMed  Google Scholar 

  • Niu L, Liao W (2016) Hydrogen peroxide signaling in pant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230

    PubMed  PubMed Central  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Annl Bot 89:841–850

    Article  CAS  Google Scholar 

  • Noctor G, De Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trend Plant Sci 12:125–134

    Article  CAS  Google Scholar 

  • Noctor G, Mhamdi A, Foyer CH (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiol 64:1636–1648

    Article  CAS  Google Scholar 

  • O’Kane D, Gill V, Boyd P, Burdon R (1996) Chilling, oxidative stress and antioxidant responses in Arabidopsis thaliana callus. Planta 198:371–377

    Article  PubMed  Google Scholar 

  • Ojeda V, Pérez-Ruiz JM, González M, Nájera VA, Sahrawy M, Serrato AJ, Geigenberger P, Cejudo FJ (2017) NADPH thioredoxin reductase C and thioredoxins act concertedly in seedling development. Plant Physiol 174:1436–1448

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okegawa Y, Motohashi K (2015) Chloroplastic thioredoxin m functions as a major regulator of Calvin cycle enzymes during photosynthesis in vivo. Plant J 84:900–913

    Article  CAS  PubMed  Google Scholar 

  • Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortiz-Espín A, Locato V, Camejo D, Schiermeyer A, De Gara L, Sevilla F, Jiménez A (2015) Over-expression of Trxo1 increases the viability of tobacco BY-2 cells under H2O2 treatment. Annl Bot 116:571–582

    Article  Google Scholar 

  • Ortiz-Espín A, Iglesias-Fernández R, Calderón A, Carbonero P, Sevilla F, Jiménez A (2017) Mitochondrial AtTrxo1 is transcriptionally regulated by AtbZIP9 and AtAZF2 and affects seed germination under saline conditions. J Exp Bot 68:1025–1038

    Article  PubMed  PubMed Central  Google Scholar 

  • Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186

    Article  CAS  PubMed  Google Scholar 

  • Panchuk II, Volkov RA, Schö F (2002) Heat stress-and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pang Q, Chen S, Dai S, Chen Y, Wang Y, Yan X (2010) Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J Proteom Res 9:2584–2599

    Article  CAS  Google Scholar 

  • Parida KA, Das AB, Mohanty P (2004) Investigations on the antioxidative defence responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regul 42:213–226

    Article  CAS  Google Scholar 

  • Park SK, Jung YJ, Lee JR, Lee YM, Jang HH, Lee SS, Park JH, Kim SY, Moon JC, Lee SY, Chae HB, Shin MR, Jung JH, Kim MG, Kim WY, Yun D-J, Lee KO, Lee SY (2009) Heat-shock and redox-dependent functional switching of an h-type Arabidopsis thioredoxin from a disulfide reductase to a molecular chaperone. Plant Physiol 150:552–561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pastori G, Foyer CH, Mullineaux P (2000) Low temperature induces changes in the distribution of H2O2 and antioxidants between the bundle sheath and mesophyll cells of maize leaves. J Exp Bot 51:107–113

    CAS  PubMed  Google Scholar 

  • Pérez-Ruiz JM, Cejudo FJ (2009) A proposed reaction mechanism for rice NADPH thioredoxin reductase C, an enzyme with protein disulfide reductase activity. FEBS Lett 583:1399–1402

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Ruiz JM, Spínola MC, Kirchsteiger K, Moreno J, Sahrawy M, Cejudo FJ (2006) Rice NTRC is a high-efficiency redox system for chloroplast protection against oxidative damage. Plant Cell 18:2356–2368

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pfeiffer S, Mayer B, Hemmens B (1999) Nitric oxide: chemical puzzles posed by a biological messenger. Angewandte Chem Int Edn 38:1714–1731

    Article  Google Scholar 

  • Pulido P, Cazalis R, Cejudo FJ (2009) An antioxidant redox system in the nucleus of wheat seed cells suffering oxidative stress. Plant J 57:132–145

