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BIOlogie et GEstion des Risques en agriculture - Champignons Pathogènes des Plantes

Publications - Bibliography

Complete list of papers 


Meyer M, Bourras S, Gervais J, Labadie K, Cruaud C, Balesdent MH, Rouxel T (2017) Impact of biotic and abiotic factors on the expression of fungal effector-encoding genes in axenic growth conditions. Fungal Genet. Biol. 99: 1-12 [DOI]

Plissonneau C, Blaise F, Ollivier B, Leflon M, Carpezat J, Rouxel T, Balesdent MH (2017) Unusual evolutionary mechanisms to escape Effector-Triggered-Immunity in the fungal phytopathogen Leptosphaeria maculans. Mol. Ecol. in press

Plissonneau C, Benevenuto J, Mohd-Assaad N, Fouché S, Hartmann FE, Croll D (2017) Using population and comparative genomics to understand the genetic basis of effector-driven fungal pathogen evolution. Front. Plant Sci. 8:119 [DOI]

Rouxel T, Balesdent MH (2017) Life, death and rebirth of avirulence effectors in a fungal pathogen of Brassica crops, Leptosphaeria maculans. New Phytol. [DOI]

Zhong Z, Marcel T, Hartmann FE, Ma X, Plissonneau C, Zala M, Ducasse A, Compain J, Lapalu N, Amselem J, McDonald BA, Croll D, Palma-Guerrero J. (2017) A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol. in press


de Marchi R, Sorel M, Mooney B, Fudal I, Goslin K, Kwasniewska K, Ryan PT, Pfalz M, Kroymann J, Pollmann S, Feechan A, Wellmer F, Rivas S, Graciet E (2016) The N-end rule pathway regulates pathogen responses in plants. Scientific Rep. 6. [DOI

Gervais J, Plissonneau C, Linglin J, Meyer M, Labadie K, Cruaud C, Fudal I, Rouxel T, Balesdent MH (2016) Different waves of effector genes with contrasted genomic location are expressed by Leptosphaeria maculans during cotyledon and stem colonisation of oilseed rape. Mol. Plant Pathol. [DOI]

Nováková M, Šašek V, Trdá L, Krutinová H, Mongin T, Valentová O, Balesdent M-H, Rouxel T, Burketová L (2016) Leptosphaeria maculans effector AvrLm4-7 affects SA- and ET-signalling and H2O2 accumulation in Brassica napus. Mol. Plant Pathol. 17: 818-831.

Plissonneau C, Daverdin G, Ollivier B, Blaise F, Degrave A, Fudal I, Rouxel T, Balesdent MH (2016) A game of hide and seek between avirulence genes AvrLm4-7 and AvrLm3 in Leptosphaeria maculans. New Phytol. 209: 1613-1624.

Plissonneau C, Stürchler A, Croll D (2016) The evolution of orphan regions in genomes of a fungal pathogen of wheat. mBio 7: e01231-16 [DOI]

Zhang  X, Peng P, Kutcher R, Balesdent MH, Delourme R, Fernando DWG. (2016). Breakdown of Rlm3 resistance in the Brassica napus–Leptosphaeria maculans pathosystem in western Canada. Eur. J. Plant Pathol. 145: 659–674 [DOI]


Balesdent MH, Plissonneau C, Coudard L, Daverdin G, Le Meur L, Carpezat J, Leflon M, Pinochet X, Ermel M, Brun H, Rouxel T (2015) Résistance du colza au phoma : où en est-on de l'efficacité de Rlm7 ? Phytoma 684: 20-24.

Blondeau K, Blaise F, Graille M, Kale SD, Linglin J, Ollivier B, Labarde A, Lazar N, Daverdin G, Balesdent MH, Choi DHY, Tyler BM, Rouxel T, van Tilbeurgh H, Fudal I (2015) Crystal structure of the effector AvrLm4–7 of Leptosphaeria maculans reveals insights into its translocation into plant cells and recognition by resistance proteins. Plant J. 83: 610-624.

Bourras S, Meyer M, Rouxel T (2015) Agrobacterium tumefaciens gene transfer: how a plant pathogen hacks the nuclei of plant and non-plant organisms. Phytopathology 105: 1288-1301.

Ghanbarnia K, Fudal I, Larkan NJ, Links MG, Balesdent M-H, Profotova B, Fernando WGD, Rouxel T, Borhan MH (2015) Rapid identification of the Leptosphaeria maculans avirulence gene AvrLm2, using an intraspecific comparative genomics approach. Mol. Plant Pathol. 16: 699-709.

