专题论坛

叶绿体硫氧还蛋白系统的调节机制

展开
  • 1 四川理工学院生物工程学院, 自贡 643000
    2 四川大学生命科学学院, 生物资源与生态环境教育部重点实验室, 成都 610064

收稿日期: 2018-02-17

  录用日期: 2018-05-23

  网络出版日期: 2019-07-31

基金资助

国家自然科学基金(31601291);四川省教育厅项目(17ZB0315);四川理工学院人才引进项目(2016RCL14)

Regulatory Mechanism of Thioredoxin (Trx) in Chloroplasts

Expand
  • 1 College of Bioengineering, Sichuan University of Science & Engineering, Zigong 643000, China;
    2 Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610064, China

Received date: 2018-02-17

  Accepted date: 2018-05-23

  Online published: 2019-07-31

摘要

硫氧还蛋白(Trx)属于巯基-二硫键氧化还原酶家族, 通过作用于底物蛋白侧链2个半胱氨酸残基之间的二硫键(还原、异构和转移)来调控胞内蛋白的结构和功能。叶绿体Trx系统包括Trx及Trx类似蛋白、铁氧还蛋白(Fd)依赖的硫氧还蛋白还原酶(FTR)和还原型烟酰腺嘌呤二核苷磷酸(NADPH)依赖的硫氧还蛋白还原酶C (NTRC)。除了基质蛋白酶类活性变化及叶绿体蛋白的转运受Trx系统调控之外, 在叶绿体中还存在1条跨类囊体膜的还原势传递途径, 把基质Trx的还原势经跨膜转运蛋白介导, 最终传递给类囊体腔蛋白。FTR和NTRC共同作用维持叶绿体的氧化还原平衡。该文对叶绿体硫氧还蛋白系统的调节机制进行了综述, 同时讨论了叶绿体硫氧还蛋白系统对维持植物光合效率的重要意义。

本文引用格式

秦童,黄震,康振辉 . 叶绿体硫氧还蛋白系统的调节机制[J]. 植物学报, 2019 , 54(1) : 119 -132 . DOI: 10.11983/CBB18047

Abstract

Thioredoxins (Trx), a family of thiol-disulfide oxidoreductases, function as protein disulfide reductases to disulfide isomerases or to disulfide transferases to regulate the structure and function of intracellular proteins by modifying disulfide bonds between two cysteine residues in the side chain of the substrate proteins. The chloroplast Trx systems includes Trx and Trx-like proteins, ferredoxin (Fd)-dependent thioredoxin reductase (FTR) and reduced nicotinamide adenine dinucleotide phosphate (NADPH)-dependent thioredoxin C (NADPH Trx reductase C, NTRC). In addition to regulating the activity of stromal enzymes and transportation of chloroplast proteins by the Trx system, the chloroplast contains a reduction potential transfer pathway across the thylakoid membrane. The reduction potential of the substrate Trx is mediated by the transmembrane transporter and finally to the thylakoid lumenal protein. FTR and NTRC coordinate to regulate chloroplast homeostasis. This paper summarizes the regulatory mechanism of the chloroplast thioredoxin system that highlights the significance of the chloroplast Trx system in maintaining photosynthetic efficiency in plants.

