Genomics of the expanding pine pathogen Lecanosticta acicola reveals patterns of ongoing genetic admixture

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• dc.contributor.author Marcet Houben, Marina
• dc.contributor.author Cruz, Fernando
• dc.contributor.author Gómez Garrido, Jèssica
• dc.contributor.author Alioto, Tyler
• dc.contributor.author Núñez Rodríguez, Juan Carlos
• dc.contributor.author Mesanza, Nebai
• dc.contributor.author Gut, Marta
• dc.contributor.author Iturritxa, Eugenia
• dc.contributor.author Gabaldón Estevan, Juan Antonio, 1973-
• dc.date.accessioned 2024-07-31T12:04:01Z
• dc.date.available 2024-07-31T12:04:01Z
• dc.date.issued 2024
• dc.description.abstract Lecanosticta acicola is the causal agent for brown spot needle blight that affects pine trees across the northern hemisphere. Based on marker genes and microsatellite data, two distinct lineages have been identified that were introduced into Europe on two separate occasions. Despite their overall distinct geographic distribution, they have been found to coexist in regions of northern Spain and France. Here, we present the first genome-wide study of Lecanosticta acicola, including assembly of the reference genome and a population genomics analysis of 70 natural isolates from northern Spain. We show that most of the isolates belong to the southern lineage but show signs of introgression with northern lineage isolates, indicating mating between the two lineages. We also identify phenotypic differences between the two lineages based on the activity profiles of 20 enzymes, with introgressed strains being more phenotypically similar to members of the southern lineage. In conclusion, we show undergoing genetic admixture between the two main lineages of L. acicola in a region of recent expansion. Importance: Lecanosticta acicola is a fungal pathogen causing severe defoliation, growth reduction, and even death in more than 70 conifer species. Despite the increasing incidence of this species, little is known about its population dynamics. Two divergent lineages have been described that have now been found together in regions of France and Spain, but it is unknown how these mixed populations evolve. Here we present the first reference genome for this important plant pathogenic fungi and use it to study the population genomics of 70 isolates from an affected forest in the north of Spain. We find signs of introgression between the two main lineages, indicating that active mating is occurring in this region which could propitiate the appearance of novel traits in this species. We also study the phenotypic differences across this population based on enzymatic activities on 20 compounds.
• dc.description.sponsorship TG group acknowledges support from the Spanish Ministry of Science and Innovation for grants PID2021-126067NB-I00, CPP2021-008552, PCI2022-135066-2, and PDC2022-133266-I00, cofounded by ERDF “A way of making Europe”; from the Catalan Research Agency (AGAUR) SGR01551; from the European Union’s Horizon 2020 research and innovation program (ERC-2016–724173); from the Gordon and Betty Moore Foundation (Grant GBMF9742); from the “La Caixa” foundation (Grant LCF/PR/HR21/00737), and the Instituto de Salud Carlos III (IMPACT Grant IMP/00019 and CIBERINFEC CB21/13/00061- ISCIII-SGEFI/ERDF).
• dc.format.mimetype application/pdf
• dc.identifier.citation Marcet-Houben M, Cruz F, Gómez-Garrido J, Alioto TS, Nunez-Rodriguez JC, Mesanza N, et al. Genomics of the expanding pine pathogen Lecanosticta acicola reveals patterns of ongoing genetic admixture. mSystems. 2024 Mar 19;9(3):e0092823. DOI: 10.1128/msystems.00928-23
• dc.identifier.doi http://dx.doi.org/10.1128/msystems.00928-23
• dc.identifier.issn 2379-5077
• dc.identifier.uri http://hdl.handle.net/10230/60868
• dc.language.iso eng
• dc.publisher American Society for Microbiology
• dc.relation.ispartof mSystems. 2024 Mar 19;9(3):e0092823
• dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/724173
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PID2021-126067NB-I00
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/CPP2021-008552
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PCI2022-135066-2
• dc.relation.projectID info:eu-repo/grantAgreement/ES/3PE/PDC2022-133266-I00
• dc.rights © 2024 Marcet-Houben et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/).
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0/
• dc.subject.keyword Lecanosticta acicola
• dc.subject.keyword Admixture
• dc.subject.keyword Comparative genomics
• dc.subject.keyword Needle blight
• dc.subject.keyword Plant pathogen
• dc.subject.keyword Population genomics
• dc.title Genomics of the expanding pine pathogen Lecanosticta acicola reveals patterns of ongoing genetic admixture
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion