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3. Genome analyses of the sunflower pathogen Plasmopara halstedii provide insights into effector evolution in downy mildews and Phytophthora

Author

Sharma, Rahul, Xia, Xiaojuan, Cano, Liliana M, Evangelisti, Edouard, Kemen, Eric, Judelson, Howard, Oome, Stan, Sambles, Christine, van den Hoogen, D Johan, Kitner, Miloslav, Klein, Joël, Meijer, Harold JG, Spring, Otmar, Win, Joe, Zipper, Reinhard, Bode, Helge B, Govers, Francine, Kamoun, Sophien, Schornack, Sebastian, Studholme, David J, Van den Ackerveken, Guido, and Thines, Marco

Subjects
Biological Sciences, Genetics, Human Genome, Biological Evolution, Fungal Proteins, Gene Expression Profiling, Genome, Fungal, Genomics, Helianthus, Heterozygote, Microsatellite Repeats, Oomycetes, Phospholipids, Phylogeny, Phytophthora, Promoter Regions, Genetic, Repetitive Sequences, Nucleic Acid, Secondary Metabolism, Signal Transduction, Virulence Factors, Comparative genomics, Core effectors, Downy mildew, Evolution, Microsatellites, Obligate biotroph, Phytohormones, Plant pathogen, Promoters, RxLR effectors, Information and Computing Sciences, Medical and Health Sciences, Bioinformatics, Biological sciences, Biomedical and clinical sciences
Abstract

BackgroundDowny mildews are the most speciose group of oomycetes and affect crops of great economic importance. So far, there is only a single deeply-sequenced downy mildew genome available, from Hyaloperonospora arabidopsidis. Further genomic resources for downy mildews are required to study their evolution, including pathogenicity effector proteins, such as RxLR effectors. Plasmopara halstedii is a devastating pathogen of sunflower and a potential pathosystem model to study downy mildews, as several Avr-genes and R-genes have been predicted and unlike Arabidopsis downy mildew, large quantities of almost contamination-free material can be obtained easily.ResultsHere a high-quality draft genome of Plasmopara halstedii is reported and analysed with respect to various aspects, including genome organisation, secondary metabolism, effector proteins and comparative genomics with other sequenced oomycetes. Interestingly, the present analyses revealed further variation of the RxLR motif, suggesting an important role of the conservation of the dEER-motif. Orthology analyses revealed the conservation of 28 RxLR-like core effectors among Phytophthora species. Only six putative RxLR-like effectors were shared by the two sequenced downy mildews, highlighting the fast and largely independent evolution of two of the three major downy mildew lineages. This is seemingly supported by phylogenomic results, in which downy mildews did not appear to be monophyletic.ConclusionsThe genome resource will be useful for developing markers for monitoring the pathogen population and might provide the basis for new approaches to fight Phytophthora and downy mildew pathogens by targeting core pathogenicity effectors.

Published
2015

7. Phytophthora Genome Sequences Uncover Evolutionary Origins and Mechanisms of Pathogenesis

Author

Tyler, Brett M., Tripathy, Sucheta, Zhang, Xuemin, Dehal, Paramvir, Aerts, Andrea, Arredondo, Felipe D., Baxter, Laura, Bensasson, Douda, Beynon, Jim L., Chapman, Jarrod, Dorrance, Anne E., Dou, Daolong, Dickerman, Allan W., Dubchak, Inna L., Garbelotto, Matteo, Gijzen, Mark, Gordon, Stuart G., Govers, Francine, Grunwald, Niklaus J., Huang, Wayne, Ivors, Kelly L., Jones, Richard W., Kamoun, Sophien, Krampis, Konstantinos, Lamour, Kurt H., Lee, Mi-Kyung, McDonald, W. Hayes, Medina, Mónica, Nordberg, Eric K., Maclean, Donald J., Ospina-Giraldo, Manuel D., Morris, Paul F., Phuntumart, Vipaporn, Putnam, Nicholas H., Rash, Sam, Sakihama, Yasuko, Salamov, Asaf A., Savidor, Alon, Scheuring, Chantel F., Smith, Brian M., Terry, Astrid, Torto-Alalibo, Trudy A., Win, Joe, Xu, Zhanyou, Zhang, Hongbin, Grigoriev, Igor V., Rokhsar, Daniel S., and Boore, Jeffrey L.