参考文献

1 孙虎, 薛保国, 杨丽荣, 全鑫, 朱自贤, 武超, 马雪娇 ( 2010). 植物硫氧还蛋白系统. 基因组学与应用生物学 29, 748-753.
2 张艳玲, 孙旭武, 张立新 ( 2009). 拟南芥叶绿体中DEG蛋白酶功能的研究进展. 植物学报 44, 37-42.
3 Arnoux P, Morosinotto T, Saga G, Bassi R, Pignol D ( 2009). A structural basis for the pH-dependent xanthophyll cycle in Arabidopsis thaliana.Plant Cell 21, 2036-2044.
4 Arsova B, Hoja U, Wimmelbacher M, Greiner E, üstün S, Melzer M, Petersen K, Lein W, B?rnke 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 22, 1498-1515.
5 Balsera M, Uberegui E, Schürmann P, Buchanan BB ( 2014). Evolutionary development of redox regulation in chloroplasts. Antioxid Redox Signal 21, 1327-1355.
6 Balsera M, Uberegui E, Susanti D, Schmitz RA, Mukhopadhyay B, Schürmann P, Buchanan BB ( 2013). Ferredoxin: thioredoxin reductase (FTR) links the regulation of oxygenic photosynthesis to deeply rooted bacteria. Planta 237, 619-635.
7 Belin C, Bashandy T, Cela J, Delorme-Hinoux V, Riondet C, Reichheld JP ( 2015). A comprehensive study of thiol reduction gene expression under stress conditions in Ara- bidopsis thaliana.Plant Cell Environ 38, 299-314.
8 Benitez-Alfonso Y, Cilia M, San Roman A, Thomas C, Maule A, Hearn S, Jackson D ( 2009). Control of Arabidopsis meristem development by thioredoxin-dependent regulation of intercellular transport. Proc Natl Acad Sci USA 106, 3615-3620.
9 Bernal-Bayard P, Ojeda V, Hervás M, Cejudo FJ, Navarro JA, Velázquez-Campoy A, Pérez-Ruiz JM ( 2014). Molecular recognition in the interaction of chloroplast 2-Cys peroxiredoxin with NADPH-thioredoxin reductase C (NTRC) and thioredoxin x. FEBS Lett 588, 4342-4347.
10 Betterle N, Ballottari M, Baginsky S, Bassi R ( 2015). High light-dependent phosphorylation of photosystem II inner antenna CP29 in monocots is STN7 independent and enhances nonphotochemical quenching. Plant Physiol 167, 457-471.
11 Bohrer AS, Massot V, Innocenti G, Reichheld JP, Issakidis-Bourguet E, Vanacker H ( 2012). New insights into the reduction systems of plastidial thioredoxins point out the unique properties of thioredoxin z from Arabidopsis. J Exp Bot 63, 6315-6323.
12 Bolter B, Soll J, Schwenkert S ( 2015). Redox meets protein trafficking. Biochim Biophys Acta 1847, 949-956.
13 Brooks MD, Sylak-Glassman EJ, Fleming GR, Niyogi KK ( 2013). A thioredoxin-like/ β-propeller protein maintains the efficiency of light harvesting in Arabidopsis.Proc Natl Acad Sci USA 110, E2733-E2740.
14 Buchanan BB ( 2016). The path to thioredoxin and redox regulation in chloroplasts. Annu Rev Plant Biol 67, 1-24.
15 Buchanan BB, Holmgren A, Jacquot JP, Scheibe R ( 2012). Fifty years in the thioredoxin field and a bountiful harvest. Biochim Biophys Acta 1820, 1822-1829.
16 Cain P, Hall M, Schr?der WP, Kieselbach T, Robinson C ( 2009). A novel extended family of stromal thioredoxins. Plant Mol Biol 70, 273-281.
17 Carrillo LR, Froehlich JE, Cruz JA, Savage LJ, Kramer DM ( 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, 654-663.
18 Cejudo FJ, Ferrández J, Cano B, Puerto-Galán L, Guinea M ( 2012). The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signaling. FEBS Lett 586, 2974-2980.
19 Chae HB, Moon JC, Shin MR, Chi YH, Jung YJ, Lee SY, Nawkar GM, Jung HS, Hyun JK, Kim WY, Kang CH, Yun DJ, Lee KO, Lee SY ( 2013). Thioredoxin reductase type C (NTRC) orchestrates enhanced thermotolerance to Arabidopsis by its redox-dependent holdase chaperone function. Mol Plant 6, 323-336.
20 Cheng F, Zhou YH, Xia XJ, Shi K, Zhou J, Yu JQ ( 2014). Chloroplastic thioredoxin-f and thioredoxin-m1/4 play important roles in brassinosteroids-induced changes in CO2 assimilation and cellular redox homeostasis in tomato. J Exp Bot 65, 4335-4347.