    Article  CAS  PubMed  Google Scholar 

  • Pulido P, Spínola MC, Kirchsteiger K, Guinea M, Pascual MB, Sahrawy M, Sandalio LM, Dietz KJ, González M, Cejudo FJ (2010) Functional analysis of the pathways for 2-Cys peroxiredoxin reduction in Arabidopsis thaliana chloroplasts. J Exp Bot 61:4043–4054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (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 5:e1000621

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rabhi M, Giuntini D, Castagna A, Remorini D, Baldan B, Smaoui A, Abdelly C, Ranieri A (2010) Sesuvium portulacastrum maintains adequate gas exchange, pigment composition, and thylakoid proteins under moderate and high salinity. J Plant Physiol 67:1336–1341

    Article  CAS  Google Scholar 

  • Raines CA (2003) The Calvin cycle revisited. Photosynt Res 75:1–10

    Article  CAS  Google Scholar 

  • Rakhra G, Sharma AD, Singh J (2015) Anti-oxidative potential of boiling soluble antioxidant enzymes in amelioration of drought-induced oxidative stress in tolerant and sensitive cultivars of Triticum aestivum. J Crop Sci Biotechnol 18:103–122

    Article  Google Scholar 

  • Rasoulnia A, Bihamta MR, Peyghambari SA, Alizadeh H, Rahnama A (2011) Proteomic response of barley leaves to salinity. Mol Biol Rep 38:5055–5063

    Article  CAS  PubMed  Google Scholar 

  • Reczek CR, Chandel NS (2015) ROS-dependent signal transduction. Curr Opi Cell Biol 33:8–13

    Article  CAS  Google Scholar 

  • Reichheld JP, Mestres-Ortega D, Laloi C, Meyer Y (2002) The multigenic family of thioredoxin h in Arabidopsis thaliana: specific expression and stress response. Plant Physiol Biochem 40:685–690

    Article  CAS  Google Scholar 

  • Reichheld JP, Meyer E, Khafif M, Bonnard G, Meyer Y (2005) AtNTRB is the major mitochondrial thioredoxin reductase in Arabidopsis thaliana. FEBS Lett 579:337–342

    Article  CAS  PubMed  Google Scholar 

  • Rey P, Pruvot G, Becuwe N, Eymery F, Rumeau D, Peltier G (1998) A novel thioredoxin-like protein located in the chloroplast is induced by water deficit in Solanum tuberosum L. plants. Plant J 49:505–514

    Article  CAS  Google Scholar 

  • Rey P, Bécuwe N, Barrault MB, Rumeau D, Havaux M, Biteau B, Toledano MB (2007) The Arabidopsis thaliana sulfiredoxin is a plastidic cysteine-sulfinic acid reductase involved in the photooxidative stress response. Plant J 49:505–514

    Article  CAS  PubMed  Google Scholar 

  • Ribas-Carbó M, Taylor NL, Giles L, Busquets S, Finnegan PM, Day DA, Lambers H, Medrano H, Berry JA, Flexas J (2005) Effects of water stress on respiration in Soybean leaves. Plant Physiol 139:466–473

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rizhsky L (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosado A, Schapire AL, Bressan RA, Harfouche AL, Hasegawa PM, Valpuesta V, Botella MA (2006) The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol 142:1113–1126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rouhier N, Jacquot JP (2005) The plant multigenic family of thiol peroxidases. Free Rad Biol Med 38:1413–1421

    Article  CAS  PubMed  Google Scholar 

  • Ruelland E, Zachowski A (2010) How plants sense temperature. Environ Exp Bot 69:225–232

    Article  Google Scholar 

  • Ruelland E, Vaultier MN, Zachowski A, Hurry V (2009) Cold signalling and cold acclimation in plants. Adv Bot Res 49:35–150

    Article  CAS  Google Scholar 

  • Sakamoto H (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold and high-salinity stress conditions. Plant Physiol 136:2734–2746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandalio LM, Romero-Puertas MC (2015) Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Annl Bot 116:475–485

