1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 66, 2015
  5. Article

Annual Review of Plant Biology

Volume 66, 2015

The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple Contributions to Plastid Physiology

Abstract

Plastids have retained from their cyanobacterial ancestor a fragment of the respiratory electron chain comprising an NADPH dehydrogenase and a diiron oxidase, which sustain the so-called chlororespiration pathway. Despite its very low turnover rates compared with photosynthetic electron flow, knocking out the plastid terminal oxidase (PTOX) in plants or microalgae leads to severe phenotypes that encompass developmental and growth defects together with increased photosensitivity. On the basis of a phylogenetic and structural analysis of the enzyme, we discuss its physiological contribution to chloroplast metabolism, with an emphasis on its critical function in setting the redox poise of the chloroplast stroma in darkness. The emerging picture of PTOX is that of an enzyme at the crossroads of a variety of metabolic processes, such as, among others, the regulation of cyclic electron transfer and carotenoid biosynthesis, which have in common their dependence on the redox state of the plastoquinone pool, set largely by the activity of PTOX in darkness.

Keyword(s): carotenoid biosynthesis, chloroplast, chlororespiration, electron transfer, PTOX, redox poise, retrograde signaling, structural model
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043014-114744
2015-04-29
2024-05-04
Loading full text...

Full text loading...

/deliver/fulltext/arplant/66/1/annurev-arplant-043014-114744.html?itemId=/content/journals/10.1146/annurev-arplant-043014-114744&mimeType=html&fmt=ahah

Literature Cited

  1. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D. 1.  et al. 2012. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 59:429–93 [Google Scholar]
  2. Ahmad N, Michoux F, Nixon PJ. 2.  2012. Investigating the production of foreign membrane proteins in tobacco chloroplasts: expression of an algal plastid terminal oxidase. PLOS ONE 7:e41722 [Google Scholar]
  3. Albertsson P. 3.  2001. A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6:349–58 [Google Scholar]
  4. Alric J, Lavergne J, Rappaport F. 4.  2010. Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii (I) aerobic conditions. Biochim. Biophys. Acta 1797:44–51 [Google Scholar]
  5. Aluru MR, Bae H, Wu D, Rodermel S. 5.  2001. The Arabidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiol. 127:67–77 [Google Scholar]
  6. Aluru MR, Stessman DJ, Spalding MH, Rodermel S. 6.  2007. Alterations in photosynthesis in Arabidopsis lacking IMMUTANS, a chloroplast terminal oxidase. Photosynth. Res. 91:11–23 [Google Scholar]
  7. Andersson ME, Nordlund P. 7.  1999. A revised model of the active site of alternative oxidase. FEBS Lett. 449:17–22 [Google Scholar]
  8. Apel K, Hirt H. 8.  2004. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55:373–99 [Google Scholar]
  9. Avenson TJ, Cruz JA, Kanazawa A, Kramer DM. 9.  2005. Regulating the proton budget of higher plant photosynthesis. PNAS 102:9709–13 [Google Scholar]
  10. Bailey S, Melis A, Mackey KRM, Cardol P, Finazzi G. 10.  et al. 2008. Alternative photosynthetic electron flow to oxygen in marine Synechococcus. Biochim. Biophys. Acta 1777:269–76 [Google Scholar]
  11. Barr J, White WS, Chen L, Bae H, Rodermel S. 11.  2004. The GHOST terminal oxidase regulates developmental programming in tomato fruit. Plant Cell Environ. 27:840–52 [Google Scholar]
  12. Bendall DS, Bonner WD. 12.  1971. Cyanide-insensitive respiration in plant mitochondria. Plant Physiol. 47:236–45 [Google Scholar]
  13. Bennoun P. 13.  1982. Evidence for a respiratory chain in the chloroplast. PNAS 79:4352–56 [Google Scholar]
  14. Bennoun P. 14.  1994. Chlororespiration revisited: mitochondrial-plastid interactions in Chlamydomonas. Biochim. Biophys. Acta 1186:59–66 [Google Scholar]
