Hybridization and Introgression Drive Genome Evolution of Dutch Elm Disease Pathogens

Overview

Journal Nat Ecol Evol

Publisher Springer Nature

Specialty Biology

Date 2020 Mar 4

PMID 32123324

Citations 26

Authors

Pauline Hessenauer

Anna Fijarczyk

Helene Martin

Julien Prunier

Guillaume Charron

Jerome Chapuis

Louis Bernier

Philippe Tanguay

Richard C Hamelin

Christian R Landry

Affiliations

Soon will be listed here.

Abstract

Hybridization and the resulting introgression can drive the success of invasive species via the rapid acquisition of adaptive traits. The Dutch elm disease pandemics in the past 100 years were caused by three fungal lineages with permeable reproductive barriers: Ophiostoma ulmi, Ophiostoma novo-ulmi subspecies novo-ulmi and Ophiostoma novo-ulmi subspecies americana. Using whole-genome sequences and growth phenotyping of a worldwide collection of isolates, we show that introgression has been the main driver of genomic diversity and that it impacted fitness-related traits. Introgressions contain genes involved in host-pathogen interactions and reproduction. Introgressed isolates have enhanced growth rate at high temperature and produce different necrosis sizes on an in vivo model for pathogenicity. In addition, lineages diverge in many pathogenicity-associated genes and exhibit differential mycelial growth in the presence of a proxy of a host defence compound, implying an important role of host trees in the molecular and functional differentiation of these pathogens.

Citing Articles

Phased T2T genome assemblies facilitate the mining of disease-resistance genes in .

Luo Y, Liu Z, Jin Z, Li P, Tan X, Cao S Hortic Res. 2025; 12(2):uhae306.

PMID: 39944989 PMC: 11817892. DOI: 10.1093/hr/uhae306.

Evaluating the Effects of Flavonoids on Insects: Implications for Managing Pests Without Harming Beneficials.

Riddick E Insects. 2025; 15(12.

PMID: 39769558 PMC: 11678172. DOI: 10.3390/insects15120956.

Hybrid adaptation is hampered by Haldane's sieve.

Bautista C, Gagnon-Arsenault I, Utrobina M, Fijarczyk A, Bendixsen D, Stelkens R Nat Commun. 2024; 15(1):10319.

PMID: 39609385 PMC: 11604976. DOI: 10.1038/s41467-024-54105-4.

Admixture in the fungal pathogen Blastomyces.

Jofre G, Dagilis A, Sepulveda V, Anspach T, Singh A, Chowdhary A Genetics. 2024; .

PMID: 39315610 PMC: 11631411. DOI: 10.1093/genetics/iyae155.

What are the 100 most cited fungal genera?.

Bhunjun C, Chen Y, Phukhamsakda C, Boekhout T, Groenewald J, McKenzie E Stud Mycol. 2024; 108:1-411.

PMID: 39100921 PMC: 11293126. DOI: 10.3114/sim.2024.108.01.

References

Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo Z, Pool J . Sequencing of 50 human exomes reveals adaptation to high altitude. Science. 2010; 329(5987):75-8. PMC: 3711608. DOI: 10.1126/science.1190371. View

Bennett P . Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol. 2008; 153 Suppl 1:S347-57. PMC: 2268074. DOI: 10.1038/sj.bjp.0707607. View

Stukenbrock E . The Role of Hybridization in the Evolution and Emergence of New Fungal Plant Pathogens. Phytopathology. 2016; 106(2):104-12. DOI: 10.1094/PHYTO-08-15-0184-RVW. View

Depotter J, Seidl M, Wood T, Thomma B . Interspecific hybridization impacts host range and pathogenicity of filamentous microbes. Curr Opin Microbiol. 2016; 32:7-13. DOI: 10.1016/j.mib.2016.04.005. View

Barton N . The role of hybridization in evolution. Mol Ecol. 2001; 10(3):551-68. DOI: 10.1046/j.1365-294x.2001.01216.x. View

Schardl C, Craven K . Interspecific hybridization in plant-associated fungi and oomycetes: a review. Mol Ecol. 2003; 12(11):2861-73. DOI: 10.1046/j.1365-294x.2003.01965.x. View

Olson A, Stenlid J . Pathogenic fungal species hybrids infecting plants. Microbes Infect. 2002; 4(13):1353-9. DOI: 10.1016/s1286-4579(02)00005-9. View

Fisher M, Henk D, Briggs C, Brownstein J, Madoff L, McCraw S . Emerging fungal threats to animal, plant and ecosystem health. Nature. 2012; 484(7393):186-94. PMC: 3821985. DOI: 10.1038/nature10947. View

Fisher M, Hawkins N, Sanglard D, Gurr S . Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science. 2018; 360(6390):739-742. DOI: 10.1126/science.aap7999. View

10.

Paoletti M, Buck K, Brasier C . Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi. Mol Ecol. 2005; 15(1):249-62. DOI: 10.1111/j.1365-294X.2005.02728.x. View

11.

Brasier C . The rise of the hybrid fungi. Nature. 2000; 405(6783):134-5. DOI: 10.1038/35012193. View

12.

Zhang D, Spiering M, Dawe A, Nuss D . Vegetative incompatibility loci with dedicated roles in allorecognition restrict mycovirus transmission in chestnut blight fungus. Genetics. 2014; 197(2):701-14. PMC: 4063925. DOI: 10.1534/genetics.114.164574. View

13.

Nigg M, Bernier L . From yeast to hypha: defining transcriptomic signatures of the morphological switch in the dimorphic fungal pathogen Ophiostoma novo-ulmi. BMC Genomics. 2016; 17(1):920. PMC: 5111228. DOI: 10.1186/s12864-016-3251-8. View

14.

Nigg M, Laroche J, Landry C, Bernier L . RNAseq Analysis Highlights Specific Transcriptome Signatures of Yeast and Mycelial Growth Phases in the Dutch Elm Disease Fungus Ophiostoma novo-ulmi. G3 (Bethesda). 2015; 5(11):2487-95. PMC: 4632067. DOI: 10.1534/g3.115.021022. View

15.

Eilertson K, Booth J, Bustamante C . SnIPRE: selection inference using a Poisson random effects model. PLoS Comput Biol. 2012; 8(12):e1002806. PMC: 3516574. DOI: 10.1371/journal.pcbi.1002806. View

16.

Gladieux P, Feurtey A, Hood M, Snirc A, Clavel J, Dutech C . The population biology of fungal invasions. Mol Ecol. 2014; 24(9):1969-86. DOI: 10.1111/mec.13028. View

17.

Menardo F, Praz C, Wyder S, Ben-David R, Bourras S, Matsumae H . Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nat Genet. 2016; 48(2):201-5. DOI: 10.1038/ng.3485. View

18.

Desprez-Loustau M, Robin C, Buee M, Courtecuisse R, Garbaye J, Suffert F . The fungal dimension of biological invasions. Trends Ecol Evol. 2007; 22(9):472-80. DOI: 10.1016/j.tree.2007.04.005. View

19.

Fijarczyk A, Dudek K, Niedzicka M, Babik W . Balancing selection and introgression of newt immune-response genes. Proc Biol Sci. 2018; 285(1884). PMC: 6111169. DOI: 10.1098/rspb.2018.0819. View

20.

Enard D, Petrov D . Evidence that RNA Viruses Drove Adaptive Introgression between Neanderthals and Modern Humans. Cell. 2018; 175(2):360-371.e13. PMC: 6176737. DOI: 10.1016/j.cell.2018.08.034. View