Increases in fruit weight of cultivated vegetables and fruits accompanied the domestication of these crops. Here we report on the positional cloning of a quantitative trait locus (QTL) controlling fruit weight in tomato. The derived allele of Cell Size Regulator (CSR-D) increases fruit weight predominantly through enlargement of the pericarp areas. The expanded pericarp tissues result from increased mesocarp cell size and not from increased number of cell layers. The effect of CSR on fruit weight and cell size is found across different genetic backgrounds implying a consistent impact of the locus on the trait. In fruits, CSR expression is undetectable early in development from floral meristems to the rapid cell proliferation stage after anthesis. Expression is low but detectable in growing fruit tissues and in or around vascular bundles coinciding with the cell enlargement stage of the fruit maturation process. CSR encodes an uncharacterized protein whose clade has expanded in the Solanaceae family. The mutant allele is predicted to encode a shorter protein due to a 1.4 kb deletion resulting in a 194 amino-acid truncation. Co-expression analyses and GO term enrichment analyses suggest association of CSR with cell differentiation in fruit tissues and vascular bundles. The derived allele arose in Solanum lycopersicum var cerasiforme and appears completely fixed in many cultivated tomato’s market classes. This finding suggests that the selection of this allele was critical to the full domestication of tomato from its intermediate ancestors.

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Published in PLOS Genetics, v. 13, issue 8, e1006930, p. 1-26.

© 2017 Mu et al.

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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This research was funded by the National Science Foundation IOS 0922661 and IOS 1564366 to EvdK. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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The raw FASTQ files for the RNA-seq libraries were deposited at NCBI Sequence Read Archive (SRA) with SRA study accession SRP089936. Gene expression data (RPKM) are available through a Tomato Functional Genomic Database (TFGD; http://ted.bti.cornell.edu/cgi-bin/TFGD/digital/home.cgi).