  15. Bennoun P. 15.  2001. Chlororespiration and the process of carotenoid biosynthesis. Biochim. Biophys. Acta 1506:133–42 [Google Scholar]
  16. Bennoun P. 16.  2002. The present model for chlororespiration. Photosynth. Res. 73:273–77 [Google Scholar]
  17. Berthold DA, Andersson ME, Nordlund P. 17.  2000. New insight into the structure and function of the alternative oxidase. Biochim. Biophys. Acta. 1460:241–54 [Google Scholar]
  18. Berthold DA, Stenmark P. 18.  2003. Membrane-bound diiron carboxylate proteins. Annu. Rev. Plant Biol. 54:497–517 [Google Scholar]
  19. Bulté L, Gans P, Rebéillé F, Wollman F-A. 19.  1990. ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020:72–80 [Google Scholar]
  20. Bulté L, Wollman F-A. 20.  1992. Evidence for a selective destabilization of an integral membrane protein, the cytochrome b6/f complex, during gametogenesis in Chlamydomonas reinhardtii. Eur. J. Biochem. 204:327–36 [Google Scholar]
  21. Burki F, Flegontov P, Oborník M, Cihlár J, Pain A. 21.  et al. 2012. Re-evaluating the green versus red signal in eukaryotes with secondary plastid of red algal origin. Genome Biol. Evol. 4:626–35 [Google Scholar]
  22. Busch F, Hüner NPA, Ensminger I. 22.  2008. Increased air temperature during simulated autumn conditions impairs photosynthetic electron transport between photosystem II and photosystem I. Plant Physiol. 147:402–14 [Google Scholar]
  23. Cardol P, Bailleul B, Rappaport F, Derelle E, Béal D. 23.  et al. 2008. An original adaptation of photosynthesis in the marine green alga Ostreococcus. PNAS 105:7881–86 [Google Scholar]
  24. Carol P, Kuntz M. 24.  2001. A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci. 6:31–36 [Google Scholar]
  25. Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G. 25.  et al. 1999. Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation. Plant Cell 11:57–68 [Google Scholar]
  26. Chai T-T, Colmer T, Finnegan P. 26.  2010. Alternative oxidase, a determinant of plant gametophyte fitness and fecundity. Plant Signal. Behav. 5:604–6 [Google Scholar]
  27. Costa JH, McDonald AE, Arnholdt-Schmitt B, Fernandes de Melo D. 27.  2014. A classification scheme for alternative oxidases reveals the taxonomic distribution and evolutionary history of the enzyme in angiosperms. Mitochondrion 19:172–83 [Google Scholar]
  28. Cramer WA, Hasan SS, Yamashita E. 28.  2011. The Q cycle of cytochrome bc complexes: a structure perspective. Biochim. Biophys. Acta 1807:788–802 [Google Scholar]
  29. Cvetkovska M, Dahal K, Alber NA, Jin C, Cheung M, Vanlerberghe GC. 29.  2014. Knockdown of mitochondrial alternative oxidase induces the “stress state” of signaling molecule pools in Nicotiana tabacum, with implications for stomatal function. New Phytol. 203:449–61 [Google Scholar]
  30. Delosme R, Olive J, Wollman F-A. 30.  1996. Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1273:150–58 [Google Scholar]
  31. Domonkos I, Kis M, Gombos Z, Ughy B. 31.  2013. Carotenoids, versatile components of oxygenic photosynthesis. Prog. Lipid Res. 52:539–61 [Google Scholar]
  32. Eberhard S, Finazzi G, Wollman F-A. 32.  2008. The dynamics of photosynthesis. Annu. Rev. Genet. 42:463–515 [Google Scholar]
  33. Feilke K, Yu Q, Beyer P, Sétif P, Krieger-Liszkay A. 33.  2014. In vitro analysis of the plastid terminal oxidase in photosynthetic electron transport. Biochim. Biophys. Acta 1837:1–30 [Google Scholar]
  34. Finazzi G, Rappaport F. 34.  1998. In vivo characterization of the electrochemical proton gradient generated in darkness in green algae and its kinetic effects on cytochrome b6f turnover. Biochemistry 37:9999–10005 [Google Scholar]
  35. Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix J-D. 35.  et al. 2002. Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep. 3:280–85 [Google Scholar]
  36. Foudree A, Aluru M, Rodermel S. 36.  2010. PDS activity acts as a rheostat of retrograde signaling during early chloroplast biogenesis. Plant Signal. Behav. 5:1629–32 [Google Scholar]
