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Chromosome-scale assembly and gene editing of Solanum americanum genome reveals the basis for thermotolerance and fruit anthocyanin composition

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Abstract

Solanum americanum serves as a promising source of resistance genes against potato late blight and is considered as a leafy vegetable for complementary food and nutrition. The limited availability of high-quality genome assemblies and gene annotations has hindered the exploration and exploitation of stress-resistance genes in S. americanum. Here, we present a chromosome-level genome assembly of a thermotolerant S. americanum ecotype and identify a crucial heat-inducible transcription factor gene, SaHSF17, essential for heat tolerance. The CRISPR/Cas9 system-mediated knockout of SaHSF17 results in remarkably reduced thermotolerance in S. americanum, exhibiting a significant suppression of multiple HSP gene expressions under heat treatment. Furthermore, our transcriptome analysis and anthocyanin component investigation of fruits indicated that delphinidins are the major anthocyanins accumulated in the mature dark-purple fruits. The accumulation of delphinidins and other pigment components during fruit ripening in S. americanum coincides with the transcriptional regulation of key genes, particularly the F3′5′H and F3′H genes, in the anthocyanin biosynthesis pathway. By integrating existing knowledge, the development of this high-quality reference genome for S. americanum will facilitate the identification and utilization of novel abiotic and biotic stress-resistance genes for improvement of Solanaceae and other crops.

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Data availability statement

All data supporting the findings of this study are available within the paper and its Supplementary Information. The genomic and Hi-C data discussed in this article have been deposited in the NCBI repository database under accession numbers PRJNA1019512. Additionally, the RNA-seq data have been deposited to relevant NCBI repository database with the dataset identifier PRJNA1020265.

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Acknowledgements

This work was supported by the Anhui Provincial Natural Science Foundation (grant 2208085Y08), National Natural Science Foundation of China (grant 32000206), National Agriculture Science and Technology Major Program (No. NK202209040302), and Key Research and Development projects of Ningxia Hui Autonomous Region (No. 2022BBF02008-03).

Funding

This work was supported by the Anhui Provincial Natural Science Foundation (grant 2208085Y08 to ZW), National Natural Science Foundation of China (grant 32000206 to ZW), National Agriculture Science and Technology Major Program (No. NK202209040302 to XZ), and Key Research and Development projects of Ningxia Hui Autonomous Region (No. 2022BBF02008-03 to XZ).

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J-KZ, XZ, and ZW conceived the project; HS, XZ, and ZW designed the experiments and analyzed the data; SY, YW, TL, and ZW performed most of the experiments; JP, DK, ZQW, HM, YG, XW, and YH provided technical assistance; ZW drafted the article; ZW, YW, XZ, and HS revised and finalized the manuscript.

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Correspondence to Xiangqiang Zhan or Zhen Wang.

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Communicated by Herman J. van Eck.

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Yu, S., Wang, Y., Li, T. et al. Chromosome-scale assembly and gene editing of Solanum americanum genome reveals the basis for thermotolerance and fruit anthocyanin composition. Theor Appl Genet 137, 15 (2024). https://doi.org/10.1007/s00122-023-04523-7

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