Century-old herbarium specimen provides insights into Pierce's disease of grapevines emergence in the Americas

Monica A Donegan; Alexandra K Kahn; Nathalie Becker; Andreina Castillo Siri; Paola E Campos; Karine Boyer; Alison Colwell; Martial Briand; Rodrigo P P Almeida; Adrien Rieux

doi:10.1016/j.cub.2024.11.029

Century-old herbarium specimen provides insights into Pierce's disease of grapevines emergence in the Americas

Curr Biol. 2024 Dec 4:S0960-9822(24)01570-7. doi: 10.1016/j.cub.2024.11.029. Online ahead of print.

Authors

Affiliations

¹ Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA 94720, USA.
² Institut de Systématique, Évolution, Biodiversité (ISyEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP 50, 75005 Paris, France.
³ Institut de Systématique, Évolution, Biodiversité (ISyEB), Muséum national d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, CP 50, 75005 Paris, France; CIRAD, UMR PVBMT, La Réunion, 97410 Saint-Pierre, La Réunion, France.
⁴ CIRAD, UMR PVBMT, La Réunion, 97410 Saint-Pierre, La Réunion, France.
⁵ Department of Plant Sciences, University of California, Davis, Davis, CA 95818, USA.
⁶ University of Angers, Institut Agro, INRAE, IRHS, SFR QUASAV, Angers, France.
⁷ Department of Environmental Science, Policy, and Management, University of California, Berkeley, Berkeley, CA 94720, USA. Electronic address: rodrigoalmeida@berkeley.edu.
⁸ CIRAD, UMR PVBMT, La Réunion, 97410 Saint-Pierre, La Réunion, France. Electronic address: adrien.rieux@cirad.fr.

PMID: 39689706
DOI: 10.1016/j.cub.2024.11.029

Abstract

Fossils and other preserved specimens are integral for informing timing and evolutionary history in every biological system. By isolating a plant pathogen genome from herbarium-preserved diseased grapevine material from 1906 (Herb_1906), we were able to answer questions about an enigmatic system. The emergence of Pierce's disease (PD) of grapevine has shaped viticultural production in North America; yet, there are uncertainties about the geographic origin of the pathogen (Xylella fastidiosa subsp. fastidiosa, Xff) and the timing and route of its introduction. We produced a high-quality, de novo genome assembly of this historical plant pathogen and confirmed degradation patterns unique to ancient DNA. Due to the inclusion of the Herb_1906 sample, we were able to generate a significant temporal signal in the genomic data. This allowed us to build a time-calibrated phylogeny, where we estimate the introduction of Xff into the US between 1734 and 1741 CE, an earlier time frame than previously inferred. In a large collection of >300 Xff genomes, the Herb_1906 sample was genetically most similar to a small population from Northern California but not basal to the entire Xff California clade. Based on phylogenetic placement and a phylogeographic reconstruction, our data support a single introduction of Xff into the Southeastern US from Central America, with multiple subsequent introductions into California.

Keywords: Pierce’s disease; Xylella fastidiosa; ancient DNA; emerging disease; grapevine; herbarium; outbreak; plant pathogen.