    Article  CAS  Google Scholar 

  • Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14(suppl 1):S401–S417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sang J, Jiang M, Lin F, Xu S, Zhang A, Tan M (2008) Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular antioxidant defense in maize plants. J Integrat Plant Biol 50:231–243

    Article  CAS  Google Scholar 

  • Sangwan V, Dhindsa RS (2002) In vivo and in vitro activation of temperature-responsive plant map kinases. FEBS Lett 531:561–564

    Article  CAS  PubMed  Google Scholar 

  • Sanz-Barrio R, Corral-Martinez P, Ancin M, Segui-Simarro JM, Farran I (2013) Overexpression of plastidial thioredoxin f leads to enhanced starch accumulation in tobacco leaves. Plant Biotechnol J 11:618–627

    Article  CAS  PubMed  Google Scholar 

  • Scheibe R (1981) Thioredoxin m in pea chloroplasts: Concentration and redox state under light and dark conditions. FEBS Lett 133:301–304

    Article  CAS  Google Scholar 

  • Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489

    Article  CAS  PubMed  Google Scholar 

  • Schmidtmann E, König A-C, Orwat A, Leister D, Hartl M, Finkemeier I (2014) Redox regulation of Arabidopsis mitochondrial citrate synthase. Mol Plant 7:156–169

    Article  CAS  PubMed  Google Scholar 

  • Schürmann P, Jacquot JP (2000) Plant thioredoxins system revised. Annl Rev Plant Physiol Plant Mol Biol 51:371–400

    Article  Google Scholar 

  • Seo PJ, Kim MJ, Song JS, Kim YS, Kim HJ, Park CM (2010) Proteolytic processing of an Arabidopsis membrane-bound NAC transcription factor is triggered by cold-induced changes in membrane fluidity. Biochem J 427:359–367

    Article  CAS  PubMed  Google Scholar 

  • Serrato AJ, Cejudo FJ (2003) Type-h thioredoxins accumulate in the nucleus of developing wheat seed tissues suffering oxidative stress. Planta 217:392–399

    Article  CAS  PubMed  Google Scholar 

  • Serrato AJ, Crespo JL, Florencio FJ, Cejudo FJ (2001) Characterization of two thioredoxins h with predominant localization in the nucleus of aleurone and scutellum cells of germinating wheat seeds. Plant Mol Biol 46:361–371

    Article  CAS  PubMed  Google Scholar 

  • Serrato AJ, Pérez-Ruiz JM, Spínola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localised in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279:43821–43827

    Article  CAS  PubMed  Google Scholar 

  • Sevilla F, Lopez-Gorge J, del Rio LA (1982) Characterization of a manganese superoxide dismutase from the higher plant Pisum sativum. Plant Physiol 70:1321–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sevilla F, Jiménez A, Lázaro JJ (2015) What do the plant mitochondrial antioxidant and redox systems have to say under salinity, drought, and extreme temperature? In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, pp 23–55

    Google Scholar 

  • Sgherri CLM, Pinzino C, Navari-Lzzo F (1996) Sunflower seedlings subjected to increasing stress by water deficit: changes in O2 production related to the composition of thylakoid membranes. Physiol Plant 96:446–452

    Google Scholar 

  • Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA (2006) Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+-permeable channels. Plant Physiol 141:1653–1665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shahpiri A, Svensson B, Finnie C (2007) The NADPH-dependent thioredoxin reductase/thioredoxin system in germinating barley seeds: gene expression, protein profiles, and interactions between isoforms of thioredoxin h and thioredoxin reductase. Plant Physiol 146:789–799

    Article  PubMed  CAS  Google Scholar 

  • Sharma R, Vishal P, Kaul S, Dhar MK (2017) Epiallelic changes in known stress-responsive genes under extreme drought conditions in Brassica juncea (L.). Plant Cell Rep 36:203–217

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Chen Y, Tan DX, Reiter RJ, Chan Z, He C (2015) Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J Pineal Res 59:102–108

