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

TitleDuplication of a domestication locus neutralized a cryptic variant that caused a breeding barrier in tomato.
Publication TypeJournal Article
Year of Publication2019
AuthorsSoyk, S, Lemmon, ZH, Sedlazeck, FJ, Jiménez-Gómez, JM, Alonge, M, Hutton, SF, Van Eck, J, Schatz, MC, Lippman, ZB
JournalNat Plants
Volume5
Issue5
Pagination471-479
Date Published2019 May
ISSN2055-0278
KeywordsCRISPR-Associated Protein 9, CRISPR-Cas Systems, Domestication, Epistasis, Genetic, Flowers, Gene Duplication, Gene Editing, Genetic Variation, Plant Breeding, Plants, Genetically Modified, Quantitative Trait Loci, Reproduction, Solanum lycopersicum
Abstract

Genome editing technologies are being widely adopted in plant breeding. 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 mutations. 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 gene. 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.

DOI10.1038/s41477-019-0422-z
Alternate JournalNat Plants
PubMed ID31061537

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