Genomic Signatures of a Major Adaptive Event in the Pathogenic Fungus Melampsora larici-populina
Abstract
The recent availability of genome-wide sequencing techniques has allowed systematic screening for molecular signatures of adaptation, including in nonmodel organisms. Host–pathogen interactions constitute good models due to the strong selective pressures that they entail. We focused on an adaptive event which affected the poplar rust fungus Melampsora larici-populina when it overcame a resistance gene borne by its host, cultivated poplar. Based on 76 virulent and avirulent isolates framing narrowly the estimated date of the adaptive event, we examined the molecular signatures of selection. Using an array of genome scan methods based on different features of nucleotide diversity, we detected a single locus exhibiting a consistent pattern suggestive of a selective sweep in virulent individuals (excess of differentiation between virulent and avirulent samples, linkage disequilibrium, genotype–phenotype statistical association, and long-range haplotypes). Our study pinpoints a single gene and further a single amino acid replacement which may have allowed the adaptive event. Although our samples are nearly contemporary to the selective sweep, it does not seem to have affected genome diversity further than the immediate vicinity of the causal locus, which can be explained by a soft selective sweep (where selection acts on standing variation) and by the impact of recombination inmore »
- Authors:
-
[4];
[6]
- National Research Institute for Agriculture, Food and the Environment, Paris (France); Universite de Lorraine, Nancy (France)
- National Research Institute for Agriculture, Food and the Environment, Paris (France); Universite de Lorraine, Nancy (France); National Institute for Ocean Science, Nantes (France)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- National Research Institute for Agriculture, Food and the Environment, Orleans (France); Montpellier University (France)
- National Research Institute for Agriculture, Food and the Environment, Paris (France); Universite de Lorraine, Nancy (France); Montpellier University (France)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); French National Research Agency; Region Lorraine and INRAE
- OSTI Identifier:
- 1892180
- Grant/Contract Number:
- AC02-05CH11231; ANR-12-ADAP-0009; ANR-18-CE32-0001; ANR-11-LABX-0002-01
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Genome Biology and Evolution
- Additional Journal Information:
- Journal Volume: 14; Journal Issue: 1; Journal ID: ISSN 1759-6653
- Publisher:
- Society for Molecular Biology and Evolution
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Population genomics; plant-pathogen interactions; coevolution; genome-wide association studies; genome scan
Citation Formats
Persoons, Antoine, Maupetit, Agathe, Louet, Clémentine, Andrieux, Axelle, Lipzen, Anna, Barry, Kerrie W., Na, Hyunsoo, Adam, Catherine, Grigoriev, Igor V., Segura, Vincent, Duplessis, Sébastien, Frey, Pascal, Halkett, Fabien, and De Mita, Stéphane. Genomic Signatures of a Major Adaptive Event in the Pathogenic Fungus Melampsora larici-populina. United States: N. p., 2021.
Web. doi:10.1093/gbe/evab279.
Persoons, Antoine, Maupetit, Agathe, Louet, Clémentine, Andrieux, Axelle, Lipzen, Anna, Barry, Kerrie W., Na, Hyunsoo, Adam, Catherine, Grigoriev, Igor V., Segura, Vincent, Duplessis, Sébastien, Frey, Pascal, Halkett, Fabien, & De Mita, Stéphane. Genomic Signatures of a Major Adaptive Event in the Pathogenic Fungus Melampsora larici-populina. United States. https://doi.org/10.1093/gbe/evab279
Persoons, Antoine, Maupetit, Agathe, Louet, Clémentine, Andrieux, Axelle, Lipzen, Anna, Barry, Kerrie W., Na, Hyunsoo, Adam, Catherine, Grigoriev, Igor V., Segura, Vincent, Duplessis, Sébastien, Frey, Pascal, Halkett, Fabien, and De Mita, Stéphane. Fri .
"Genomic Signatures of a Major Adaptive Event in the Pathogenic Fungus Melampsora larici-populina". United States. https://doi.org/10.1093/gbe/evab279. https://www.osti.gov/servlets/purl/1892180.
