NDH-1 and NDH-2 Plastoquinone Reductases in Oxygenic Photosynthesis

Annual Review of Plant Biology

Volumn 67, Issue , 2016, Pages 55-80

  Peltier, Gilles ^a   Aro, Eva Mari ^b   Shikanai, Toshiharu ^c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITY OF TURKU   (Finland)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Chloroplast; Chlororespiration; Cyanobacteria; Cyclic electron flow; NDH; Photosynthesis; Respiration

Indexed keywords

FERREDOXIN; NADH DEHYDROGENASE II; OXYGEN; PHOTOSYSTEM I; PHOTOSYSTEM II; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

ADAPTATION; CELL RESPIRATION; CHLOROPLAST; CYANOBACTERIUM; ELECTRON TRANSPORT; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM I; PHOTOSYSTEM II; PHYSIOLOGY; PLANT;

ADAPTATION, PHYSIOLOGICAL; CELL RESPIRATION; CHLOROPLASTS; CYANOBACTERIA; ELECTRON TRANSPORT; FERREDOXINS; NADH DEHYDROGENASE; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS; QUINONE REDUCTASES;

EID: 84968906511     PISSN: 15435008     EISSN: 15452123     Source Type: Book Series    
DOI: 10.1146/annurev-arplant-043014-114752     Document Type: Review

References (152)

1. Alric J. 2014. Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii: (II) involvement of the PGR5-PGRL1 pathway under anaerobic conditions. Biochim. Biophys. Acta 1837:825-34
2. Appel J, SchulzR. 1998. Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising J. Photochem. Photobiol. B 47:1-11
3. Armbruster U, Ruehle T, Kreller R, Strotbek C, Zuehlke J, et al. 2013. The PHOTOSYNTHESIS AFFECTED MUTANT68-LIKE protein evolved from a PSII assembly factor to mediate assembly of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell 25:3926-43
4. Armbruster U, Zuehlke J, Rengstl B, Kreller R, Makarenko E, et al. 2010. The Arabidopsis thylakoid protein PAM68 is required for efficient D1 biogenesis and photosystem II assembly. Plant Cell 22: 3439-60
5. Arteni AA, Zhang P, Battchikova N, Ogawa T, Aro E-M, Boekema EJ. 2006. Structural characterization of NDH-1 complexes of Thermosynechococcus elongatus by single particle electron microscopy. Biochim. Biophys. Acta 1757:1469-75
6. Baltz A, Dang KV, Beyly A, Auroy P, Richaud P, et al. 2014. Plastidial expression of type II NAD(P)H dehydrogenase increases the reducing state of plastoquinones and hydrogen photoproduction rate by the indirect pathway in Chlamydomonas reinhardtii. Plant Physiol. 165:1344-52
7. Bandeiras TM, Salgueiroa CA, Huber H, Gomes CM, Teixeira M. 2003. The respiratory chain of the thermophilic archaeon Sulfolobus metallicus: studies on the type-II NADH dehydrogenase. Biochim. Biophys. Acta 1557:13-19
8. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA. 2013. Crystal structure of the entire respiratory complex I. Nature 494:443-48
9. Battchikova N, Eisenhut M, Aro E-M. 2011. Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim. Biophys. Acta 1807:935-44
10. Battchikova N, Vainonen JP, Vorontsova N, Keranen M, Carmel D, Aro E-M. 2010. Dynamic changes in the proteome of Synechocystis 6803 in response to CO2 limitation revealed by quantitative proteomics. J. Proteome Res. 9:5896-912
11. Battchikova N, Wei L, Du L, Bersanini L, Aro E-M, Ma W. 2011. Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH:plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC6803. J. Biol. Chem. 286:36992-7001
12. Bazil JN, Pannala VR, Dash RK, Beard DA. 2014. Determining the origins of superoxide and hydrogen peroxide in the mammalian NADH:ubiquinone oxidoreductase. Free Radic. Biol. Med. 77:121-29
13. Bennoun P. 1982. Evidence for a respiratory chain in the chloroplast. PNAS 79:4352-56
14. Bernat G, Appel J, Ogawa T, Roegner M. 2011. Distinct roles of multiple NDH-1 complexes in the cyanobacterial electron transport network as revealed by kinetic analysis of P700+ reduction in various ndh-deficient mutants of Synechocystis sp. strain PCC6803. J. Bacteriol. 193:292-95
