Subchromoplast sequestration of carotenoids affects regulatory mechanisms in tomato lines expressing different carotenoid gene combinations

Plant Cell

Volumn 25, Issue 11, 2013, Pages 4560-4579

  Nogueira, Marilise ^a   Mora, Leticia ^a,b   Enfissi, Eugenia M A ^a   Bramley, Peter M ^a   Fraser, Paul D ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; FARNESYL TRANS TRANSFERASE; OXIDOREDUCTASE; PHYTOENE DEHYDROGENASE; PHYTOENE SYNTHASE;

ARTICLE; CELL FRACTIONATION; ECHOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLASTID; SECONDARY METABOLISM; TOMATO; TRANSGENIC PLANT;

CAROTENOIDS; FARNESYLTRANSTRANSFERASE; GENE EXPRESSION REGULATION, PLANT; GERANYLGERANYL-DIPHOSPHATE GERANYLGERANYLTRANSFERASE; LYCOPERSICON ESCULENTUM; OXIDOREDUCTASES; PLANTS, GENETICALLY MODIFIED; PLASTIDS; SECONDARY METABOLISM; SUBCELLULAR FRACTIONS;

EID: 84891498869     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.116210     Document Type: Article

References (55)

1. Angaman, D.M., Petrizzo, R., Hernández-Gras, F., Romero-Segura, C., Pateraki, I., Busquets, M., and Boronat, A. (2012). Precursor uptake assays and metabolic analyses in isolated tomato fruit chromoplasts. Plant Methods 8: 1.
2. Atkinson, R.G., Bolitho, K.M., Wright, M.A., Iturriagagoitia-Bueno, T., Reid, S.J., and Ross, G.S. (1998). Apple ACC-oxidase and polygalacturonase: Ripening-specific gene expression and promoter analysis in transgenic tomato. Plant Mol. Biol. 38: 449-460.
3. Auldridge, M.E., McCarty, D.R., and Klee, H.J. (2006). Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr. Opin. Plant Biol. 9: 315-321.
4. Barsan, C., Zouine, M., Maza, E., Bian, W.P., Egea, I., Rossignol, M., Bouyssie, D., Pichereaux, C., Purgatto, E., Bouzayen, M., Latché, A., and Pech, J.C. (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.
5. Beyer, P. (2010). Golden Rice and 'Golden' crops for human nutrition. New Biotechnol. 27: 478-481.
6. Cao, H., Zhang, J., Xu, J., Ye, J., Yun, Z., Xu, Q., Xu, J., and Deng, X. (2012). Comprehending crystalline b-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus. J. Exp. Bot. 63: 4403-4417.
7. Carvalho, L.J.C.B., Lippolis, J., Chen, S., Batista de Souza, C.R., Vieira, E.A., and Anderson, J.V. (2012). Characterization of carotenoid-protein complexes and gene expression analysis associated with carotenoid sequestration in pigmented cassava (Manihot esculenta Crantz) storage root. The Open Biochem. J. 6: 116-130.
8. Dall'Osto, L., Fiore, A., Cazzaniga, S., Giuliano, G., and Bassi, R. (2007). Different roles of alpha-and beta-branch xanthophylls in photosystem assembly and photoprotection. J. Biol. Chem. 282: 35056-35068.
9. De Camilli, P., Harris, S.M., Jr., Huttner, W.B., and Greengard, P. (1983). Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J. Cell Biol. 96: 1355-1373.
10. Demmig-Adams, B., and Adams, W.W., III., (2002). Antioxidants in photosynthesis and human nutrition. Science 298: 2149-2153.
11. Diretto, G., Al-Babili, S., Tavazza, R., Papacchioli, V., Beyer, P., and Giuliano, G. (2007). Metabolic engineering of potato carotenoid content through tuber-specific overexpression of a bacterial minipathway. PLoS ONE 2: e350.
12. Dogbo, O., Laferriére, A., D'Harlingue, A., and Camara, B. (1988). Carotenoid biosynthesis: Isolation and characterization of a bifunctional enzyme catalyzing the synthesis of phytoene. Proc. Natl. Acad. Sci. USA 85: 7054-7058.
13. Egea, I., Barsan, C., Bian, W.P., Purgatto, E., Latché, A., Chervin, C., Bouzayen, M., and Pech, J.C. (2010). Chromoplast differentiation: Current status and perspectives. Plant Cell Physiol. 51: 1601-1611.
14. Enfissi, E., et al. (2010). Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22: 1190-1215.
15. Fraser, P.D., and Bramley, P.M. (2004). The biosynthesis and nutritional uses of carotenoids. Prog. Lipid Res. 43: 228-265.