  37. Foudree A, Putarjunan A, Kambakam S, Nolan T, Fussell J. 37.  et al. 2012. The mechanism of variegation in immutans provides insight into chloroplast biogenesis. Front. Plant Sci. 3:260 [Google Scholar]
  38. Fu A, Aluru M, Rodermel S. 38.  2009. Conserved active site sequences in Arabidopsis plastid terminal oxidase (PTOX): in vitro and in planta mutagenesis studies. J. Biol. Chem. 284:22625–32 [Google Scholar]
  39. Fu A, Liu H, Yu F, Kambakam S, Luan S, Rodermel S. 39.  2012. Alternative oxidases (AOX1a and AOX2) can functionally substitute for plastid terminal oxidase in Arabidopsis chloroplasts. Plant Cell 24:1579–95 [Google Scholar]
  40. Fu A, Park S, Rodermel S. 40.  2005. Sequences required for the activity of PTOX (IMMUTANS), a plastid terminal oxidase: in vitro and in planta mutagenesis of iron-binding sites and a conserved sequence that corresponds to Exon 8. 28042489–96
  41. Galzerano D, Feilke K, Schaub P, Beyer P, Krieger-Liszkay A. 41.  2014. Effect of constitutive expression of bacterial phytoene desaturase CRTI on photosynthetic electron transport in Arabidopsis thaliana. Biochim. Biophys. Acta 1837:1–9 [Google Scholar]
  42. Goss R, Jakob T. 42.  2010. Regulation and function of xanthophyll cycle-dependent photoprotection in algae. Photosynth. Res. 106:103–22 [Google Scholar]
  43. Gräber P. 43.  1994. The H+-ATPase from chloroplasts: energetics of the catalytic cycle. Biochim. Biophys. Acta 1187:171–76 [Google Scholar]
  44. Grossman AR, Lohr M, Im CS. 44.  2004. Chlamydomonas reinhardtii in the landscape of pigments. Annu. Rev. Genet. 38:119–73 [Google Scholar]
  45. Gupta KJ, Zabalza A, van Dongen JT. 45.  2009. Regulation of respiration when the oxygen availability changes. Physiol. Plant. 137:383–91 [Google Scholar]
  46. Gwak Y, Hwang Y-S, Wang B, Kim M, Jeong J. 46.  et al. 2014. Comparative analyses of lipidomes and transcriptomes reveal a concerted action of multiple defensive systems against photooxidative stress in Haematococcus pluvialis. J. Exp. Bot. 65:4317–34 [Google Scholar]
  47. Harris EH. 47.  2008. The Chlamydomonas Sourcebook. 1 Introduction to Chlamydomonas and Its Laboratory Use Oxford, UK: Academic, 2nd ed.. [Google Scholar]
  48. Hart SE, Schlarb-Ridley BG, Bendall DS, Howe CJ. 48.  2005. Terminal oxidases of cyanobacteria. Biochem. Soc. Trans. 33:832–35 [Google Scholar]
  49. Hassani BKB, Steunou A-SA, Liotenberg SS, Reiss-Husson FF, Astier CC, Ouchane SS. 49.  2010. Adaptation to oxygen: role of terminal oxidases in photosynthesis initiation in the purple photosynthetic bacterium, Rubrivivax gelatinosus. J. Biol. Chem. 285:19891–99 [Google Scholar]
  50. Heyno E, Gross CM, Laureau C, Culcasi M, Pietri S, Krieger-Liszkay A. 50.  2009. Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J. Biol. Chem. 284:31174–80 [Google Scholar]
  51. Houille-Vernes L, Rappaport F, Wollman F-A, Alric J, Johnson X. 51.  2011. Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. PNAS 108:20820–25 [Google Scholar]
  52. Hüner NPA, Bode R, Dahal K, Hollis L, Rosso D. 52.  et al. 2012. Chloroplast redox imbalance governs phenotypic plasticity: the “grand design of photosynthesis” revisited. Front. Plant Sci. 3:255 [Google Scholar]
  53. Ibáñez H, Ballester A, Muñoz R, Quiles MJ. 53.  2010. Chlororespiration and tolerance to drought, heat and high illumination. J. Plant Physiol. 167:732–38 [Google Scholar]
  54. Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M. 54.  et al. 2012. Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth. Res. 113:191–206 [Google Scholar]
  55. Janero DR, Barrnett R. 55.  1982. Thylakoid membrane biogenesis in Chlamydomonas reinhardtii 137+. II. Cell-cycle variations in the synthesis and assembly of pigment. J. Cell Biol. 93:411–16 [Google Scholar]
  56. Jans F, Mignolet E, Houyoux P-A, Cardol P, Ghysels B. 56.  et al. 2008. A type II NAD(P)H dehydrogenase mediates light-independent plastoquinone reduction in the chloroplast of Chlamydomonas. PNAS 105:20546–51 [Google Scholar]