15. Birungi M, Folea M, Battchikova N, Xu M, Mi H, et al. 2010. Possibilities of subunit localization with fluorescent protein tags and electron microscopy exemplified by a cyanobacterial NDH-1 study. Biochim. Biophys. Acta 1797:1681-86
16. Blazier JC, Guisinger MM, Jansen RK. 2011. Recent loss of plastid-encoded ndh genes within Erodium (Geraniaceae). Plant Mol. Biol. 76:263-72
17. Bohm R, Sauter M, Bock A. 1990. Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol. Microbiol. 4:231-43
18. BraukmannTWA,Kuzmina M, Stefanovic S. 2009. Loss of all plastid ndh genes inGnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Curr. Genet. 55:323-37
19. Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ. 1998. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17:868-76
20. Casano LM, Martin M, Sabater B. 2001. Hydrogen peroxide mediates the induction of chloroplastic Ndh complex under photooxidative stress in barley. Plant Physiol. 125:1450-58
21. Cleland RE, Bendall DS. 1992. Photosystem I cyclic electron transport: measurement of ferredoxinplastoquinone reductase activity. Photosynth. Res. 34:409-18
22. Corneille S, Cournac L, Guedeney G, Havaux M, Peltier G. 1998. Reduction of the plastoquinone pool by exogenous NADH and NADPH in higher plant chloroplasts. Characterization of a NAD(P)Hplastoquinone oxidoreductase activity. Biochim. Biophys. Acta 1363:59-69
23. Cournac L,GuedeneyG, Peltier G, Vignais PM. 2004. Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J. Bacteriol. 186:1737-46
24. Cournac L, Mus F, Bernard L, Guedeney G, Vignais P, Peltier G. 2002. Limiting steps of hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analyzed by light-induced gas exchange transients. Int. J. Hydrogen Energy 27:1229-37
25. Cournac L, Redding K, Ravenel J, Rumeau D, Josse E-M, et al. 2000. Electron flow between photosystem-II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J. Biol. Chem. 275:17256-62
26. Courteille A, Vesa S, Sanz-Barrio R, Cazale A-C, Becuwe-Linka N, et al. 2013. Thioredoxin m4 controls photosynthetic alternative electron pathways in Arabidopsis. Plant Physiol. 161:508-20
27. Dai H, Zhang L, Zhang J, Mi H, Ogawa T, Ma W. 2013. Identification of a cyanobacterial CRR6 protein, Slr1097, required for efficient assembly of NDH-1 complexes in Synechocystis sp. PCC 6803. Plant J. 75:858-66
28. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Nemann DS, et al. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273-85
29. DesplatsC,BeylyA,Cuine S, BernardL,CournacL, Peltier G. 2007. Modification of substrate specificity in single point mutants of Agrobacterium tumefaciens type II NADH dehydrogenase. FEBS Lett. 581: 4017-22
30. Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G. 2009. Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284:4148-57
31. Efremov RG, Sazanov LA. 2012. The coupling mechanism of respiratory complex I-a structural and evolutionary perspective. Biochim. Biophys. Acta 1817:1785-95
32. Endo T, Mi HL, Shikanai T, Asada K. 1997. Donation of electrons to plastoquinone by NAD(P)H dehydrogenase and by ferredoxin-quinone reductase in spinach chloroplasts. Plant Cell Physiol. 38: 1272-77
33. Endo T, Shikanai T, Takabayashi A, Asada K, Sato F. 1999. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 457:5-8
34. Esquivel MG, Amaro HM, Pinto TS, Fevereiro PS, XavierMalcata F. 2011. Efficient H2 production via Chlamydomonas reinhardtii. Trends Biotechnol. 29:595-600
35. Fan X, Zhang J, Li W, Peng L. 2015. The NdhV subunit is required to stabilize the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant J. 82:221-31
36. Fang J, Beattie DS. 2002. Novel FMN-containing rotenone-insensitive NADH dehydrogenase from Trypanosoma brucei mitochondria: isolation and characterization. Biochemistry 41:3065-72