21 Chibani K, Tarrago L, Schürmann P, Jacquot JP, Rouhier N ( 2011). Biochemical properties of poplar thioredoxin z. FEBS Lett 585, 1077-1081.
22 Cook KM, Hogg PJ ( 2013). Post-translational control of protein function by disulfide bond cleavage. Antioxid Redox Signal 18, 1987-2015.
23 Courteille A, Vesa S, Sanz-Barrio R, Cazalé AC, Becuwe- Linka N, Farran I, Havaux M, Rey P, Rumeau D ( 2013). Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol 161, 508-520.
24 Couturier J, Chibani K, Jacquot JP, Rouhier N ( 2013). Cysteine-based redox regulation and signaling in plants. Front Plant Sci 4, 105.
25 Da QE, Wang P, Wang ML, Sun T, Jin HL, Liu B, Wang JF, Grimm B, Wang HB ( 2017). Thioredoxin and NADPH- dependent thioredoxin reductase C regulation of tetrapyrrole biosynthesis. Plant Physiol 175, 652-666.
26 Dangoor I, Peled-Zehavi H, Levitan A, Pasand O, Danon A ( 2009). A small family of chloroplast atypical thioredoxins. Plant Physiol 149, 1240-1250.
27 Dangoor I, Peled-Zehavi H, Wittenberg G, Danon A ( 2012). A chloroplast light-regulated oxidative sensor for moderate light intensity in Arabidopsis. Plant Cell 24, 1894-1906.
28 Díaz MG, Hernández-Verdeja T, Kremnev D, Crawford T, Dubreuil C, Strand ? ( 2018). Redox regulation of PEP activity during seedling establishment in Arabidopsis tha- liana.Nat Commun 9, 50.
29 Dietz KJ, Pfannschmidt T ( 2011). Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155, 1477-1485.
30 Dutton RJ, Wayman A, Wei JR, Rubin EJ, Beckwith J, Boyd D ( 2010). Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc Natl Acad Sci USA 107, 297-301.
31 Eliyahu E, Rog I, Inbal D, Danon A ( 2015). ACHT4-driven oxidation of APS1 attenuates starch synthesis under low light intensity in Arabidopsis plants. Proc Natl Acad Sci USA 112, 12876-12881.
32 Feng WK, Wang L, Lu Y, Wang XY ( 2011). A protein oxidase catalysing disulfide bond formation is localized to the chloroplast thylakoids. FEBS J 278, 3419-3430.
33 Fufezan C, Simionato D, Morosinotto T ( 2012). Identification of key residues for pH dependent activation of violaxanthin de-epoxidase from Arabidopsis thaliana.PLoS One 7, e35669.
34 Furt F, Van Oostende C, Widhalm JR, Dale MA, Wertz J, Basset GJC ( 2010). A bimodular oxidoreductase mediates the specific reduction of phylloquinone (vitamin K1) in chloroplasts. Plant J 64, 38-46.
35 Geigenberger P, Fernie AR ( 2014). Metabolic control of redox and redox control of metabolism in plants. Antioxid Redox Signal 21, 1389-1421.
36 Goss R, Lepetit B ( 2015). Biodiversity of NPQ. J Plant Physiol 172, 13-32.
37 Gütle DD, Roret T, Hecker A, Reski R, Jacquot JP ( 2017). Dithiol disulphide exchange in redox regulation of chloroplast enzymes in response to evolutionary and structural constraints. Plant Sci 255, 1-11.
38 Gütle DD, Roret T, Müller SJ, Couturier J, Lemaire SD, Hecker A, Dhalleine T, Buchanan BB, Reski R, Einsle O, Jacquot JP ( 2016). Chloroplast FBPase and SBPase are thioredoxin-linked enzymes with similar architecture but different evolutionary histories. Proc Natl Acad Sci USA 113, 6779-6784.
39 Hall M, Mata-Cabana A, ?kerlund HE, Florencio FJ, Schr?der WP, Lindahl M, Kieselbach T ( 2010). Thioredoxin targets of the plant chloroplast lumen and their implications for plastid function. Proteomics 10, 987-1001.
40 Hallin EI, Guo K, ?kerlund HE ( 2015). Violaxanthin de-epo- xidase disulphides and their role in activity and thermal stability. Photosynth Res 124, 191-198.
