Solanum pan-genetics reveals paralogues as contingencies in crop engineering

Pan-genomics and genome-editing technologies are revolutionizing breeding of global crops<sup>1,2</sup>. 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)<sup>3-5</sup> 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 crops<sup>6,7</sup>. Here, by establishing a pan-genome of the crop-rich genus Solanum<sup>8</sup> 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 cultivars<sup>9</sup> 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)<sup>10,11</sup> 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.

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Journal
Nature
Published
2025-03-05
DOI
https://doi.org/10.1038/s41586-025-08619-6
Citations
38
Primary Topic
Plant tissue culture and regeneration
Type
article
Field-Weighted Citation Impact
30.63
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article

Solanum pan-genetics reveals paralogues as contingencies in crop engineering

Anat Hendelman, Zachary B. Lippman, Jesse A Gillis, Andrés Orejuela et al.
38 citations
Nature
Plant tissue culture and regeneration
30.63
article

Solanum pan-genetics reveals paralogues as contingencies in crop engineering

Anat Hendelman, Zachary B. Lippman, Jesse A Gillis, Andrés Orejuela, Hamsini Suresh, Nicholas G. Karavolias, Edeline Gagnon, Sandra Knapp, James Satterlee, Matthias Benoit, Michael C. Schatz, Michael J. Passalacqua, Hagai Shohat, Federico Roda, Katharine M. Jenike, Kerry Swartwood, W. Richard McCombie, Gina M. Robitaille, Iacopo Gentile, Sara Goodwin, Michael Alonge, Tiina Särkinen, Shujun Ou, Joyce Van Eck, B. P. Fitzgerald, Yumi Green, Xingang Wang, Srividya Ramakrishnan, Jia He, Amy Frary, Elizabeth Balyejusa Kizito, Hezi Golan, Ryan Santos, Gina P. Sierra
article en
38 citations

Abstract

Pan-genomics and genome-editing technologies are revolutionizing breeding of global crops<sup>1,2</sup>. 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)<sup>3-5</sup> 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 crops<sup>6,7</sup>. Here, by establishing a pan-genome of the crop-rich genus Solanum<sup>8</sup> 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 cultivars<sup>9</sup> 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)<sup>10,11</sup> 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.

NatureVol. 640(8057)
Centre National de la Recherche Scientifique (FR), Natural History Museum (GB), Howard Hughes Medical Institute (US), Johns Hopkins University (US), Mount Holyoke College (US), University of Cartagena (CO), Royal Botanic Garden Edinburgh (GB), Université Fédérale de Toulouse Midi-Pyrénées (FR), University of Toronto (CA), Cornell University (US), Cold Spring Harbor Laboratory (US), Johns Hopkins Medicine (US), Universidad Nacional de Colombia (CO), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Occupational Cancer Research Centre (CA), Verve Therapeutics (United States) (US), APT Therapeutics (United States) (US), The Ohio State University (US), Technical University of Munich (DE), University of Guelph (CA), Ithaca College (US), Uganda Christian University (UG)
Zero hunger
Openalex Percentile: Top 0%
Plant tissue culture and regeneration
30.63
DOIOpen Access PDFOpenAlex
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