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This study was supported by a National Science Foundation Postdoctoral Fellowship in Biology (IOS-2305651) (J.W.S.); a postdoctoral fellowship (RYC2021-031999-I) funded by MCIN/AEI /10.13039/501100011033 and by "European Union NextGenerationEU/PRTR"(P.G.); a predoctoral fellowship (FPU18/01742) from Spanish Ministerio de Ciencia, Innovacion y Universidades (A.A.); apredoctoral fellowship (PRE2019-089256) funded by MCIN/AEI/10.13039/501100011033 and by "ESF investing in your future"(G.V.); Plant Health and Environment Department of the French National Institute for Agriculture, Food, and Environment (INRAE) (M.Beno.); Biologie et amelioration des Plantes departments of INRAE (M.Bend.); the William Randolph Hearst Scholarship from the Cold Spring Harbor School of Biological Sciences (M.J.P.); Fonds de recherche du Quebec en Nature et Technologies Postdoctoral Fellowship (E.G.); the Sibbald Trust Research Fellowship (R.H.); a grant of the German Research Association DFG (STE 1120/17-1) (N.S.); NSF Planetary Biodiversity Initiative grant "PBI Solanum: a worldwide initiative"(DEB-0316614)(S.K.); National Geographic Society Northern Europe Award GEFNE49-12 (T.S.); National Institutes of Health grant R01MH113005 (J.G.); grant CIPROM/2021/020 funded by Conselleria d'Innovacio, Universitats, Ciencia i Societat Digital of the Generalitat Valenciana (J.P.); grant PID2021-128148OB-I00 funded by MCIN/AEI/10.13039/501100011033/ and "ERDF A way of making Europe"(J.P.); grant PDC2022-133513-I00 funded by MCIN/AEI/10.13039/501100011033/ and by "European Union NextGenerationEU/PRTR"(J.P.); National Science Foundation Plant Genome Research Program grant IOS-2216612 (A.F., J.G.,J.V.E., M.C.S., and Z.B.L.); and the Howard Hughes Medical Institute (Z.B.L.).

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Convergent evolution of plant prickles by repeated gene co-option over deep time

Publicated to:Science. 385 (6708): eado1663- - 2024-08-02 385(6708), DOI: 10.1126/science.ado1663

Authors: Satterlee, James W; Alonso, David; Gramazio, Pietro; Jenike, Katharine M; He, Jia; Arrones, Andrea; Villanueva, Gloria; Plazas, Mariola; Ramakrishnan, Srividya; Benoit, Matthias; Gentile, Iacopo; Hendelman, Anat; Shohat, Hagai; Fitzgerald, Blaine; Robitaille, Gina M; Green, Yumi; Swartwood, Kerry; Passalacqua, Michael J; Gagnon, Edeline; Hilgenhof, Rebecca; Huggins, Trevis D; Eizenga, Georgia C; Gur, Amit; Rutten, Twan; Stein, Nils; Yao, Shengrui; Poncet, Adrien; Bellot, Clement; Frary, Amy; Knapp, Sandra; Bendahmane, Mohammed; Saerkinen, Tiina; Gillis, Jesse; Van Eck, Joyce; Schatz, Michael C; Eshed, Yuval; Prohens, Jaime; Vilanova, Santiago; Lippman, Zachary B

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Abstract

An enduring question in evolutionary biology concerns the degree to which episodes of convergent trait evolution depend on the same genetic programs, particularly over long timescales. In this work, we genetically dissected repeated origins and losses of prickles-sharp epidermal projections-that convergently evolved in numerous plant lineages. Mutations in a cytokinin hormone biosynthetic gene caused at least 16 independent losses of prickles in eggplants and wild relatives in the genus Solanum. Homologs underlie prickle formation across angiosperms that collectively diverged more than 150 million years ago, including rice and roses. By developing new Solanum genetic systems, we leveraged this discovery to eliminate prickles in a wild species and an indigenously foraged berry. Our findings implicate a shared hormone activation genetic program underlying evolutionarily widespread and recurrent instances of plant morphological innovation.

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