Respiratory processes in non-photosynthetic plastids

Frontiers in Plant Science

Volumn 6, Issue JULY, 2015, Pages

  Renato, Marta ^a,b   Boronat, Albert ^a,b   Azcón Bieto, Joaquín ^a  

^a UNIVERSITY OF BARCELONA   (Spain)

^b CSIC   (Spain)

Author keywords

Amyloplast; Chlororespiration; Chromoplast; Chromorespiration; Etioplast; Plastid; Plastid respiration; PTOX

Indexed keywords

LYCOPERSICON ESCULENTUM;

EID: 84937433594     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00496     Document Type: Review

References (67)

1. Aluru, M. R., Bae, H., Wu, D., and Rodermel, S. R. (2001). The Arabidopsis immutans mutation affects plastid differentiation and the morphogenesis of white and green sectors in variegated plants. Plant Physiol. 127, 67-77. doi: 10.1104/pp.127.1.67
2. Andon, N. L., Hollingworth, S., Koller, A., Yates, J. R., Haynes, P. A., and Hill, J. (2002). Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2, 1156-1168. doi: 10.1002/1615-9861(200209)2:9<1156::AID-PROT1156>3.0.CO;2-4
3. Angaman, D. M., Petrizzo, R., Hernandez-Gras, F., Romero-Segura, C., Pateraki, I., Busquets, M., et al. (2012). Precursor uptake assays and metabolic analyses in isolated tomato fruit chromoplasts. Plant Methods 8, 1-10. doi: 10.1186/1746-4811-8-1
4. Balmer, Y., Vensel, W. H., DuPont, F. M., Buchanan, B. B., and Hurkman, W. J. (2006). Proteome of amyloplasts isolated from developing wheat endosperm presents evidence of broad metabolic capability. J. Exp. Bot. 57, 1591-1602. doi: 10.1093/jxb/erj156
5. Barr, J., White, W. S., Chen, L., Bae, H., and Rodermel, S. (2004). The GHOST terminal oxidase regulates developmental programming in tomato fruit. Plant Cell Environ. 27, 840-852. doi: 10.1111/j.1365-3040.2004.01190.x
6. Barsan, C., Sanchez-Bel, P., Rombaldi, C., Egea, I., Rossignol, M., Bouzayen, M., et al. (2010). Characteristics of the tomato chromoplast revealed by proteomic analysis. J. Exp. Bot. 61, 2413-2431. doi: 10.1093/jxb/erq070
7. Barsan, C., Zouine, M., Maza, E., Bian, W., Egea, I., Rossignol, M., et al. (2012). Proteomic analysis of chloroplast-to-chromoplast transition in tomato reveals metabolic shifts coupled with disrupted thylakoid biogenesis machinery and elevated energy-production components. Plant Physiol. 160, 708-725. doi: 10.1104/pp.112.203679
8. Bédard, J., and Jarvis, P. (2005). Recognition and envelope translocation of chloroplast preproteins. J. Exp. Bot. 56, 2287-2320. doi: 10.1093/jxb/eri243
9. Bennoun, P. (1982). Evidence for a respiratory chain in the chloroplast. Proc. Natl. Acad. Sci. U.S.A. 79, 4352-4356. doi: 10.1073/pnas.79.14.4352
10. Beyer, P., Nievelstein, V., Albabili, S., Bonk, M., and Kleinig, H. (1994). Biochemical aspects of carotene desaturation and cyclization in chromoplast membranes from Narcissus pseudonarcissus. Pure Appl. Chem. 66, 1047-1056. doi: 10.1351/pac199466051047
11. Burrows, P. A., Sazanov, L. A., Svab, Z., Maliga, P., and Nixon, P. J. (1998). Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J. 17, 868-876. doi: 10.1093/emboj/17.4.868
12. Camara, B., Hugueney, P., Bouvier, F., Kuntz, M., and Monéger, R. (1995). Biochemistry and molecular biology of chromoplast development. Int. Rev. Cytol. 163, 175-247. doi: 10.1016/S0074-7696(08)62211-1
13. Carol, P., Stevenson, D., Bisanz, C., Breitenbach, J., Sandmann, G., Mache, R., 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. doi: 10.1105/tpc.11.1.57
14. Carrie, C., Murcha, M. W., Kuehn, K., Duncan, O., Barthet, M., Smith, P. M., et al. (2008). Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079. doi: 10.1016/j.febslet.2008.07.061