  57. Joët T, Genty B, Josse E-M, Kuntz M, Cournac L, Peltier G. 57.  2002. Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J. Biol. Chem. 277:31623–30 [Google Scholar]
  58. Johnson GN. 58.  2011. Physiology of PSI cyclic electron transport in higher plants. Biochim. Biophys. Acta 1807:384–89 [Google Scholar]
  59. Johnson MP, Vasilev C, Olsen JD, Hunter CN. 59.  2014. Nanodomains of cytochrome b6f and photosystem II complexes in spinach grana thylakoid membranes. Plant Cell 26:3051–61 [Google Scholar]
  60. Johnson X, Alric J. 60.  2012. Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J. Biol. Chem. 287:26445–52 [Google Scholar]
  61. Johnson X, Alric J. 61.  2013. Central carbon metabolism and electron transport in Chlamydomonas reinhardtii: metabolic constraints for carbon partitioning between oil and starch. Eukaryot. Cell 12:776–93 [Google Scholar]
  62. Joliot PA, Béal D, Joliot A. 62.  2004. Cyclic electron flow under saturating excitation of dark-adapted Arabidopsis leaves. Biochim. Biophys. Acta 1656:166–76 [Google Scholar]
  63. Joliot PA, Johnson GN. 63.  2011. Regulation of cyclic and linear electron flow in higher plants. PNAS 108:13317–22 [Google Scholar]
  64. Joliot PA, Joliot A. 64.  2002. Cyclic electron transfer in plant leaf. PNAS 99:10209–14 [Google Scholar]
  65. Joliot PA, Joliot A. 65.  2005. Quantification of cyclic and linear flows in plants. PNAS 102:4913–18 [Google Scholar]
  66. Joliot PA, Joliot A. 66.  2008. Quantification of the electrochemical proton gradient and activation of ATP synthase in leaves. Biochim. Biophys. Acta 1777:676–83 [Google Scholar]
  67. Josse E-M, Alcaraz J-P, Laboure A-M, Kuntz M. 67.  2003. In vitro characterization of a plastid terminal oxidase (PTOX). Eur. J. Biochem. 270:3787–94 [Google Scholar]
  68. Josse E-M, Simkin AJ, Gaffé J, Laboure AM, Kuntz M, Carol P. 68.  2000. A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 123:1427–36 [Google Scholar]
  69. Kanervo E, Singh M, Suorsa M, Paakkarinen V, Aro E. 69.  et al. 2008. Expression of protein complexes and individual proteins upon transition of etioplasts to chloroplasts in pea (Pisum sativum). Plant Cell Physiol. 49:396–410 [Google Scholar]
  70. Keeling PJ. 70.  2013. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 64:583–607 [Google Scholar]
  71. Keeling PJ, Palmer JD. 71.  2008. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 9:605–18 [Google Scholar]
  72. Kido Y, Sakamoto K, Nakamura K, Harada M, Suzuki T. 72.  et al. 2010. Purification and kinetic characterization of recombinant alternative oxidase from Trypanosoma brucei brucei. Biochim. Biophys. Acta 1797:443–50 [Google Scholar]
  73. Kim C, Meskauskiene R, Apel K, Laloi C. 73.  2008. No single way to understand singlet oxygen signalling in plants. EMBO Rep. 9:435–39 [Google Scholar]
  74. Kirchhoff H. 74.  2014. Diffusion of molecules and macromolecules in thylakoid membranes. Biochim. Biophys. Acta 1837:495–502 [Google Scholar]
  75. Kolberg M, Strand KR, Graff P, Andersson KK. 75.  2004. Structure, function, and mechanism of ribonucleotide reductases. Biochim. Biophys. Acta 1699:1–34 [Google Scholar]
  76. Kramer DM, Cruz JA, Kanazawa A. 76.  2003. Balancing the central roles of the thylakoid proton gradient. Trends Plant Sci. 8:27–32 [Google Scholar]
  77. Krebs C, Bollinger JM, Booker SJ. 77.  2011. Cyanobacterial alkane biosynthesis further expands the catalytic repertoire of the ferritin-like “di-iron-carboxylate” proteins. Curr. Opin. Chem. Biol. 15:291–303 [Google Scholar]
  78. Kurtz DM Jr. 78.  2006. Avoiding high-valent iron intermediates: superoxide reductase and rubrerythrin. J. Inorg. Biochem. 100:679–93 [Google Scholar]
  79. Laureau C, de Paepe R, Latouche G, Moreno-Chacón M, Finazzi G. 79.  et al. 2013. Plastid terminal oxidase (PTOX) has the potential to act as a safety valve for excess excitation energy in the alpine plant species Ranunculus glacialis L. Plant Cell Environ. 36:1296–310 [Google Scholar]
