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Functional Genomics of Phytophthora Infestans Effectors and Solanum Resistance Genes

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Functional Genomics of Phytophthora Infestans Effectors and Solanum Resistance Genes Functional Genomics of Phytophthora infestans Effectors and Solanum Resistance Genes Nicolas Champouret Thesis committee Thesis supervisors Prof. dr. Richard G.F. Visser Professor of Plant Breeding Wageningen University Prof. dr. Evert Jacobsen Professor of Plant Breeding Wageningen University Thesis co-supervisor Dr. Vivianne G.A.A. Vleeshouwers Researcher Wageningen University Other members Prof. Dr. Ir. Pierre J. G. M. de Wit, Wageningen University, The Netherlands Prof. Dr. Martien Groenen, Wageningen University, The Netherlands Prof. Dr. Ir. Corné Pieterse, Utrecht University, The Netherlands Dr. Brande Wulff, The Sainsbury Laboratory, Norwich, UK This research was conducted under the auspices of the Graduate School of Experimental Plant Sciences. II Functional Genomics of Phytophthora infestans Effectors and Solanum Resistance Genes Nicolas Champouret Thesis submitted in partial fulfillment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. dr. M.J. Kropff in the presence of the Thesis Committee appointed by the Doctorate Board to be defended in public on Wednesday 9 June 2010 at 4 p.m. in the Aula. III Nicolas Champouret Functional Genomics of Phytophthora infestans Effectors and Solanum Resistance Genes. 162 pages Thesis, Wageningen University, Wageningen, NL (2010) With references, with summaries in Dutch and English ISBN 978-90-8585-658-0 IV CONTENTS Abstract VII Chapter 1 1 General introduction Chapter 2 15 Phytophthora infestans Isolates Lacking Class I ipiO Variants Are Virulent on Rpi-blb1 Potato Chapter 3 43 Evolutionary and Functional Analyses Reveal a Diverse Family of R2 Late Blight Resistance Genes in Mexican Solanum Species Chapter 4 75 Diversity of PiAvr2/PexRD11 and R2 gene families underpins co-evolution between Phytophthora infestans and Mexican Solanum species Chapter 5 90 Functional allele-mining with Avr3a reveals active R3a in S. stoloniferum and hints at two centres of R3a evolution in Mexico and Argentina Chapter 6 117 General discussion References 127 Summary 139 Samenvatting 142 Acknoledgements 147 About the author 151 V VI ABSTRACT Potato (Solanum tuberosum L.) is nowadays the most important non-cereal food crop in the world. It is prone to huge annual losses due to late blight, the disease caused by the oomycete pathogen Phytophthora infestans. Modern management of late blight necessitates the use of multiple resistance (R) genes, which requires efficient pipelines for identification, isolation and characterization of R genes. This thesis employs effectoromics, i.e. the use of effectors (pathogenic secreted protein) to probe corresponding R gene(s) in a host plant and sort out their functional redundancy and specificity. Using cytoplasmic RXLR effectors of P. infestans to probe resistant Solanum germplasm for late blight R genes, we were able to: (i) assess the biodiversity of Avr-blb1, characterize the genomic structure of virulent P. infestans isolates on Rpi-blb1 plants and thus provide a technical solution for long-term disease management; (ii) identify the centre of origin of R3a, characterize R3a gene homologues and a functional R gene (Rpi-sto2), and (iii) uncover the potential co-evolution at both R and Avr side for the R2/PiAvr2-PexRD11 interactions, providing more diversity and specificity of R2 homologues, which may be valuable for potato breeding. VII VIII General Introduction CHAPTER 1 General Introduction Part of this introduction will be published in: Plants and oomycetes, an intimate relationship: Co-evolutionary principles and impact on agricultural practice (submitted). Hendrik Rietman 1,3, Nicolas Champouret 1,3, Ingo Hein 2, Rients Niks 1 and Vivianne G.A.A. Vleeshouwers 1 1 Wageningen UR Plant Breeding, P.O. Box 386, 6700 AJ Wageningen, The Netherlands, 2 Scottish Crop Research Institute, Genetics Programme, Invergowrie – Dundee DD2 5DA, United Kingdom, 3 The Graduate School Experimental Plant Sciences, Wageningen University, Wageningen, The Netherlands Chapter 1 Potato Potato (Solanum tuberosum L.) is currently, the most consumed crop worldwide by men after wheat and rice. In the early ages, potato was already an important food crop for people inhabiting the South American Andes region, and excavated food plant remains from archaeological sites date back as far as 2500 BC and 5000 BC (Hawkes 1990). The exact origin of European potato is still unclear, since Chile and Peru are both competing for this honour. However, potato was brought from South America to Europe in the late 16th century, in Spain (1570) and England (between 1588 and 1593) (Hawkes 1990). Since then European potato breeding came up and nowadays, the