PLANT PHYSIOLOGY , Vol 105, Issue 1 405-413, Copyright © 1994 by American Society of Plant Biologists

METABOLISM AND ENZYMOLOGY

Carotenoid Biosynthesis during Tomato Fruit Development (Evidence for Tissue-Specific Gene Expression)

P. D. Fraser, M. R. Truesdale, C. R. Bird, W. Schuch and P. M. Bramley
Department of Biochemistry, Royal Holloway, University of London, Egham Surrey, TW20 0EX, United Kingdom (P.D.F., M.R.T., P.M.B.)

Tomato (Lycopersicon esculentum Mill. cv Ailsa Craig) fruit, at five stages of development, have been analyzed for their carotenoid and chlorophyll (Chl) contents, in vitro activities of phytoene synthase, phytoene desaturase, and lycopene cyclase, as well as expression of the phytoene synthase (Psy) and phytoene desaturase (Pds) genes. During ripening, the total carotenoids increased with a concomitant decrease in Chl. Although the highest carotenoid content (consisting mainly of lycopene and [beta]-carotene) was found in ripe fruit, the greatest carotenogenic enzymic activities were found in green fruit. Phytoene synthase was located in the plastid stroma, whereas the metabolism of phytoene was associated with plastid membranes during all stages of fruit development. The in vitro products of phytoene desaturation altered from being predominantly phytofluence and [zeta]-carotene in chloroplasts to becoming mainly lycopene in chromoplasts. The expression of Psy was detected in breaker and ripe fruit, as well as flowers, but was not detectable by northern blot analysis in leaves or green fruits. The Pds gene transcript was barely detectable in green fruit and leaves but was expressed in flowers and breaker fruit. These results suggest that transcription of Psy and Pds is regulated developmentally, with expression being considerably elevated in chromoplast-containing tissues. Antiserum to the Synechococcus phytoene synthase cross-reacted with phytoene synthase of green fruit only on western blots and not with the enzyme from ripe fruit. In contrast, a monoclonal antibody to the Psy gene product only cross-reacted with phytoene synthase from ripe fruit. The enzymes from green and ripe fruit had different molecular masses of 42 and 38 kD, respectively. The absence of detectable Psy and Pds mRNA in green tissues using northern blot analyses, despite high levels of phytoene synthase and desaturase activity, lends support to the hypothesis of divergent genes encoding these enzymes.

This article has been cited by other articles:

				C. Yamamizo, S. Kishimoto, and A. Ohmiya Carotenoid composition and carotenogenic gene expression during Ipomoea petal development J. Exp. Bot., November 20, 2009; (2009) erp335v1. [Abstract] [Full Text] [PDF]

				O. Ahrazem, A. Rubio-Moraga, R. C. Lopez, and L. Gomez-Gomez The expression of a chromoplast-specific lycopene beta cyclase gene is involved in the high production of saffron's apocarotenoid precursors J. Exp. Bot., September 18, 2009; (2009) erp283v1. [Abstract] [Full Text] [PDF]

				C. Ampomah-Dwamena, T. McGhie, R. Wibisono, M. Montefiori, R. P. Hellens, and A. C. Allan The kiwifruit lycopene beta-cyclase plays a significant role in carotenoid accumulation in fruit J. Exp. Bot., September 1, 2009; 60(13): 3765 - 3779. [Abstract] [Full Text] [PDF]

				A. Tadiello, A. Pavanello, D. Zanin, E. Caporali, L. Colombo, G. L. Rotino, L. Trainotti, and G. Casadoro A PLENA-like gene of peach is involved in carpel formation and subsequent transformation into a fleshy fruit J. Exp. Bot., February 1, 2009; 60(2): 651 - 661. [Abstract] [Full Text] [PDF]

				S. Mathieu, V. D. Cin, Z. Fei, H. Li, P. Bliss, M. G. Taylor, H. J. Klee, and D. M. Tieman Flavour compounds in tomato fruits: identification of loci and potential pathways affecting volatile composition J. Exp. Bot., January 1, 2009; 60(1): 325 - 337. [Abstract] [Full Text] [PDF]

				R. Welsch, F. Wust, C. Bar, S. Al-Babili, and P. Beyer A Third Phytoene Synthase Is Devoted to Abiotic Stress-Induced Abscisic Acid Formation in Rice and Defines Functional Diversification of Phytoene Synthase Genes Plant Physiology, May 1, 2008; 147(1): 367 - 380. [Abstract] [Full Text] [PDF]

				S. Moco, E. Capanoglu, Y. Tikunov, R. J. Bino, D. Boyacioglu, R. D. Hall, J. Vervoort, and R. C. H. De Vos Tissue specialization at the metabolite level is perceived during the development of tomato fruit J. Exp. Bot., December 7, 2007; (2007) erm271v1. [Abstract] [Full Text] [PDF]

				Q. Liu, J. Xu, Y. Liu, X. Zhao, X. Deng, L. Guo, and J. Gu A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck) J. Exp. Bot., December 1, 2007; 58(15-16): 4161 - 4171. [Abstract] [Full Text] [PDF]

				P. D. Fraser, E. M.A. Enfissi, J. M. Halket, M. R. Truesdale, D. Yu, C. Gerrish, and P. M. Bramley Manipulation of Phytoene Levels in Tomato Fruit: Effects on Isoprenoids, Plastids, and Intermediary Metabolism PLANT CELL, October 1, 2007; 19(10): 3194 - 3211. [Abstract] [Full Text] [PDF]