  80. Lavergne J. 80.  2009. Clustering of electron transfer components: kinetic and thermodynamic consequences. Photosynthesis Silico: Understanding Complexity from Molecules to Ecosystems A Laisk, L Nedbal, Govindjee 177–205 Dordrecht, Neth.: Springer [Google Scholar]
  81. Lavergne J, Joliot PA. 81.  1991. Restricted diffusion in photosynthetic membranes. Trends Biochem. Sci. 16:129–34 [Google Scholar]
  82. Lennon AM, Prommeenate P, Nixon PJ. 82.  2003. Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218:254–60 [Google Scholar]
  83. Li F, Murillo C, Wurtzel ET. 83.  2007. Maize Y9 encodes a product essential for 15-cis-ζ-carotene isomerization. Plant Physiol. 144:1181–89 [Google Scholar]
  84. Li Y, Sommerfeld M, Chen F, Hu Q. 84.  2008. Consumption of oxygen by astaxanthin biosynthesis: a protective mechanism against oxidative stress in Haematococcus pluvialis (Chlorophyceae). J. Plant Physiol. 165:1783–97 [Google Scholar]
  85. Li Z, Wakao S, Fischer BB, Niyogi KK. 85.  2009. Sensing and responding to excess light. Annu. Rev. Plant Biol. 60:239–60 [Google Scholar]
  86. Losada M. 86.  1992. The double function of oxygen in bioenergetics. Bioelectrochem. Bioenerg. 28:31–42 [Google Scholar]
  87. Majeran W, Olive J, Drapier D, Vallon O, Wollman F-A. 87.  2001. The light sensitivity of ATP synthase mutants of Chlamydomonas reinhardtii. Plant Physiol. 126:421–33 [Google Scholar]
  88. Martín M, Sabater B. 88.  2010. Plastid ndh genes in plant evolution. Plant Physiol. Biochem. 48:636–45 [Google Scholar]
  89. McDonald AE. 89.  2008. Alternative oxidase: an inter-kingdom perspective on the function and regulation of this broadly distributed “cyanide-resistant” terminal oxidase. Funct. Plant Biol. 35:535 [Google Scholar]
  90. McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel S, Hüner NPA. 90.  2011. Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim. Biophys. Acta 1807:954–67 [Google Scholar]
  91. McDonald AE, Vanlerberghe GC. 91.  2006. Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp. Biochem. Physiol. D 1:357–64 [Google Scholar]
  92. Moore AL, Shiba T, Young L, Harada S, Kita K, Ito K. 92.  2013. Unraveling the heater: new insights into the structure of the alternative oxidase. Annu. Rev. Plant Biol. 64:637–63 [Google Scholar]
  93. Moseley JL, Chang CW, Grossman AR. 93.  2006. Genome-based approaches to understanding phosphorus deprivation responses and PSR1 control in Chlamydomonas reinhardtii. Eukaryot. Cell 5:26–44 [Google Scholar]
  94. Müller P, Li XP, Niyogi KK. 94.  2001. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125:1558–66 [Google Scholar]
  95. Munekage Y, Hashimoto M, Miyake C, Tomizawa KI, Endo T. 95.  et al. 2004. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–82 [Google Scholar]
  96. Muñoz R, Quiles M. 96.  2013. Water deficit and heat affect the tolerance to high illumination in hibiscus plants. Int. J. Mol. Sci. 14:5432–44 [Google Scholar]
  97. Nandha B, Finazzi G, Joliot PA, Hald S, Johnson GN. 97.  2007. The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim. Biophys. Acta 1767:1252–59 [Google Scholar]
  98. Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S. 98.  et al. 2010. An orange ripening mutant links plastid NAD(P)H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22:1977–97 [Google Scholar]
  99. Neimanis K, Staples JF, Hüner NPA, McDonald AE. 99.  2013. Identification, expression, and taxonomic distribution of alternative oxidases in non-angiosperm plants. Gene 526:275–86 [Google Scholar]
  100. Nevo R, Charuvi D, Tsabari O, Reich Z. 100.  2012. Composition, architecture and dynamics of the photosynthetic apparatus in higher plants. Plant J. 70:157–76 [Google Scholar]
  101. Nicholls DG. 101.  1982. Bioenergetics London: Academic
  102. Niyogi KK. 102.  2000. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3:455–60 [Google Scholar]
  103. Nott A, Jung H-S, Koussevitzky S, Chory J. 103.  2006. Plastid-to-nucleus retrograde signaling. Annu. Rev. Plant Biol. 57:739–59 [Google Scholar]
