Plant Physiol. Journal of Pharmacology and Experimental Therapeutics
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Published on October 27, 2006; 10.1104/pp.106.088534


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Received August 26, 2006
Accepted October 17, 2006

Integrated Analysis of Metabolite and Transcript Levels Reveals the Metabolic Shifts that Underlie Tomato Fruit Development and Highlight Regulatory Aspects of Metabolic Network Behavior

Fernando Carrari , Charles Baxter , Björn Usadel , Ewa Urbanczyk-Wochniak , Maria-Ines Zanor , Adriano Nunes-Nesi , Victoria Nikiforova , Danilo Centero , Antje Ratzka , Markus Pauly , Lee Sweetlove , and Alisdair R. Fernie *

Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 Golm-Postdam, Germany; Instituto de Biotecnología, CICVyA, Instituto Nacional de Tecnología Agrícola (IB-INTA) Argentina, partner group of the Max Planck Institut für Molekulare Pflanzenphysiologie
Department of Plant Sciences, University of Oxford, South Parks Rd, Oxford, OX1 3RB, United Kingdom
Max-Planck-Institut für Molekulare Pflanzenphysiologie, Am Mühlenberg 1, 14476 Golm-Postdam, Germany

* Corresponding author; email: fernie{at}mpimp-golm.mpg.de.

Tomato is a well studied model of fleshy fruit development and ripening. Tomato fruit development is well understood from a hormonal-regulatory perspective and developmental changes in pigment and cell wall metabolism are also well characterized. However, more general aspects of metabolic change during fruit development have not been studied despite the importance of metabolism in the context of final composition of the ripe fruit. In this study we quantified the abundance of a broad range of metabolites by GC-MS, analyzed a number of the principal metabolic fluxes and in parallel analyzed transcriptomic changes during tomato fruit development. Metabolic profiling revealed pronounced shifts in the abundance of metabolites of both primary and secondary metabolism during development. The metabolite changes were reflected in the flux analysis which revealed a general decrease in metabolic activity during ripening. However, there were several distinct patterns of metabolite profile and statistical analysis demonstrated that metabolites in the same (or closely related) pathways changed in abundance in a coordinated manner indicating a tight regulation of metabolic activity. The metabolite data alone allowed investigations of likely routes through the metabolic network and as an example we analyze the operational feasibility of different pathways of ascorbate synthesis. When combined with the transcriptomic data, several aspects of the regulation of metabolism during fruit ripening were revealed. First, it was apparent that transcript abundance was less strictly coordinated by functional group than metabolite abundance suggesting that post-translational mechanisms dominate metabolic regulation. Nevertheless, there were some correlations between specific transcripts and metabolites and several novel associations were identified that could provide potential targets for manipulation of fruit compositional traits. Finally, there was a strong relationship between ripening-associated transcripts and specific metabolite groups such as TCA cycle organic acids and sugar phosphates underlining the importance of the respective metabolic pathways during fruit development.




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