				H. T. Horner, R. A. Healy, G. Ren, D. Fritz, A. Klyne, C. Seames, and R. W. Thornburg Amyloplast to chromoplast conversion in developing ornamental tobacco floral nectaries provides sugar for nectar and antioxidants for protection Am. J. Botany, January 1, 2007; 94(1): 12 - 24. [Abstract] [Full Text] [PDF]

				F. Carrari, C. Baxter, B. Usadel, E. Urbanczyk-Wochniak, M.-I. Zanor, A. Nunes-Nesi, V. Nikiforova, D. Centero, A. Ratzka, M. Pauly, et al. Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts That Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior Plant Physiology, December 1, 2006; 142(4): 1380 - 1396. [Abstract] [Full Text] [PDF]

				R. Alba, P. Payton, Z. Fei, R. McQuinn, P. Debbie, G. B. Martin, S. D. Tanksley, and J. J. Giovannoni Transcriptome and Selected Metabolite Analyses Reveal Multiple Points of Ethylene Control during Tomato Fruit Development PLANT CELL, November 1, 2005; 17(11): 2954 - 2965. [Abstract] [Full Text] [PDF]

				R. Castillo, J.-A. Fernandez, and L. Gomez-Gomez Implications of Carotenoid Biosynthetic Genes in Apocarotenoid Formation during the Stigma Development of Crocus sativus and Its Closer Relatives Plant Physiology, October 1, 2005; 139(2): 674 - 689. [Abstract] [Full Text] [PDF]

				A. K. Bruno and C. M. Wetzel The early light-inducible protein (ELIP) gene is expressed during the chloroplast-to-chromoplast transition in ripening tomato fruit J. Exp. Bot., December 1, 2004; 55(408): 2541 - 2548. [Abstract] [Full Text] [PDF]

				M. Kato, Y. Ikoma, H. Matsumoto, M. Sugiura, H. Hyodo, and M. Yano Accumulation of Carotenoids and Expression of Carotenoid Biosynthetic Genes during Maturation in Citrus Fruit Plant Physiology, February 1, 2004; 134(2): 824 - 837. [Abstract] [Full Text] [PDF]

				M.-J. Rodrigo, J. F. Marcos, F. Alferez, M. D. Mallent, and L. Zacarias Characterization of Pinalate, a novel Citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content J. Exp. Bot., February 1, 2003; 54(383): 727 - 738. [Abstract] [Full Text] [PDF]

				K. A. PYKE and C. A. HOWELLS Plastid and Stromule Morphogenesis in Tomato Ann. Bot., November 1, 2002; 90(5): 559 - 566. [Abstract] [Full Text] [PDF]

				L. Alexander and D. Grierson Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening J. Exp. Bot., October 1, 2002; 53(377): 2039 - 2055. [Abstract] [Full Text] [PDF]

				P. M. Bramley Regulation of carotenoid formation during tomato fruit ripening and development J. Exp. Bot., October 1, 2002; 53(377): 2107 - 2113. [Abstract] [Full Text] [PDF]

				P. D. Fraser, S. Romer, C. A. Shipton, P. B. Mills, J. W. Kiano, N. Misawa, R. G. Drake, W. Schuch, and P. M. Bramley Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner PNAS, January 22, 2002; 99(2): 1092 - 1097. [Abstract] [Full Text] [PDF]

				F. D. Vecchia, R. Barbato, N. La Rocca, I. Moro, and N. Rascio Responses to bleaching herbicides by leaf chloroplasts of maize plants grown at different temperatures J. Exp. Bot., April 15, 2001; 52(357): 811 - 820. [Abstract] [Full Text] [PDF]

				G. O. Sozzi, A. A. Fraschina, and M. A. Castro Ripening-Associated Microstructural Changes in Antisense ACC Synthase Tomato Fruit Food Science and Technology International, February 1, 2001; 7(1): 59 - 71. [Abstract] [PDF]

				E. T. Wurtzel, R. Luo, and O. Yatou A simple approach to identify the first rice mutants blocked in carotenoid biosynthesis J. Exp. Bot., January 1, 2001; 52(354): 161 - 166. [Abstract] [Full Text] [PDF]

				J. Gaffe, J.-P. Bru, M. Causse, A. Vidal, L. Stamitti-Bert, J.-P. Carde, and P. Gallusci LEFPS1, a Tomato Farnesyl Pyrophosphate Gene Highly Expressed during Early Fruit Development Plant Physiology, August 1, 2000; 123(4): 1351 - 1362. [Abstract] [Full Text]

				R. Alba, M.-M. Cordonnier-Pratt, and L. H. Pratt Fruit-Localized Phytochromes Regulate Lycopene Accumulation Independently of Ethylene Production in Tomato Plant Physiology, May 1, 2000; 123(1): 363 - 370. [Abstract] [Full Text]

				A. J. Thompson, M. Tor, C. S. Barry, J. Vrebalov, C. Orfila, M. C. Jarvis, J. J. Giovannoni, D. Grierson, and G. B. Seymour Molecular and Genetic Characterization of a Novel Pleiotropic Tomato-Ripening Mutant Plant Physiology, June 1, 1999; 120(2): 383 - 390. [Abstract] [Full Text]

				G. Ronen, L. Carmel-Goren, D. Zamir, and J. Hirschberg An alternative pathway to beta -carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato PNAS, September 26, 2000; 97(20): 11102 - 11107. [Abstract] [Full Text] [PDF]