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QIP

QUANTITATIVE IMMUNITY IN PLANTS

Quantitative Immunity in Plants : Research overview
 

The importance and complexity of pathogen perception and signaling pathways in the regulation and execution of plant immune responses have become apparent during the last years. Notably, R gene-mediated immunity has been shown to provide complete resistance in plant populations.

However R-gene mediated resistance is usually rapidly overcome by pathogens in the field, and it is never observed in response to certain pathogens. Additional forms of resistance have gained increasing attention for breeding purposes, such as quantitative resistance, but they are still poorly understood.
 

In the absence of qualitative resistance, an incomplete resistance designated as quantitative resistance is often observed, leading to the reduction rather than absence of disease. A number of loci conferring quantitative resistance were found durable, but very little is known on the molecular mechanisms underlying quantitative immune responses in plants. 

 

 

 

 

 

 

 

 

 

 

 






 

Figure legend :

 

LEFT : A typical R-gene mediated resistance response in the wild, observed on oaks infected by the sudden oak death pathogen Phytophthora ramorum (Photo credits: D. Rizzo, National Science Foundation); the scheme below illustrates in a simplified manner the underlying molecular bases (brown = pathogen cell, green= plant cell).

 

RIGHT: Typical quantitative resistance response observed in the wild (Photo credits: G. Gilbert, National Science Foundation), with a simplified model of the hypothetical molecular bases shown below. Recommended reading:Roux F, Voisin D, Badet T, Balagué C, Barlet X, Huard-Chauveau C, Roby D, Raffaele S. Resistance to phytopathogens e tutti quanti: placing plant quantitative disease resistance on the map. Mol Plant Pathol. 2014 Jun;15(5):427-32.

To decipher the molecular mechanisms associated with quantitative immunity, we are developing a multidisciplinary research programme focused on the use of the model plant Arabidopsis thaliana challenged with the bacterial pathogen Xanthomonas campestris or the fungal pathogen Sclerotinia sclerotiorum. These are two major pathogens of Brassica plants (rapeseed, cabbage, turnip,  mustard...) with distinct lifestyles allowing to explore the diversity of quantitative immunity in plants.

Xanthomonas species are a major constraint for seed and plant production in vegetables crops, especially in Brassica and Solanaceae, causing black rot and bacterial spot, respectively.

 

Plant pathogenic Xanthomonas species have a wide geographical distribution, causing reduction in yield and quality and are expected to increase in incidence and range under climate change. Beside resistance gene deployment, there is no other efficient method to control Xanthomonas species. Therefore, we adopted an interdisciplinary strategy using molecular genetics and evolutionary biology in collaboration with Fabrice Roux (LIPM, Toulouse) for the identification of key components of QDR to Xanthomonas. Our aims are the following: (i) decipher the resistance pathways operating in QDR and their potential placement in known disease resistance pathways; (ii) elucidate the ecological and evolutionary forces shaping the natural genetic diversity observed at these QDR genes.

The white and stem mold pathogen Sclerotinia sclerotiorum is a generalist fungal pathogen, infecting a broad range of host species (>400) in nature. It is among the most devastating plant pathogens worldwide and causes disease on many crops including soybean, rapeseed, sunflower and most vegetables, but very limited solutions for the genetic control of the disease exist to date. S. Sclerotiorum naturally infects wild and cultivated Brassica species, including the model plant Arabidopsis thaliana.  We are developing a multidisciplinary research programme centered on the A. thaliana – S. sclerotiorum to address the following questions: (i) Which plant genes are involved in quantitative immunity to Sclerotinia? How do they contribute to disease resistance? (ii) What are the mechanisms used by Sclerotinia to colonize its hosts? How did they evolve ?

Figure legend : Illustration of the two main pathosystems used in the group. Left picture: A Xanthomonas campestris (Xcc) bacterium culture in vitro; Right picture: Sclerotinia sclerotiorum (Ss) fungus cultures in vitro. Middle: A composite image of an Arabidopsis thaliana plant showing symptoms caused by Xcc on the left side and by Ss on the right side.

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RESEARCH THEMES

RKS1 dependent immunity pathways
 

We recently identified in Arabidopsis thaliana by map-based cloning and Genome Wide Association (GWA) mapping, the RKS1 gene underlying a major QTL controlling resistance to most pathovars of Xcc originally identified on cruciferous cultivated plants. This gene encodes an atypical kinase. The functional analysis of this gene (and its molecular variants) and the characterization of the regulatory pathway(s) controlling and controlled by RKS1, are under investigation. RKS1 (and other candidate genes) will also be directly tested in a high throughput manner, and through a non-GMO approach, for their potential value (alleles or orthologs) to control pathogens in plants of agronomic interest (Brassica, tomato, pepper) in breeding programs



















Selected recent publications :

ZRK atypical kinases: emerging signaling components of plant immunity. Roux F, Noël L, Rivas S, Roby D. New Phytol. 2014 Aug;203(3):713-6.

