Shapes of edible plant organs vary dramatically among and within crop plants. To explain and ultimately employ this variation towards crop improvement, we determined the genetic, molecular and cellular bases of fruit shape diversity in tomato. Through positional cloning, protein interaction studies, and genome editing, we report that OVATE Family Proteins and TONNEAU1 Recruiting Motif proteins regulate cell division patterns in ovary development to alter final fruit shape. The physical interactions between the members of these two families are necessary for dynamic relocalization of the protein complexes to different cellular compartments when expressed in tobacco leaf cells. Together with data from other domesticated crops and model plant species, the protein interaction studies provide possible mechanistic insights into the regulation of morphological variation in plants and a framework that may apply to organ growth in all plant species.
Domestication of fruit and vegetables resulted in a huge diversity of shapes and sizes of the produce. Selections that took place over thousands of years of alleles that increased fruit weight and altered shape for specific culinary uses provide a wealth of resources to study the molecular bases of this diversity. Tomato (Solanum lycopersicum) evolved from a wild ancestor (S. pimpinellifolium) bearing small and round edible fruit. Molecular genetic studies led to the identification of two genes selected for fruit weight: FW2.2 encoding a member of the Cell Number Regulator family; and FW3.2 encoding a P450 enzyme and the ortholog of KLUH. Four genes were identified that were selected for fruit shape: SUN encoding a member of the IQD family of calmodulin-binding proteins leading to fruit elongation; OVATE encoding a member of the OVATE family proteins involved in transcriptional repression leading to fruit elongation; LC encoding most likely the ortholog of WUSCHEL controlling meristem size and locule number; FAS encoding a member in the YABBY family controlling locule number leading to flat or oxheart shape. For this article, we will provide an overview of the putative function of the known genes, when during floral and fruit development they are hypothesized to act and their potential importance in regulating morphological diversity in other fruit and vegetable crops.
Bulk segregant analysis coupled with whole genome sequencing is a powerful approach and cost-effective method to identify loci controlling fruit traits in tomato. Domestication of fruit and vegetable crops was accompanied by selection for weight of the edible parts. Increases in fruit weight are controlled by multiple quantitative trait loci (QTL). To date, only two fruit weight genes have been cloned and a third has been fine-mapped. Genes that control locule number also impact fruit weight and two of them are known. To efficiently identify additional tomato fruit weight (FW) and locule number (LC) loci, six F2 populations were generated from crosses between closely related tomato accessions for which the alleles of the cloned FW and LC genes were known. We employed the bulk segregant approach coupled to whole genome sequencing (QTL-seq) which led to the identification of three highly significant and newly mapped FW QTL. fw11.2 was located in the distal part of chromosome 11 above the known loci fas and fw11.3; fw1.1 in the pericentromeric region of chromosome 1; and fw3.3 located ~1.6 Mb below the known fruit weight gene, SlKLUH/FW3.2. In addition, we mapped three LC QTL (lcn2.4, lcn5.1, and lcn6.1) although their significance was generally low. To confirm the location of the gene underlying fw11.2, we developed additional markers and conducted progeny tests. These results allowed us to narrow down the fw11.2 QTL to a region of ~750 kb corresponding to 66 candidate genes. Our research approach provided a cost-effective and time-efficient method for the identification of additional genes involved in FW and LC that could be used for both fruit development studies and crop improvement programs.
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.
HighlightWe combined fine-mapping, gene expression, genome sequence variation, and morphological and histological analyses to select candidate genes underlying fs8.1, a major tomato fruit shape QTL located in a pericentromeric region.
Elongated tomato fruit shape is the result of the action of the fruit shape genes possibly in coordination with the phytohormone auxin. To investigate the possible link between auxin and the fruit shape genes, a series of auxin (2,4-D) treatments were performed on the wild-type and the fruit shape nearisogenic lines (NILs) in Solanum pimpinellifolium accession LA1589 background. Morphological and histological analyses indicated that auxin application approximately 3 weeks before anthesis led to elongated pear-shaped ovaries and fruits, which was mainly attributed to the increase of ovary/ fruit proximal end caused by the increase of both cell number and cell size. Fruit shape changes caused by SUN, OVATE and fs8.1 were primarily due to the alterations of cell number along different growth axes. Particularly, SUN caused elongation by extending cell number along the entire proximaldistal axis, whereas OVATE caused fruit elongation in the proximal area, which was most similar to the effect of auxin on ovary shape. Expression analysis of flower buds at different stages in fruit shape NILs indicated that SUN had a stronger impact on the transcriptome than OVATE and fs8.1. The sun NIL differentially expressed genes were enriched in several biological processes, such as lipid metabolism, ion transmembrane and actin cytoskeleton organization. Additionally, SUN also shifted the expression of the auxinrelated genes, including those involved in auxin biosynthesis, homeostasis, signal transduction and polar transport, indicating that SUN may regulate ovary/fruit shape through modifying the expression of auxin-related genes very early during the formation of the ovary in the developing flower.
Within large-fruited germplasm, fruit size is influenced by flat and globe shapes. Whereas flat fruits are smaller and retain better marketability, globe fruits are larger and more prone to cuticle disorders. Commercial hybrids are often developed from crosses between flat and globe shaped parents because flat shape is thought to be dominant and fruit size intermediate. The objectives of this study were to determine the genetic basis of flat/globe fruit shape in large-fruited fresh-market tomato germplasm and to characterize its effects on several fruit traits. Twenty-three advanced single plant selections from the Fla. 8000 × Fla. 8111B cross were selectively genotyped using a genome-wide SNP array, and inclusive composite interval mapping identified a single locus on the upper arm of chromosome 12 associated with shape, which we termed globe. A 238-plant F2 population and 69 recombinant inbred lines for this region from the same parents delimited globe to approximately 392-kilobases. A germplasm survey representing materials from multiple breeding programs demonstrated that the locus explains the flat/globe shape broadly. A single base insertion in an exon of Solyc12g006860, a gene annotated as a brassinosteroid hydroxylase, segregated completely with shape in all populations tested. CRISPR/Cas9 knock out plants confirmed this gene as underlying the globe locus. In silico analysis of the mutant allele of GLOBE among 595 wild and domesticated accessions suggested that the allele arose very late in the domestication process. Fruit measurements in three genetic backgrounds evidenced that globe impacts fruit size and several fruit shape attributes, pedicel length/width, and susceptibility of fruit to weather check. The mutant allele of GLOBE appears mostly recessive for all traits except fruit size where it acts additively.
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