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DEVELOPMENT AND HORMONE ACTION

A Reevaluation of the Key Factors That Influence Tomato Fruit Softening and Integrity^1,[W],[OA]

Department of Plant Biology (M.S., A.J.M., T.I., K.J.N., J.K.C.R.) and Department of Horticulture (C.B.W.), Cornell University, Ithaca, New York 14853; Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (M.A.J., S.M.G.); College of Horticulture, Northwest Agricultural & Forestry University, Yangling, Shaanxi 712100, China (R.X.); Department of Plant Sciences, University of California, Davis, California 95616 (J.M.L., K.A.S.); Max-Planck-Institut für Molekulare Pflanzenphysiologie, 14476 Potsdam-Golm, Germany (A.R.F., A.L.); and Complex Carbohydrate Research Center and Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602 (M.A.O.)

The softening of fleshy fruits, such as tomato (Solanum lycopersicum), during ripening is generally reported to result principally from disassembly of the primary cell wall and middle lamella. However, unsuccessful attempts to prolong fruit firmness by suppressing the expression of a range of wall-modifying proteins in transgenic tomato fruits do not support such a simple model. ‘Delayed Fruit Deterioration’ (DFD) is a previously unreported tomato cultivar that provides a unique opportunity to assess the contribution of wall metabolism to fruit firmness, since DFD fruits exhibit minimal softening but undergo otherwise normal ripening, unlike all known nonsoftening tomato mutants reported to date. Wall disassembly, reduced intercellular adhesion, and the expression of genes associated with wall degradation were similar in DFD fruit and those of the normally softening ‘Ailsa Craig’. However, ripening DFD fruit showed minimal transpirational water loss and substantially elevated cellular turgor. This allowed an evaluation of the relative contribution and timing of wall disassembly and water loss to fruit softening, which suggested that both processes have a critical influence. Biochemical and biomechanical analyses identified several unusual features of DFD cuticles and the data indicate that, as with wall metabolism, changes in cuticle composition and architecture are an integral and regulated part of the ripening program. A model is proposed in which the cuticle affects the softening of intact tomato fruit both directly, by providing a physical support, and indirectly, by regulating water status.

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: Jocelyn K.C. Rose (jr286{at}cornell.edu).

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www.plantphysiol.org/cgi/doi/10.1104/pp.107.097477

^* Corresponding author; e-mail jr286{at}cornell.edu; fax 607–255–5407.

Received February 2, 2007; accepted April 12, 2007; published April 20, 2007.

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