Pascal Frey

Dr Pascal FREY, PhD.

Senior scientist (DR2, HDR)

INRAE, University of Lorraine

“Ecology of Forest Pathogenic Fungi” team

IAM Department, UMR 1136

F-54280 Champenoux, France

Phone: + 33 383 394 056

Mobile: + 33 631 459 407

E-mail: pascal.frey<at>

Twitter: @pascal_frey


Head of the IAM Department

President of the French Society of Phytopathology (SFP) 2008-2011 & 2011-2014 (member since 1990).



Research interests

My main research interests are epidemiology and population biology of forest pathogenic fungi – and fungus-like oomycetes. My main model species are the poplar rust fungus Melampsora larici-populina and the emerging interspecific hybrid oomycete Phytophthora alni causing alder decline. My recent work is focused on:

  • the combination of epidemiology and population genetics approaches in order to study the evolution of fungal populations and adaptation to qualitative and quantitative plant resistances
  • the study of emerging forest diseases and biological invasions, in relation with the evolution of fungal pathogen populations

Research keywords: epidemiology, population genetics, population genomics, emerging diseases, biological invasions, phylogeny, life history traits, adaptation to host.


Full-text PDFs are available upon request.

My publications on HAL.

Saubin M., Coville J., Xhaard C., Frey P., Soubeyrand S., Halkett F., Fabre F. 2023. A mechanistic-statistical approach to infer dispersal and demography from invasion dynamics, applied to a plant pathogen. Peer Community in Mathematical and Computational Biology. Full text

Saubin M., Louet C., Bousset L., Fabre F., Frey P., Fudal I., Grognard F., Mailleret L., Stoeckel S., Touzeau S., Petre B., Halkett, F. 2023. Improving the design of sustainable crop protection strategies by integrating population genetics concepts. Molecular Ecology 32: 2461–2471. Abstract

Louet C., Saubin M., Andrieux A., Persoons A., Gorse M., Pétrowski J., De Mita S., Fabre B., Duplessis S., Frey P., Halkett F. 2023. A point mutation and large deletion at the candidate avirulence locus AvrMlp7 in the poplar rust fungus correlate with poplar RMlp7 resistance breakdown. Molecular Ecology 32: 2472–2483. Abstract

Guerillot P., Salamov A., Louet C., Morin E., Frey P., Grigoriev I. V., Duplessis S. 2023. A remarkable expansion of oligopeptide transporter genes in rust fungi (Pucciniales) suggests a specialization in nutrients acquisition for obligate biotrophy. Phytopathology 113: 252-264. Abstract

Louet C., Duplessis S., Frey P., Petre B. 2022. A survey of highly influential studies on plant pathogen effectors during the last two decades (2000-2020). Frontiers in Plant Science 13: 920281. Full text

Louet C., Blot C., Shelest E., Guerillot P., Salamov A., Zannini F., Pétrowski J., Grigoriev I. V., Frey P., Duplessis S. 2022. Annotation survey and life-cycle transcriptomics of transcription factors in rust fungi (Pucciniales) identify a possible role for cold shock proteins in dormancy exit. Fungal Genetics and Biology 161: 10369. Abstract

Persoons A., Maupetit A., Louet C., Andrieux A., Lipzen A., Barry K., Na H., Adam C., Grigoriev I., Segura V., Duplessis S., Frey P., Halkett F., De Mita S. 2022. Genomic signatures of a major adaptive event in the pathogenic fungus Melampsora larici-populina. Genome Biology & Evolution 14: evab279. Full text

Fabre B., Bastien C., Husson C., Marçais B., Frey P., Halkett F. 2021. Un effet papillon dans les peupleraies françaises : les répercussions d’un contournement de résistance sur les méthodes de sélection variétale. In: Lannou C., Roby D., Ravigné V., Hannachi M., Moury B., Eds. L’immunité des plantes : Pour des cultures résistantes aux maladies. Editions Quae, Versailles, 329-339. Book chapter.

