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Low frequency of the wild-type freezing-tolerance LsCBF7 allele among lettuce population suggests a negative selection during domestication and breeding

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Abstract

Key message

Sustainable winter production in lettuce requires freezing tolerant varieties. This study identified a wild-type allele of LsCBF7 that could contribute to freezing tolerance improvement in lettuce.

Abstract

Lettuce is one of the most consumed vegetables globally. While ideally grown in 13–21 °C, its cultivation extends into winter in milder climates. However, occasional freezing temperatures can significantly reduce yields. Therefore, the development of freezing-tolerant lettuce varieties has become a long-term goal of lettuce breeding programs. Despite its significance, our understanding of freezing tolerance in lettuce remains limited. Plants have evolved a coping mechanism against freezing, known as cold acclimation, whereby they can increase freezing tolerance when pre-exposed to low nonfreezing temperatures. The CBF pathway is well-known for its central role in cold acclimation. Previously, we identified 14 CBF genes in lettuce and discovered that one of them, LsCBF7, had a loss-of-function mutation. In this study, we uncovered that accessions from colder regions carried the wild-type allele of LsCBF7 and this allele likely contributed to increased freezing tolerance, with 14% of the lettuce population carrying this allele. Interestingly, in wild lettuce (L. serriola) that is considered a progenitor of cultivated lettuce, this wild-type allele was much more common, with a frequency of 90%. This finding suggests that this wild-type allele may have undergone negative selection during the domestication or breeding of lettuce. Our data strongly indicate that this allele could be linked to early bolting, an undesirable trait in lettuce, which may have driven the negative selection. While this wild-type allele shows promise for improving freezing tolerance in lettuce, it is crucial to decouple it from the early bolting trait to fully harness its potential in lettuce breeding.

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Data availability

The RNA-seq data are available in the Gene Expression Omnibus (www.ncbi.nlm.nih.gov/geo/) under accession number GSE241604. All relevant data are included in the manuscript and the Supporting Information files.

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Acknowledgements

We appreciate Dr. Lyndel W. Meinhardt for critical review of the manuscript. This research used resources provided by the SCINet project of the USDA Agricultural Research Service, ARS project number 0500-00093-001-00-D. Mention of a trade name, proprietary product, or vendor does not constitute an endorsement, guarantee, or warranty by the USDA and does not imply its approval to the exclusion of other products or vendors that may be suitable.

Funding

This research was supported by grants from the USDA-AMS Specialty Crop Multistate Program (Award No. 16SCCMAR0001), the USDA-NIFA Agriculture and Food Research Initiative (Award No. 2016-68004-24931), and the USDA-NIFA Specialty Crop Research Initiative (Award No. 2015-51181-24283, 2017-51181-26830, and 2021-51181-35903).

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Contributions

B.M. and A.S. obtained funding for this investigation. S.P. and B.M. conceptualized the study and designed experiments. S.P conducted the experiments, analyzed the results with the help of B.M., and wrote the first draft of the manuscript. The results were validated by B.M, and A.S, both of whom also contributed to writing the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Sunchung Park.

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The authors have no relevant financial or non-financial interests to disclose.

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Communicated by Diane E. Mather.

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Park, S., Shi, A. & Mou, B. Low frequency of the wild-type freezing-tolerance LsCBF7 allele among lettuce population suggests a negative selection during domestication and breeding. Theor Appl Genet 137, 135 (2024). https://doi.org/10.1007/s00122-024-04643-8

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  • DOI: https://doi.org/10.1007/s00122-024-04643-8

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