Dr. Salim BOURRAS
We are investigating how pathogens cause disease by interacting with their host and other pathogens from the local pathobiome. We are focusing on interactions between foliar fungal pathogens of cereals (mildews, rusts, and blotches), and the particular role of mobile molecules such as effectors and small RNAs in regulating disease interactions and tradeoffs in disease resistance responses. We aim at producing translational research that probes fundamental aspects in plant-pathogen interactions to set the ground for field applications.
MECHANISMS OF R GENE SUPPRESSION BY FUNGAL PATHOGENS IN CEREALS
Our first line of research aims at understanding the mode of action of pathogen encoded suppressors of major R genes in wheat. We also want to understand their broader impact on intra-species interactions and host-specificity of cereal mildews. In a continued close collaboration with the group of Prof. Beat Keller at the University of Zurich (Switzerland), we are characterizing the SvrPm3 RNase-like effector from wheat powdery mildew, which is capable of suppressing the resistance response induced upon AvrPm3 recognition by the wheat Pm3 resistance gene. Active SvrPm3 variants are found in all mildew races worldwide, and they are most frequently present in combination with active forms of the AvrPm3 genes they suppress. We are currently characterizing 11 additional haplotype variants of this gene, and investigating the molecular and biochemical mechanisms underlying its mode of action.
Figure 1. SvrPm3 is a quantitative suppressor of the AvrPm3-Pm3 interaction.
(A) Suppression of the AvrPm3-Pm3 induced hypersensitive cell death (HR) response in the heterologous Nicotiana benthamiana host. HR is revealed using HSR imaging technology allowing accurate quantification of cell death. (B) HR quantification data showing statistically significant differences when the active suppressor is added to an AvrPm3-Pm3 combination. (C) Three dimensional structural modelling suggests SvrPm3 folds like a fungal ribonuclease (RNase)-like protein. [Credits: Carol Kälin, Lukas Kunz, Salim Bourras]
THE MOLECULAR BASIS OF DISEASE INTERACTIONS IN CEREALS
Our second line of research aims at understanding the contribution of pathogen-pathogen interactions and fungal pathobiomes to multi-pathogen response and disease resistance in cereals. We are focusing on major foliar/stem diseases of wheat as a working system which include primarily powdery mildews, septoria leaf blotches, and rusts. Our working hypothesis is that pathogen-pathogen interactions impose tradeoffs of resistance responses in the host, and actively modify the local pathobiome. Such interactions are likely to be mediated by mobile molecules that can be directed to the extracellular host/microbial environment, and we propose that pathogen effectors and small RNAs are highly relevant candidates to play such role. We are currently probing these hypotheses using lab controlled metagenomics and experimental evolution approaches, and employing large scale functional screens. We are also probing these questions using field metagenomics and population genomics approaches essentially in wheat powdery mildew and Zymoseptoria tritici.
Figure 2. Natural co-occurrence of powdery mildew, septoria leaf blotch, and leaf rust.
Natural co-occurrence of powdery mildew (white arrows), septoria leaf blotch (yellow arrows), and leaf rust (red arrows) on wheat. (A-B) Natural co-occurrence of powdery mildew and septoria leaf blotch diseases. (B) Magnification from (A) illustrating typical long conservation fruiting bodies (black dots) from mildew (chasmothecia on white mycelim) and septoria (pycnidia on necrotic lesion). (C) Natural co-occurrence of septoria leaf blotch and leaf rust. (D) Natural co-occurrence of all three diseases. Picture were taken during the 2018 field season, near Zurich (Switzerland). [Credits: Carol Kälin, Salim Bourras]
DEVELOPMENT OF FIELD APPLICATIONS BASED ON PATHOGEN INFORMATION
Our third line of research aims at exploring possible field application based on pathogen information. In collaboration with the Agricultural Research Council (ARC, Pretoria, South Africa) and the University of Zurich (Prof. Beat Keller lab, Switzerland) we are establishing a field meta-transcriptomics approach for monitoring pathogen populations (primarily powdery mildew). We are particularly interested in applying information on Avr gene content and haplotype frequencies in the pathogen to rationalize R gene deployment, and cultivar development in the host. We have recently established a working procedure/pipeline for field sampling, Avr mining, and meta-transcriptome analysis, which we would like to apply systematically in collaboration with wheat growers in South Africa.