Maupetit A., Fabre B., Pétrowski J., Andrieux A., De Mita S., Frey P., Halkett F., Hayden K. J. 2021. Evolution of morphological but not aggressiveness-related traits following a major resistance breakdown in the poplar rust fungus, Melampsora larici-populina. Evolutionary Applications 14: 513–523. Full text

Maupetit A., Larbat R., Pernaci M., Andrieux A., Guinet C., Boutigny A.-L., Fabre B., Frey P., Halkett F. 2018. Defense compounds rather than nutrient availability shape aggressiveness trait variation along a leaf maturity gradient in a biotrophic plant pathogen. Frontiers in Plant Science 9: 1396. Full text

Lorrain C., Marchal C., Hacquard S., Delaruelle C., Pétroswki J., Petre B., Hecker A., Frey P., Duplessis S. 2018. The rust fungus Melampsora larici-populina expresses a conserved genetic program and distinct sets of secreted protein genes during infection of its two host plants, larch and poplar. Molecular Plant-Microbe Interactions, 31: 695-706. Abstract

Persoons A., Hayden K. J., Fabre B., Frey P., De Mita S., Tellier A., Halkett F. 2017. The escalatory Red Queen: Population extinction and replacement following arms race dynamics in poplar rust. Molecular Ecology 26: 1902–1918 (Special Issue on Microbial Local Adaptation). Abstract

Aguayo J., Halkett F., Husson C., Nagy Z. A., Szigethy A., Bakonyi J., Frey P., Marçais B. 2016. Genetic diversity and origins of the homoploid-type hybrid Phytophthora ×alni. Applied and Environmental Microbiology 82: 7142–7153. Full text

Becheler R., Xhaard C., Klein E. K., Hayden K. J., Frey P., De Mita S., Halkett F. 2016. Genetic signatures of a range expansion in natura: when clones play leapfrog. Ecology and Evolution 6: 6625-6632. Full text

Guinet C., Boutigny A.-L., Vialle A., Hamelin R. C., Frey P., Ioos R. 2016. Simultaneous monitoring and quantification of Melampsora allii-populina and Melampsora larici-populina on infected poplar leaves using a duplex real-time PCR assay. Plant Pathology 65: 380-391. Abstract

Husson C., Aguayo J., Revellin C., Frey P., Ioos R., Marçais B. 2015. Evidence for homoploid speciation in Phytophthora alni supports taxonomic reclassification in this species complex. Fungal Genetics and Biology 77: 12-21. Abstract

Pernaci M., De Mita S., Andrieux A., Pétrowski J., Halkett F., Duplessis S., Frey P. 2014. Genome-wide patterns of segregation and linkage disequilibrium: the construction of a linkage genetic map of the poplar rust fungus Melampsora larici-populina. Frontiers in Plant Science 5: 454. Full text

Persoons A., Morin E., Delaruelle C., Payen T., Halkett F., Frey P., De Mita S., Duplessis S. 2014. Patterns of genomic variation in the poplar rust fungus Melampsora larici-populina identify pathogenesis-related factors. Frontiers in Plant Science 5: 450. Full text

Elefsen S. E., Frey P., Sverrisson H., Hallsson J. H. 2014. Microsatellite analysis of Icelandic populations of the poplar fungal pathogen Melampsora larici-populina shows evidence of repeated colonization events. European Journal of Plant Pathology 139: 597-608. Abstract

Hacquard S., Delaruelle C., Frey P., Tisserant E., Kohler A., Duplessis S. 2013. Transcriptome analysis of poplar rust telia reveals overwintering adaptation and tightly coordinated karyogamy and meiosis processes. Frontiers in Plant Science 4: 456. Full text

Boutigny A.-L., Guinet C., Vialle A., Hamelin R.C., Andrieux A., Frey P., Husson C., Ioos R. 2013. Optimization of a real-time PCR assay for the detection of the quarantine pathogen Melampsora medusae f. sp. deltoidae. Fungal Biology 117: 389-398. Abstract

Boutigny A.-L., Guinet C., Vialle A., Hamelin R.C., Frey P., Ioos R. 2013. A sensitive real-time PCR assay for the detection of the two Melampsora medusae formae speciales on infected poplar leaves. European Journal of Plant Pathology 136: 433-441Abstract

Husson C., Ioos R., Andrieux A., Frey P. 2013. Development and use of new sensitive molecular tools for diagnosis and detection of Melampsora rusts on cultivated poplar. Forest Pathology 43: 1-11. Abstract

Covarelli L., Beccari G., Tosi L., Fabre B., Frey P. 2013. Three-year investigations on leaf rust in poplar cultivated for biomass production in Umbria, Central Italy. Biomass & Bioenergy 49: 315-322. Abstract

Vialle A., Feau N., Frey P., Bernier L., Hamelin R.C. 2013. Phylogenetic species recognition reveals host-specific lineages among poplar rust fungi. Molecular Phylogenetics and Evolution 66: 628–644. Abstract

Aguayo J., Adams G. C., Halkett F., Catal M., Husson C., Nagy Z. A., Hansen E. M., Marçais B., Frey P. 2013. Strong genetic differentiation between North American and European populations of Phytophthora alni subsp. uniformis. Phytopathology 103: 190-199. Full text

