Format: ORAL

James W. Satterlee1,2, David Alonso3, Pietro Gramazio3, Jia He1,2, Andrea Arrones3, Gloria Villanueva3, Mariola Plazas3, Katharine Jenike4,5, Srividya Ramakrishnan4,5, Matthias Benoit6, Iacopo Gentile1,7, Anat Hendelman1,2, Hagai Shohat1, Blaine Fitzgerald1,2, Gina M. Robitaille1,2, Yumi Green8, Kerry Swartwood8, Edeline Gagnon9, Rebecca Hilgenhof9, Trevis D. Huggins10, Georgia C. Eizenga10, Nils Stein11,12, Shengrui Yao13,14, Clement Bellot15, Mohammed Bendahmane15, Sandra Knapp16, Tiina Srkinen9, Joyce Van Eck8,17, Michael Schatz4,5, Yuval Eshed18, Jaime Prohens3, Santiago Vilanova3, Zachary B. Lippman1,2,7

1 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA 2 Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA 3 Universitat Politècnica de València, Valencia, Spain 4 Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA 5 Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA 6 INRAE, CNRS, Laboratory of Plant-Microbe Interactions, Toulouse, France 7 School of Biological Sciences, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA 8 Boyce Thompson Institute, Ithaca, New York, USA 9 Royal Botanic Garden Edinburgh, Edinburgh, UK 10 USDA-ARS, Dale Bumpers National Rice Research Center, Stuttgart, AR, USA 11 Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany 12 Department of Crop Sciences, Center for Integrated Breeding Research, Georg-August-University, Göttingen, Germany 13 Department of Plant and Environmental Sciences, New Mexico State University, Las Cruces, NM, USA 14 Sustainable Agriculture Science Center, New Mexico State University, Alcalde, NM, USA 15 Laboratoire Reproduction et Developpement des Plantes, INRAE, CNRS, Université de Lyon, Ecole Normale Superieure de Lyon, Lyon, France 16 Natural History Museum, London, UK 17 Plant Breeding and Genetics Section, Cornell University, Ithaca, NY, USA 18 Department of Plant and Environmental Sciences, The Weizmann Institute of Science, Rehovot, Israel

Solanum is one of the largest genera in the plant kingdom with approximately 1,250 species. The largest monophyletic group within Solanum is the Leptostemonum Clade, with more than 500 species. A distinctive characteristic of this clade is the presence of epidermal prickles on vegetative organs; these are a synapomorphy of the Clade and represent a single origin evolutionary innovation in the genus. Prickles have been lost independently in several taxa. In cultivated species, breeders favored selection of prickleless (pl) materials during crop domestication. Interspecific mapping populations between pl eggplant (Solanum melongena) and wild prickled species revealed that the pl phenotype is recessive and consistent with one Mendelian locus. Advanced backcrosses of prickle-bearing wild species into the S. melongena background pointed to a region at the end of chromosome 6 containing the causal genetic locus. Fine mapping of the region narrowed the causal interval to a 600 kb genomic region containing 13 annotated genes that included a LONELY-GUY (LOG) cytokinin biosynthesis gene harboring a splice-site mutation. Other prickleless cultivated eggplants were found to have either splice-site mutations (S. macrocarpon) or a deletion (S. aethiopicum) in this gene, identifying it as PL. Sequencing of PL in prickleless species from the Leptostemonum clade revealed 15 independent mutations (i.e. frameshift, splice-site, TE insertion, and deletion alleles). The key role of PL in the development of prickles was further confirmed by CRISPR-Cas9 gene editing of PL in the prickly Australian wild species S. cleistogamum and S. prinophyllum, which recapitulated the phenotype. Our results indicate that PL may have had a major role in the evolution of an adaptive morphological novelty in the Leptostemonum Clade, as well as serving as a key genetic target during multiple instances of crop domestication.