Huard-Chauveau C, Perchepied L, Debieu M, Rivas S, Kroj T, Kars I, Bergelson J, Roux F, Roby D. An atypical kinase under balancing selection confers broad-spectrum disease resistance in Arabidopsis. PLoS Genet. 2013;9(9):e1003766. doi: 10.1371/journal.pgen.1003766. Epub 2013 Sep 12. PubMed PMID: 24068949; PubMed Central PMCID: PMC3772041.

 

Contact : Dominique Roby

Genetic and molecular bases of resistance in the natural pathosystem A. thaliana-Xanthomonas

Xanthomonas is one of a few known natural pathogens of A. thaliana, and is highly prevalent in natural populations of A. thaliana. In collaboration with Fabrice Roux (LIPM, Toulouse) and Joy Bergelson (University of Chicago), we identified strains of Xanthomonas in natural populations of Arabidopsis. 

 

Now our research aims are to (i) finely map by GWA mapping genomic regions associated with natural variation of quantitative resistance to Xc, (ii) functionally validate candidate genes, and (iii) elucidate the ecological and evolutionary forces shaping the natural genetic diversity observed for these quantitative resistance genes.

Selected recent publications :

Debieu M, Huard-Chauveau C, Genissel A, Roux F, Roby D. Quantitative disease resistance to the bacterial pathogen Xanthomonas campestris involves an Arabidopsis immune receptor pair and a gene of unknown function. Mol Plant Pathol. 2016 May;17(4):510-20.

Le Roux C, Del Prete S, Boutet-Mercey S, Perreau F, Balagué C, Roby D, Fagard  M, Gaudin V. The hnRNP-Q protein LIF2 participates in the plant immune response.  PLoS One. 2014 Jun 10;9(6):e99343.

Contact : Dominique Roby

Characterization of molecular mechanisms underlying Arabidopsis quantitative immunity to the fungus Sclerotinia sclerotiorum

Using worldwide Arabidopsis thaliana populations, we documented extensive variation in quantitative immunity to S. sclerotiorum, opening the way to the molecular characterization of plant and pathogen determinants underlying this interaction. The overall objectives of this project are to identify which plant genes are involved in quantitative immunity to Sclerotinia and understand how they contribute to disease resistance ?

 

For this, we are developing notably genome wide association mapping, functional genetics, transcriptomics and high throughput quantitative phenotyping approaches.

Figure legend:

 

A) The range of symptoms on Arabidopsis thaliana leaves inoculated by S. sclerotiorum with an illustration of image processing used to quantify disease.

 

B) Molecular structure of a fungal protein predicted to facilitate host colonization.

 

C) Genome wide association mapping of plant genes contributing to quantitative disease resistance, with a world map indicating the origin of plant accessions used. 

Selected recent publications :

Le Roux C, Huet G, Jauneau A, Camborde L, Trémousaygue D, Kraut A, Zhou B, Levaillant M, Adachi H, Yoshioka H, Raffaele S, Berthomé R, Couté Y, Parker JE, Deslandes L. A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell. 2015 May 21;161(5):1074-88.

Roux F, Voisin D, Badet T, Balagué C, Barlet X, Huard-Chauveau C, Roby D, Raffaele S. Resistance to phytopathogens e tutti quanti: placing plant quantitative disease resistance on the map. Mol Plant Pathol. 2014 Jun;15(5):427-32.

Bozkurt TO, Richardson A, Dagdas YF, Mongrand S, Kamoun S, Raffaele S. The Plant Membrane-Associated REMORIN1.3 Accumulates in Discrete Perihaustorial Domains and Enhances Susceptibility to Phytophthora infestans. Plant Physiol. 2014 May 7;165(3):1005-1018.

Contact : Sylvain Raffaele

Thigmoimmunity: contribution of mechanical signal perception to quantitative immunity against Sclerotinia

During their interaction with plants, and prior to plant tissue penetration or degradation, fungal pathogens develop important mechanical loads susceptible to emit Mechanical loads are due to the tremendous turgor pressure created by water in the vacuole of appressoria and fungal cell wall mechanical preperties. This mechanical stress is generally sufficient to penetrte plant cells. Mechanosensing occurs at the plant cell level and relies on the internal mechanical state of the cell.

Recent studies demonstrated the link between mechanosensing and plant immune response to B. cinerea in Arabidopsis thaliana: plants submitted to MS exhibited higher resistance to fungal infection suggesting a priming effect operated by sterile mechanosensing. Future work should aim at addressing whether mechanosensing for fungal contact or penetration per se, in addition to PAMP perception, leads to enhanced plant immunity.