Plissonneau C, Daverdin G, Coudard L, Ollivier B, Rouxel T, Balesdent MH (2015) Phoma du colza : recyclage du gène de résistance Rlm3. Phytoma 684: 25-28.

Soyer JL, Hamiot A, Ollivier B, Balesdent MH, Rouxel T, Fudal I (2015) The APSES transcription factor LmStuA is required for sporulation, pathogenic development and effector gene expression in Leptosphaeria maculans. Mol. Plant Pathol. 16: 1000-1005.

Soyer JL, Möller M, Schotanus K, Connolly L, Galazka JM, Freitag M, Stukenbrock E (2015) Chromatin analyses of Zymoseptoria tritici: methods for chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq). Fungal Genet. Biol. 79: 63-70.

Soyer JL, Rouxel T, Fudal I (2015) Chromatin-based control of effector gene expression in plant-associated fungi. Curr. Op. Plant Biol. 26: 51–56


Carpezat, J, Bothorel S, Daverdin G, Balesdent MH, Leflon M (2014) Use of high resolution melting analysis to genotype the avirulence AvrLm4-7 gene of Leptosphaeria maculans, a fungal pathogen of Brassica napus.  Ann. Appli. Biol. 164 :430–44.

Delourme R, Bousset L, Ermel E, Duffé P, Besnard AL, Marquer B, Fudal I, Linglin J, Chadoeuf J, Brun H (2014) Quantitative resistance affects the speed of frequency increase but not the diversity of the virulence alleles overcoming a major resistance gene to Leptosphaeria maculans in oilseed rape. Infect. Genet. Evol. 27: 490–499.

Grandaubert J, Balesdent MH, Rouxel T (2014) Evolutionary and adaptive role of transposable elements in fungal genomes. In Francis Martin, editor: Fungi, Vol 70, Ann. Bot. Res., UK: Academic Press, pp. 79-107.

Grandaubert J, Lowe RGT, Soyer JL, Schoch CL, Van de Wouw AP, Fudal I, Robbertse B, Lapalu N, Links MG, Ollivier B, Linglin J, Barbe V, Mangenot S, Cruaud C, Borhan H, Howlett BJ, Balesdent MH, Rouxel T (2014) Transposable element-assisted evolution and adaptation to host plant within the Leptosphaeria maculans-Leptosphaeria biglobosa species complex of fungal pathogens. BMC Genomics 15: 891.

Lowe RGT, Cassin A, Grandaubert J, Clark B, Van de Wouw AP, Rouxel T, Howlett BJ (2014) Genomes and transcriptomes of partners in plant-fungal- interactions between canola (Brassica napus) and two Leptosphaeria species. PLoS One 9: e103098.

Soyer JL, El Ghalid M, Glaser N, Ollivier B, Linglin J, Grandaubert J, Balesdent MH, Connolly LR, Freitag M, Rouxel T, Fudal I (2014) Epigenetic control of effector gene expression in the plant pathogenic fungus Leptosphaeria maculans. PLoS Genet. 10: e1004227.


Balesdent MH, Fudal I, Ollivier B, Bally P, Grandaubert J, Eber F, Chèvre AM, Leflon M, Rouxel T (2013). The dispensable chromosome of Leptosphaeria maculans shelters an effector gene conferring avirulence toward Brassica rapa. New Phytol. 198: 887-898.

Dilmaghani A, Gout L, Moreno-Rico O, Dias JS, Coudard L, Castillo-Torres N, Balesdent MH, Rouxel T (2013) Clonal populations of Leptosphaeria maculans contaminating cabbage in Mexico. Plant Pathol.  62: 520-532

Godinho JS, Dias JS, Balesdent MH, and Mendes-Pereira E (2013) Molecular characterisation of Portuguese isolates of Leptosphaeria maculans using PCR-ISSR and RAPD markers. Acta Horticulturae 1005: 573-580.

Grandaubert J, Balesdent MH, Rouxel T (2013). Incidence des Eléments Transposables sur l’évolution des génomes des champignons phytopathogènes et sur leur potentiel adaptatif. Biol Auj. 207:277-290

Rouxel T & Balesdent MH (2013) From model to crop plant-pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus. New Phytol. 197:356-358 (Invited commentary).

Tyler BM, Kale SD, Wang Q, Tao K, Clark HR, Drews K, Antignani V, Rumore A, Hayes T, Plett JM, Fudal I, Gu B, Chen Q, Affeldt KJ, Berthier E, Fischer GJ, Dou D, Shan W, Keller N, Martin F, Rouxel T, Lawrence CB (2013). Microbe-independent entry of oomycete RxLR effectors and fungal RxLR-like effectors into plant and animal cells is specific and reproducible. Mol. Plant-Microbe Interact. 26: 611-616.