37. Fatihi A, Latimer S, Schmollinger S, Block A, Dussault PH, et al. 2015. A dedicated type II NADPH dehydrogenase performs the penultimate step in the biosynthesis of Vitamin K1 in Synechocystis and Arabidopsis. Plant Cell 27:1730-41
38. Favory JJ, Kobayshi M, Tanaka K, Peltier G, Kreis M, et al. 2005. Specific function of a plastid sigma factor for ndhF gene transcription. Nucleic Acids Res. 33:5991-99
39. Feng Y, Li WF, Li J, Wang JW, Ge JP, et al. 2012. Structural insight into the type-II mitochondrial NADH dehydrogenases. Nature 491:478-82
40. Deleted in proof
41. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. 2012. Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63:1637-61
42. Friedrich T. 2001. Complex I: a chimaera of a redox and conformation-driven proton pump J. Bioenerg. Biomembr. 33:169-77
43. Friedrich T, ScheideD. 2000. The respiratory complex I of bacteria, archaea and eukarya and itsmodule common with membrane-bound multisubunit hydrogenases. FEBS Lett. 479:1-5
44. Friedrich T, Steinmuller K,Weiss H. 1995. The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett. 367:107-11
45. Friedrich T, Weiss H. 1997. Modular evolution of the respiratory NADH:ubiquinone oxidoreductase and the origin of its modules. J. Theor. Biol. 187:529-40
46. Garcia-Andrade J, Ramirez V, Lopez A, Vera P. 2013. Mediated plastid RNA editing in plant immunity. PLOS Pathog. 9:e1003713
47. Geisler DA, Broselid C, Hederstedt L, Rasmusson AG. 2007. Ca2+-binding and Ca2+-independent respiratory NADH and NADPH dehydrogenases of Arabidopsis thaliana. J. Biol. Chem. 282:28455-64
48. Gutekunst K, Chen X, Schreiber K, Kaspar U, Makam S, Appel J. 2014. The bidirectional NiFehydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions. J. Biol. Chem. 289:1930-37
49. Hashimoto M, Endo T, Peltier G, Tasaka M, Shikanai T. 2003. A nucleus-encoded factor, CRR2, is essential for the expression of chloroplast ndhB in Arabidopsis. Plant J. 36:541-49
50. He Z, Zheng F,Wu Y, Li Q, Lv J, et al. 2015. NDH-1L interacts with ferredoxin via the subunit NdhS in Thermosynechococcus elongatus. Photosynth. Res. 126:341-49
51. Heber UW, Santarius KA. 1965. Compartmentation and reduction of pyridine nucleotides in relation to photosynthesis. Biochim. Biophys. Acta 109:390-408
52. Heikal A, Nakatani Y, Dunn E, Weimar MR, Day CL, et al. 2014. Structure of the bacterial type II NADHdehydrogenase: amonotopicmembrane protein with an essential role in energy generation. Mol. Microbiol. 91:950-64
53. Hernandez-PrietoMA,SchoenV,Georg J, BarreiraL, Varela J, et al. 2012. Iron deprivation in Synechocystis: inference of pathways, non-coding RNAs, and regulatory elements from comprehensive expression profiling. G3 2:1475-95
54. HerranenM, Battchikova N, Zhang PP, Graf A, Sirpio S, et al. 2004. Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol. 134:470-81
55. Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, et al. 2013. PGRL1 is the elusive ferredoxinplastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell 49:511-23
56. Hopkinson BM, Young JN, Tansik AL, Binder BJ. 2014. The minimal CO2-concentrating mechanism of Prochlorococcus spp. MED4 is effective and efficient. Plant Physiol. 166:2205-U1519
57. Horvath EM, Peter SO, Joet T, Rumeau D, Cournac L, et al. 2000. Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol. 123:1337-49
58. Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X. 2011. Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. PNAS 108:20820-25
59. Howitt CA, Udall PK, Vermaas WF. 1999. Type 2 NADH dehydrogenases in the cyanobacterium Synechocystis sp. strain PCC 6803 are involved in regulation rather than respiration. J. Bacteriol. 181:3994-4003
60. Hu P, Lv J, Fu P, Mi H. 2013. Enzymatic characterization of an active NDH complex from Thermosynechococcus elongatus. FEBS Lett. 587:2340-45
61. Ido K, Nield J, Fukao Y, Nishimura T, Sato F, Ifuku K. 2014. Cross-linking evidence for multiple interactions of the PsbP and PsbQ proteins in a higher plant photosystem II supercomplex. J. Biol. Chem. 289:20150-57