    Article  CAS  PubMed  Google Scholar 

  • Sies H (2017) Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: oxidative eustress. Redox Biol 11:613–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinha P, Pazhamala LT, Singh VK, Saxena RK, Krishnamurthy L, Azam S, Varshney RK (2016) Identification and validation of selected universal stress protein domain containing drought-responsive genes in Pigeonpea (Cajanus cajan L.). Front Plant Sci 6:1065

    Article  PubMed  PubMed Central  Google Scholar 

  • Stacy RAP, Norcleng TW, Culiáñez-Macià FA, Aalen RB (1999) The dormancy-related peroxiredoxin anti-oxidant, PER1, is localized to the nucleus of barley embryo and aleurone cells. Plant J 19:1–8

    Article  CAS  PubMed  Google Scholar 

  • Stoimenova M, Igamberdiev AU, Gupta KJ, Hill RD (2007) Nitrite-driven anaerobic ATP synthesis in barley and rice root mitochondria. Planta 226:465–474

    Article  CAS  PubMed  Google Scholar 

  • Suske G, Wagner W, Follmann H (1979) NADPH-dependent thioredoxin reductase and a new thioredoxin from Wheat. Z Naturforsch Sect C J Biosci 34:214–221

    Google Scholar 

  • Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

    Article  CAS  Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanaka T, Hosoi F, Yamaguchi-Iwai Y, Nakamura H, Masutani H, Ueda S, Nishiyama A, Takeda S, Wada H, Spyrou G, Yodoi J (2002) Thioredoxin-2 (TRX-2) is an essential gene regulating mitochondria-dependent apoptosis. EMBO J 21:1695–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanou G, Molassiotis A, Diamantidis G (2009) Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913

    Article  CAS  PubMed  Google Scholar 

  • Thines B, Harmon FG (2010) Ambient temperature response establishes ELF3 as a required component of the core Arabidopsis circadian clock. Proc Natl Acad Sci U S A 107:3257–3262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thormählen I, Ruber J, Von Roepenack-Lahaye E, Ehrlich SM, Massot V, Hümmer C, Tezycka J, Issakidis-Bourguet E, Geigenberger P (2013) Inactivation of thioredoxin f1 leads to decreased light activation of ADP-glucose pyrophosphorylase and altered diurnal starch turnover in leaves of Arabidopsis plants. Plant Cell Environ 36:16–29

    Article  PubMed  CAS  Google Scholar 

  • Toivola J, Nikkanen L, Dahlström KM, Salminen TA, Lepistö A, Vignols F, Rintamäki E (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 4:389

    Article  PubMed  PubMed Central  Google Scholar 

  • Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trend Plant Sci 14:219–228

    Article  CAS  Google Scholar 

  • Tripathi BN, Bhatt I, Dietz KJ (2009) Peroxiredoxins: a less studied component of hydrogen peroxide detoxification in photosynthetic organisms. Protoplasma 235:3–15

    Article  CAS  PubMed  Google Scholar 

  • Turan S, Tripathy BC (2015) Salt-stress induced modulation of chlorophyll biosynthesis during de-etiolation of rice seedlings. Physiol Plant 153:477–491

    Article  CAS  PubMed  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vacca RA, de Pinto MC, Valenti D, Passarella S, Marra E, de Gara L (2004) Production of reactive oxygen species, alteration of cytosolic ascorbate peroxidase, and impairment of mitochondrial metabolism are early events in heat shock-induced programmed cell death in tobacco BrightYellow 2 cells. Plant Physiol 134:1100–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461

    Article  CAS  PubMed  Google Scholar 

  • Van Breusegem F, Bailey-Serres J, Mittler R (2008) Unraveling the tapestry of networks involving reactive oxygen species in plants. Plant Physiol 147:978–984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vieira Dos Santos C, Laugier E, Tarrago L, Massot V, Issakidis-Bourguet E, Rouhier N, Rey P (2007) Specificity of thioredoxins and glutaredoxins as electron donors to two distinct classes of Arabidopsis plastidial methionine sulfoxide reductases B. FEBS Lett 581:4371–4376

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Yang P, Gao Q, Liu X, Kuang T, Shen S, He Y (2008) Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 228:167–177