Tyler BM & Rouxel T (2013) Effectors of fungi and oomycetes: their virulence and avirulence functions, and translocation from pathogen to host cells. In Molecular Plant Immunity. G. Sessa, Ed., Wiley Blackwell Press, Chap. 7, pp. 123-167.


Bourras S, Meyer M, Grandaubert J, Lapalu N, Fudal I, Linglin J, Ollivier B, Blaise F, Balesdent MH, Rouxel T (2012) The incidence of genome structure, DNA asymmetry and cell physiology on T-DNA integration in chromosomes of the phytopathogenic fungus Leptosphaeria maculans. G3 2:891-904.

Daverdin G, Rouxel T, Gout L, Aubertot JN, Fudal I, Meyer M, Parlange F, Carpezat J, Balesdent MH (2012) Genome structure and reproductive behaviour influence the evolutionary potential of a fungal phytopathogen. PLoS Pathog. 8: e1003020.

Dilmaghani A*, Gladieux P*, Gout L, Giraud T Brunner P, Stachowiak A, Balesdent MH, Rouxel T (2012) Migration patterns and changes in population biology associated with the worldwide spread of the oilseed rape pathogen Leptosphaeria maculans. Mol. Ecol. 21:2519-2533


Rouxel T, De Wit PJGM (2011) Dothideomycete effectors facilitating biotrophic and necrotrophic life styles. In: Effectors in Plant-Microbe Interactions. F. Martin and S. Kamoun, Eds. Wiley Blackwell Press

Rouxel T, Grandaubert J, Hane JK, Hoede C, Van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Cuifetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GHJ, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, T urgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent MH, Howlett BJ (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat. Commun. 2:202. [DOI]


Bally P, Grandaubert J, Rouxel T, Balesdent MH (2010) FONZIE: an optimized pipeline for minisatellite marker discovery and primer design from large sequence data sets. BMC Res. Notes 3:322

Dilmaghani A, Balesdent MH, Rouxel T, Moreno-Rico O (2010) First report of Leptosphaeria biglobosa (Blackleg) on Brassica oleracea (Cabbage) in Mexico. Plant Dis. 94:791. [DOI]

Huang YJ, Balesdent MH, Li ZQ, Evans N, Rouxel T, Fitt BDL (2010) Fitness cost of virulence differs between the AvrLm1 and AvrLm4 loci in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur. J. Plant Pathol. 126:279-291. [DOI]

Kale SD, Gu B, Capelluto DGS, Dou D, Feldman E, Rumore A, D. Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM (2010) External lipid PI-3-P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284-295. [DOI]

Kutcher HR, Balesdent MH, Rimmer SR, Rouxel T, Chèvre AM, Delourme R, Brun H (2010) Frequency of avirulence genes in Leptosphaeria maculans in western Canada. Can. J. Plant Pathol. 32:77-85. [DOI]

Hane JK, Rouxel T, Howlett BJ, Kema GHJ, Goodwin SB, Oliver RP (2011) A novel mode of chromosomal evolution peculiar to filamentous Ascomycete fungi. Genome Biol. 12:R45.

Rouxel T, Balesdent MH (2010) Avirulence genes. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester.[DOI]


Cardin L, Vincenot L, Balesdent MH (2009). First report of Pilidium concavum on Bergenia crassifolia in France. Plant Dis. 93: 548.

Dilmaghani A, Balesdent MH, Didier JP, Wu C, Davey J, Barbetti MJ, Hua Li, Moreno-Rico O, Phillips D, Despeghel JP, Vincenot L, Gout L, Rouxel T (2009) The Leptosphaeria maculans-Leptosphaeria biglobosa species complex in the American continent. Plant Pathol. 58:1044-1058. [DOI]

Fudal I, Ross S, Brun H, Besnard AL, Ermel M, Kuhn ML, Balesdent MH, Rouxel T (2009). Repeat-induced point mutation (RIP) as an alternative mechanism of evolution towards virulence in Leptosphaeria maculans. Mol. Plant-Microbe Interact. 22:932-941

Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH, Blaise F, Grezes-Besset B, Rouxel T (2009) Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol. Microbiol. 71:851-863. [DOI]

Remy E, Meyer M, Blaise F, Simon UK, Kuhn D, Balesdent MH, Rouxel T (2009) A key enzyme of the Leloir pathway is involved in pathogenicity of Leptosphaeria maculans towards oilseed rape. Mol. Plant-Microbe Interact. 22:725-736.