62. Ifuku K, Endo T, Shikanai T, Aro E-M. 2011. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 52:1560-68
63. Ishihara S,Takabayashi A, IdoK, EndoT, Ifuku K, Sato F. 2007. Distinct functions for the two PsbP-like proteins PPL1 and PPL2 in the chloroplast thylakoid lumen of Arabidopsis. Plant Physiol. 145:668-79
64. IshikawaN, Takabayashi A, Ishida S,Hano Y, Endo T, Sato F. 2008. NDF6: a thylakoid protein specific to terrestrial plants is essential for activity of chloroplastic NAD(P)H dehydrogenase in Arabidopsis. Plant Cell Physiol. 49:1066-73
65. Jans F, Mignolet E, Houyoux PA, Cardol P, Ghysels B, et al. 2008. A type II NAD(P) H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. PNAS 105:20546-51
66. Joet T, Cournac L, Horvath EM, Medgyesy P, Peltier G. 2001. Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol. 125:1919-29
67. Johnson GN. 2011. Physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta 1807:384-89
68. Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P, et al. 2014. Proton Gradient Regulation 5-mediated cyclic electron flow under ATP-or redox-limited conditions: a study of -ATPase pgr5 and -rbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol. 165:438-52
69. Klughammer B, Sultemeyer D, Badger MR, Price GD. 1999. The involvement of NAD(P)H dehydrogenase subunits, NdhD3 and NdhF3, in high-affinity CO2 uptake in Synechococcus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol. Microbiol. 32:1305-15
70. Kouril R, Strouhal O, Nosek L, Lenobel R, Chamrad I, et al. 2014. Structural characterization of a plant photosystem I and NAD(P)H dehydrogenase supercomplex. Plant J. 77:568-76
71. Lascano HR, Casano LM, Martin M, Sabater B. 2003. The activity of the chloroplastic Ndh complex is regulated by phosphorylation of the NDH-F subunit. Plant Physiol. 132:256-62
72. Livingston AK, Cruz JA, Kohzuma K, Dhingra A, Kramer DM. 2010. An Arabidopsis mutant with high cyclic electron flow around photosystem I (hcef ) involving the NADPH dehydrogenase complex. Plant Cell 22:221-33
73. Livingston AK, Kanazawa A, Cruz JA, Kramer DM. 2010. Regulation of cyclic electron flow in C3 plants: differential effects of limiting photosynthesis at ribulose-1,5-bisphosphate carboxylase/oxygenase and glyceraldehyde-3-phosphate dehydrogenase. Plant Cell Environ. 33:1779-88
74. Maeda S, Badger MR, Price GD. 2002. Novel gene products associated with NdhD3/D4-containing NDH-1 complexes are involved in photosynthetic CO2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol. Microbiol. 43:425-35
75. Maier UG, Bozarth A, Funk HT, Zauner S, Rensing SA, et al. 2008. Complex chloroplast RNA metabolism: just debugging the genetic programme BMC Biol. 6:36
76. Marreiros BC, Batista AP,Duarte AMS, Pereira MM. 2013. Amissing link between complex I and group 4 membrane-bound NiFe hydrogenases. Biochim. Biophys. Acta 1827:198-209
77. Martin M, Funk HT, Serrot PH, Poltnigg P, Sabater B. 2009. Functional characterization of the thylakoid Ndh complex phosphorylation by site-directed mutations in the ndhF gene. Biochim. Biophys. Acta 1787:920-28
78. Mathiesen C,Hagerhall C. 2002. Transmembrane topology of the NuoL,MandNsubunits ofNADH: quinone oxidoreductase and their homologues among membrane-bound hydrogenases and bona fide antiporters. Biochim. Biophys. Acta 1556:121-32
79. Mathiesen C, Hagerhall C. 2003. The "antiporter module" of respiratory chain complex I includes the MrpC/NuoK subunit-a revision of the modular evolution scheme. FEBS Lett. 549:7-13
80. MatsubayashiT,WakasugiT, ShinozakiK, Yamaguchi-ShinozakiK, ZaitaN, et al. 1987. Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol. Gen. Genet. 210:385-93
81. Melis A, Happe T. 2001. Hydrogen production. Green algae as a source of energy. Plant Physiol. 127: 740-48