  104. Ohashi KK, Tanaka AA, Tsuji HH. 104.  1989. Formation of the photosynthetic electron transport system during the early phase of greening in barley leaves. Plant Physiol. 91:409–14 [Google Scholar]
  105. Okegawa Y, Kobayashi Y, Shikanai T. 105.  2010. Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. Plant J. 63:458–68 [Google Scholar]
  106. Ort DR, Baker NR. 106.  2002. A photoprotective role for O2 as an alternative electron sink in photosynthesis?. Curr. Opin. Plant Biol. 5:193–98 [Google Scholar]
  107. Pan K, Qin J, Li S, Dai W, Zhu B. 107.  et al. 2011. Nuclear monoploidy and asexual propagation of Nannochloropsis oceanica (Eustigmatophyceae) as revealed by its genome. J. Phycol. 47:1425–32 [Google Scholar]
  108. Paredes M, Quiles MJ. 108.  2013. Stimulation of chlororespiration by drought under heat and high illumination in Rosa meillandina. J. Plant Physiol. 170:165–71 [Google Scholar]
  109. Pateraki I, Renato M, Azcón-Bieto J, Boronat A. 108a.  2013. An ATP synthase harboring an atypical γ–subunit is involved in ATP synthesis in tomato fruit chromoplasts. Plant J. 74:74–85 [Google Scholar]
  110. Peltier G, Cournac L. 109.  2002. Chlororespiration. Annu. Rev. Plant Biol. 53:523–50 [Google Scholar]
  111. Peltier G, Ravenel J, Verméglio A. 110.  1987. Inhibition of a respiratory activity by short saturating flashes in Chlamydomonas: evidence for a chlororespiration. Biochim. Biophys. Acta 893:83–90 [Google Scholar]
  112. Peltier G, Schmidt GW. 111.  1991. Chlororespiration: an adaptation to nitrogen deficiency in Chlamydomonas reinhardtii. PNAS 88:4791–95 [Google Scholar]
  113. Perotti VE, Moreno AS, Podestá FE. 112.  2014. Physiological aspects of fruit ripening: the mitochondrial connection. Mitochondrion 17:1–6 [Google Scholar]
  114. Plaxton WC. 113.  1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Biol. 47:185–214 [Google Scholar]
  115. Pogson BJ, Woo NS, Förster B, Small ID. 114.  2008. Plastid signalling to the nucleus and beyond. Trends Plant Sci. 13:602–9 [Google Scholar]
  116. Putarjunan A, Liu X, Nolan T, Yu F, Rodermel S. 115.  2013. Understanding chloroplast biogenesis using second-site suppressors of immutans and var2. Photosynth. Res. 116:437–53 [Google Scholar]
  117. Queval G, Foyer CH. 116.  2012. Redox regulation of photosynthetic gene expression. Philos. Trans. R. Soc. B 367:3475–85 [Google Scholar]
  118. Rappaport F, Finazzi G, Pierre Y, Bennoun P. 117.  1999. A new electrochemical gradient generator in thylakoid membranes of green algae. Biochemistry 38:2040–47 [Google Scholar]
  119. Rasmussen A, Depuydt S, Goormachtig S, Geelen D. 118.  2013. Strigolactones fine-tune the root system. Planta 238:615–26 [Google Scholar]
  120. Rasmusson AG, Fernie AR, van Dongen JT. 119.  2009. Alternative oxidase: a defence against metabolic fluctuations?. Physiol. Plant. 137:371–82 [Google Scholar]
  121. Rebéillé F, Gans P. 120.  1988. Interaction between chloroplasts and mitochondria in microalgae role of glycolysis. Plant Physiol. 88:973–75 [Google Scholar]
  122. Rédei GP. 121.  1967. Biochemical aspects of a genetically determined variegation in Arabidopsis. Genetics 56:431–43 [Google Scholar]
  123. Renato M, Pateraki I, Boronat A, Azcón-Bieto J. 121a.  2014. Tomato fruit chromoplasts behave as respiratory bioenergetic organelles during ripening. Plant Physiol. 166:920–33 [Google Scholar]
  124. Rich PR, Harper R. 122.  1990. Partition coefficients of quinones and hydroquinones and their relation to biochemical reactivity. FEBS Lett. 269:139–44 [Google Scholar]
  125. Roach T, Krieger-Liszkay A. 123.  2014. Regulation of photosynthetic electron transport and photoinhibition. Curr. Protein Pept. Sci. 15:351–62 [Google Scholar]
  126. Rochaix J-D. 124.  2011. Regulation of photosynthetic electron transport. Biochim. Biophys. Acta 1807:375–83 [Google Scholar]
  127. Roose JL, Frankel LK, Bricker TM. 125.  2011. Developmental defects in mutants of the PsbP domain protein 5 in Arabidopsis thaliana. PLOS ONE 6:e28624 [Google Scholar]