@article{osti_1892180,
title = {Genomic Signatures of a Major Adaptive Event in the Pathogenic Fungus Melampsora larici-populina},
author = {Persoons, Antoine and Maupetit, Agathe and Louet, Clémentine and Andrieux, Axelle and Lipzen, Anna and Barry, Kerrie W. and Na, Hyunsoo and Adam, Catherine and Grigoriev, Igor V. and Segura, Vincent and Duplessis, Sébastien and Frey, Pascal and Halkett, Fabien and De Mita, Stéphane},
abstractNote = {The recent availability of genome-wide sequencing techniques has allowed systematic screening for molecular signatures of adaptation, including in nonmodel organisms. Host–pathogen interactions constitute good models due to the strong selective pressures that they entail. We focused on an adaptive event which affected the poplar rust fungus Melampsora larici-populina when it overcame a resistance gene borne by its host, cultivated poplar. Based on 76 virulent and avirulent isolates framing narrowly the estimated date of the adaptive event, we examined the molecular signatures of selection. Using an array of genome scan methods based on different features of nucleotide diversity, we detected a single locus exhibiting a consistent pattern suggestive of a selective sweep in virulent individuals (excess of differentiation between virulent and avirulent samples, linkage disequilibrium, genotype–phenotype statistical association, and long-range haplotypes). Our study pinpoints a single gene and further a single amino acid replacement which may have allowed the adaptive event. Although our samples are nearly contemporary to the selective sweep, it does not seem to have affected genome diversity further than the immediate vicinity of the causal locus, which can be explained by a soft selective sweep (where selection acts on standing variation) and by the impact of recombination in mitigating the impact of selection. Therefore, it seems that properties of the life cycle of M. larici-populina, which entails both high genetic diversity and outbreeding, has facilitated its adaptation.},
doi = {10.1093/gbe/evab279},
journal = {Genome Biology and Evolution},
number = 1,
volume = 14,
place = {United States},
year = {Fri Dec 17 00:00:00 EST 2021},
month = {Fri Dec 17 00:00:00 EST 2021}
}
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Works referenced in this record:
Molecular mechanisms involved in functional macroevolution of plant transcription factors
journal, February 2021
- Romani, Facundo; Moreno, Javier E.
- New Phytologist, Vol. 230, Issue 4
LOCALIZER: subcellular localization prediction of both plant and effector proteins in the plant cell
journal, March 2017
- Sperschneider, Jana; Catanzariti, Ann-Maree; DeBoer, Kathleen
- Scientific Reports, Vol. 7, Issue 1
Obligate biotrophy features unraveled by the genomic analysis of rust fungi
journal, May 2011
- Duplessis, S.; Cuomo, C. A.; Lin, Y. -C.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 22
Comparison of Genetic and Virulence Diversity of Melampsora larici-populina Populations on Wild and Cultivated Poplar and Influence of the Alternate Host
journal, September 2006
- Gérard, Pierre R.; Husson, Claude; Pinon, Jean
- Phytopathology®, Vol. 96, Issue 9
Finding candidate genes under positive selection in Non-model species: examples of genes involved in host specialization in pathogens: LOOKING FOR GENES INVOLVED IN HOST SPECIALIZATION
journal, January 2010
- Aguileta, G.; Lengelle, J.; Marthey, S.
- Molecular Ecology, Vol. 19, Issue 2
On the unfounded enthusiasm for soft selective sweeps II: Examining recent evidence from humans, flies, and viruses
journal, December 2018
- Harris, Rebecca B.; Sackman, Andrew; Jensen, Jeffrey D.
- PLOS Genetics, Vol. 14, Issue 12
A New Approach for Using Genome Scans to Detect Recent Positive Selection in the Human Genome
journal, June 2007
- Tang, Kun; Thornton, Kevin R.; Stoneking, Mark
- PLoS Biology, Vol. 5, Issue 7
The genome sequence of African rice (Oryza glaberrima) and evidence for independent domestication
journal, July 2014
- Wang, Muhua; Yu, Yeisoo; Haberer, Georg
- Nature Genetics, Vol. 46, Issue 9
Coevolution Drives the Emergence of Complex Traits and Promotes Evolvability
journal, December 2014
- Zaman, Luis; Meyer, Justin R.; Devangam, Suhas
- PLoS Biology, Vol. 12, Issue 12
A Population Genomics Perspective on the Emergence and Adaptation of New Plant Pathogens in Agro-Ecosystems
journal, September 2012
- Stukenbrock, Eva H.; Bataillon, Thomas
- PLoS Pathogens, Vol. 8, Issue 9
Host–parasite co-evolution and its genomic signature
journal, August 2020
- Ebert, Dieter; Fields, Peter D.