82. Melo AM, Bandeiras TM, Teixeira M. 2004. New insights into type II NAD(P)H:quinone oxidoreductases. Microbiol. Mol. Biol. Rev. 68:603-16
83. Michalecka AM, Svensson AS, Johansson FI, Agius SC, Johanson U, et al. 2003. Arabidopsis genes encoding mitochondrial type II NAD(P)H dehydrogenases have different evolutionary origin and show distinct responses to light. Plant Physiol. 133:642-52
84. Mimaki M, Wang X, McKenzie M, Thorburn DR, Ryan MT. 2012. Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 1817:851-62
85. Moparthi VK, Kumar B,Mathiesen C, Hagerhall C. 2011. Homologous protein subunits from Escherichia coli NADH:quinone oxidoreductase can functionally replace MrpA andMrpD in Bacillus subtilis. Biochim. Biophys. Acta 1807:427-36
86. Munekage Y, HashimotoM,Miyaka C, Tomizawa KI, Endo T, et al. 2004. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579-82
87. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361-71
88. Mus F, Cournac L, Cardettini V, Caruana A, Peltier G. 2005. Inhibitor studies on non-photochemical plastoquinone reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1708:322-32
89. Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Ewollman F-A. 2015. The plastid terminal oxidase: Its elusive function points tomultiple contributions to plastid physiology. Annu. Rev. Plant Biol. 66:49-74
90. NeuhausHE, EmesMJ. 2000. Nonphotosyntheticmetabolism in plastids. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:111-40
91. Neyland R,Urbatsch LE. 1996. The ndhF chloroplast gene detected in all vascular plant divisions. Planta 200:273-77
92. Obayashi T, Kinoshita K, Nakai K, Shibaoka M, Hayashi S, et al. 2007. ATTED-II: a database of coexpressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res. 35:D863-69
93. Ogawa T. 1991. A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. PNAS 88:4275-79
94. Ohkawa H, Pakrasi HB, Ogawa T. 2000. Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp. strain PCC6803. J. Biol. Chem. 275:31630-34
95. Ohkawa H, Sonoda M, Shibata M, Ogawa T. 2001. Localization of NAD(P)H dehydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 183:4938-39
96. Ohyama K, FukuzawaH,KohchiT, ShiraiH, SanoT, et al. 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572-74
97. Ohyama K, Kohchi T, Sano T, Yamada Y. 1988. Newly identified groups of genes in chloroplasts. Trends Biochem. Sci. 13:19-22
98. Peltier G, Cournac L. 2002. Chlororespiration. Annu. Rev. Plant Biol. 53:523-50
99. Peltier G, Tolleter D, Billon E, Cournac L. 2010. Auxiliary electron transport pathways in chloroplasts of microalgae. Photosynth. Res. 106:19-31
100. Peng L, Cai W, Shikanai T. 2010. Chloroplast stromal proteins, CRR6 and CRR7, are required for assembly of the NAD(P)H dehydrogenase subcomplex A in Arabidopsis. Plant J. 63:203-11
101. Peng L, Fukao Y, Fujiwara M, Shikanai T. 2012. Multistep assembly of chloroplast NADH dehydrogenase-like subcomplex A requires several nucleus-encoded proteins, including CRR41 and CRR42, in Arabidopsis. Plant Cell 24:202-14
102. Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T. 2009. Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21:3623-40
103. Peng L, Fukao Y, Myouga F, Motohashi R, Shinozaki K, Shikanai T. 2011. A chaperonin subunit with unique structures is essential for folding of a specific substrate. PLOS Biol. 9:e1001040
104. Peng L, Shikanai T. 2011. Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol. 155:1629-39
105. Peng L, Shimizu H, Shikanai T. 2008. The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283:34873-79
106. Peng L, Yamamoto H, Shikanai T. 2011. Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochim. Biophys. Acta 1807:945-53
107. Peredo EL, King UM, Les DH. 2013. The plastid genome of Najas flexilis: Adaptation to submersed environments is accompanied by the complete loss of theNDHcomplex in an aquatic angiosperm. PLOS ONE 8:e68591