  128. Rosso D, Bode R, Li W, Krol M, Saccon D. 126.  et al. 2009. Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 21:3473–92 [Google Scholar]
  129. Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L. 127.  et al. 2006. IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis during steady-state photosynthesis. Plant Physiol. 142:574–85 [Google Scholar]
  130. Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM. 128.  et al. 2007. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–78 [Google Scholar]
  131. Rumeau D, Peltier G, Cournac L. 129.  2007. Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30:1041–51 [Google Scholar]
  132. Rutherford AW, Osyczka A, Rappaport F. 130.  2012. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett. 586:603–16 [Google Scholar]
  133. Sandmann G. 131.  2009. Evolution of carotene desaturation: the complication of a simple pathway. Arch. Biochem. Biophys. 483:169–74 [Google Scholar]
  134. Savitch LV, Ivanov AG, Krol M, Sprott DP, Oquist G, Hüner NPA. 132.  2010. Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of lodgepole pine is oxygen dependent. Plant Cell Physiol. 51:1555–70 [Google Scholar]
  135. Scheibe R. 133.  2004. Malate valves to balance cellular energy supply. Physiol. Plant. 120:21–26 [Google Scholar]
  136. Schertl P, Braun H-P. 134.  2014. Respiratory electron transfer pathways in plant mitochondria. Front. Plant Sci. 5:163 [Google Scholar]
  137. Schmitt F-J, Renger G, Friedrich T, Kreslavski VD, Zharmukhamedov SK. 135.  et al. 2014. Reactive oxygen species: re-evaluation of generation, monitoring and role in stress-signalling in phototrophic organisms. Biochim. Biophys. Acta 1837:835–48 [Google Scholar]
  138. Seto Y, Kameoka H, Yamaguchi S, Kyozuka J. 136.  2012. Recent advances in strigolactone research: chemical and biological aspects. Plant Cell Physiol. 53:1843–53 [Google Scholar]
  139. Shiba T, Kido Y, Sakamoto K, Inaoka DK, Tsuge C. 137.  et al. 2013. Structure of the trypanosome cyanide-insensitive alternative oxidase. PNAS 110:4580–85 [Google Scholar]
  140. Shikanai T. 138.  2014. Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr. Opin. Biotechnol. 26:25–30 [Google Scholar]
  141. Shumskaya M, Wurtzel ET. 139.  2013. The carotenoid biosynthetic pathway: thinking in all dimensions. Plant Sci. 208:58–63 [Google Scholar]
  142. Simkin AJ, Moreau H, Kuntz M, Pagny G, Lin C. 140.  et al. 2008. An investigation of carotenoid biosynthesis in Coffea canephora and Coffea arabica. J. Plant Physiol. 165:1087–106 [Google Scholar]
  143. Sonnhammer E, Koonin E. 141.  2002. Orthology, paralogy and proposed classification for paralog subtypes. Trends Genet 18:619–20 [Google Scholar]
  144. Stepien P, Johnson GN. 142.  2009. Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol. 149:1154–65 [Google Scholar]
  145. Streb P, Josse E-M, Gallouet E, Baptist F, Kuntz M, Cornic G. 143.  2005. Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ. 28:1123–35 [Google Scholar]
  146. Stroebel D, Choquet Y, Popot JL, Picot D. 144.  2003. An atypical haem in the cytochrome b6f complex. Nature 426:413–18 [Google Scholar]
  147. Suarez JV, Banks S, Thomas PG, Day A. 145.  2014. A new F131V mutation in Chlamydomonas phytoene desaturase locates a cluster of norflurazon resistance mutations near the FAD-binding site in 3D protein models. PLOS ONE 9:e99894 [Google Scholar]
  148. Sun X, Wen T. 146.  2011. Physiological roles of plastid terminal oxidase in plant stress responses. J. Biosci. 36:951–56 [Google Scholar]
  149. Takahashi H, Clowez S, Wollman F-A, Vallon O, Rappaport F. 147.  2013. Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4:1954 [Google Scholar]
  150. Tamiru M, Abe A, Utsushi H, Yoshida K, Takagi H. 148.  et al. 2013. The tillering phenotype of the rice plastid terminal oxidase (PTOX) loss-of-function mutant is associated with strigolactone deficiency. New Phytol. 202:116–31 [Google Scholar]