    Article  CAS  PubMed  Google Scholar 

  • Wang XQ, Yang PF, Liu Z, Liu WZ, Hu Y, Chen H, Kuang TY, Pei ZM, Shen SH, He YK (2009) Exploring the mechanism of Physcomitrella patens desiccation tolerance through a proteomic strategy. Plant Physiol 49:1739–1750

    Article  Google Scholar 

  • Wang P, Liu J, Liu B, Feng D, Da Q, Wang P, Shu S, Su J, Zhang Y, Wang J, Wang HB (2013) Evidence for a role of chloroplastic m-type thioredoxins in the biogenesis of photosystem II in Arabidopsis. Plant Physiol 163:1710–1728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang N, Zhao J, He X, Sun H, Zhang G, Wu F (2015a) Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. BMC Genom 16:432

    Article  CAS  Google Scholar 

  • Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015b) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618

    Article  CAS  PubMed  Google Scholar 

  • Watkinson JI, Hendricks L, Sioson AA, Heath LS, Bohnert HJ, Grene R (2008) Tuber development phenotypes in adapted and acclimated, drought-stressed Solanum tuberosum ssp. Andigena have distinct expression profiles of genes associated with carbon metabolism. Plant Physiol Biochem 46:34–45

    Article  CAS  PubMed  Google Scholar 

  • Wenderoth I, Scheibe R, von Schaewen A (1997) Identification of the cysteine residues involved in redox modification of plant plastidic glucose-6-phosphate dehydrogenase. J Biol Chem 272:26985–26990

    Article  CAS  PubMed  Google Scholar 

  • Wijngaard PW, Sinnige MP, Roobeek I, Reumer A, Schoonheim PJ, Mol JN, de Boer AH (2005) Abscisic acid and 14-3-3 proteins control K+ channel activity in barley embryonic root. Plant J 41:43–55

    Article  PubMed  CAS  Google Scholar 

  • Wolosiuk RA, Buchanan BB, Crawford NA (1977) Regulation of NADP-malate dehydrogenase by the light-actuated ferredoxin/thioredoxin system of chloroplasts. FEBS Lett 81:253–258

    Article  CAS  Google Scholar 

  • Wong JH, Kim YB, Ren PH, Cai N, Cho MJ, Hedden P, Lemaux PG, Buchanan BB (2002) Transgenic barley grain overexpressing thioredoxin shows evidence that the starchy endosperm communicates with the embryo and the aleurone. Proc Natl Acad Sci U S A 99:16325–16330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodson JD, Chory J (2008) Coordination of gene expression between organellar and nuclear genomes. Nat Rev Genet 9:383–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu T, Xiang PK, Xiao JZ, Li D-P, Li D-Q (2011) Expression analysis of five maize MAP kinase genes in response to various abiotic stresses and signal molecules. Mol Biol Rep 38:3967–3975

    Article  CAS  PubMed  Google Scholar 

  • Wu F, Li Q, Yan H, Zhang D, Jiang G, Jiang Y, Duan X (2016) Characteristics of three thioredoxin genes and their role in chilling tolerance of harvested banana fruit. Int J Mol Sci 17:1526

    Article  PubMed Central  CAS  Google Scholar 

  • Xie G, Kato H, Sasaki K, Imai R (2009) A cold-induced thioredoxin h of rice, OsTrx23, negatively regulates kinase activities of OsMPK3 and OsMPK6 in vitro. FEBS Lett 583:2734–2738

    Article  CAS  PubMed  Google Scholar 

  • Xue LJ, Guo W, Yuan Y, Anino EO, Nyamdar B, Wilson MC, Tsai CJ (2013) Constitutively elevated salicylic acid levels alter photosynthesis and oxidative state but not growth in transgenic populus. Plant Cell 25:2714–2730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamori W, von Caemmerer S (2010) Effect of rubisco activase deficiency on the temperature response of CO2 assimilation rate and rubisco activation state: insights from transgenic Tobacco with reduced amounts of rubisco activase. Plant Physiol 151:2073–2082