Published
2006

10. Genome sequence of the necrotrophic plant pathogen, Pythium ultimum, reveals original pathogenicity mechanisms and effector repertoire

Author

Lévesque, C André, Brouwer, Henk, Cano, Liliana, Hamilton, John P, Holt, Carson, Huitema, Edgar, Raffaele, Sylvain, Robideau, Gregg P, Thines, Marco, Win, Joe, Zerillo, Marcelo M, Beakes, Gordon W, Boore, Jeffrey L, Busam, Dana, Dumas, Bernard, Ferriera, Steve, Fuerstenberg, Susan I, Gachon, Claire MM, Gaulin, Elodie, Govers, Francine, Grenville-Briggs, Laura, Horner, Neil, Hostetler, Jessica, Jiang, Rays HY, Johnson, Justin, Krajaejun, Theerapong, Lin, Haining, Meijer, Harold JG, Moore, Barry, Morris, Paul, Phuntmart, Vipaporn, Puiu, Daniela, Shetty, Jyoti, Stajich, Jason E, Tripathy, Sucheta, Wawra, Stephan, van West, Pieter, Whitty, Brett R, Coutinho, Pedro M, Henrissat, Bernard, Martin, Frank, Thomas, Paul D, Tyler, Brett M, De Vries, Ronald P, Kamoun, Sophien, Yandell, Mark, Tisserat, Ned, and Buell, C Robin

Abstract

Abstract Background Pythium ultimum is a ubiquitous oomycete plant pathogen responsible for a variety of diseases on a broad range of crop and ornamental species. Results The P. ultimum genome (42.8 Mb) encodes 15,290 genes and has extensive sequence similarity and synteny with related Phytophthora species, including the potato blight pathogen Phytophthora infestans. Whole transcriptome sequencing revealed expression of 86% of genes, with detectable differential expression of suites of genes under abiotic stress and in the presence of a host. The predicted proteome includes a large repertoire of proteins involved in plant pathogen interactions, although, surprisingly, the P. ultimum genome does not encode any classical RXLR effectors and relatively few Crinkler genes in comparison to related phytopathogenic oomycetes. A lower number of enzymes involved in carbohydrate metabolism were present compared to Phytophthora species, with the notable absence of cutinases, suggesting a significant difference in virulence mechanisms between P. ultimum and more host-specific oomycete species. Although we observed a high degree of orthology with Phytophthora genomes, there were novel features of the P. ultimum proteome, including an expansion of genes involved in proteolysis and genes unique to Pythium. We identified a small gene family of cadherins, proteins involved in cell adhesion, the first report of these in a genome outside the metazoans. Conclusions Access to the P. ultimum genome has revealed not only core pathogenic mechanisms within the oomycetes but also lineage-specific genes associated with the alternative virulence and lifestyles found within the pythiaceous lineages compared to the Peronosporaceae.

Published
2010

11. Foreword

Author

Boonekamp, Piet M., Pieterse, Corné M. J., Govers, Francine, and Cornelissen, Ben J. C.

Published
2019
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17. Convergent evolution of immune receptors underpins distinct elicitin recognition in closely related Solanaceous plants

Author

Chen, Zhaodan, primary, Liu, Fan, additional, Zeng, Mengzhu, additional, Wang, Lei, additional, Liu, Hanmei, additional, Sun, Yujing, additional, Wang, Lan, additional, Zhang, Zhichao, additional, Chen, Zhiyuan, additional, Xu, Yuanpeng, additional, Zhang, Mingmei, additional, Xia, Yeqiang, additional, Ye, Wenwu, additional, Dong, Suomeng, additional, Govers, Francine, additional, Wang, Yan, additional, and Wang, Yuanchao, additional

Published
2023
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27. Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants

Author

Gilroy, Eleanor M., Breen, Susan, Whisson, Stephen C., Squires, Julie, Hein, Ingo, Kaczmarek, Maciej, Turnbull, Dionne, Boevink, Petra C., Lokossou, Anoma, Cano, Liliana M., Morales, Juan, Avrova, Anna O., Pritchard, Leighton, Randall, Eva, Lees, Alison, Govers, Francine, van West, Pieter, Kamoun, Sophien, Vleeshouwers, Vivianne G. A. A., Cooke, David E. L., and Birch, Paul R. J.