- Nature Reviews Genetics, Vol. 21, Issue 12
Genome evolution in filamentous plant pathogens: why bigger can be better
journal, May 2012
- Raffaele, Sylvain; Kamoun, Sophien
- Nature Reviews Microbiology, Vol. 10, Issue 6
The need for speed: compartmentalized genome evolution in filamentous phytopathogens: Multiple 'speeds' in phytopathogen genomes
journal, December 2018
- Frantzeskakis, Lamprinos; Kusch, Stefan; Panstruga, Ralph
- Molecular Plant Pathology, Vol. 20, Issue 1
An efficient multi-locus mixed-model approach for genome-wide association studies in structured populations
journal, June 2012
- Segura, Vincent; Vilhjálmsson, Bjarni J.; Platt, Alexander
- Nature Genetics, Vol. 44, Issue 7
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
Genetic structure of the poplar rust fungus Melampsora larici-populina: Evidence for isolation by distance in Europe and recent founder effects overseas
journal, September 2008
- Barrès, Benoît; Halkett, Fabien; Dutech, Cyril
- Infection, Genetics and Evolution, Vol. 8, Issue 5
Feature-based prediction of non-classical and leaderless protein secretion
journal, May 2004
- Bendtsen, J. D.; Jensen, L. J.; Blom, N.
- Protein Engineering Design and Selection, Vol. 17, Issue 4
Robust Identification of Local Adaptation from Allele Frequencies
journal, July 2013
- Günther, Torsten; Coop, Graham
- Genetics, Vol. 195, Issue 1
The escalatory Red Queen: Population extinction and replacement following arms race dynamics in poplar rust
journal, January 2017
- Persoons, Antoine; Hayden, Katherine J.; Fabre, Bénédicte
- Molecular Ecology, Vol. 26, Issue 7
Effector Biology of Plant-Associated Organisms: Concepts and Perspectives
journal, January 2012
- Win, J.; Chaparro-Garcia, A.; Belhaj, K.
- Cold Spring Harbor Symposia on Quantitative Biology, Vol. 77, Issue 0
SignalP 5.0 improves signal peptide predictions using deep neural networks
journal, February 2019
- Almagro Armenteros, José Juan; Tsirigos, Konstantinos D.; Sønderby, Casper Kaae
- Nature Biotechnology, Vol. 37, Issue 4
Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server
journal, May 2007
- Kall, L.; Krogh, A.; Sonnhammer, E. L. L.
- Nucleic Acids Research, Vol. 35, Issue Web Server
The advantages and limitations of trait analysis with GWAS: a review
journal, January 2013
- Korte, Arthur; Farlow, Ashley
- Plant Methods, Vol. 9, Issue 1
Soft sweeps and beyond: understanding the patterns and probabilities of selection footprints under rapid adaptation
journal, November 2016
- Hermisson, Joachim; Pennings, Pleuni S.
- Methods in Ecology and Evolution, Vol. 8, Issue 6
The coming of age of EvoMPMI: evolutionary molecular plant–microbe interactions across multiple timescales
journal, August 2018
- Upson, Jessica L.; Zess, Erin K.; Białas, Aleksandra
- Current Opinion in Plant Biology, Vol. 44
Show me the way: rust effector targets in heterologous plant systems
journal, December 2018
- Lorrain, Cécile; Petre, Benjamin; Duplessis, Sébastien
- Current Opinion in Microbiology, Vol. 46
Genome-wide detection and characterization of positive selection in human populations
journal, October 2007
- Sabeti, Pardis C.; Varilly, Patrick; Fry, Ben
- Nature, Vol. 449, Issue 7164
The Bottleneck Effect and Genetic Variability in Populations
journal, March 1975
- Nei, Masatoshi; Maruyama, Takeo; Chakraborty, Ranajit
- Evolution, Vol. 29, Issue 1
Current Status of the Gene-For-Gene Concept
journal, September 1971
- Flor, H. H.