Rouxel T, Duplessis S, Viaud M, Amselem J, Lebrun MH (2009) La génomique fongique. Biofutur 296:31-35.

Van de Wouw AP, Marcroft SJ, Barbetti MJ, Li H, Salisbury PA, Gout L, Rouxel T, Howlett BJ, Balesdent MH (2009) Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with ‘sylvestris-derived’ resistance, suggests involement of two resistance genes. Plant Pathol. 58:305-313. [DOI]

Vincent D, Balesdent MH, Gibon J, Claverol S, Lapaillerie D, Lomenech AM, Blaise F, Rouxel T, Martin F, Bonneu M, Amselem J, Dominguez V, Howlett BJ, Wincker P, Joets J, Lebrun MH, Plomion C (2009) Hunting down fungal secretomes using liquid-phase IEF prior to high resolution 2-DE. Electrophoresis 30:4118-4136. [DOI]


Remy E, Meyer M, Blaise F, Chabirand M, Wolff N, Balesdent MH, Rouxel T (2008) The Lmpma1 gene of Leptosphaeria maculans encodes a plasma membrane H+-ATPase isoform essential for pathogenicity towards oilseed rape. Fungal Genet. Biol. 45:1122-1134. [DOI]

Remy E, Meyer M, Blaise F, Simon UK, Kuhn D, Chabirand M, Riquelme M, Balesdent MH, Rouxel T (2008) The Lmgpi15 gene, encoding a component of the glycosylphosphatidylinositol anchor biosynthesis pathway, is required for morphogenesis and pathogenicity in Leptosphaeria maculans. New Phytol. 179:1105-1120. [DOI]

Vincenot L, Balesdent MH, Li H, Barbetti MJ, Sivasithamparam S, Gout L, Rouxel T (2008) Occurrence of a new subclade of Leptosphaeria biglobosa in Western Australia. Phytopathology 98:321-329. [DOI]


Fudal I, Ross S, Gout L, Blaise F, Kuhn ML, Eckert MR, Cattolico L, Bernard-Samain S, Balesdent MH, Rouxel T (2007). Heterochromatin-like regions as ecological niches for avirulence genes in the Leptosphaeria maculans genome: map-based cloning of AvrLm6. Mol. Plant-Microbe Interact. 20:459-470.

Gout L, Kuhn ML, Vincenot L, Bernard-Samain S, Cattolico L, Barbetti M, Moreno-Rico O, Balesdent MH, Rouxel T (2007) Genome structure impacts molecular evolution at the AvrLm1 avirulence locus of the plant pathogen Leptosphaeria maculans. Environ. Microbiol. 9:2978-2992.

Leflon M, Brun H, Eber F, Delourme R, Lucas M, Vallee P, Ermel M, Balesdent MH, Chevre, AM (2007). Detection, introgression and localization of genes conferring specific resistance to Leptosphaeria maculans from Brassica rapa into B. napus. Theor. Appl. Genet. 115:897-906.


Balesdent MH, Louvard K, Pinochet X, Rouxel T (2006) A large-scale survey of races of Leptosphaeriamaculans occurring on oilseed rape in France. Eur. J. Plant Pathol. 114:53-65.

Blaise F, Remy E, Meyer M, Zhou L, Narcy JP, Roux J, Balesdent MH, Rouxel T (2006). A critical assessment of Agrobacteriumtumefaciens-mediated transformation as a tool for pathogenicity gene discovery in the phytopathogenic fungus Leptosphaeriamaculans.FungalGenet.Biol. 44:123-138.

Delourme R, Chèvre AM, Brun H, Rouxel T, Balesdent MH, Dias JS, Salisbury P, Renard M, Rimmer SR (2006) Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur. J. Plant Pathol. 114:41-52.

Evans N, Fitt BDL, van den Bosch F, Huang Y, Pietravalle S, Eckert M, Papastamati K, Demon I, Karolewski Z, Rouxel T, Balesdent MH, Fudal I, Gout L, Brun H, Andrivon D, Bousset L, Gladders P, Pinochet X, Penaud A, Jedryczka M, Kachlicki P, Stachowiak A, Olechnowicz J, Podlesna A, Happstadius I, Meyer J (2006). SECURE - stem canker of oilseed rape: molecular methods and mathematical modeling to deploy durable resistance (QLK5-CT-2002-01813). Bull. OILB/SROP 29:43-48.

Gout L, Eckert M, Rouxel T, Balesdent MH (2006) Genetic variability and distribution of mating-type alleles in field populations of Leptosphaeria maculans from France. Appl. Environ. Microbiol. 72:185-191.

Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent MH, Rouxel T (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the Dothideomycete Leptosphaeria maculans. Mol. Microbiol. 60 :67-80.