41 Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D ( 2013). PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49, 511-523.
42 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.
43 Jacquot JP, Eklund H, Rouhier N, Schürmann P ( 2009). Structural and evolutionary aspects of thioredoxin reductases in photosynthetic organisms. Trends Plant Sci 14, 336-343.
44 J?rvi S, Gollan PJ, Aro EM ( 2013). Understanding the roles of the thylakoid lumen in photosynthesis regulation. Front Plant Sci 4, 434.
45 Kang ZH, Wang GX ( 2016). Redox regulation in the thylakoid lumen. J Plant Physiol 192, 28-37.
46 Karamoko M, Cline S, Redding K, Ruiz N, Hamel PP ( 2011). Lumen Thiol Oxidoreductase 1, a disulfide bond- forming catalyst, is required for the assembly of photosystem II in Arabidopsis. Plant Cell 23, 4462-4475.
47 Karamoko M, Gabilly ST, Hamel PP ( 2013). Operation of trans-thylakoid thiol-metabolizing pathways in photosynthesis.Front Plant Sci 4, 476.
48 Kieselbach T ( 2013). Oxidative folding in chloroplasts. Antioxid Redox Signal 19, 72-82.
49 Kim MR, Khaleda L, Jung IJ, Kim JY, Lee SY, Cha JY, Kim WY ( 2017). Overexpression of chloroplast-localized NAD- PH-dependent thioredoxin reductase C (NTRC) enhances tolerance to photo-oxidative and drought stresses in Ara- bidopsis thaliana.J Plant Biol 60, 175-180.
50 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.
51 Kirchsteiger K, Pulido P, González M, Cejudo FJ ( 2009). NADPH thioredoxin reductase C controls the redox status of chloroplast 2-Cys peroxiredoxins in Arabidopsis thalia- na.Mol Plant 2, 298-307.
52 K?nig J, Muthuramalingam M, Dietz KJ ( 2012). Mechanisms and dynamics in the thiol/disulfide redox regulatory network: transmitters, sensors and targets. Curr Opin Plant Biol 15, 261-268.
53 Laugier E, Tarrago L, Courteille A, Innocenti G, Eymery F, Rumeau D, Issakidis-Bourguet E, Rey P ( 2013). Involvement of thioredoxin y2 in the preservation of leaf methionine sulfoxide reductase capacity and growth under high light. Plant Cell Environ 36, 670-682.
54 Lepist? A, Kangasj?rvi S, Luomala EM, Brader G, Sipari N, Ker?nen M, Kein?nen M, Rintam?ki E ( 2009). Chlo- roplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol 149, 1261-1276.
55 Lindahl M, Kieselbach T ( 2009). Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria. J Proteomics 72, 416-438.
56 Lindahl M, Mata-Cabana A, Kieselbach T ( 2011). The disulfide proteome and other reactive cysteine proteomes: analysis and functional significance. Antioxid Redox Signal 14, 2581-2642.
57 Lu Y, Wang HR, Li H, Cui HR, Feng YG, Wang XY ( 2013). A chloroplast membrane protein LTO1/AtVKOR involving in redox regulation and ROS homeostasis. Plant Cell Rep 32, 1427-1440.
58 Luo T, Fan TT, Liu YN, Rothbart M, Yu J, Zhou SX, Grimm B, Luo MZ ( 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, 118-130.
59 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.
60 Meyer Y, Buchanan BB, Vignols F, Reichheld JP ( 2009). Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43, 335-367.
61 Michalska J, Zauber H, Buchanan BB, Cejudo FJ, Geigenberger P ( 2009). NTRC links built-in thioredoxin to light and sucrose in regulating starch synthesis in chloroplasts and amyloplasts. Proc Natl Acad Sci USA 106, 9908-9913.
62 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.
63 Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB ( 2009). Thioredoxin targets in plants: the first 30 years. J Proteomics 72, 452-474.