108. Piller LE, Besagni C, Ksas B, Rumeau D, Brehelin C, et al. 2011. Chloroplast lipid droplet type II NAD(P)H quinone oxidoreductase is essential for prenylquinone metabolism and Vitamin K1 accumulation. PNAS 108:14354-59
109. Piller LE, Glauser G, Kessler F, Besagni C. 2014. Role of plastoglobules in metabolite repair in the tocopherol redox cycle. Front. Plant Sci. 5:298
110. Price GD, Badger MR, Woodger FJ, Long BM. 2008. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J. Exp. Bot. 59:1441-61
111. Queval G, Foyer CH. 2012. Redox regulation of photosynthetic gene expression. Philos. Trans. R. Soc. B 367:3475-85
112. Ravenel J, Peltier G, Havaux M. 1994. The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251-59
113. Rumeau D, Becuwe-Linka N, Beyly A, Louwagie M, Garin J, Peltier G. 2005. New subunits NDH-M,-N, and-O, encoded by nuclear genes, are essential for plastidNdh complex functioning in higher plants. Plant Cell 17:219-32
114. Rumeau D, Peltier G, Cournac L. 2007. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30:1041-51
115. Sazanov LA, Burrows PA, Nixon PJ. 1998. The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes. PNAS 95:1319-24
116. Scherer S. 1990.Dophotosynthetic and respiratory electron transport chains share redox proteins. Trends Biochem. Sci. 15:458-62
117. Schwarz D, Schubert H, Georg J, Hess WR, Hagemann M. 2013. The gene sml0013 of Synechocystis species strain PCC 6803 encodes for a novel subunit of the NAD(P)H oxidoreductase or complex I that is ubiquitously distributed among cyanobacteria. Plant Physiol. 163:1191-202
118. Shibata M, Ohkawa H, Kaneko T, Fukuzawa H, Tabata S, et al. 2001. Distinct constitutive and low-CO2-induced CO2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. PNAS 98:11789-94
119. Shikanai T. 2015. RNA editing in plants: machinery and flexibility of site recognition. Biochim. Biophys. Acta 1847:779-85
120. Shikanai T, Aro E-M. 2016. Evolution of photosynthetic NDH-1: structure and physiological function. In Advances in Photosynthesis and Respiration, ed. Govindjee, TD Sharkey. Dordrecht, Neth.: Springer. In press
121. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A. 1998. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. PNAS 95:9705-9
122. Shimizu H, Shikanai T. 2007. Dihydrodipicolinate reductase-like protein, CRR1, is essential for chloroplast NAD(P)H dehydrogenase in Arabidopsis. Plant J. 52:539-47
123. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N, et al. 1986. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 5:2043-49
124. Sirpioe S, Allahverdiyeva Y, Holmstrom M, Khrouchtchova A, Haldrup A, et al. 2009. Novel nuclearencoded subunits of the chloroplast NAD(P)H dehydrogenase complex. J. Biol. Chem. 284:905-12
125. Stefanovic S, Olmstead RG. 2005. Down the slippery slope: plastid genome evolution in Convolvulaceae. J. Mol. Evol. 61:292-305
126. Strand DD, Livingston AK, Satoh-Cruz M, Froehlich JE, Maurino VG, Kramer DM. 2015. Activation of cyclic electron flow by hydrogen peroxide in vivo. PNAS 112:5539-44
127. SuorsaM,Sirpio S, PaakkarinenV,KumariN,HolmstromM,Aro E-M. 2010.Twoproteins homologous to PsbQ are novel subunits of the chloroplast NAD(P)H dehydrogenase. Plant Cell Physiol. 51:877-83
128. Takabayashi A, Ishikawa N, Obayashi T, Ishida S, Obokata J, et al. 2009. Three novel subunits of Arabidopsis chloroplastic NAD(P)H dehydrogenase identified by bioinformatic and reverse genetic approaches. Plant J. 57:207-19
129. Takabayashi A, Kishine M, Asada K, Endo T, Sato F. 2005. Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. PNAS 102:16898-903
130. Takenaka M, Zehrmann A, Verbitskiy D, Haertel B, Brennicke A. 2013. RNA editing in plants and its evolution. Annu. Rev. Genet. 47:335-52
131. Terashima M, Petroutsos D, Hüdig M, Tolstygina I, Trompelt K, et al. 2012. Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. PNAS 109:17717-22
