We study molecular plant-microbe interactions particularly those involving filamentous plant pathogens such as the oomycete Phytophthora.

Current research

Oomycete genomics. We continue to be actively involved in several genome sequencing projects (Tyler et al. 2006, Science 313:1261), particularly the P. infestans and P. capsici genome projects. Our group contributes to annotations and interpretation of the genomes, and provides complementary resources such as cDNA sequences and proteomics data sets. Click here for more on oomycete genomics.

Effector evolution in the P. infestans species complex. We started cataloguing the effector secretome of species phylogenetically related to P. infestans but that infect unrelated host plants. This has resulted in some interesting insights into effector evolution and adaptation to the distinct cellular environments of the respective hosts.

RXLR effector trafficking. Our objective is to unravel the host translocation machinery of oomycetes. To this purpose, a number of candidate secreted chaperone proteins that may function in delivery of cytoplasmic effectors inside host cells are being studied. See the model of Morgan and Kamoun, Curr Opin Microbiol 2007, 10:332

RXLR effector function. Our group studies the structure and function of several RXLR effectors, including P. infestans Avr3a. Extensive structure-function analyses have been performed to gain insight in the molecular basis of AVR3a effector activities. Distinct amino acids of AVR3a condition R3a hypersensitivity and cell death suppression. Other activities include characterization of plant targets of Avr3a and other RXLR effectors (in collaboration with Paul Birch at the Scottish Crop Research Institute).

Novel P. infestans avirulence genes AvrBlb1 and AvrBlb2. We cloned the avirulence genes AvrBlb1 and AvrBlb2 that match two late blight resistance genes, Rpi-blb1 and Rpi-blb2, that have entered the commercialization pipeline. The discovered effectors are providing mode of action information as well as a tool for monitoring pathogen populations for virulence.

Effector-omics and potato breeding. In collaboration with Vivianne Vleeshouwers and Edwin van der Vossen at the Laboratory of Plant Breeding, Wageningen University, effector expression libraries are used to identify and characterize novel sources of resistance to P. infestans in Solanum. Selected lines that respond to specific P. infestans effectors have been incorporated into a breeding program. This has accelerated the cloning and profiling of novel resistance genes and provides a compelling example of translational genomics research (Vleeshouwers et al. 2006 Mol Plant Pathol 7:499).

Role of P. infestans protease inhibitors and their target proteases in disease. Current activities focus on understanding how inhibition of the tomato proteases PIP1 and P69B by P. infestans apoplastic effectors affects disease progress and expand on earlier findings (Tian et al. 2004, J Biol Chem 279:26370; 2005, Plant Physiol 138:1785; 2007, Plant Physiol 143:364).

Molecular basis of flower mimicry by the rust fungus Puccinia monoica. P. monoica is a spectacular plant pathogenic fungus that triggers the formation of flower-like structure in its host plant Boechera stricta. Although much ecological research has been performed on rust pseudoflowers, this system has not been investigated at a molecular or genomic level. We aim at understanding how P. monoica manipulates its host and identifying the effectors that reprogram host morphology and physiology (in collaboration with Saskia Hogenhout).

Past research highlights

Kamoun and collaborators cloned and characterized the elicitin multigene family of Phytophthora infestans (Kamoun et al. 1997, MPMI 10:13; Huitema et al. 2005, MPMI 18:183). The major elicitin INF1 confers hypersensitivity and avirulence in some plants (Kamoun et al. 1998, Plant Cell 10:1413). INF1 is routinely used by researchers worldwide in basic studies on plant defense. Also, the inf1 gene was used in the first experiments demonstrating RNAi and internuclear transfer of gene silencing in oomycetes (Kamoun et al. 1998, Plant Cell 10:1413; van West et al. 1999, Mol Cell 3:339).

Our group pioneered the design and application of functional genomics pipelines for the identification of novel secreted protein genes from sequence data. This approach, first described by Torto et al. (2003, Genome Res 13:1675) and reviewed in Kamoun (2006, Annu Rev Phytopathol 44:41), resulted in the identification of several novel classes of oomycete effectors.

Kamoun and his students published the first report of a protease inhibitor in any plant-associated microbe (Tian et al. 2004, J Biol Chem 279:26370). Since this publication, protease inhibitors have been reported in two plant pathogenic fungal species (Cladosporium fulvum and flax rust) suggesting that inhibition of plant proteases by pathogens is a general counterdefense mechanism.

Kamoun was one of the scientists directly involved in the discovery of the RXLR host translocation motif of oomycete effectors (Rehmany et al. 2005, Plant Cell 17:1839; Armstrong et al., 2005, PNAS 102:7766; Birch et al. 2006, Trends Microbiol 14:8; Morgan and Kamoun 2007, Curr Opin Microbiol 10:332). This was followed by the demonstration that the RXLR domain functions in the human parasite Plasmodium suggesting that plant and animal eukaryotic pathogens share similar mechanisms for effector secretion inside host cells (Bhattacharjee et al. 2006, PLoS Pathog 2:e50).

With our collaborators at the Scottish Crop Research Institute, we discovered Avr3a, the first avirulence gene to be cloned from P. infestans (Armstrong et al., 2005, PNAS 102:7766), using an association genetics strategy detailed in an earlier report (Bos et al. 2003, New Phytol 159:63). A follow-up paper established that Avr3a is a modular protein that suppresses the hypersensitive cell death induced by INF1 elicitin (Bos et al. 2006, Plant J 48:165). This was the first report of a cell death suppressor from a filamentous plant pathogen (discussed in Kamoun 2007, Curr Opin Plant Biol 10:358).

Our group demonstrated that both apoplastic and cytoplasmic oomycete effectors are the target of positive selection (adaptive evolution) (Liu et al. 2005, Mol Biol Evol 22:659; Win et al. 2007, Plant Cell 19:2349). This work stands out as a clear illustration of positive selection mainly affecting the effector region of the proteins, which is consistent with the modular structure of the effectors.

We have been taking a leading role in community efforts to obtain high-quality sequences of the genomes of several oomycetes species, particularly P. infestans in collaboration with the MIT Broad Institute, and Phytophthora capsici in collaboration with the Department of Energy Joint Genome Institute (reviewed in Lamour et al. 2007, FEMS Microbiol Letters 274:1). Prior to these activities, we published one of the first cDNA sequencing projects for a plant pathogen (Kamoun et al. 1999, Fungal Genet Biol 28:94) and were among the key members of the Syngenta Phytophthora Genomics Consortium (Randall et al. 2005, MPMI 18:229). Also, with funding from NSF, Kamoun and collaborators established and maintained the Phytophthora Functional Genomics Database (PFGD) (Gajendran et al. 2006, Nucleic Acids Res 34:D465).

In collaboration with several labs, we contributed to a number of technological developments with applications in both basic and applied biology (Kanneganti et al. 2007, Plant J 50:149; Pons et al. 2006, Systematic Biol 55:595; Matsumura et al. 2003, PNAS 100:15718; Kamoun et al. 2003, MPMI 16:7).

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