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First published online April 25, 2008; 10.1104/pp.108.116004

Plant Physiology 147:823-851 (2008)
© 2008 American Society of Plant Biologists

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SYSTEMS BIOLOGY, MOLECULAR BIOLOGY, AND GENE REGULATION

Gene Expression and Metabolism in Tomato Fruit Surface Tissues1,[C],[W]

Shira Mintz-Oron2, Tali Mandel2, Ilana Rogachev2, Liron Feldberg, Ofra Lotan, Merav Yativ, Zhonghua Wang, Reinhard Jetter, Ilya Venger, Avital Adato and Asaph Aharoni*

Department of Plant Sciences, Weizmann Institute of Science, Rehovot 76100, Israel (S.M.-O., T.M., I.R., L.F., O.L., M.Y., I.V., A. Adato, A. Aharoni); Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, Faculty of Agricultural, Food, and Environmental Quality Sciences, The Hebrew University of Jerusalem, Rehovot 76100, Israel (T.M.); and Departments of Botany (Z.W., R.J.) and Chemistry (R.J.), University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4

The cuticle, covering the surface of all primary plant organs, plays important roles in plant development and protection against the biotic and abiotic environment. In contrast to vegetative organs, very little molecular information has been obtained regarding the surfaces of reproductive organs such as fleshy fruit. To broaden our knowledge related to fruit surface, comparative transcriptome and metabolome analyses were carried out on peel and flesh tissues during tomato (Solanum lycopersicum) fruit development. Out of 574 peel-associated transcripts, 17% were classified as putatively belonging to metabolic pathways generating cuticular components, such as wax, cutin, and phenylpropanoids. Orthologs of the Arabidopsis (Arabidopsis thaliana) SHINE2 and MIXTA-LIKE regulatory factors, activating cutin and wax biosynthesis and fruit epidermal cell differentiation, respectively, were also predominantly expressed in the peel. Ultra-performance liquid chromatography coupled to a quadrupole time-of-flight mass spectrometer and gas chromatography-mass spectrometry using a flame ionization detector identified 100 metabolites that are enriched in the peel tissue during development. These included flavonoids, glycoalkaloids, and amyrin-type pentacyclic triterpenoids as well as polar metabolites associated with cuticle and cell wall metabolism and protection against photooxidative stress. Combined results at both transcript and metabolite levels revealed that the formation of cuticular lipids precedes phenylpropanoid and flavonoid biosynthesis. Expression patterns of reporter genes driven by the upstream region of the wax-associated SlCER6 gene indicated progressive activity of this wax biosynthetic gene in both fruit exocarp and endocarp. Peel-associated genes identified in our study, together with comparative analysis of genes enriched in surface tissues of various other plant species, establish a springboard for future investigations of plant surface biology.

1 The work was supported by the William Z. and Eda Bess Novick Young Scientist Fund, Mrs. Louise Gartner, Dallas, TX, the Y. Leon Benoziyo Institute for Molecular Medicine, the European Union project META-PHOR (contract no. FOODCT–2006–036220), the Agriculture and Agri-Food Canada/Binational Agricultural Research and Development Fund (research project no. C–9105–06), and the Minerva Foundation. Work by R.J. and Z.W. was supported by a Special Research Opportunity Grant from the Natural Sciences and Engineering Research Council of Canada. A. Aharoni is an incumbent of the Adolfo and Evelyn Blum Career Development Chair.

2 These authors contributed equally to the article.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Asaph Aharoni (asaph.aharoni{at}weizmann.ac.il).

[C] Some figures in this article are displayed in color online but in black and white in the print edition.

[W] The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.116004

* Corresponding author; e-mail asaph.aharoni{at}weizmann.ac.il.

Received January 9, 2008; accepted April 8, 2008; published April 25, 2008.




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