Duplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato

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Název: Duplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato
Autoři: José M. Jiménez-Gómez, Sebastian Soyk, Zachary B. Lippman, Michael C. Schatz, Zachary H. Lemmon, Fritz J. Sedlazeck, Samuel F. Hutton, Joyce Van Eck, Michael Alonge
Přispěvatelé: Jimenez-Gomez, Jose, Cold Spring Harbor Laboratory (CSHL), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, Baylor College of Medecine, University of Florida Gainesville (UF), Boyce Thompson Institute Ithaca, Cornell University New York, Johns Hopkins University (JHU), Department of Surgery Johns Hopkins Medicine, The Johns Hopkins Hospital, European Molecular Biology Organization (EMBO) ALTF 1589-2014, National Science Foundation Postdoctoral Research Fellowship in Biology Grant IOS-1523423, National Institute of Health Research Project with Complex Structure Cooperative Agreement 3UM1HG008898-01S2, US-Israel Binational Science Foundation IS-4818-15, US-Israel Binational Science Foundation, Agriculture and Food Research Initiative competitive grant of the USDA National Institute of Food and Agriculture 2016-67013-24452, ational Science Foundation (NSF) NSF - Office of the Director (OD) IOS-1732253, ANR-17-CE20-0024,tomaTE,Contribution des éléments transposables (ET) à la domestication et à l'amélioration de la tomate(2017)
Zdroj: Nature Plants. 5:471-479
Informace o vydavateli: Springer Science and Business Media LLC, 2019.
Rok vydání: 2019
Témata: MESH: Gene Editing, 0301 basic medicine, MESH: CRISPR-Cas Systems, MESH: Domestication, [SDV]Life Sciences [q-bio], Quantitative Trait Loci, MESH: Plants, MESH: Epistasis, Genetically Modified, Flowers, MESH: CRISPR-Associated Protein 9, MESH: Reproduction, Domestication, 03 medical and health sciences, Genetic, Solanum lycopersicum, MESH: Lycopersicon esculentum, CRISPR-Associated Protein 9, Gene Duplication, MESH: Genetic Variation, Gene Editing, 2. Zero hunger, 0303 health sciences, Reproduction, MESH: Gene Duplication, Genetic Variation, Epistasis, Genetic, MESH: Flowers, Plants, Genetically Modified, MESH: Quantitative Trait Loci, [SDV] Life Sciences [q-bio], Plant Breeding, MESH: Plant Breeding, CRISPR-Cas Systems
Popis: Genome editing technologies are being widely adopted in plant breeding1. However, a looming challenge of engineering desirable genetic variation in diverse genotypes is poor predictability of phenotypic outcomes due to unforeseen interactions with pre-existing cryptic mutations2-4. In tomato, breeding with a classical MADS-box gene mutation that improves harvesting by eliminating fruit stem abscission frequently results in excessive inflorescence branching, flowering and reduced fertility due to interaction with a cryptic variant that causes partial mis-splicing in a homologous gene5-8. Here, we show that a recently evolved tandem duplication carrying the second-site variant achieves a threshold of functional transcripts to suppress branching, enabling breeders to neutralize negative epistasis on yield. By dissecting the dosage mechanisms by which this structural variant restored normal flowering and fertility, we devised strategies that use CRISPR-Cas9 genome editing to predictably improve harvesting. Our findings highlight the under-appreciated impact of epistasis in targeted trait breeding and underscore the need for a deeper characterization of cryptic variation to enable the full potential of genome editing in agriculture.
Druh dokumentu: Article
Jazyk: English
ISSN: 2055-0278
DOI: 10.1038/s41477-019-0422-z
Přístupová URL adresa: https://pubmed.ncbi.nlm.nih.gov/31061537
https://pubmed.ncbi.nlm.nih.gov/31061537/
https://www.nature.com/articles/s41477-019-0422-z.pdf
https://www.ncbi.nlm.nih.gov/pubmed/31061537
https://repository.cshl.edu/id/eprint/37823/
https://europepmc.org/abstract/MED/31061537
https://www.nature.com/articles/s41477-019-0422-z
Rights: Springer Nature TDM
Přístupové číslo: edsair.doi.dedup.....50a28bf141aeddaa7641852b0c998901
Databáze: OpenAIRE
Popis
Abstrakt:Genome editing technologies are being widely adopted in plant breeding1. However, a looming challenge of engineering desirable genetic variation in diverse genotypes is poor predictability of phenotypic outcomes due to unforeseen interactions with pre-existing cryptic mutations2-4. In tomato, breeding with a classical MADS-box gene mutation that improves harvesting by eliminating fruit stem abscission frequently results in excessive inflorescence branching, flowering and reduced fertility due to interaction with a cryptic variant that causes partial mis-splicing in a homologous gene5-8. Here, we show that a recently evolved tandem duplication carrying the second-site variant achieves a threshold of functional transcripts to suppress branching, enabling breeders to neutralize negative epistasis on yield. By dissecting the dosage mechanisms by which this structural variant restored normal flowering and fertility, we devised strategies that use CRISPR-Cas9 genome editing to predictably improve harvesting. Our findings highlight the under-appreciated impact of epistasis in targeted trait breeding and underscore the need for a deeper characterization of cryptic variation to enable the full potential of genome editing in agriculture.
ISSN:20550278
DOI:10.1038/s41477-019-0422-z