Solanum pan-genetics reveals paralogues as contingencies in crop engineering

Matthias Benoit, Katharine M. Jenike, James W. Satterlee, Srividya Ramakrishnan, Iacopo Gentile, Anat Hendelman, Michael J. Passalacqua, Hamsini Suresh, Hagai Shohat, Gina M. Robitaille, Blaine Fitzgerald, Michael Alonge, Xingang Wang, Ryan Santos, Jia He, Shujun Ou, Hezi Golan, Yumi Green, Kerry Swartwood, Nicholas G. Karavolias, Gina P. Sierra, Andres Orejuela, Federico Roda, Sara Goodwin, W. Richard McCombie, Elizabeth B. Kizito, Edeline Gagnon, Sandra Knapp, Tiina E. Särkinen, Amy Frary, Jesse Gillis (), Joyce Eck (), Michael C. Schatz () and Zachary B. Lippman ()
Additional contact information
Matthias Benoit: Cold Spring Harbor Laboratory
Katharine M. Jenike: Johns Hopkins School of Medicine
James W. Satterlee: Cold Spring Harbor Laboratory
Srividya Ramakrishnan: Johns Hopkins University
Iacopo Gentile: Cold Spring Harbor Laboratory
Anat Hendelman: Cold Spring Harbor Laboratory
Michael J. Passalacqua: Cold Spring Harbor Laboratory
Hamsini Suresh: Cold Spring Harbor Laboratory
Hagai Shohat: Cold Spring Harbor Laboratory
Gina M. Robitaille: Cold Spring Harbor Laboratory
Blaine Fitzgerald: Cold Spring Harbor Laboratory
Michael Alonge: Johns Hopkins University
Xingang Wang: Cold Spring Harbor Laboratory
Ryan Santos: Cold Spring Harbor Laboratory
Jia He: Cold Spring Harbor Laboratory
Shujun Ou: Johns Hopkins University
Hezi Golan: SiteKicks.ai
Yumi Green: Boyce Thompson Institute
Kerry Swartwood: Boyce Thompson Institute
Nicholas G. Karavolias: Cold Spring Harbor Laboratory
Gina P. Sierra: Universidad Nacional de Colombia
Andres Orejuela: Universidad de Cartagena
Federico Roda: Universidad Nacional de Colombia
Sara Goodwin: Cold Spring Harbor Laboratory
W. Richard McCombie: Cold Spring Harbor Laboratory
Elizabeth B. Kizito: Uganda Christian University
Edeline Gagnon: University of Guelph
Sandra Knapp: Natural History Museum
Tiina E. Särkinen: Royal Botanic Garden Edinburgh
Amy Frary: Mount Holyoke College
Jesse Gillis: Cold Spring Harbor Laboratory
Joyce Eck: Boyce Thompson Institute
Michael C. Schatz: Johns Hopkins School of Medicine
Zachary B. Lippman: Cold Spring Harbor Laboratory

Nature, 2025, vol. 640, issue 8057, 135-145

Abstract: Abstract Pan-genomics and genome-editing technologies are revolutionizing breeding of global crops1,2. A transformative opportunity lies in exchanging genotype-to-phenotype knowledge between major crops (that is, those cultivated globally) and indigenous crops (that is, those locally cultivated within a circumscribed area)3–5 to enhance our food system. However, species-specific genetic variants and their interactions with desirable natural or engineered mutations pose barriers to achieving predictable phenotypic effects, even between related crops6,7. Here, by establishing a pan-genome of the crop-rich genus Solanum8 and integrating functional genomics and pan-genetics, we show that gene duplication and subsequent paralogue diversification are major obstacles to genotype-to-phenotype predictability. Despite broad conservation of gene macrosynteny among chromosome-scale references for 22 species, including 13 indigenous crops, thousands of gene duplications, particularly within key domestication gene families, exhibited dynamic trajectories in sequence, expression and function. By augmenting our pan-genome with African eggplant cultivars9 and applying quantitative genetics and genome editing, we dissected an intricate history of paralogue evolution affecting fruit size. The loss of a redundant paralogue of the classical fruit size regulator CLAVATA3 (CLV3)10,11 was compensated by a lineage-specific tandem duplication. Subsequent pseudogenization of the derived copy, followed by a large cultivar-specific deletion, created a single fused CLV3 allele that modulates fruit organ number alongside an enzymatic gene controlling the same trait. Our findings demonstrate that paralogue diversifications over short timescales are underexplored contingencies in trait evolvability. Exposing and navigating these contingencies is crucial for translating genotype-to-phenotype relationships across species.

Date: 2025
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DOI: 10.1038/s41586-025-08619-6

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