Pfabel C., Eckhardt K.-U., Baum C., Struck C., Frey P., Weih M. 2012. Impact of ectomycorrhizal colonisation and rust infection on the secondary metabolism of poplar (Populus trichocarpa × deltoides). Tree Physiology 32: 1357-1364. Full text

Barrès B., Dutech C., Andrieux A., Halkett F., Frey P. 2012. Exploring the role of asexual multiplication in poplar rust epidemics: impact on diversity and genetic structure. Molecular Ecology 21: 4996-5008. Abstract

Xhaard C., Barrès B., Andrieux A., Bousset L., Halkett F., Frey P. 2012. Disentangling the genetic origins of a plant pathogen during disease spread using an original molecular epidemiology approach. Molecular Ecology 21: 2383-2398. Abstract

Hacquard S., Joly D.L., Lin Y.C., Tisserant E., Feau N., Delaruelle C., Legué V., Kohler A., Tanguay P., Pêtre B., Frey P., Van de Peer Y., Rouzé P., Martin F. Hamelin R.C., Duplessis S. 2012. A comprehensive analysis of genes encoding small secreted proteins identifies candidate effectors in Melampsora larici-populina (poplar leaf rust). Molecular Plant-Microbe Interactions 25: 279-293. Full text

Vialle A., Frey P., Hambleton S., Bernier L., Hamelin R.C. 2011. Poplar rust systematics and refinement of Melampsora species delineation. Fungal Diversity 50: 227-248. Abstract

Hacquard S., Pêtre B., Frey P., Hecker A., Rouhier N., Duplessis S. 2011. The poplar-poplar rust interaction: insights from genomics and transcriptomics. Journal of Pathogens 2011: 716041. Full text

Philibert A., Desprez-Loustau M.-L., Fabre B., Frey P., Halkett F., Husson C., Lung-Escarmant B., Marçais B., Robin C., Vacher C., Makowski D. 2011. Predicting invasion success in forest pathogenic fungi from species traits. Journal of Applied Ecology 48: 1381-1390. Full text

Xhaard C., Fabre B., Andrieux A., Gladieux P., Barrès B., Frey P., Halkett F. 2011. The genetic structure of the plant pathogenic fungus Melampsora larici-populina on its wild host is extensively impacted by host domestication. Molecular Ecology 20 : 2739-2755. Abstract

Duplessis S., Cuomo C. A., Lin Y.-C., Aerts A., Tisserant E., Veneault-Fourrey C., Joly D. L., Hacquard S., Amselem J., Cantarel B. L., Chiu R., Coutinho P. M., Feau N., Field M., Frey P., Gelhaye E., Goldberg J., Grabherr M. G., Kodira C. D., Kohler A., Kües U., Lindquist E. A., Lucas S. M., Mago R., Mauceli E., Morin E., Murat C., Pangilinan J. L., Park R., Pearson M., Quesneville H., Rouhier N., Sakthikumar S., Salamov A. A., Schmutz J., Selles B., Shapiro H., Tanguay P., Tuskan G. A., Henrissat B., Van de Peer Y., Rouzé P., Ellis J. G., Dodds P. N., Schein J. E., Zhong S., Hamelin R. C., Grigoriev I. V., Szabo L. J., Martin F. 2011. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proceedings of the National Academy of Sciences 108: 9166-9171. Full text

Husson C., Scala B., Caël O., Frey P., Feau N., Ioos R., Marçais B. 2011. Chalara fraxinea is an invasive pathogen in France. European Journal of Plant Pathology 130: 311–324. Abstract

Duplessis S., Hacquard S., Delaruelle C., Tisserant E., Frey P., Martin F., Kohler A. 2011. Melampsora larici-populina transcript profiling during germination and time-course infection of poplar leaves reveals dynamic expression patterns associated with virulence and biotrophy. Molecular Plant-Microbe Interactions 24: 808-818. Full text

Malausa T., Gilles A., Meglécz E., Blanquart H., Duthoy S., Costedoat C., Dubut V., Pech N., Castagnone-Sereno P., Délye C., Feau N., Frey P., Gauthier P., Guillemaud T., Hazard L., Le Corre V., Lung-Escarmant B., Malé P.-J., Ferreira S., Martin J.-F. 2011. High-throughput microsatellite isolation through 454 GS-FLX Titanium pyrosequencing of enriched DNA libraries. Molecular Ecology Resources 11 : 638–644. Abstract

Hacquard S., Veneault-Fourrey C., Delaruelle C., Frey P., Martin F., Duplessis S. 2011. Validation of Melampsora larici-populina reference genes for in plantaRT-quantitative PCR expression profiling during time-course infection of poplar leaves. Physiological and Molecular Plant Pathology 75: 106-112. Abstract

