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

Authors: SATTERLEE, JAMES - Cold Spring Harbor Laboratory; ALONSO, DAVID - Polytechnical University Of Valencia; GRAMAZIO, PIETO - Polytechnical University Of Valencia; JENIKE, KATHARINE - Johns Hopkins University; HE, JIA - Cold Spring Harbor Laboratory; ARRONES, ANDREA - Polytechnic University Of Valencia (UPV); VILLANUEVA, GLORIA - Polytechnic University Of Valencia (UPV); PLAZAS, MARIOLA - Polytechnic University Of Valencia (UPV); RAMAKRISHNAN, SRIVIDYA - Johns Hopkins University; BENOIT, MATTHIAS - French National Institute For Agricultural Research; GENTILE, IACOPO - Cold Spring Harbor Laboratory; HENDELMAN, ANAT - Cold Spring Harbor Laboratory; SHOHAT, HAGAI - Cold Spring Harbor Laboratory; FITZGERALD, BLAINE - Cold Spring Harbor Laboratory; ROBITAILLE, GINA - Cold Spring Harbor Laboratory; GREEN, YUMI - Boyce Thompson Institute; SWARTWOOD, KERRY - Boyce Thompson Institute; PASSALACQUA, MICHAEL - Cold Spring Harbor Laboratory; GAGNON, EDELINE - University Of Guelph; HILGENHOF, REBECCA - Royal Botanic Gardens, Kew; Huggins, Trevis; Eizenga, Georgia; GUR, AMIT - Newe Ya'Ar Research Center; RUTTEN, RUTTEN - Leibniz Institute Of Plant Genetics And Crop Plant Research; STEIN, NILS - Leibniz Institute Of Plant Genetics And Crop Plant Research; YAO, SHENGRUI - Leibniz Institute Of Plant Genetics And Crop Plant Research; BELLOT, CLEMENT - Ecole Normale Superieure (ENS) De Lyon; BENDAHMANE, MOHAMED - Ecole Normale Superieure (ENS) De Lyon; FRAR, AMY - Mount Holyoke College; KNAPP, SANDRA - Natural History Museum - London; SARKINEN, TIINA - Royal Botanical Gardens; GILLS, JESSE - Cold Spring Harbor Laboratory; VAN ECK, JOYCE - Boyce Thompson Institute; SCHATZ, MICHAEL - Johns Hopkins University; ESHED, YUVAL - Weizmann Institite Of Science; PROHENS, JAIME - Polytechnic University Of Valencia (UPV); VILANOVA, SANTIAGO - Polytechnic University Of Valencia (UPV); LIPPMAN, ZACHARY - Cold Spring Harbor Laboratory; PONCET, ADRIEN - Ecole Normale Superieure (ENS) De Lyon

Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2024
Publication Date: 8/2/2024
Citation: Satterlee, J.W., Alonso, D.D., Gramazio, P.P., Jenike, K.K., He, J.J., Arrones, A.A., Villanueva, G.G., Plazas, M.M., Ramakrishnan, S.S., Benoit, M.B., Gentile, I.I., Hendelman, A.A., Shohat, H.H., Fitzgerald, B.B., Robitaille, G.G., Green, Y.Y., Swartwood, K.K., Passalacqua, M.M., Gagnon, E.E., Hilgenhof, R.R., Huggins, T.D., Eizenga, G.C., Gur, A., Rutten, R., Stein, N., Yao, S.S., Bellot, C.C., Bendahmane, M.M., Frar, A., Knapp, S.S., Sarkinen, T.T., Gills, J., Van Eck, J.J., Schatz, M.M., Eshed, Y., Prohens, J.Y., Vilanova, S.S., Lippman, Z.Z., Poncet, A. 2024. Convergent evolution of plant prickles is driven by repeated gene co-option over deep time. Science. https://doi.org/10.1101/2024.02.21.581474.
DOI: https://doi.org/10.1101/2024.02.21.581474

Interpretive Summary: In the agriculturally important genus Solanum crops like eggplants and the desert raisin (forage) have prickles which are the short, slender, sharp-pointed epidermal outgrowths and confer critical fitness advantages like defense against herbivores, improving plant competition, permitting a climbing growth habit and improving water retention. In other crops like rice and barley, prickles are the referred to as “barbs” on the awns, “thorns” on roses and citrus trees, or the “stipular spines” on Chinese date and sour jujube. In rice and barley, these barbs (prickles) are undesirable because they damage harvesting equipment, causing it to wear-out faster and in the case of hand-harvesting, injure the person harvesting. Similar problems are noted in other crops, thus understanding genetic control of prickle development will aid in designing genetic studies to develop prickleless crops or crops with prickles, if so desired. There are approximately 1,500 Solanum species worldwide and approximately 450 species cluster into subgroups which have prickles. A survey of these three subgroups identified 30 species which did not have prickles. The DNA sequence of nine species with prickles and five prickleless species was examined and it was determined that various mutations in the LONELY GUY (LOG) gene which activates plant cell division by promoting cytokinin biosynthesis caused decreased cytokinin production and lack of prickles which was validated in studies with transgenic plants. Across crop plants, mutations in the same LOG gene were associated with loss of barbs on awns in rice and barley, thornless roses, loss of stipular spines on Chinese date trees and fruit, and a prickleless desert raisin. This study demonstrates how genetic knowledge can be widely used to easily eliminate prickles across a broad range of row crops like rice and barley, horticultural crops like eggplant and Chinese, date and ornamental crops like roses and giant spider flowers. In the case of crop plants prickleless varieties would reduce injury when hand harvesting and decrease “wear-and-tear” on equipment when mechanically harvesting. This serves as a model for designing studies to eliminate other undesirable traits (or incorporate desirable traits) using the extensive DNA sequence data currently available.

Technical 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. Here 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. Strikingly, homologs promote prickle development across angiosperms that collectively diverged over 150 million years ago. By developing new Solanum genetic systems, we leveraged this discovery to eliminate prickles in a weed species and an indigenous foraged berry. Our findings implicate a shared cytokinin-based genetic program underlying evolutionarily widespread and recurrent instances of plant morphological innovation.