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ENO regulates tomato fruit size through the floral meristem development network.

ABSTRACT: A dramatic evolution of fruit size has accompanied the domestication and improvement of fruit-bearing crop species. In tomato (Solanum lycopersicum), naturally occurring cis-regulatory mutations in the genes of the CLAVATA-WUSCHEL signaling pathway have led to a significant increase in fruit size generating enlarged meristems that lead to flowers with extra organs and bigger fruits. In this work, by combining mapping-by-sequencing and CRISPR/Cas9 genome editing methods, we isolated EXCESSIVE NUMBER OF FLORAL ORGANS (ENO), an AP2/ERF transcription factor which regulates floral meristem activity. Thus, the ENO gene mutation gives rise to plants that yield larger multilocular fruits due to an increased size of the floral meristem. Genetic analyses indicate that eno exhibits synergistic effects with mutations at the LOCULE NUMBER (encoding SlWUS) and FASCIATED (encoding SlCLV3) loci, two central players in the evolution of fruit size in the domestication of cultivated tomatoes. Our findings reveal that an eno mutation causes a substantial expansion of SlWUS expression domains in a flower-specific manner. In vitro binding results show that ENO is able to interact with the GGC-box cis-regulatory element within the SlWUS promoter region, suggesting that ENO directly regulates SlWUS expression domains to maintain floral stem-cell homeostasis. Furthermore, the study of natural allelic variation of the ENO locus proved that a cis-regulatory mutation in the promoter of ENO had been targeted by positive selection during the domestication process, setting up the background for significant increases in fruit locule number and fruit size in modern tomatoes.

SUBMITTER: Yuste-Lisbona FJ

PROVIDER: S-EPMC7148573 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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ENO regulates tomato fruit size through the floral meristem development network.

Yuste-Lisbona Fernando J FJ Fernández-Lozano Antonia A Pineda Benito B Bretones Sandra S Ortíz-Atienza Ana A García-Sogo Begoña B Müller Niels A NA Angosto Trinidad T Capel Juan J Moreno Vicente V Jiménez-Gómez José M JM Lozano Rafael R

Proceedings of the National Academy of Sciences of the United States of America 20200316 14

A dramatic evolution of fruit size has accompanied the domestication and improvement of fruit-bearing crop species. In tomato (Solanum lycopersicum), naturally occurring cis-regulatory mutations in the genes of the CLAVATA-WUSCHEL signaling pathway have led to a significant increase in fruit size generating enlarged meristems that lead to flowers with extra organs and bigger fruits. In this work, by combining mapping-by-sequencing and CRISPR/Cas9 genome editing methods, we isolated EXC ...[more]

PMID: 32179669

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Project description:BACKGROUND:Domestication and selection of crops have notably reshaped fruit morphology. With its large phenotypic diversity, tomato (Solanum lycopersicum) illustrates this evolutive trend. Genes involved in flower meristem development are known to regulate also fruit morphology. To decipher the genetic variation underlying tomato fruit morphology, we assessed the nucleotide diversity and selection footprints of candidate genes involved in flower and fruit development and performed genome-wide association studies. RESULTS:Thirty candidate genes were selected according to their similarity with genes involved in meristem development or their known causal function in Arabidopsis thaliana. In tomato, these genes and flanking regions were sequenced in a core collection of 96 accessions (including cultivated, cherry-type and wild relative accessions) maximizing the molecular diversity, using the Roche 454 technology. A total amount of 17 Mb was sequenced allowing the discovery of 6,106 single nucleotide polymorphisms (SNPs). The annotation of the 30 gene regions identified 231 exons carrying 517 SNPs. Subsequently, the nucleotide diversity (?) and the neutral evolution of each region were compared against genome-wide values within the collection, using a SNP array carrying 7,667 SNPs mainly distributed in coding sequences.About half of the genes revealed footprints of selection and polymorphisms putatively involved in fruit size variation by showing negative Tajima's D and nucleotide diversity reduction in cultivated tomato compared to its wild relative. Among the candidates, FW2.2 and BAM1 sequences revealed selection footprints within their promoter regions suggesting their potential involvement in their regulation. Two associations co-localized with previously identified loci: LC (locule number) and Ovate (fruit shape). CONCLUSION:Compared to whole genome genotypic data, a drastic reduction of nucleotide diversity was shown for several candidate genes. Strong selection patterns were identified in 15 candidates highlighting the critical role of meristem maintenance genes as well as the impact of domestication on candidates. The study highlighted a set of polymorphisms putatively important in the evolution of these genes.

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ENO regulates tomato fruit size through the floral meristem development network.

Publications

<i>ENO</i> regulates tomato fruit size through the floral meristem development network.

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