16. Fraser, P.D., Enfissi, E.M., and Bramley, P.M. (2009). Genetic engineering of carotenoid formation in tomato fruit and the potential application of systems and synthetic biology approaches. Arch. Biochem. Biophys. 483: 196-204.
17. Fraser, P.D., Romer, S., Shipton, C.A., Mills, P.B., Kiano, J.W., Misawa, N., Drake, R.G., Schuch, W., and Bramley, P.M. (2002). Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc. Natl. Acad. Sci. USA 99: 1092-1097.
18. Fraser, P.D., Schuch, W., and Bramley, P.M. (2000). Phytoene synthase from tomato (Lycopersicon esculentum) chloroplasts-Partial purification and biochemical properties. Planta 211: 361-369.
19. Fraser, P.D., Truesdale, M.R., Bird, C.R., Schuch, W., and Bramley, P.M. (1994). Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol. 105: 405-413.
20. Harris, W.M., and Spurr, A.R. (1969). Chromoplasts of tomato fruits. II. The red tomato. Am. J. Bot. 56: 380-389.
21. Heinig, U., Gutensohn, M., Dudareva, N., and Aharoni, A. (2013). The challenges of cellular compartmentalization in plant metabolic engineering. Curr. Opin. Biotechnol. 24: 239-246.
22. Hirschberg, J. (2001). Carotenoid biosynthesis in flowering plants. Curr. Opin. Plant Biol. 4: 210-218.
23. Jones, M.O., Piron-Prunier, F., Marcel, F., Piednoir-Barbeau, E., Alsadon, A.A., Wahb-Allah, M.A., Al-Doss, A.A., Bowler, C., Bramley, P.M., Fraser, P.D., and Bendahmane, A. (2012). Characterisation of alleles of tomato light signalling genes generated by TILLING. Phytochemistry 79: 78-86.
24. Kachanovsky, D.E., Filler, S., Isaacson, T., and Hirschberg, J. (2012). Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc. Natl. Acad. Sci. USA 109: 19021-19026.
25. Kilambi, H.V., Kumar, R., Sharma, R., and Sreelakshmi, Y. (2013). Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol. 161: 2085-2101.
26. Ko, K., Bornemisza, O., Kourtz, L., Ko, Z.W., Plaxton, W.C., and Cashmore, A.R. (1992). Isolation and characterization of a cDNA clone encoding a cognate 70-kDa heat shock protein of the chloroplast envelope. J. Biol. Chem. 267: 2986-2993.
27. Krinsky, N.I., and Johnson, E.J. (2005). Carotenoid actions and their relation to health and disease. Mol. Aspects Med. 26: 459-516.
28. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
29. Li, L., Yang, Y., Xu, Q., Owsiany, K., Welsch, R., Chitchumroonchokchai, C., Lu, S., Van Eck, J., Deng, X.X., Failla, M., and Thannhauser, T.W. (2012). The Or gene enhances carotenoid accumulation and stability during post-harvest storage of potato tubers. Mol. Plant 5: 339-352.
30. Maass, D., Arango, J., Wüst, F., Beyer, P., and Welsch, R. (2009). Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS ONE 4: e6373.
31. Marechal, E., Block, M.A., Dorne, A.J., Douce, R., and Joyard, J. (1997). Lipid synthesis and metabolism in the plastid envelope. Physiol. Plant. 100: 65-77.
32. Misawa, N., Masamoto, K., Hori, T., Ohtani, T., Boger, P., and Sandmann, G. (1994). Expression of an erwinia phytoene desaturase gene not only confers multiple resistance to herbicides interfering with carotenoid biosynthesis but also alters xanthophyll metabolism in transgenic plants. Plant J. 6: 481-489.
33. Misawa, N., Nakagawa, M., Kobayashi, K., Yamano, S., Izawa, Y., Nakamura, K., and Harashima, K. (1990). Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of gene products expressed in Escherichia coli. J. Bacteriol. 172: 6704-6712.
34. Misawa, N., Yamano, S., and Ikenaga, H. (1991). Production of betacarotene in Zymomonas mobilis and Agrobacterium tumefaciens by introduction of the biosynthesis genes from Erwinia uredovora. Appl. Environ. Microbiol. 57: 1847-1849.
35. Montero, O., Sánchez-Guijo, A., Lubián, L.M., and Martínez-Rodríguez, G. (2012). Changes in membrane lipids and carotenoids during light acclimation in a marine cyanobacterium Synechococcus sp. J. Biosci. 37: 635-645.