Links :

http://journal.frontiersin.org/article/10.3389/fpls.2016.00422/full

Mechanoperception and thigmomorphogenesis at INRA

http://www6.ara.inra.fr/piaf_eng/About/Teams/MECA

Selected recent publications :

Mbengue M, Navaud O, Peyraud R, Barascud M, Badet T, Vincent R, Barbacci A, Raffaele S. Emerging Trends in Molecular Interactions between Plants and the Broad Host Range Fungal Pathogens Botrytis cinerea and Sclerotinia sclerotiorum.  Front Plant Sci. 2016 Mar 31;7:422.

Barbacci A, Magnenet V, Lahaye M. Thermodynamical journey in plant biology. Front Plant Sci. 2015 Jun 30;6:481.

Contact : Adelin Barbacci

Fungal adaptations to plant quantitative immunity

Fungal plant pathogens are major and rising threats for global food security and environment sustainability. Generalist fungal pathogens such as S. sclerotiorum, infecting a broad range of host species in nature, are among the most devastating plant pathogens worldwide. The range of hosts that pathogens can infect in nature is a key determinant of the emergence and spread of diseases. How pathogens evolve the ability to infect many diverse hosts remains enigmatic. Through this project, we are addressing the following questions: What are the mechanisms used by Sclerotinia to colonize its hosts? What are the evolutionary processes that shaped the extent fungal virulence and plant immunity processes ? This work relies mostly on comparative genomics, transcriptomics, phylogeny, and systems biology approaches.

Figure legend :

 

A) S. sclerotiorum colonizing an Arabidopsis leaf imaged using a strain expressing the green fluorescent protein.

 

B) A Circos diagram illustrating comparative genomics of fungal species related to S. sclerotiorum.

 

C) A phylogenetic tree of fungi from the Sclerotiniaceae family.

Selected recent publications :

Dong S, Raffaele S, Kamoun S. The two-speed genomes of filamentous pathogens:  waltz with plants. Curr Opin Genet Dev. 2015 Dec;35:57-65. doi: 10.1016/j.gde.2015.09.001.

Badet T, Peyraud R, Raffaele S. Common protein sequence signatures associate with Sclerotinia borealis lifestyle and secretion in fungal pathogens of the Sclerotiniaceae. Front Plant Sci. 2015 Sep 24;6:776.

Guyon K, Balagué C, Roby D, Raffaele S. Secretome analysis reveals effector candidates associated with broad host range necrotrophy in the fungal plant pathogen Sclerotinia sclerotiorum. BMC Genomics. 2014 May 4;15:336.

Contact : Sylvain Raffaele

Collaborations

  • Bruno Grezes-Besset; Biogemma Mondonville

  • Fabrice Roux; LIPM Toulouse

  • Sébastien Mongrand; LBM Bordeaux

  • John P. Clarkson; University of Warwick (UK)

  • Richard P. Oliver, Mark Derbyshire, Matthew Denton-Giles; Curtin University (Aus)

  • Lone Buschwaldt; University of Saskatchewan (Can)

  • Jan van Kan, Michael Siedl; Wageningen University (NL)

  • Sophien Kamoun; The Sainsbury Laboratory Norwich (UK)

  • Jean-Charles Portais, Pierre Millard; LISBP Toulouse

  • Ludovic Cottret, Lucas Marmiesse; LIPM Toulouse

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Funding

  • Contract ANR-Investissement d’Avenir LabEx TULIP, 2011-2020, Coordinators ROBY Dominique /Danchin Etienne, 9 000 k€

  • Contract Marie Curie CIG grant – European commission FP7, « Identification of Sclerotinia sclerotiorum Effector Proteins mediating virulence on Arabidopsis thaliana ecotypes (SEPAraTE) », 2013-17, Coordinator Sylvain Raffaele, 100 k€

  • Contract ERC Starting Grant Conseil Européen « Understanding White mold disease quantitative resistance using natural variation (VariWhiM) », scientific coordinator Sylvain Raffaele, 2013-2018, 1500 k€.

  • TULIP “New Frontiers” project “Virulence function and evolution of Sclerotinia signals manipulating plant RNA silencing pathways (ScleRNAi)”, Coordinator S. Raffaele, 2014-16, 119 k€.

  • Contract ANR RIPOSTE “Exploitation of pathogen quantitative resistance diversity to improve disease tolerance in crops”, Coordinator D. Roby, 2014-2018, 248 k€.

  • Project Plant Health & Environment Division INRA – SPE. “Identification of genetic factors underlying potential disease outbreaks of the bacterial pathogen Xanthomonas campestris” PI : Fabrice Roux, 2016 – 2017, 40k€.

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