Figure 3. A subset of wheat powdery mildew effector families is highly active in the field.
Individual powdery mildew effector gene families are represented with circles. The size of each circle is relative to the size of the family. Differentially active families are highlighted in “red” (left panel) and “blue” (right panel). [Credits: Coraline Praz, Carol Kälin, Manuel Poretti, Barend Wentzel, Salim Bourras]
We are also analyzing meta-data from the field in light of pathobiome composition and the host response to multi-pathogen attack. In particular, we are mining 30 years of systematic disease scoring data for leaf spot, blotches, mildews, brown rust, yellow rust, and black spot, on several cereals (including winter wheat, spring wheat, triticale, rye, Oat, winter barley, and spring barley) in collaboration with the Swedish Board of Agriculture. We are analyzing this data in light of possible synergistic or antagonistic trends linked to the co-occurrence of several pathogens, and how they co-exist and persist in the same ecological-niches.
CO-WORKERS AND COLLABORATORS
- Carol Kälin (Master student) [Beat Keller lab, University of Zurich, Switzerland]
- Lukas Kunz (PhD student) [Beat Keller lab, University of Zurich, Switzerland]
- Manuel Poretti (PhD student) [Thomas Wicker lab, University of Zurich, Switzerland]
- Lukas Meile (PhD student) [Andrea Sanchez-Vallet lab, ETH Zurich, Switzerland]
- Dr. Andrea Sanchez-Vallet [Bruce McDonald lab, ETH Zurich, Switzerland]
- Dr. Barend Wentzel [Agricultural Research Council (ARC), South Africa]
- Dr. Scott Sydenham [Agricultural Research Council (ARC), South Africa]
- Anders Arvidsson [Swedish Board of Agriculture]
DEPARTMENT OF PLANT AND MICROBIAL BIOLOGY. University of Zurich. Switzerland.Prof. Beat Keller
INSTITUTE OF INTEGRATIVE BIOLOGY. ETH Zurich. Switzerland.Prof. Bruce McDonald, Dr. Andrea Sanchez-Vallet.
AGRICULTURAL RESEARCH COUNCIL (ARC). Crop Improvement Division. Pretoria. South Africa.Dr. Barend Wentzel, Dr. Scott Sydenham
SWEDISH BOARD OF AGRICULTUREAnders Arvidsson
16# Bourras S*¤, Kunz L*, Xue M*, Praz CR, Müller MC, Kälin C, Schläfli M, Ackermann P, Flückiger S, Parlange F, Menardo F, Schaefer LK, Ben David R, Roffler S, Oberhaensli S, Widrig V, Lindner S, Isaksson S, Wicker T, Yu D¤ and Keller B¤(2019). The AvrPm3-Pm3 effector-NLR interactions control both race-specific resistance and host-specificity of cereal mildews on wheat. Nature Communications. DOI: 10.1038/s41467-019-10274-1. In press. *joint first authors.¤corresponding authors
15# Sánchez-Martín J, Bourras S and Keller B (2018). Diseases affecting wheat and barley: powdery mildew. Integrated disease management of wheat and barley. Burleigh Dodds Science Publishing. doi: 10.19103/AS.2018.0039.04. [BOOK CHAPTER]
14# Müller MC, Praz CR, Alexandros GS, Menardo F, Kunz L, Schudel S, Oberhänsli S, Poretti M, Wehrli A, Bourras S, Keller B and Wicker T (2018). A chromosome-scale genome assembly reveals a highly dynamic effector repertoire of wheat powdery mildew. New Phytologist 221:2176-2189. doi:DOI:10.1111/nph.15529.
13# Bourras S, Praz CR, Spanu PD and Keller B (2018). Cereal powdery mildew effectors: a complex toolbox for an obligate pathogen. Current Opinion in Microbiology 46:26-33. doi: 10.1016/j.mib.2018.01.018.
12# Praz CR, Menardo F, Robinson MD, Müller MC, Wicker T, Bourras S* and Keller B* (2018). Non-parent of origin expression of numerous effector genes indicates a role of gene regulation in host adaption of the hybrid triticale powdery mildew pathogen. Frontiers in Plant Science 9:49. doi: 10.3389/fpls.2018.00049. *corresponding authors.
