Natural alleles at a tomato fruit size quantitative trait locus differ by heterochronic regulatory mutations

Abstract

fw2.2 is a major quantitative trait locus that accounts for as much as 30% of the difference in fruit size between wild and cultivated tomatoes. Evidence thus far indicates that fw2.2 alleles modulate fruit size through changes in gene regulation rather than in the FW2.2 protein itself. To investigate the nature of these regulatory changes and the manner in which they may affect fruit size, a pair of nearly isogenic lines has been subjected to detailed developmental, transcriptional, mitotic, and in situ hybridization studies. The results indicate that the large-and small-fruited alleles of fw2.2 differ in peak transcript levels by Ϸ1 week. Moreover, this difference in timing of expression is associated with concomitant changes in mitotic activity in the early stage of fruit development. The changes in timing of gene expression (heterochronic allelic variation), combined with overall differences in total transcript levels, are sufficient to account for a large portion phenotypic differences in fruit weight associated with the two alleles. C ell division and expansion are generally considered two distinct phases during tomato fruit development (1). The rate of both cell growth and cell proliferation, which might be coordinated and instructed by cellular mechanisms, is critically important in determining final fruit size (2). Despite the fact that cell expansion may account for the greatest increase in volume, cell division is also an essential factor of fruit organogenesis because it determines the final cell number within the fruit. Therefore, fruit size is, in part, the result of a defined number of cell divisions that occur during development (3). High levels of cell division often take place in the first few weeks after anthesis, but mitotic cells can still be found in later phases of development, even in ripening fruit (4).Recently, increasing knowledge in molecular genetics has allowed the characterization of a number of molecular events that influence cell division or cell expansion. Many genes have been shown to control final organ size in Drosophila via cell division and cell expansion, such as dMYC (5), CyclinD͞Cdk4 (6), RAS (7), TSC1 and TSC2 (8), etc. In plants, recent research has yielded much evidence of the molecular and genetic control of cell division and expansion as well as organ size; for example, AINTEGUMENTA (ANT) (9, 10), ANGUSTIFOLIA and RO-TUNDIFOLIA3 (11), ABP1 (12), CLV and WUS (13), NtKIS1a (14), and CYC1At (15). Despite this recent progress, the precise molecular mechanisms governing organ size by cell division or expansion in plants remain far less clear than in Drosophila. Moreover, most genes characterized to control organ size in plants are associated with the development of leaves, roots, and shoot apical meristems. Less attention has been paid to developmental and molecular mechanisms that regulate fruit weight and size.Recently, molecular marker studies have found 28 quantitative trait loci (QTLs) affecting tomato fruit weight and size in crosses between the domesticated tomato...

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

“…locular tissue), others (e.g. exocarp) retain mitotic activity late during fruit development (Joubès et al, 1999;Cong et al, 2002). The relative development of the various fruit tissues will affect both fruit size and anatomy but also fruit quality.…”

Differences in regulation of carbohydrate metabolism during early fruit development between domesticated tomato and two wild relatives

“…The diVerence between the domesticated and the wild alleles is in the regulation of expression rather than in changes in the fw2.2. protein (Cong et al 2002). Fw2.2 is associated with a modulation of the size of pre-anthesis ovaries.…”

Molecular Plant Breeding as the Foundation for 21st Century Crop Improvement

“…The molecular cloning of QTLs has yielded novel insights about the biology of quantitative traits that were not likely to be discovered from the analysis of gene knockouts or overexpression strategies, in particular the impacts of regulatory variation on phenotypic variation and evolution (e.g. Cong et al, 2002;Clark et al, 2006;Yan et al, 2004;Salvi et al, 2007). Furthermore, molecular markers, genomics, and biotechnology are now applied in an iterative network to exploit genetic diversity for crop improvement.…”