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Nat Plants. 2019 May;5(5):471-479. doi: 10.1038/s41477-019-0422-z. Epub 2019 May 6.

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

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Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, USA.
Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, France.
Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA.
Horticultural Sciences Department, University of Florida, Wimauma, FL, USA.
The Boyce Thompson Institute, Ithaca, NY, USA.
Plant Breeding and Genetics Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, USA.
Department of Oncologye, Johns Hopkins Medicine, Baltimore, MD, USA.
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.
Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA.


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.

[Indexed for MEDLINE]

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