15. Catala, R., Sabater, B., and Guera, A. (1997). Expression of the plastid ndhF gene product in photosynthetic and non-photosynthetic tissues of developing barley seedlings. Plant Cell Physiol. 38, 1382-1388. doi: 10.1093/oxfordjournals.pcp.a029133
16. Cournac, L., Redding, K., Ravenel, J., Rumeau, D., Josse, E. M., Kuntz, 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, 17256-17262. doi: 10.1074/jbc.M908732199
17. Desplats, C., Mus, F., Cuiné, S., Billon, E., Cournac, L., and Peltier, G. (2009). Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J. Biol. Chem. 284, 4148-4157. doi: 10.1074/jbc.M804546200
18. Dupont, F. M. (2008). Metabolic pathways of the wheat (Triticum aestivum) endosperm amyloplast revealed by proteomics. BMC Plant Biol. 8:39. doi: 10.1186/1471-2229-8-39
19. Endo, T., Shikanai, T., Sato, F., and Asada, K. (1998). NAD(P)H dehydrogenase-dependent, antimycin A-sensitive electron donation to plastoquinone in tobacco chloroplasts. Plant Cell Physiol. 39, 1226-1231. doi: 10.1093/oxfordjournals.pcp.a029324
20. Fischer, M., Fun, K. E., and Steinmuller, K. (1997). The expression of subunits of the mitochondrial complex I-homologous NAD(P)H-plastoquinone-oxidoreductase during plastid development. Z. Naturforsch. C 52, 481-486.
21. Foudree, A., Putarjunan, A., Kambakam, S., Nolan, T., Fussell, J., Pogorelko, G., et al. (2012). The mechanism of variegation in immutans provides insight into chloroplast biogenesis. Front. Plant Sci. 3:260. doi: 10.3389/fpls.2012.00260
22. Gould, S. B., Waller, R. F., and McFadden, G. I. (2008). Plastid evolution. Annu. Rev. Plant Biol. 59, 491-517. doi: 10.1146/annurev.arplant.59.032607.092915
23. Guera, A., de Nova, P. G., and Sabater, B. (2000). Identification of the Ndh (NAD(P)H-plastoquinone-oxidoreductase) complex in etioplast membranes of barley: changes during photomorphogenesis of chloroplasts. Plant Cell Physiol. 41, 49-59. doi: 10.1093/pcp/41.1.49
24. Hart, S., Schlarb-Ridley, B., Bendall, D., and Howe, C. (2005). Terminal oxidases of cyanobacteria. Biochem. Soc. Trans. 33, 832-835. doi: 10.1042/BST0330832
25. Heyno, E., Gross, C. M., Laureau, C., Culcasi, M., Pietri, S., and Krieger-Liszkay, A. (2009). Plastid alternative oxidase (PTOX) promotes oxidative stress when overexpressed in tobacco. J. Biol. Chem. 284, 31174-31180. doi: 10.1074/jbc.M109.021667
26. Ho, K. K., Kerfeld, C. A., and Krogmann, D. W. (2011). “The water-soluble cytochromes of cyanobacteria,” in Bioenergetic Processes in Cyanobacteria, eds G. A. Peschek, C. Obinger, and G. Renger (Dordrecht: Springer Science + Business media), 515-540.
27. Joët, T., Genty, B., Josse, E. M., Kuntz, M., Cournac, L., and Peltier, G. (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, 31623-31630. doi: 10.1074/jbc.M203538200
28. Josse, E. M., Simkin, A. J., Gaffé, J., Labouré, A. M., Kuntz, M., and Carol, P. (2000). A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 123, 1427-1436. doi: 10.1104/pp.123.4.1427
29. Kahlau, S., and Bock, R. (2008). Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell 20, 856-874. doi: 10.1105/tpc.107.055202
30. Kanervo, E., Singh, M., Suorsa, M., Paakkarinen, V., Aro, E., Battchikova, N., 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. doi: 10.1093/pcp/pcn016
31. Karcher, D., and Bock, R. (2002). The amino acid sequence of a plastid protein is developmentally regulated by RNA editing. J. Biol. Chem. 277, 5570-5574. doi: 10.1074/jbc.M107074200
32. Kohzuma, K., Dal Bosco, C., Kanazawa, A., Dhingra, A., Nitschke, W., Meurer, J., et al. (2012). Thioredoxin-insensitive plastid ATP synthase that performs moonlighting functions. Proc. Natl. Acad. Sci. U.S.A. 109, 3293-3298. doi: 10.1073/pnas.1115728109