64 Motohashi K, Hisabori T ( 2010). CcdA is a thylakoid membrane protein required for the transfer of reducing equivalents from stroma to thylakoid lumen in the higher plant chloroplast. Antioxid Redox Signal 13, 1169-1176.
65 Naranjo B, Díaz-Espejo A, Lindahl M, Cejudo FJ ( 2016 a). 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, 1951-1964.
66 Naranjo B, Mignée C, Krieger-Liszkay A, Hornero-Méndez D, Gallardo-Guerrero L, Cejudo FJ, Lindahl M ( 2016 b). 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.
67 Née G, Zaffagnini M, Trost P, Issakidis-Bourguet E ( 2009). Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: a new role for f-type thioredoxin. FEBS Lett 583, 2827-2832.
68 Nikkanen L, Rintam?ki E ( 2014). Thioredoxin-dependent regulatory networks in chloroplasts under fluctuating light conditions. Philos Trans Roy Soc Lond B Biol Sci 369, 20130224.
69 Nikkanen L, Toivola J, Diaz MG, Rintam?ki E ( 2017). Chloroplast thioredoxin systems: prospects for improving photosynthesis. Philos Trans Roy Soc Lond B Biol Sci 372, 20160474.
70 Nikkanen L, Toivola J, Rintam?ki E ( 2016). Crosstalk between chloroplast thioredoxin systems in regulation of photosynthesis. Plant Cell Environ 39, 1691-1705.
71 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.
72 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.
73 Onoa B, Schneider AR, Brooks MD, Grob P, Nogales E, Geissler PL, Niyogi KK, Bustamante C ( 2014). Atomic force microscopy of photosystem II and its unit cell clustering quantitatively delineate the mesoscale variability in Arabidopsis thylakoids. PLoS One 9, e101470.
74 Pérez-Ruiz JM, González M, Spínola MC, Sandalio LM, Cejudo FJ ( 2009). The quaternary structure of NADPH thioredoxin reductase C is redox-sensitive. Mol Plant 2, 457-467.
75 Pérez-Ruiz JM, Guinea M, Puerto-Galán L, Cejudo FJ ( 2014). NADPH thioredoxin reductase C is involved in redox regulation of the Mg-chelatase I subunit in Arabidopsis thaliana chloroplasts.Mol Plant 7, 1252-1255.
76 Pérez-Ruiz JM, Naranjo B, Ojeda V, Guinea M, Cejudo FJ ( 2017). NTRC-dependent redox balance of 2-Cys peroxiredoxins is needed for optimal function of the photosynthetic apparatus. Proc Natl Acad Sci USA 114, 12069-12074.
77 Puerto-Galán L, Pérez-Ruiz JM, Guinea M, Cejudo FJ ( 2015). The contribution of NADPH thioredoxin reductase C (NTRC) and sulfiredoxin to 2-Cys peroxiredoxin overoxidation in Arabidopsis thaliana chloroplasts.J Exp Bot 66, 2957-2966.
78 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.
79 Rey P, Sanz-Barrio R, Innocenti G, Ksas B, Courteille A, Rumeau D, Issakidis-Bourguet E, Farran I ( 2013). Overexpression of plastidial thioredoxins f and m differentially alters photosynthetic activity and response to oxidative stress in tobacco plants. Front Plant Sci 4, 390.
80 Richter AS, Grimm B ( 2013). Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway in plants. Front Plant Sci 4, 371.
81 Richter AS, Peter E, Rothbart M, Schlicke H, Toivola J, Rintam?ki E, Grimm B ( 2013). Posttranslational influence of NADPH-dependent thioredoxin reductase C on enzymes in tetrapyrrole synthesis. Plant Physiol 162, 63-73.
82 Rouhier N, Cerveau D, Couturier J, Reichheld JP, Rey P ( 2015). Involvement of thiol-based mechanisms in plant development. Biochim Biophys Acta 1850, 1479-1496.
83 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.
84 Sanz-Barrio R, Fernández-San Millán A, Carballeda J, Corral-Martínez P, Seguí-Simarro JM, Farran I ( 2012). Chaperone-like properties of tobacco plastid thioredoxins f and m. J Exp Bot 63, 365-379.