132. Terashima M, Specht M, Naumann B, Hippler M. 2010. Characterizing the anaerobic response of Chlamydomonas reinhardtii by quantitative proteomics. Mol. Cell. Proteom. 9:1514-32
133. Thomas J-C, Ughy B, Lagoutte B, Ajlani G. 2006. A second isoform of the ferredoxin: NADP oxidoreductase generated by an in-frame initiation of translation. PNAS 103:18368-73
134. Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, et al. 2011. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619-30
135. Turmel M, Gagnon M-C, O'Kelly CJ, Otis C, Lemieux C. 2009. The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. Mol. Biol. Evol. 26:631-48
136. Ueda M, Kuniyoshi T, Yamamoto H, Sugimoto K, Ishizaki K, et al. 2012. Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. Plant J. 72:683-93
137. Vogel RO, Dieteren CEJ, van den Heuvel LPWJ, Willems PHGM, Smeitink JAM, et al. 2007. Identification of mitochondrial complex I assembly intermediates by tracing tagged NDUFS3 demonstrates the entry point of mitochondrial subunits. J. Biol. Chem. 282:7582-90
138. Wagner V, Ullmann K,Mollwo A, KaminskiM,MittagM, Kreimer G. 2008. The phosphoproteome of a Chlamydomonas reinhardtii eyespot fraction includes key proteins of the light signaling pathway. Plant Physiol. 146:772-88
139. Wang C, Yamamoto H, Shikanai T. 2015. Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim. Biophys. Acta 1847:931-38
140. Wang HL, Postier BL, Burnap RL. 2004. Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J. Biol. Chem. 279:5739-51
141. Wang Y, Stessman DJ, Spalding MH. 2015. The CO2 concentrating mechanism and photosynthetic carbon assimilation in limiting CO2: howChlamydomonas works against the gradient. Plant J. 82:429-48
142. Wulfhorst H, Franken LE, Wessinghage T, Boekema EJ, Nowaczyk MM. 2014. The 5 kDa protein NdhP is essential for stable NDH-1L assembly in Thermosynechococcus elongatus. PLOS ONE 9:e103584
143. Xu L, Law SR, Murcha MW,Whelan J, Carrie C. 2013. The dual targeting ability of type II NAD(P)H dehydrogenases arose early in land plant evolution. BMC Plant Biol. 13:100
144. Xu M, Ogawa T, Pakrasi HB, Mi H. 2008. Identification and localization of the CupB protein involved in constitutive CO2 uptake in the cyanobacterium, Synechocystis sp. strain PCC 6803. Plant Cell Physiol. 49:994-97
145. Yabuta S, Ifuku K, Takabayashi A, Ishihara S, Ido K, et al. 2010. Three PsbQ-like proteins are required for the function of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Cell Physiol. 51:866-76
146. Yamamoto H, Peng L, Fukao Y, Shikanai T. 2011. An Src homology 3 domain-like fold protein forms a ferredoxin binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23:1480-93
147. Yamamoto H, Shikanai T. 2013. In planta mutagenesis of Src homology 3 domain-like fold of NdhS, a ferredoxin-binding subunit of the chloroplast NADH dehydrogenase-like complex in Arabidopsis: a conserved Arg-193 plays a critical role in ferredoxin binding. J. Biol. Chem. 288:36328-37
148. Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A. 2011. Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J. 68:966-76
149. Zhang PP, Battchikova N, Jansen T, Appel J, Ogawa T, AroE-M. 2004. Expression and functional roles of the two distinct NDH-1 complexes and the carbon acquisition complex NdhD3/NdhF3/CupA/Sll1735 in Synechocystis sp. PCC 6803. Plant Cell 16:3326-40
150. Zhang PP, Battchikova N, Paakkarinen V, Katoh H, Iwai M, et al. 2005. Isolation, subunit composition and interaction of theNDH-1complexes from Thermosynechococcus elongatus BP-1. Biochem. J. 390:513-20
151. Zhao J, Gao F,Zhang J, Ogawa T,MaW.2014. NdhO, a subunit ofNADPHdehydrogenase, destabilizes medium size complex of the enzyme in Synechocystis sp. strain PCC 6803. J. Biol. Chem. 289:26669-76
152. Zhao J, Rong W, Gao F, Ogawa T, Ma W. 2015. Subunit Q is required to stabilize the large complex of NADPH dehydrogenase in Synechocystis sp. strain PCC 6803. Plant Physiol. 168:443-51