European Cultivated Potato Database (ECPD) records 4,100 cultivated varieties. In 2005, the estimated potato cultivation area was almost 20 million hectares with a total world production of over 300 million tons (Haverkort et al. 2009). Potato is used for human consumption (boiled, steamed, baked, “sauté” or fried, and processed into French fries, chips or noodles) or for industrial purposes mainly for starch production which can be processed in textile, papermaking, glue, coating, sizing, flocculating agents and building materials. More uses can be anticipated for the future such as biopharmaceuticals for encapsulation and controlled release of functional ingredients (Bradshaw et al. 2006a; Li et al. 2009). Potato is part of the tuber-bearing Solanum species that belong to the section Petota. Solanum section Petota species occur in the Andes of South America and a secondary centre of diversity exists in the central Mexican highlands (Hawkes 1990; Spooner et al. 2004). Hawkes postulated that the ancestral potato species originated from Central America, subsequently migrated to South America, and a return migration back to Mexico, followed by hybridizations and allopolyploidisations within Central American taxa, then led to species with various ploidy levels (Hawkes 1990). Solanum species can easily hybridize with each other, making classification challenging (Hawkes 1990; Jacobs et al. 2008; Spooner and Hijmans 2001). Due to increased insights in potato taxonomy, the number of species is being reduced, in recent reviews. Hawkes (1990) recognized 227 tuber bearing species (7 cultivated species included) and 9 non-tuber-bearing species within section Petota. Spooner and Hijmans (Spooner and Hijmans 2001) recognized 203 tuber-bearing species including 7 cultivated species. Finally, Spooner and Salas (2006), reduced the number further to 189 species (including 1 cultivated species) in section Petota. However, one thing for sure, wild Solanum species are well spread from North to South America and highly diverse. Diploid, triploid, tetraploid, pentaploid and hexaploid species exist, and a polyploid species can contain genes with high homology to genes in one of its diploid progenitors, which increases the potential of diversification of genes in polyploid species to adapt to there environment. Consequently more diversity can occur for each gene homologue in the tuber-bearing Solanum species gene-pool, which can be used to improve various quality traits in breeding programs. 2 General Introduction Phytophthora infestans Phytophthora infestans (Mont.) de Bary, the responsible pathogen for the Irish famine in the middle of the 1840’s, was the first ‘plant destroyer’ described (Fry 2008; Large 1940; Schumann 1991). P. infestans is the causal agent of late blight, which is nowadays the most devastating disease on potato and tomato. It infects foliage, stems and can also infect fruits and tubers (Fry 2008). This notorious disease entails global yield losses of 16% of the potato crop, representing an annual financial loss of € 5.2 billion worldwide (Haverkort et al. 2009). Figure 1. Plant pathogenic oomycetes secrete apoplastic effectors into the plant extracellular space and cytoplasmic effectors inside the plant cell. A) Schematic view of the early stages of infection by Phytophthora infestans of a host plant illustrating the sites of action of the apoplastic and cytoplasmic effectors. B) Cross-section of the view in panel A illustrating the delivery of apoplastic and cytoplasmic effectors to their cellular target. One class of cytoplasmic effectors is known to target the plant nucleus. Apoplastic effectors interact with extracellular targets or surface receptors. Pathogen structures are shown in dark grey and plant structures in clear grey. Apoplastic effector and effector targets are outside of the plant cell, whereas cytoplasmic effectors and their targets are in the plant cell. Adapted from Kamoun (2006). 3 Chapter 1 P. infestans is a near-obligate hemi-biotrophic pathogen. The infection is based on a first biotrophic stage which is followed by a necrotrophic phase. Infection starts with the formation of an appressorium which breaks through the first physical layer of defence of the host (Figure 1). During the biotrophic stage, an intracellular infection vesicle is formed. From there, hyphae emerge, and hyphal growth expands in the extracellular space of the host. Then specialized infection structures called haustoria invaginate host cells and make near-direct contact with the host plasma membrane (Birch et al. 2006). From that point on, the infection switches to a necrotrophic phase and mycelium spreads rapidly through the host tissue and forms spores. During its life cycle P. infestans adopts two types of reproduction. The asexual cycle, as described above, enables dramatically rapid population
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