33. Laureau, C., de Paepe, R., Latouche, G., Moreno-Chacón, M., Finazzi, G., Kuntz, M., 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, 1296-1310. doi: 10.1111/pce.12059
34. Lennon, A. M., Prommeenate, P., and Nixon, P. J. (2003). Location, expression and orientation of the putative chlororespiratory enzymes, Ndh and IMMUTANS, in higher-plant plastids. Planta 218, 254-260. doi: 10.1007/s00425-003-1111-7
35. Li, L., and Yuan, H. (2013). Chromoplast biogenesis and carotenoid accumulation. Arch. Biochem. Biophys. 539, 102-109. doi: 10.1016/j.abb.2013.07.002
36. Mayer, M. P., Nievelstein, V., and Beyer, P. (1992). Purification and characterization of a NADPH dependent oxidoreductase from chromoplasts of Narcissus pseudonarcissus: a redox-mediator possibly involved in carotene desaturation. Plant Physiol. Biochem. 30, 389-398.
37. McDonald, A. E., Ivanov, A. G., Bode, R., Maxwell, D. P., Rodermel, S. R., and Hüner, N. P. A. (2011). Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim. Biophys. Acta 1807, 954-967. doi: 10.1016/j.bbabio.2010.10.024
38. Morstadt, L., Gräber, P., Pascalis, L., Kleining, H., Speth, V., and Beyer, P. (2002). Chemiosmotic ATP synthesis in photosynthetically inactive chromoplasts from Narcissus pseudonarcissus L. linked to a redox pathway potentially also involved in carotene desaturation. Planta 215, 134-140. doi: 10.1007/s00425-001-0724-y
39. Nashilevitz, S., Melamed-Bessudo, C., Izkovich, Y., Rogachev, I., Osorio, S., Itkin, M., 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. doi: 10.1105/tpc.110.074716
40. Nawrocki, W. J., Tourasse, N. J., Taly, A., and Rappaport, F. (2015). The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annu. Rev. Plant Biol. 66, 1-26. doi: 10.1146/annurev-arplant-043014-114744
41. Nievelstein, V., Vandekerckhove, J., Tadros, M. H., Lintig, J. V., Nitschke, W., and Beyer, P. (1995). Carotene desaturation is linked to a respiratory redox pathway in Narcissus pseudonarcissus chromoplast membranes. Involvement of a 23-kDa oxygen-evolving-complex-like protein. Eur. J. Biochem. 233, 864-872. doi: 10.1111/j.1432-1033.1995.864_3.x
42. Nixon, P. J., and Rich, P. R. (2006). “Chlororespiratory pathways and their physiological significance,” in The Structure and Function of Plastids, eds R. R. Wise and J. K. Hoober (Dordrecht: Springer), 237-248.
43. Norris, S. R., Barrette, T. R., and DellaPenna, D. (1995). Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinone as an essential component of phytoene desaturation. Plant Cell 7, 2139-2149. doi: 10.1105/tpc.7.12.2139
44. Paredes, M., and Quiles, M. J. (2013). Stimulation of chlororespiration by drought under heat and high illumination in Rosa meillandina. J. Plant Physiol. 170, 165-171. doi: 10.1016/j.jplph.2012.09.010
45. Pateraki, I., Renato, M., Azcón-Bieto, J., and Boronat, A. (2013). An ATP synthase harboring an atypical ?-subunit is involved in ATP synthesis in tomato fruit chromoplasts. Plant J. 74, 74-85. doi: 10.1111/tpj.12109
46. Peltier, G., and Cournac, L. (2002). Chlororespiration. Annu. Rev. Plant Biol. 53, 523-550. doi: 10.1146/annurev.arplant.53.100301.135242
47. Peng, L., and 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, 1629-1639. doi: 10.1104/pp.110.171264
48. Peng, L., Shimizu, H., and Shikanai, T. (2008). The chloroplast NAD(P)H dehydrogenase complex interacts with photosystem I in Arabidopsis. J. Biol. Chem. 283, 34873-34879. doi: 10.1074/jbc.M803207200
49. Plöscher, M., Reisinger, V., and Eichacker, L. A. (2011). Proteomic comparison of etioplast and chloroplast protein complexes. J. Proteomics 74, 1256-1265. doi: 10.1016/j.jprot.2011.03.020
