Modern tools for unveiling the genetic basis of prickliness in plants and their applications in plant breeding

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

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Modern tools for unveiling the genetic basis of prickliness in plants and their applications in plant breeding

Jaime Prohens

^{*

1},

James W. Satterlee

^{2, 3},

David Alonso

¹,

Pietro Gramazio

¹,

Katharine M. Jenike

^{4, 5},

Jia He

^{2, 3},

Andrea Arrones

¹,

Gloria Villanueva

¹,

Mariola Plazas

¹,

Srividya Ramakrishnan

^{4, 5},

Matthias Benoit

⁶,

Iacopo Gentile

⁷,

Anat Hendelman

^{2, 3},

Hagai Shohat

²,

Blaine Fitzgerald

^{2, 3},

Gina M. Robitaille

^{2, 3},

Yumi Green

⁸,

Kerry Swartwood

⁸,

Michael J. Passalacqua

⁷,

Edeline Gagnon

^{9, 10},

Rebecca Hilgenhof

¹⁰,

Trevis D. Huggins

¹¹,

Georgia C. Eizenga

¹¹,

Amit Gur

¹²,

Twan Rutten

¹³,

Nils Stein

^{13, 14},

Shengrui Yao

^{15, 16},

Adrien Poncet

¹⁷,

Clement Bellot

¹⁷,

Amy Frary

¹⁸,

Sandra Knapp

¹⁹,

Mohammed Bendahmane

¹⁷,

Tiina Särkinen

¹⁰,

Jesse Gillis

^{2, 20},

Joyce Van Eck

^{8, 21},

Michael C. Schatz

^{4, 5},

Yuval Eshed

²²,

Santiago Vilanova

¹,

Zachary B. Lippman

^{2, 3, 7}

¹ Instituto de Conservación y Mejora de la Agrodiversidad Valenciana, Universitat Politècnica de València, Valencia, Spain
² Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
³ Howard Hughes Medical Institute, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, USA
⁴ Department of Computer Science, Johns Hopkins University, Baltimore, MD, USA
⁵ Department of Genetic Medicine, Johns Hopkins University, Baltimore, MD, USA
⁶ French National Institute for Agriculture, Food, and Environment, 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, NY, USA
⁹ Department of Integrative Biology, University of Guelph, Guelph, ON, Canada
¹⁰ Royal Botanic Garden Edinburgh, Edinburgh, UK
¹¹ USDA-ARS, Dale Bumpers National Rice Research Center, Stuttgart, AR, USA
¹² Cucurbits Section, Department of Vegetable Sciences, Agricultural Research Organization, Newe Ya’ar Research Center, Ramat Yishay, Israel
¹³ Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany
¹⁴ Crop Plant Genetics, Martin Luther University of Halle- Wittenberg, Halle (Saale), Germany
¹⁵ Department of Plant and Environmental Sciences, New Mexico State University, Las Cruces, NM, USA
¹⁶ Sustainable Agriculture Sciences Center, New Mexico State University, Alcalde, NM, USA
¹⁷ Laboratoire Reproduction et Developpement des Plantes, INRAE, CNRS, Universite Lyon, Ecole Normale Superieure de Lyon, Lyon, France
¹⁸ Department of Biological Sciences, Mount Holyoke College, South Hadley, MA, USA
¹⁹ Natural History Museum, London, UK
²⁰ Physiology Department and Donnelly Centre for Cellular and Biomolecular Research, University of Toronto, Toronto, ON, Canada
²¹ Plant Breeding and Genetics Section, Cornell University, Ithaca, NY, USA
²² Department of Plant and Environmental Sciences, The Weizmann Institute of Science, Rehovot, Israel

Academic Editor: Dilantha Fernando

Published: 31 March 2025 by MDPI in Plants 2025: From Seeds to Food Security session Emerging Technologies in Plant Breeding

Abstract:

Prickles, sharp projections of plant epidermis, serve as a defense mechanism against herbivory but present significant challenges in agricultural contexts, complicating cultivation, harvesting, and postharvest processes. We used advanced tools to uncover the genetic basis of prickle formation and its convergent loss across highly divergent plant lineages. Using interspecific mapping populations of eggplant (Solanum melongena) with introgressions of prickly wild relatives, we fine-mapped the locus designated prickleless (pl) and identified a LONELY GUY (LOG) gene, which regulates cytokinin biosynthesis, as a critical factor in prickle development. High-quality genome assemblies and sequencing of diverse Solanum accessions revealed 16 independent LOG mutations associated with prickle loss in cultivated and wild species, highlighting recurrent co-option of LOG paralogs during evolution. Beyond Solanum, mutations in LOG genes were identified in distant prickly taxa, such as roses (Rosa sp.), jujube (Ziziphus jujuba), and the giant spider-flower (Tarenaya hassleriana). LOG family genes are also involved in the prickly barbs of the awns of rice (Oryza sativa) and barley (Hordeum vulgare), underscoring a conserved genetic mechanism underlying this trait. Genome editing with CRISPR-Cas9 was utilized to knock-out the LOG gene to eliminate prickles in the scarlet eggplant (S. aethiopicum), in the foraged Australian desert raisin (S. cleistogamum), and in the forest nightshade (S. prinophyllum) without pleiotropic effects, demonstrating the practical application of our findings in crop improvement. These insights pave the way for breeding prickleless varieties in economically significant plants, improving safety and efficiency in cultivation and harvesting, as well as for domesticating wild prickly foraged plants. Our work also deepens the understanding of the convergent evolution of plant innovations, such as the development of prickles.