Hacquard S., Delaruelle C., Legué V., Tisserant E., Kohler A., Frey P., Martin F., Duplessis S. 2010. Laser capture microdissection of uredinia formed byMelampsora larici-populina revealed a transcriptional switch between biotrophy and sporulation. Molecular Plant-Microbe Interactions 23: 1275-1286. Full text

Ioos R., Fabre B., Saurat C., Fourrier C., Frey P., Marçais B. 2010. Development, comparison, and validation of real-time and conventional PCR tools for the detection of the fungal pathogens causing brown spot and red band needle blights of pines. Phytopathology 100:105-114. Full text

Xhaard C., Andrieux A., Halkett F., Frey P. 2009. Characterization of 41 microsatellite loci developed from the genome sequence of the poplar rust fungus,Melampsora larici-populina. Conservation Genetics Resources 1: 21-25. Abstract

Feau N., Vialle A., Allaire M., Tanguay P., Joly D.L., Frey P., Callan B.E., Hamelin R.C. 2009. Fungal pathogen (mis-) identification: A case study with DNA barcodes on Melampsora rusts of aspen and white poplar. Mycological Research 113: 713-724. Abstract

Bastien C., Chenault N., Dowkiw A., Villar M., Klein E., Frey P. 2009. Interactions entre populations naturelles et cultivées : l’exemple du peuplier. Biofutur, 28 (305): 31-34.

Frey P. 2009. L’hybridation interspécifique chez les champignons phytopathogènes à l’origine de nouvelles maladies. Biofutur, 28 (296): 36-39.

Barrès B., Halkett F., Dutech C., Andrieux A., Pinon J., Frey P. 2008. Genetic structure of the poplar rust fungus Melampsora larici-populina: evidence for isolation by distance in Europe and recent founder effects overseas. Infection Genetics and Evolution 8: 577-587. Abstract

Husson C., Delatour C., Frey P., Marçais B., Saurat C., Schenck N. 2007. First report of Phytophthora ramorum on ornamental plants in France. Plant Disease 91: 1359. Full text

Ioos R., Panabières F., Industri B., Andrieux A., Frey P. 2007. Distribution and expression of elicitin genes in the interspecific hybrid oomycete Phytophthora alni. Applied and Environmental Microbiology 73: 5587-5597. Full text

Rinaldi C., Kohler A., Frey P., Duchaussoy F., Ningre N., Couloux A., Wincker P., Le Thiec D., Fluch S., Martin F., Duplessis S. 2007. Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melampsora larici-populina. Plant Physiology 144: 347-366. Full text

Ioos R., Barrès B., Andrieux A., Frey P. 2007. Characterization of microsatellite markers in the interspecific hybrid Phytophthora alni subsp. alni, and cross-amplification with related taxa. Molecular Ecology Notes 7: 133-137. Abstract

Ioos R., Laugustin L., Schenck N., Rose S., Husson C., Frey P. 2006. Usefulness of single copy genes containing introns in Phytophthora for the development of detection tools for the regulated species P. ramorum and P. fragariae. European Journal of Plant Pathology 116: 171-176. Abstract

Husson C., Thoirain B., Ioos R., Frey P., Marçais B. 2006. L’eau, vecteur d’agents pathogènes : cas du Phytophthora de l’Aulne. Revue Forestière Française 58: 351-360. Full text

Gérard P.R., Husson C., Pinon J., Frey P. 2006. Comparison of genetic and virulence diversity of Melampsora larici-populina populations on wild and cultivated poplar and influence of the alternate host. Phytopathology 96: 1027-1036. Full text

Ioos R., Andrieux A., Marçais B., Frey P. 2006. Genetic characterization of the natural hybrid species Phytophthora alni as inferred from nuclear and mitochondrial DNA analyses. Fungal Genetics and Biology 43: 511-529. Abstract

Pinon J., Frey P., Husson C. 2006. Wettability of poplar leaves influences dew formation and infection by Melampsora larici-populina. Plant Disease 90: 177-184. Full text

Barrès B., Dutech C., Andrieux A., Caron H., Pinon J., Frey P. 2006. Isolation and characterization of 15 microsatellite loci in the poplar rust fungus,Melampsora larici-populina, and cross-amplification in related species. Molecular Ecology Notes 6: 60-64. Abstract

Ioos R., Husson C., Andrieux A., Frey P. 2005. SCAR-based PCR primers to detect the hybrid pathogen Phytophthora alni and its subspecies causing alder disease in Europe. European Journal of Plant Pathology 112: 323-335. Abstract

