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ARS Home » Southeast Area » Stuttgart, Arkansas » Dale Bumpers National Rice Research Center » Research » Publications at this Location » Publication #413008

Research Project: Broadening and Strengthening the Genetic Base of Rice for Adaptation to a Changing Climate, Crop Production Systems, and Markets

Location: Dale Bumpers National Rice Research Center

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

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

Submitted to: Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/6/2024
Publication Date: N/A
Citation: N/A

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.