Gene Expression and Metabolism in Tomato Fruit Surface Tissues    

Abstract

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.

The Tomato FRUITFULL Homologs TDR4/FUL1 and MBP7/FUL2 Regulate Ethylene-Independent Aspects of Fruit Ripening

“…Because pericarp thickness did not differ between wild-type and transgenic tomatoes, we investigated if altered epidermis characteristics could explain the increased water loss. The epidermal cell layer is the outermost layer of the fruit pericarp and is covered by a waxy cuticle that thickens as the fruit ages, protecting the fruit from desiccation (Mintz-Oron et al, 2008). The thickness of the waxy cuticle can be determined with Sudan staining, which has a high affinity for lipids.…”

“…The cuticle has been reported to be an important transpiration barrier (Mintz-Oron et al, 2008); therefore, the altered expression of fatty acid biosynthesis genes may contribute to the increased water loss of the FUL1/2 silenced fruits. We found several genes related to cutin and fatty acid synthesis to be downregulated in FUL1/2 silenced fruits, among which were a glycerol-3-Pacyltransferase (log 2 = 21.2) and a cytochrome P450 hydroperoxide lyase (HPL) (log 2 = 21.8).…”

Analyses of Tomato Fruit Brightness Mutants Uncover Both Cutin-Deficient and Cutin-Abundant Mutants and a New Hypomorphic Allele of GDSL Lipase

“…The plasma membrane ATP-binding cassette transporters have been implicated in the transport of both wax and cutin to the apoplast, whereas lipid transfer proteins very likely contribute to the transport of cutin monomers through the cell wall to the cutin layer (Yeats and Rose, 2013). The implication of enzymes of the GDSL lipase family in cutin assembly, which is long suspected (Reina et al, 2007;Mintz-Oron et al, 2008), was recently demonstrated in tomato (Solanum lycopersicum; Girard et al, 2012;Yeats et al, 2012a).…”

Gene and Metabolite Regulatory Network Analysis of Early Developing Fruit Tissues Highlights New Candidate Genes for the Control of Tomato Fruit Composition and Development

“…Both the nutritional and the sensorial attributes are built throughout the successive phases of fruit development, namely cell division, cell expansion, and ripening. While the fruitripening process is obviously important (Giovannoni, 2001), there is also a growing body of evidence that supports the key role of early fruit development for the acquisition of several fruit quality traits, including the accumulation of sugars and organic acids (Guillet et al, 2002;Lemaire-Chamley et al, 2005;Petreikov et al, 2006), the determination of cell wall and texture characteristics (Chaïb et al, 2007), and the cuticle biosynthesis (Mintz-Oron et al, 2008). In the growing fruit, these processes mainly take place during the cell expansion phase, which sustains fruit growth by allowing a large increase in fruit cell volume linked with membrane and cell wall/synthesis and the con-comitant accumulation of water, mineral ions, and metabolites in the vacuoles, thereby conferring its fleshy characteristics to the fruit.…”

“…Coexpression analyses allowed the identification of genes regulating tissue and cell development (Persson et al, 2005;Gifford et al, 2008), environmental responses , and plant metabolism Gutiérrez et al, 2008) and were further validated by reverse genetics strategies. With the current availability of large-scale gene expression and metabolite profiling techniques in many plants, including tomato (Alba et al, 2004(Alba et al, , 2005Lemaire-Chamley et al, 2005;Moco et al, 2006;Mounet et al, 2007;Saito et al, 2007;Mintz-Oron et al, 2008;Schauer et al, 2008), large gene expression and metabolite data sets can be combined through correlation and clustering analyses (Urbanczyk-Wochniak et al, 2003) and further represented as a network of relationships between genes and metabolites Saito et al, 2007;Hoefgen and Nikiforova, 2008). These approaches have been successfully applied to the discovery of regulatory and biosynthetic genes involved in the control of metabolite production, such as the glucosinolate metabolism (Hirai et al, 2004.…”