50. Reisinger, V., Hertle, A. P., Plöscher, M., and Eichacker, L. A. (2008). Cytochrome b6f is a dimeric protochlorophyll a binding complex in etioplasts. FEBS J. 275, 1018-1024. doi: 10.1111/j.1742-4658.2008.06268.x
51. Renato, M., Pateraki, I., Boronat, A., and Azcón-Bieto, J. (2014). Tomato fruit chromoplasts behave as respiratory bioenergetic organelles during ripening. Plant Physiol. 166, 920-933. doi: 10.1104/pp.114.243931
52. Rodríguez-Villalón, A., Gas, E., and Rodríguez-Concepción, M. (2009). Colors in the dark: a model for the regulation of carotenoid biosynthesis in etioplasts. Plant Signal. Behav. 4, 965-967. doi: 10.4161/psb.4.10.9672
53. Rosso, D., Ivanov, A. G., Fu, A., Geisler-Lee, J., Hendrickson, L., Geisler, M., 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, 574-585. doi: 10.1104/pp.106.085886
54. Rumeau, D., Bécuwe-Linka, N., Beyly, A., Louwagie, M., Garin, J., and Peltier, G. (2005). New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17, 219-232. doi: 10.1105/tpc.104.028282
55. Rumeau, D., Peltier, G., and Cournac, L. (2007). Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ. 30, 1041-1051. doi: 10.1111/j.1365-3040.2007.01675.x
56. Samra, H. S., Gao, F., He, F., Hoang, E., Chen, Z., Gegenheimer, P. A., et al. (2006). Structural analysis of the regulatory dithiol-containing domain of the chloroplast ATP synthase ? subunit. J. Biol. Chem. 281, 31041-31049. doi: 10.1074/jbc.M603315200
57. Sazanov, L. A., Burrows, P. A., and Nixon, P. J. (1998). The chloroplast Ndh complex mediates the dark reduction of the plastoquinone pool in response to heat stress in tobacco leaves. FEBS Lett. 429, 115-118. doi: 10.1016/S0014-5793(98)00573-0
58. Shahbazi, M., Gilbert, M., Labouré, A. M., and Kuntz, M. (2007). Dual role of the plastid terminal oxidase in tomato. Plant Physiol. 145, 691-702. doi: 10.1104/pp.107.106336
59. Siddique, M. A., Grossmann, J., Gruissem, W., and Baginsky, S. (2006). Proteome analysis of bell pepper (Capsicum annuum L.) chromoplasts. Plant Cell Physiol. 47, 1663-1673. doi: 10.1093/pcp/pcl033
60. Trouillard, M., Shahbazi, M., Moyet, L., Rappaport, F., Joliot, P., Kuntz, M., et al. (2012). Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim. Biophys. Acta 1817, 2140-2148. doi: 10.1016/j.bbabio.2012.08.006
61. Wang, Y. Q., Yang, Y., Fei, Z., Yuan, H., Fish, T., Thannhauser, T. W., et al. (2013). Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. J. Exp. Bot. 64, 949-961. doi: 10.1093/jxb/ers375
62. Wastl, J., Bendall, D. S., and Howe, C. J. (2002). Higher plants contain a modified cytochrome c6. Trends Plant Sci. 7, 244-245. doi: 10.1016/s1360-1385(02)02280-x
63. Whatley, J. M. (1978). A suggested cycle of plastid developmental interrelationships. New Phytol. 80, 489-502. doi: 10.1111/j.1469-8137.1978.tb01581.x
64. Wu, D., Wright, D. A., Wetzel, C., Voytas, D. F., and Rodermel, S. (1999). The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11, 43-55. doi: 10.2307/3870837
65. Yu, Q., Feilke, K., Krieger-Liszkay, A., and Beyer, P. (2014). Functional and molecular characterization of plastid terminal oxidase from rice (Oryza sativa). Biochim. Biophys. Acta. 1837, 1284-1292. doi: 10.1016/j.bbabio.2014.04.007
66. Zeng, Y., Pan, Z., Ding, Y., Zhu, A., Cao, H., Xu, Q., et al. (2011). A proteomic analysis of the chromoplasts isolated from sweet orange fruits [Citrus sinensis (L.) Osbeck]. J. Exp. Bot. 62, 5297-5309. doi: 10.1093/jxb/err140
67. Zivcak, M., Brestic, M., Balatova, Z., Drevenakova, P., Olsovska, K., Kalaji, H. M., et al. (2013). Photosynthetic electron transport and specific photoprotective responses in wheat leaves under drought stress. Photosynth. Res. 117, 529-546. doi: 10.1007/s11120-013-9885-3