Frey P., Gérard P., Feau N., Husson C., Pinon J. 2005. Variability and population biology of Melampsora rusts on poplars. In Pei M. H., McCracken A. R., eds. Rust diseases of Willow and Poplar. CAB International, Wallingford, UK, 63-72. Abstract

Pinon J., Frey P. 2005. Interactions between poplar clones and Melampsora populations and their implications for breeding for durable resistance. In Pei M. H., McCracken A. R., eds. Rust diseases of Willow and Poplar. CAB International, Wallingford, UK, 139-154. Abstract

Rouhier N., Gelhaye E., Gualberto J. M., Jordy M. N., De Fay E., Hirasawa M., Duplessis S., Lemaire S. D., Frey P., Martin F., Manieri W., Knaff D. B., Jacquot J. P. 2004. Poplar peroxiredoxin Q. A chloroplast antioxidant functional in pathogen defense. Plant Physiology 134: 1027-1038. Full text

Innes L., Marchand L., Frey P., Bourassa M., Hamelin R.C. 2004. First report of Melampsora larici-populina on Populus spp. in Eastern North America. Plant Disease 88: 85. Full text

Frey P., Pinon J. 2004. La rouille du peuplier : un pathosystème modèle [Poplar rust: a model pathosystem]. Biofutur, 23 (247): 28-32.

Dowkiw A., Husson C., Frey P., Pinon J, Bastien C. 2003. Partial resistance to Melampsora larici-populina leaf rust in hybrid poplars: genetic variability in inoculated excised leaf disk bioassay and relationship with complete resistance. Phytopathology 93: 421-427. Full text

Nageleisen L. M., Pinon J., Frey P., Marçais B., Frochot H., Ningre F., Wehrlen L., Renaud J.P. 2002. Végétation accompagnatrice et agresseurs biotiques. Revue Forestière Française 54: 577-584. Full text

Ioos R., Frey P. 2000. Genomic variation within Monilinia laxaM. fructigena and M. fructicola, and application to species identification by PCR. European Journal of Plant Pathology 106: 373-378. Abstract

Ioos R., Frey P. 2000. Application de la variabilité génétique de l’ADNr chez Monilinia laxa, M. fructigena et M. fructicola à l’identification des espèces par PCR. Bulletin OEPP / EPPO Bulletin 30: 499-505. Abstract

Vasse J., Génin S., Frey P., Boucher C., Brito B. 2000. The hrpB and hrpG regulatory genes of Ralstonia solanacearum are required for different stages of the tomato root infection process. Molecular Plant-Microbe Interactions 13: 259-267. Full text

Miot S., Frey P., Pinon J. 1999. Varietal mixture of poplar clones: effects on infection by Melampsora larici-populina and plant growth. European Journal of Forest Pathology 29: 411-423. Abstract

Frey P., Pinon J. 1997. Variability in pathogenicity of Melampsora allii-populina expressed on poplar cultivars. European Journal of Forest Pathology 27: 397-407. Abstract

Pinon J., Frey P. 1997. Structure of Melampsora larici-populina populations on wild and cultivated poplar. European Journal of Plant Pathology 103: 159-173. Abstract

Frey P., Frey-Klett P., Garbaye J., Berge O., Heulin T. 1997. Metabolic and genotypic fingerprinting of fluorescent pseudomonads associated with the Douglas Fir – Laccaria bicolor mycorrhizosphere. Applied and Environmental Microbiology 63: 1852-1860. Full text

Frey P., Smith J.J., Albar L., Prior P., Saddler G.S., Trigalet-Demery D., Trigalet A. 1996. Bacteriocin typing of Burkholderia (Pseudomonas) solanacearumrace 1 of the French West Indies and correlation with genomic variation of the pathogen. Applied and Environmental Microbiology 62: 473-479. Full text

Vasse J., Frey P., Trigalet A. 1995. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Molecular Plant-Microbe Interactions 8: 241-251. Full text

Trigalet A., Frey P., Trigalet-Demery D. 1994. Biological control of bacterial wilt caused by Pseudomonas solanacearum: state of the art and understanding, in: Hayward AC, Hartman GL (Eds), Bacterial wilt: The disease and its causative agent Pseudomonas solanacearum. CAB International, Wallingford, UK, pp. 225-233.

Frey P., Prior P., Marie C., Kotoujansky A., Trigalet-Demery D., Trigalet A. 1994. Hrp- mutants of Pseudomonas solanacearum as potential biocontrol agents of tomato bacterial wilt. Applied and Environmental Microbiology 60: 3175-3181. Full text