11# McNally KE, Menardo F, Lüthi L, Praz CR, Müller MC, Kunz L, Ben-David R, Chandrasekhar K, Dinoor A, Cowger C, Meyers E, Xue M, Zeng F, Gong S, Yu D, Bourras S* and Keller B* (2018). Distinct domains of the AVRPM3A2/F2 avirulence protein from wheat powdery mildew are involved in immune receptor recognition and putative effector function. New Phytologist 218:681-695. doi: 10.1111/nph.15026. *corresponding authors.
10# Praz CR*, Bourras S*, Zeng F, Sánchez-Martín J, Menardo F, Xue M, Yang L, Roffler S, Böni R, Herren G, McNally KE, Ben-David R, Parlange F, Oberhaensli S, Flückiger S, Schäfer L, Wicker T, Yu D and Keller B (2017). AvrPm2 encodes an RNase-like avirulence effector which is conserved in the two different specialized forms of wheat and rye powdery mildew. New Phytologist 213:1301-1314. doi: 10.1111/nph.14372. *joint first authors.
9# Meyer M, Bourras S, Gervais J, Labadie K, Cruaud C, Balesdent M-H, Rouxel T. (2017) Impact of biotic and abiotic factors on the expression of fungal effector-encoding genes in axenic growth conditions. Fungal Genetics and Biology 99:1-12. doi: 10.1016/j.fgb.2016.12.008
8# Feehan JM, Scheibel KE, Bourras S, Underwood W, Keller B and Somerville SC. (2017) Purification of High Molecular Weight Genomic DNA from Powdery Mildew for Long-Read Sequencing. JoVE. 31:121. doi: 10.3791/55463.
7# Bourras S, McNally KE, Müller MC, Wicker T and Keller B. (2016) Avirulence genes in cereal powdery mildews: the gene-for-gene hypothesis 2.0. Frontiers in Plant Science 7:241. doi:10.3389/fpls.2016.00241.
6# Menardo F, Praz CR, Wyder S, Ben-David R, Bourras S, Matsumae H, McNally KE, Parlange F, Riba A, Roffler S, Schaefer LK, Schimizu KK, Valenti L, Zbinden H, Wicker T and Keller B. (2016) Hybridization of powdery mildew strains gives rise to pathogens on novel agricultural crop species. Nature Genetics 48(2):201-205. doi: 10.1038/ng.3485.
5# Bourras S*, McNally KE*, Ben-David R, Parlange F, Roffler S, Praz CR, Oberhaensli S, Menardo F, Stirnweis D, Frenkel Z, Schaefer LK, Flückiger S, Treier G, Herren G, Korol AB, Wicker T and Keller B. (2015) Multiple avirulence loci and allele-specific effector recognition control the Pm3 race-specific resistance of wheat to powdery mildew. Plant Cell 27: 2991-3012. doi: 10.1105/tpc.15.00171. *joint first authors.
4# Bourras S, Rouxel T, Meyer M. (2015) Agrobacterium tumefaciens Gene Transfer: How a plant pathogen hacks the nuclei of plant and nonplant organisms. Phytopathology 105:1288-301. doi: 10.1094/PHYTO-12-14-0380-RVW.
3# Parlange F, Roffler S, Menardo F, Ben-David R, Bourras S, McNally KE, Oberhaensli S, Stirnweis D, Buchmann G, Wicker T and Keller B. (2015) Genetic and molecular characterization of a locus involved in avirulence of Blumeria graminis f. sp. tritici on wheat Pm3 resistance alleles. Fungal Genetics and Biology. 82:181-92. doi: 10.1016/j.fgb.2015.06.009.
2# Bourras S, Meyer M, Grandaubert J, Lapalu N, Fudal I, Linglin J, Ollivier B, Blaise F, Balesdent M-H and Rouxel T. (2012). Incidence of genome structure, DNA ssymmetry, and cell physiology on T-DNA integration in chromosomes of the phytopathogenic fungus Leptosphaeria maculans. G3: Genes,Genomes,Genetics 2:891-904
1# Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S et al. (2011) Diversification of effectors within compartments of the Leptosphaeria maculans genome affected by RIP mutations. Nature Communications 2: 202.