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

Author:

Satterlee James W.12ORCID,Alonso David3ORCID,Gramazio Pietro3ORCID,Jenike Katharine M.45ORCID,He Jia12ORCID,Arrones Andrea3ORCID,Villanueva Gloria3ORCID,Plazas Mariola3ORCID,Ramakrishnan Srividya45,Benoit Matthias6ORCID,Gentile Iacopo7,Hendelman Anat12ORCID,Shohat Hagai1ORCID,Fitzgerald Blaine12ORCID,Robitaille Gina M.12ORCID,Green Yumi8,Swartwood Kerry8ORCID,Passalacqua Michael J.7ORCID,Gagnon Edeline910ORCID,Hilgenhof Rebecca10ORCID,Huggins Trevis D.11ORCID,Eizenga Georgia C.11ORCID,Gur Amit12ORCID,Rutten Twan13ORCID,Stein Nils1314ORCID,Yao Shengrui1516,Poncet Adrien17,Bellot Clement17ORCID,Frary Amy18ORCID,Knapp Sandra19ORCID,Bendahmane Mohammed17ORCID,Särkinen Tiina10ORCID,Gillis Jesse120ORCID,Van Eck Joyce821ORCID,Schatz Michael C.45ORCID,Eshed Yuval22ORCID,Prohens Jaime3ORCID,Vilanova Santiago3ORCID,Lippman Zachary B.127ORCID

Affiliation:

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. Instituto de Conservación y Mejora de la Agrodiversidad Valenciana, 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. 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.

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.

Publisher

American Association for the Advancement of Science (AAAS)

Cited by 1 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. Convergent evolution of prickles across crops;Nature Reviews Genetics;2024-08-22

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