36. Mora, L., Bramley, P.M., and Fraser, P.D. (2013). Development and optimisation of a label-free quantitative proteomic procedure and its application in the assessment of genetically modified tomato fruit. Proteomics 13: 2016-2030.
37. Neta-Sharir, I., Isaacson, T., Lurie, S., and Weiss, D. (2005). Dual role for tomato heat shock protein 21: Protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17: 1829-1838.
38. Pulido, P., Perello, C., and Rodriguez-Concepcion, M. (2012). New insights into plant isoprenoid metabolism. Mol. Plant 5: 964-967.
39. Ravanello, M.P., Ke, D., Alvarez, J., Huang, B., and Shewmaker, C.K. (2003). Coordinate expression of multiple bacterial carotenoid genes in canola leading to altered carotenoid production. Metab. Eng. 5: 255-263.
40. Robertson, F.P., Koistinen, P.K., Gerrish, C., Halket, J.M., Patel, R.K.P., Fraser, P.D., and Bramley, P.M. (2012). Proteome changes in tomato lines transformed with phytoene synthase-1 in the sense and antisense orientations. J. Exp. Bot. 63: 6035-6043.
41. Römer, S., Fraser, P.D., Kiano, J.W., Shipton, C.A., Misawa, N., Schuch, W., and Bramley, P.M. (2000). Elevation of the provitamin A content of transgenic tomato plants. Nat. Biotechnol. 18: 666-669.
42. Rosso, S.W. (1967). An ultrastructural study of the mature chromoplasts of the tangerine tomato (Lycopersicon esculentum var. "golden jubilee"). J. Ultrastruct. Res. 20: 179-189.
43. Rosso, S.W. (1968). The ultrastructure of chromoplast development in red tomatoes. J. Ultrastruct. Res. 25: 307-322.
44. Sandmann, G. (2009). Evolution of carotene desaturation: The complication of a simple pathway. Arch. Biochem. Biophys. 483: 169-174.
45. Schweiggert, R.M., Steingass, C.B., Heller, A., Esquivel, P., and Carle, R. (2011). Characterization of chromoplasts and carotenoids of red-and yellow-fleshed papaya (Carica papaya L.). Planta 234: 1031-1044.
46. Shimada, H., Kondo, K., Fraser, P.D., Miura, Y., Saito, T., and Misawa, N. (1998). Increased carotenoid production by the food yeast Candida utilis through metabolic engineering of the isoprenoid pathway. Appl. Environ. Microbiol. 64: 2676-2680.
47. Shumskaya, M., and Wurtzel, E.T. (2013). The carotenoid biosynthetic pathway: Thinking in all dimensions. Plant Sci. 208: 58-63.
48. Simkin, A.J., Gaffé, J., Alcaraz, J.P., Carde, J.P., Bramley, P.M., Fraser, P.D., and Kuntz, M. (2007). Fibrillin influence on plastid ultrastructure and pigment content in tomato fruit. Phytochemistry 68: 1545-1556.
49. Spurr, A.R., and Harris, M. (1968). Ultrastructure of chloroplasts and chromoplasts in Capsicum annuum l. Thylakoid membrane changes during fruit ripening. Am. J. Bot. 55: 1210-1224.
50. Szilágyi, A., Sommarin, M., and Akerlund, H.E. (2007). Membrane curvature stress controls the maximal conversion of violaxanthin to zeaxanthin in the violaxanthin cycle-Influence of alpha-tocopherol, cetylethers, linolenic acid, and temperature. Biochim. Biophys. Acta 1768: 2310-2318.
51. Vasquez-Caicedo, A.L., Heller, A., Neidhart, S., and Carle, R. (2006). Chromoplast morphology and beta-carotene accumulation during postharvest ripening of Mango Cv. 'Tommy Atkins'. J. Agric. Food Chem. 54: 5769-5776.
52. Wellburn, A. (1994). The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Plant Physiol. 144: 307-313.
53. Wrischer, M., Prebeg, T., Magnus, V., and Ljubesic, N. (2007). Crystals and fibrils in chromoplast plastoglobules of Solanum capsicastrum fruit. Acta Bot. Croat. 66: 81-87.
54. Xiao, Y.M., Savchenko, T., Baidoo, E.E.K., Chehab, W.E., Hayden, D.M., Tolstikov, V., Corwin, J.A., Kliebenstein, D.J., Keasling, J.D., and Dehesh, K. (2012). Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149: 1525-1535.
55. Zhong, S., Fei, Z., Chen, Y.R., Zheng, Y., Huang, M., Vrebalov, J., McQuinn, R., Gapper, N., Liu, B., Xiang, J., Shao, Y., and Giovannoni, J.J. (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat. Biotechnol. 31: 154-159.