85 Serrato AJ, Fernández-Trijueque J, Barajas-López JDD, Chueca A, Sahrawy M ( 2013). Plastid thioredoxins: a “one-for-all” redox-signaling system in plants. Front Plant Sci 4, 463.
86 Simionato D, Basso S, Zaffagnini M, Lana T, Marzotto F, Trost P, Morosinotto T ( 2015). Protein redox regulation in the thylakoid lumen: the importance of disulfide bonds for violaxanthin de-epoxidase. FEBS Lett 589, 919-923.
87 Stenbaek A, Jensen PE ( 2010). Redox regulation of chlorophyll biosynthesis. Phytochemistry 71, 853-859.
88 Strand DD, Fisher N, Davis GA, Kramer DM ( 2016). Redox regulation of the antimycin A sensitive pathway of cyclic electron flow around photosystem I in higher plant thylakoids. Biochim Biophys Acta 1857, 1-6.
89 Tarrago L, Laugier E, Zaffagnini M, Marchand CH, Le Maréchal P, Lemaire SD, Rey P ( 2010). Plant thioredoxin CDSP32 regenerates 1-cys methionine sulfoxide reductase B activity through the direct reduction of sulfenic acid. J Biol Chem 285, 14964-14972.
90 Thorm?hlen I, Meitzel T, Groysman J, ?chsner AB, von Roepenack-Lahaye E, Naranjo B, Cejudo FJ, Geigenberger P ( 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, 1766-1786.
91 Thorm?hlen 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.
92 Thorm?hlen I, Zupok A, Rescher J, Leger J, Weissenberger S, Groysman J, Orwat A, Chatel-Innocenti G, Issakidis-Bourguet E, Armbruster U, Geigenberger P ( 2017). Thioredoxins play a crucial role in dynamic acclimation of photosynthesis in fluctuating light. Mol Plant 10, 168-182.
93 Tikkanen M, Grieco M, Kangasj?rvi S, Aro EM ( 2010). Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152, 723-735.
94 Toivola J, Nikkanen L, Dahlstr?m KM, Salminen TA, Lepist? A, Vignols F, Rintam?ki 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.
95 Wang P, Liu J, Liu B, Da QE, Feng DR, Su JB, Zhang Y, Wang JF, Wang HB ( 2014). Ferredoxin: thioredoxin reductase is required for proper chloroplast development and is involved in the regulation of plastid gene expression in Arabidopsis thaliana.Mol Plant 7, 1586-1590.
96 Wang P, Liu J, Liu B, Feng DR, Da QE, Wang P, Shu SY, Su JB, Zhang Y, Wang Jf, 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.
97 Wang XY, Dutton RJ, Beckwith J, Boyd D ( 2011). Membrane topology and mutational analysis of Mycobacterium tuberculosis VKOR, a protein involved in disulfide bond formation and a homologue of human vitamin K epoxide reductase.Antioxid Redox Signal 14, 1413-1420.
98 Wulff RP, Lundqvist J, Rutsdottir G, Hansson A, Stenbaek A, Elmlund D, Elmlund H, Jensen PE, Hansson M ( 2011). The activity of barley NADPH-dependent thioredoxin reductase C is independent of the oligomeric state of the protein: tetrameric structure determined by cryoelec- tron microscopy. Biochemistry 50, 3713-3723.
99 Yoshida K, Hara S, Hisabori T ( 2015). Thioredoxin selecti- vity for thiol-based redox regulation of target proteins in chloroplasts. J Biol Chem 290, 14278-14288.
100 Yoshida K, Hisabori T ( 2016). Two distinct redox cascades cooperatively regulate chloroplast functions and sustain plant viability. Proc Natl Acad Sci USA 113, E3967-E3976.
101 Yoshida K, Hisabori T ( 2017). Distinct electron transfer from ferredoxin-thioredoxin reductase to multiple thioredoxin isoforms in chloroplasts. Biochem J 474, 1347-1360.
102 Yoshida K, Matsuoka Y, Hara S, Konno H, Hisabori T ( 2014). Distinct redox behaviors of chloroplast thiol enzymes and their relationships with photosynthetic electron transport in Arabidopsis thaliana.Plant Cell Physiol 55, 1415-1425.
文章导航

/

674-3466/bottom_cn.htm"-->