    Article  CAS  Google Scholar 

  • Yang X, Lu C (2005) Photosynthesis is improved by exogenous glycinebetaine in salt-stressed maize plants. Physiol Plant 124:343–352

    Article  CAS  Google Scholar 

  • Yang Y, Yan CQ, Cao BH, Xu HX, Chen JP, Jiang DA (2007) Some photosynthetic responses to salinity resistance are transferred into the somatic hybrid descendants from the wild soybean Glycine cyrtoloba ACC547. Physiol Plant 129:658–669

    Article  CAS  Google Scholar 

  • Yano H, Wong JH, Cho MJ, Buchanan BB (2001) Redox changes accompanying the degradation of seed storage proteins in germinating rice. Plant Cell Physiol 42:879–883

    Article  CAS  PubMed  Google Scholar 

  • Yoshida K, Hisabori T (2016) Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability. Proc Natl Acad Sci U S A 113:E3967–E3976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida K, Hara S, Hisabori T (2015) Thioredoxin selectivity for thiol-based redox regulation of target proteins in chloroplasts. J Biol Chem 290:14278–14288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Richardson DR (2011) Cellular iron depletion stimulates the JNK and p38 MAPK signaling transduction pathways, dissociation of ASK1-thioredoxin, and activation of ASK1. J Biol Chem 286:15413–15427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156

    Article  CAS  PubMed  Google Scholar 

  • Yu X, James AT, Yang A, Jones A, Mendoza-Porras O, Bétrix CA, Ma H, Colgrave ML (2016) A comparative proteomic study of drought-tolerant and drought-sensitive soybean seedlings under drought stress. Crop Past Sci 67:528–540

    Article  CAS  Google Scholar 

  • Zadražnik T, Hollung K, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J (2013) Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteom 78:254–272

    Article  CAS  Google Scholar 

  • Zaffagnini M, Morisse S, Bedhomme M, Marchand CH, Festa M, Rouhier N, Lemaire SD, Trost P (2013) Mechanisms of nitrosylation and denitrosylation of cytoplasmic glyceraldehyde-3-phosphate dehydrogenase from Arabidopsis thaliana. J Biol Chem 288:22777–22789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zagdanska B, Wisniewski K (1996) Changes in the thiol/disulfide redox potential in wheat leaves upon water deficit. Plant Physiol 149:462–465

    Article  CAS  Google Scholar 

  • Zagorchev L, Seal CE, Kranner I, Odjakova M (2013) A central role for thiols in plant tolerance to abiotic stress. Int J Mol Sci 14:7405–7432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555

    Article  CAS  PubMed  Google Scholar 

  • Zhang CJ, Zhao BC, Ge WN, Zhang YF, Song Y, Sun DY, Guo Y (2011) An apoplastic h-type thioredoxin is involved in the stress response through regulation of the apoplastic reactive oxygen species in rice. Plant Physiol 157:1884–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhang L, Lv H, Yu Z, Zhang D, Zhu W (2014) Identification of changes in Triticum aestivum L. leaf proteome in response to drought stress by 2D-PAGE and MALDI-TOF/TOF mass spectrometry. Acta Physiol Plant 36:1385–1398

    Article  CAS  Google Scholar 

  • Zheng C, Jiang D, Liu F, Dai T, Jing Q, Cao W (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trend Plant Sci 6:66–71

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by MINECO/FEDER (project BFU2014-52452-P and FPI grant of A S-G) and Séneca Foundation, Murcia, Spain (Project 19876/GERM/15 and contract of A O-E). The authors apologize to the scientists that are not cited because of space limitations and thank Steve Hasler for proofreading the written English of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Jiménez .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Calderón, A., Sevilla, F., Jiménez, A. (2018). Redox Protein Thioredoxins: Function Under Salinity, Drought and Extreme Temperature Conditions. In: Gupta, D., Palma, J., Corpas, F. (eds) Antioxidants and Antioxidant Enzymes in Higher Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-75088-0_7

Download citation

Publish with us

Policies and ethics