- Annual Review of Phytopathology, Vol. 9, Issue 1
Fifteen years of genomewide scans for selection: trends, lessons and unaddressed genetic sources of complication
journal, September 2015
- Haasl, Ryan J.; Payseur, Bret A.
- Molecular Ecology, Vol. 25, Issue 1
The plant immune system
journal, November 2006
- Jones, Jonathan D. G.; Dangl, Jeffery L.
- Nature, Vol. 444, Issue 7117
Detecting Selective Sweeps: A New Approach Based on Hidden Markov Models
journal, April 2009
- Boitard, Simon; Schlötterer, Christian; Futschik, Andreas
- Genetics, Vol. 181, Issue 4
PROVEAN web server: a tool to predict the functional effect of amino acid substitutions and indels
journal, April 2015
- Choi, Yongwook; Chan, Agnes P.
- Bioinformatics, Vol. 31, Issue 16
Population genomics of domestic and wild yeasts
journal, February 2009
- Liti, Gianni; Carter, David M.; Moses, Alan M.
- Nature, Vol. 458, Issue 7236
The population genomics of plant adaptation
journal, August 2010
- Siol, Mathieu; Wright, Stephen I.; Barrett, Spencer C. H.
- New Phytologist, Vol. 188, Issue 2
Genomic scans for selective sweeps using SNP data
journal, October 2005
- Nielsen, Rasmus; Williamson, Scott; Kim, Yuseob
- Genome Research, Vol. 15, Issue 11
A Composite of Multiple Signals Distinguishes Causal Variants in Regions of Positive Selection
journal, January 2010
- Grossman, S. R.; Shylakhter, I.; Karlsson, E. K.
- Science, Vol. 327, Issue 5967
Interior design: how plant pathogens optimize their living conditions
journal, November 2020
- Meisrimler, Claudia‐Nicole; Allan, Claudia; Eccersall, Sophie
- New Phytologist, Vol. 229, Issue 5
Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce
journal, August 2008
- Namroud, Marie-Claire; Beaulieu, Jean; Juge, Nicolas
- Molecular Ecology, Vol. 17, Issue 16
Whole-genome sequencing of Berkshire (European native pig) provides insights into its origin and domestication
journal, April 2014
- Li, Mingzhou; Tian, Shilin; Yeung, Carol K. L.
- Scientific Reports, Vol. 4, Issue 1
Evolutionary trees from DNA sequences: A maximum likelihood approach
journal, November 1981
- Felsenstein, Joseph
- Journal of Molecular Evolution, Vol. 17, Issue 6
Advances in understanding obligate biotrophy in rust fungi
journal, February 2019
- Lorrain, Cécile; Gonçalves dos Santos, Karen Cristine; Germain, Hugo
- New Phytologist, Vol. 222, Issue 3
Distribution of gene Frequency as a test of the Theory of the Selective Neutrality of Polymorphisms
journal, May 1973
- Lewontin, R. C.; Krakauer, Jesse
- Genetics, Vol. 74, Issue 1
ApoplastP : prediction of effectors and plant proteins in the apoplast using machine learning
journal, December 2017
- Sperschneider, Jana; Dodds, Peter N.; Singh, Karam B.
- New Phytologist, Vol. 217, Issue 4
The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication
journal, June 2011
- Xhaard, C.; Fabre, B.; Andrieux, A.
- Molecular Ecology, Vol. 20, Issue 13
Population Genomics: Whole-Genome Analysis of Polymorphism and Divergence in Drosophila simulans
journal, November 2007
- Begun, David J.; Holloway, Alisha K.; Stevens, Kristian
- PLoS Biology, Vol. 5, Issue 11
Patterns of genomic variation in the poplar rust fungus Melampsora larici-populina identify pathogenesis-related factors
journal, September 2014
- Persoons, Antoine; Morin, Emmanuelle; Delaruelle, Christine
- Frontiers in Plant Science, Vol. 5
Grinding up Wheat: A Massive Loss of Nucleotide Diversity Since Domestication
journal, April 2007
- Haudry, A.; Cenci, A.; Ravel, C.
