Changes in Transcriptional Profiles Are Associated with Early Fruit Tissue Specialization in Tomato

Abstract

The cell expansion phase contributes in determining the major characteristics of a fleshy fruit and represents two-thirds of the total fruit development in tomato (Solanum lycopersicum). So far, it has received very little attention. To evaluate the interest of a genomic scale approach, we performed an initial sequencing of approximately 1,200 cell expansion stage-related sequence tags from tomato fruit at 8, 12, and 15 d post anthesis. Interestingly, up to approximately 35% of the expressed sequence tags showed no homology with available tomato expressed sequence tags and up to approximately 21% with any known gene. Microarrays spotted with expansion phase-related cDNAs and other fruit cDNAs involved in various developmental processes were used (1) to profile gene expression in developing fruit and other plant organs and (2) to compare two growing fruit tissues engaged mostly in cell division (exocarp) or in cell expansion (locular tissue surrounding the seeds). Reverse transcription-polymerase chain reaction analysis was further used to confirm microarray results and to specify expression profiles of selected genes (24) in various tissues from expanding fruit. The wide range of genes expressed in the exocarp is consistent with a protective function and with a high metabolic activity of this tissue. In addition, our data show that the expansion of locular cells is concomitant with the expression of genes controlling water flow, organic acid synthesis, sugar storage, and photosynthesis and suggest that hormones (auxin and gibberellin) regulate this process. The data presented provide a basis for tissue-specific analyses of gene function in growing tomato fruit.After ovule fertilization, early tomato (Solanum lycopersicum) fruit development is characterized by a period of cell division followed by cell expansion, resulting in the formation of large vacuolated cells (Mohr and Stein, 1969). Cell expansion is the longest phase in fruit development and may contribute to 90% of the increase in fruit weight, depending on the cultivar. In addition, cell expansion contributes, along with ripening, to the major structural, biochemical, and physiological changes that characterize a fleshy fruit. The cell wall changes associated with cell enlargement and the continuous accumulation in the vacuole of water, sugars, organic acids, and other compounds are necessary to maintain the turgor pressure of the expanding cells. In addition, these physiological processes contribute significantly to the flavor, texture, and overall attractiveness of the ripe fruit. The succession of the different phases of tomato fruit development is not, however, as clear cut as described above. It varies greatly according to the fruit tissue considered (Joubès et al., 1999). Tomato fruit is a complex organ composed of two or more carpels separated by a radially orientated tissue called septum, which results from the fusion of two adjacent carpel walls (or pericarp). The pericarp encloses the locular cavity containing the seeds attached to a central pa...

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

“…Its quantitative importance remains stable throughout fruit development. The differentiation of the locular tissue during fruit development is particularly impressive: in the cultivar studied here, it starts to develop from columella at around 4 d postanthesis (DPA; Lemaire-Chamley et al, 2005; data not shown) and fills the locular cavity as early as 20 DPA (Fig. 1C).…”

“…Raw data (intensity median with no background subtraction) were submitted to R/MAANOVA version 1.2.1 software (R package for the analysis of microarray) for data visualization, regional Lowess normalization, and statistical analysis, including multiple test adjustments (FDR) as described by Lemaire-Chamley et al (2005). We used F statistics computed on the James-Stein shrinkage estimates of the error variance (Wu et al, 2003) and selected genes with P , 0.01 and FDR , 0.05 as significantly expressed.…”

“…For early stages of fruit development, auxin and brassinosteroids are believed to act as major regulatory signals (Balbi and Lomax, 2003;Montoya et al, 2005). The auxin-dependent signal transduction network has been the most studied because of its role in fruit set and cell expansion phases (Gillaspy et al, 1993;Catala et al, 2000;Balbi and Lomax, 2003;Lemaire-Chamley et al, 2005). In addition, cross talk between auxin and ethylene has been suggested for regulating early fruit development (Balbi and Lomax, 2003) and the onset of ripening (Jones et al, 2002).…”

“…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.…”

“…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.…”