Howlett BJ, Gardiner DM, Cozijnsen AJ, Wilson LM, Cattolico L, Pedras SMC, Rouxel T, Attard A, Gout L, Parlange F, Ross S, Balesdent MH (2006). Sequence analysis of two genomic regions of  Leptosphaeria maculans, the fungus that causes blackleg disease (Phoma stem canker) of Brassica napus. Acta Horticulturae 706:55-62.

Huang YJ, Li ZQ, Evans N, Rouxel T, Fitt BDL, Balesdent MH (2006) Fitness cost associated with loss of the AvrLm4 avirulence function in Leptosphaeria maculans (phoma stem canker of oilseed rape). Eur. J. Plant Pathol. 114 :77-89.

Kuhn ML, Gout L, Howlett BJ, Melayah D, Meyer M, Balesdent MH, Rouxel T (2006) Genetic linkage maps and genomic organization in Leptosphaeria maculans. Eur. J. Plant Pathol. 114 :17-31.

Sprague SJ, Balesdent MH, Brun H, Hayden HL, Marcroft SJ, Pinochet X, Rouxel T, Howlett BJ (2006) Major gene resistance in Brassica napus (oilseed rape) is overcome by changes in virulence of populations of Leptosphaeria maculans in France and Australia. Eur. J. Plant Pathol. 114 :33-40.

Stachowiak A, Olechnowicz J, Jedryczka M, Rouxel T, Balesdent MH, Happstadius I, Gladders P, Latunde-Dada A, Evans N (2006) Frequency of avirulence alleles in field populations of Leptosphaeria maculans in Europe. Eur. J. Plant Pathol. 114:67-75.

Sustainable strategies for managing Brassica napus (oilseed rape) resistance to Leptosphaeria maculans (Phoma stem canker). (2006) B.D.L. Fitt, N. Evans, B.J. Howlett & B.M. Cooke (Eds.), Springer, The Netherlands, 126 pp.


Attard A, Gout L, Ross S, Parlange F, Cattolico L, Balesdent MH, Rouxel T (2005) Truncated and RIP-degenerated copies of the LTR retrotransposon Pholy are clustered in a pericentromeric region of the Leptosphaeria maculans genome. FungalGenet.Biol. 42:30-41.

Balesdent MH, Barbetti MJ, Hua Li, Sivasithamparam K, Gout L, Rouxel T (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology 95:1061-107.

Eckert M, Gout L, Rouxel T, Blaise F, Jedryczka M, Fitt BDL, Balesdent MH (2005) Identification and characterisation of polymorphic minisatellites in the phytopathogenic ascomycete Leptosphaeria maculans. Curr.Genet. 47 :37-48.

Rouxel T, Balesdent MH (2005) The stem canker (blackleg) fungus, Leptosphaeriamaculans, enters the genomic era. Mol. Plant Pathol. 6:225-241.


Delourme R, Pilet-Nayel ML, Archipiano M, Horvais R, Tanguy X, Rouxel T, Brun H, Renard M, Balesdent MH (2004) A cluster of major specific resistance genes to Leptosphaeria maculans in Brassica napus. Phytopathology 94 :578-583.

Rouxel T, Mendes-Pereira E, Brun H, Balesdent MH (2004) Species complex of fungal phytopathogens: the Leptosphaeria maculans-L. biglobosa case study. In: Plant Genome: Biodiversity and Evolution. Vol. 2: Cryptogams. A.K. Sharma & A. Sharma (Eds.), Science Publishers, Inc., Enfield, USA, pp. 33–75.


Mendes-Pereira E, Balesdent MH, Brun H, Rouxel T (2003). Molecular phylogeny of the Leptosphaeria maculans-L. biglobosa species complex. Mycol. Res. 107:1287-1304.

Penaud A, Rouxel T, Gout L, Balesdent MH (2003). L’évolution des souches de Phoma et le contournement des résistances. Oléoscope 73: 12-15

Pinochet X, Mestries E, Penaud A, Delourme R, Chèvre AM, Renard M, Brun H, Bousset L, Balesdent MH, Rouxel T, Aubertot JN (2003). Towards a durable management of genetic resistances to Leptosphaeria maculans. OCLm.iano M, Horvais R, Tanguy X, Rouxel Tp8Fud A1ra E, Brun H, BalAM, Renard A, DelourmeH, Rouxe’évol M, Brun H, Schmie structure and reproent oA ten-yephahaeria in France and Australia. Eur. J. Plaindf po isofr>Leptn the Lepgeneti resis1eed rape, and circumvGenet. Evol. 27: :67-75.

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