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Population analysis reveals the roles of DNA methylation in tomato domestication and metabolic diversity

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Abstract

DNA methylation is an important epigenetic marker, yet its diversity and consequences in tomato breeding at the population level are largely unknown. We performed whole-genome bisulfite sequencing (WGBS), RNA sequencing, and metabolic profiling on a population comprising wild tomatoes, landraces, and cultivars. A total of 8,375 differentially methylated regions (DMRs) were identified, with methylation levels progressively decreasing from domestication to improvement. We found that over 20% of DMRs overlapped with selective sweeps. Moreover, more than 80% of DMRs in tomato were not significantly associated with single-nucleotide polymorphisms (SNPs), and DMRs had strong linkages with adjacent SNPs. We additionally profiled 339 metabolites from 364 diverse accessions and further performed a metabolic association study based on SNPs and DMRs. We detected 971 and 711 large-effect loci via SNP and DMR markers, respectively. Combined with multi-omics, we identified 13 candidate genes and updated the polyphenol biosynthetic pathway. Our results showed that DNA methylation variants could complement SNP profiling of metabolite diversity. Our study thus provides a DNA methylome map across diverse accessions and suggests that DNA methylation variation can be the genetic basis of metabolic diversity in plants.

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Data availability

Data supporting the findings of this work are available within the paper and its Supplementary Information files. Tomato genome sequence data for this article were downloaded from the SGN (https://solgenomics.net/). The expression profiles of 35 tomatoes are available in Table S5 in Supporting Information. The raw values obtained from the metabolomic datasets are available in Table S7 in Supporting Information. The sequence files of WGBS and RNA-seq are available at Genome Sequence Archive at the Big Data Center under project accession PRJCA009995 with the accession number CRA007189 at http://bigd.big.ac.cn/gsa.

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Acknowledgements

This work was supported by the Hainan Province Science and Technology Special Fund (ZDYF2022XDNY144), the National Natural Science Foundation of China (32100212), the National Key Research and Development Program of China (2021YFA0909600, 2022YFF1001900), the Young Elite Scientists Sponsorship Program by CAST (2019QNRC001), the Hainan Provincial Academician Innovation Platform Project (HD-YSZX-202003, HD-YSZX-202004), the Hainan University Startup Fund (KYQD(ZR)1916, KYQD(ZR)21025).

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Correspondence to Shouchuang Wang.

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Supplementary Information

Population analysis reveals the roles of DNA methylation in tomato domestication and metabolic diversity

Population analysis reveals the roles of DNA methylation in tomato domestication and metabolic diversity

Summary of collected tomato accessions

Summary of WGBS data generated in the current study

Population-wide differentially methylated regions in the CG and CHG contexts

Summary of RNA-Seq data generated in the current study

TPM value of thirty-five cultivated and wild lines in the current study

Detailed information for metabolites detected in the current study

The raw dataset of metabolites among populations

The significant mGWAS signals for all the metabolites

The significant mEWAS signals for all the metabolites

meQTL analysis of metabolome-variome-methylome network

Primers used in the current study

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Guo, H., Cao, P., Wang, C. et al. Population analysis reveals the roles of DNA methylation in tomato domestication and metabolic diversity. Sci. China Life Sci. 66, 1888–1902 (2023). https://doi.org/10.1007/s11427-022-2299-5

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