- Molecular Biology and Evolution, Vol. 24, Issue 7
Detection of hard and soft selective sweeps from Drosophila melanogaster population genomic data
journal, February 2021
- Garud, Nandita R.; Messer, Philipp W.; Petrov, Dmitri A.
- PLOS Genetics, Vol. 17, Issue 2
Adaptive introgression from maize has facilitated the establishment of teosinte as a noxious weed in Europe
journal, September 2020
- Le Corre, Valérie; Siol, Mathieu; Vigouroux, Yves
- Proceedings of the National Academy of Sciences, Vol. 117, Issue 41
Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates
journal, October 2015
- Gautier, Mathieu
- Genetics, Vol. 201, Issue 4
Predicting transmembrane protein topology with a hidden markov model: application to complete genomes11Edited by F. Cohen
journal, January 2001
- Krogh, Anders; Larsson, Björn; von Heijne, Gunnar
- Journal of Molecular Biology, Vol. 305, Issue 3
Predicting the Functional Effect of Amino Acid Substitutions and Indels
journal, October 2012
- Choi, Yongwook; Sims, Gregory E.; Murphy, Sean
- PLoS ONE, Vol. 7, Issue 10
On the unfounded enthusiasm for soft selective sweeps
journal, October 2014
- Jensen, Jeffrey D.
- Nature Communications, Vol. 5, Issue 1
Plant-Parasite Coevolution: Bridging the Gap between Genetics and Ecology
journal, September 2011
- Brown, James K. M.; Tellier, Aurélien
- Annual Review of Phytopathology, Vol. 49, Issue 1
EggLib: processing, analysis and simulation tools for population genetics and genomics
journal, January 2012
- De Mita, Stéphane; Siol, Mathieu
- BMC Genetics, Vol. 13, Issue 1
Interactive Tree Of Life (iTOL) v4: recent updates and new developments
journal, April 2019
- Letunic, Ivica; Bork, Peer
- Nucleic Acids Research, Vol. 47, Issue W1
A Comprehensive Analysis of Genes Encoding Small Secreted Proteins Identifies Candidate Effectors in Melampsora larici-populina (Poplar Leaf Rust)
journal, March 2012
- Hacquard, Stéphane; Joly, David L.; Lin, Yao-Cheng
- Molecular Plant-Microbe Interactions, Vol. 25, Issue 3
How does adaptation sweep through the genome? Insights from long-term selection experiments
journal, October 2012
- Burke, Molly K.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1749
Population genomics and local adaptation in wild isolates of a model microbial eukaryote
journal, January 2011
- Ellison, C. E.; Hall, C.; Kowbel, D.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 7
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
MycoCosm portal: gearing up for 1000 fungal genomes
journal, December 2013
- Grigoriev, Igor V.; Nikitin, Roman; Haridas, Sajeet
- Nucleic Acids Research, Vol. 42, Issue D1
The Genomics of Speciation in Drosophila: Diversity, Divergence, and Introgression Estimated Using Low-Coverage Genome Sequencing
journal, July 2009
- Kulathinal, Rob J.; Stevison, Laurie S.; Noor, Mohamed A. F.
- PLoS Genetics, Vol. 5, Issue 7
Discriminant analysis of principal components: a new method for the analysis of genetically structured populations
journal, January 2010
- Jombart, Thibaut; Devillard, Sébastien; Balloux, François
- BMC Genetics, Vol. 11, Issue 1
Next-Generation DNA Sequencing Methods
journal, September 2008
- Mardis, Elaine R.
- Annual Review of Genomics and Human Genetics, Vol. 9, Issue 1
Population genomics of rapid adaptation by soft selective sweeps
journal, November 2013
- Messer, Philipp W.; Petrov, Dmitri A.
- Trends in Ecology & Evolution, Vol. 28, Issue 11