  151. Theg SM, Cline K, Finazzi G, Wollman F-A. 149.  2005. The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10:153–54 [Google Scholar]
  152. Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I. 150.  et al. 2011. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–30 [Google Scholar]
  153. Tran PT, Sharifi MN, Poddar S, Dent RM, Niyogi KK. 151.  2012. Intragenic enhancers and suppressors of phytoene desaturase mutations in Chlamydomonas reinhardtii. PLOS ONE 7:e42196 [Google Scholar]
  154. Trouillard M, Shahbazi M, Moyet L, Rappaport F, Joliot PA. 152.  et al. 2012. Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim. Biophys. Acta 1817:2140–48 [Google Scholar]
  155. Umbach AL, Ng VS, Siedow JN. 153.  2006. Regulation of plant alternative oxidase activity: a tale of two cysteines. Biochim. Biophys. Acta 1757:135–42 [Google Scholar]
  156. Vanlerberghe G. 154.  2013. Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int. J. Mol. Sci. 14:6805–47 [Google Scholar]
  157. Vener AV, van Kan PJ, Rich PR, Ohad I, Andersson B. 155.  1997. Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. PNAS 94:1585–90 [Google Scholar]
  158. Wagner AM, Krab K, Wagner MJ, Moore AL. 156.  2008. Regulation of thermogenesis in flowering Araceae: the role of the alternative oxidase. Biochim. Biophys. Acta 1777:993–1000 [Google Scholar]
  159. Wang J, Sommerfeld M, Hu Q. 157.  2009. Occurrence and environmental stress responses of two plastid terminal oxidases in Haematococcus pluvialis (Chlorophyceae). Planta 230:191–203 [Google Scholar]
  160. Wei L, Derrien B, Gautier A, Houille-Vernes L, Boulouis A. 158.  et al. 2014. Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. Plant Cell 26:353–72 [Google Scholar]
  161. Wetzel CM, Jiang CZ, Meehan LJ, Voytas DF, Rodermel S. 159.  1994. Nuclear-organelle interactions: the immutans variegation mutant of Arabidopsis is plastid autonomous and impaired in carotenoid biosynthesis. Plant J. 6:161–75 [Google Scholar]
  162. Wikström M, Verkhovsky MI. 160.  2007. Mechanism and energetics of proton translocation by the respiratory heme-copper oxidases. Biochim. Biophys. Acta 1767:1200–14 [Google Scholar]
  163. Wollman F-A. 161.  2001. State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20:3623–30 [Google Scholar]
  164. Wu D, Wright DA, Wetzel C, Voytas DF, Rodermel S. 162.  1999. The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11:43–55 [Google Scholar]
  165. Yamamoto H, Peng L, Fukao Y, Shikanai T. 163.  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 [Google Scholar]
  166. Yoshikawa S, Muramoto K, Shinzawa-Itoh K. 164.  2011. Proton-pumping mechanism of cytochrome c oxidase. Annu. Rev. Biophys. 40:205–23 [Google Scholar]
  167. Young L, May B, Pendlebury-Watt A, Shearman J, Elliott C. 165.  et al. 2014. Probing the ubiquinol-binding site of recombinant Sauromatum guttatum alternative oxidase expressed in E. coli membranes through site-directed mutagenesis. Biochim. Biophys. Acta 1837:1219–25 [Google Scholar]
  168. Young L, Shiba T, Harada S, Kita K, Albury MS, Moore AL. 166.  2013. The alternative oxidases: simple oxidoreductase proteins with complex functions. Biochem. Soc. Trans. 41:1305–11 [Google Scholar]
  169. Yu Q, Feilke K, Krieger-Liszkay A, Beyer P. 167.  2014. Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim. Biophys. Acta 1837:1284–92 [Google Scholar]
  170. Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman F-A. 168.  1999. The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J. 18:2961–69 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043014-114744
Loading
The Plastid Terminal Oxidase: Its Elusive Function Points to Multiple Contributions to Plastid Physiology
Annual Review of Plant Biology 66, 49 (2015); https://doi.org/10.1146/annurev-arplant-043014-114744
/content/journals/10.1146/annurev-arplant-043014-114744
/content/journals/10.1146/annurev-arplant-043014-114744
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error