Published
2011

30. Signatures of Adaptation to Obligate Biotrophy in the Hyaloperonospora arabidopsidis Genome

Author

Baxter, Laura, Tripathy, Sucheta, Ishaque, Naveed, Boot, Nico, Cabral, Adriana, Kemen, Eric, Thines, Marco, Ah-Fong, Audrey, Anderson, Ryan, Badejoko, Wole, Bittner-Eddy, Peter, Boore, Jeffrey L., Chibucos, Marcus C., Coates, Mary, Dehal, Paramvir, Delehaunty, Kim, Dong, Suomeng, Downton, Polly, Dumas, Bernard, Fabro, Georgina, Fronick, Catrina, Fuerstenberg, Susan I., Fulton, Lucinda, Gaulin, Elodie, Govers, Francine, Hughes, Linda, Humphrey, Sean, Jiang, Rays H. Y., Judelson, Howard, Kamoun, Sophien, Kyung, Kim, Meijer, Harold, Minx, Patrick, Morris, Paul, Nelson, Joanne, Phuntumart, Vipa, Qutob, Dinah, Rehmany, Anne, Rougon-Cardoso, Alejandra, Ryden, Peter, Torto-Alalibo, Trudy, Studholme, David, Wang, Yuanchao, Win, Joe, Wood, Jo, Clifton, Sandra W., Rogers, Jane, Van den Ackerveken, Guido, Jones, Jonathan D. G., McDowell, John M., Beynon, Jim, and Tyler, Brett M.

Published
2010

32. Uncovering the Role of Metabolism in Oomycete-Host Interactions Using Genome-Scale Metabolic Models

Author

Rodenburg, Sander Y A, Seidl, Michael F, de Ridder, Dick, Govers, Francine, Sub Bioinformatics, and Theoretical Biology and Bioinformatics

Subjects
Microbiology (medical), plant pathogenic oomycetes, Phytophthora infestans, genome-scale metabolic model, metabolic networks, systems biology, Microbiology, plant–pathogen interactions
Abstract

Metabolism is the set of biochemical reactions of an organism that enables it to assimilate nutrients from its environment and to generate building blocks for growth and proliferation. It forms a complex network that is intertwined with the many molecular and cellular processes that take place within cells. Systems biology aims to capture the complexity of cells, organisms, or communities by reconstructing models based on information gathered by high-throughput analyses (omics data) and prior knowledge. One type of model is a genome-scale metabolic model (GEM) that allows studying the distributions of metabolic fluxes, i.e., the "mass-flow" through the network of biochemical reactions. GEMs are nowadays widely applied and have been reconstructed for various microbial pathogens, either in a free-living state or in interaction with their hosts, with the aim to gain insight into mechanisms of pathogenicity. In this review, we first introduce the principles of systems biology and GEMs. We then describe how metabolic modeling can contribute to unraveling microbial pathogenesis and host-pathogen interactions, with a specific focus on oomycete plant pathogens and in particular Phytophthora infestans. Subsequently, we review achievements obtained so far and identify and discuss potential pitfalls of current models. Finally, we propose a workflow for reconstructing high-quality GEMs and elaborate on the resources needed to advance a system biology approach aimed at untangling the intimate interactions between plants and pathogens.

Published
2021

40. Mining oomycete proteomes for metalloproteases leads to identification of candidate virulence factors in Phytophthora infestans

Author

Schoina, Charikleia, Rodenburg, Sander Y.A., Meijer, Harold J.G., Seidl, Michael F., Lacambra, Lysette T., Bouwmeester, Klaas, Govers, Francine, Sub Bioinformatics, Theoretical Biology and Bioinformatics, Sub Bioinformatics, and Theoretical Biology and Bioinformatics

Subjects
0106 biological sciences, 0301 basic medicine, Proteome, Gene Expression, Nicotiana benthamiana, Plant Science, 01 natural sciences, MEROPS, Cluster Analysis, Laboratory of Entomology, skin and connective tissue diseases, Pathogen, Phylogeny, Genetics, Oomycete, biology, peptidase, Biosystematiek, plant pathogen, Phytophthora infestans, Original Article, Phytophthora, secreted metalloproteases, congenital, hereditary, and neonatal diseases and abnormalities, Virulence Factors, Bioinformatics, Virulence, Soil Science, 03 medical and health sciences, Biointeractions and Plant Health, Protein Domains, Tobacco, Bioinformatica, oomycete, Molecular Biology, Plant Diseases, nutritional and metabolic diseases, Original Articles, biology.organism_classification, Laboratorium voor Entomologie, Laboratorium voor Phytopathologie, Gene expression profiling, virulence, 030104 developmental biology, Laboratory of Phytopathology, Metalloproteases, Biosystematics, stramenopile, EPS, Agronomy and Crop Science, 010606 plant biology & botany
Abstract

Pathogens deploy a wide range of pathogenicity factors, including a plethora of proteases, to modify host tissue or manipulate host defences. Metalloproteases (MPs) have been implicated in virulence in several animal and plant pathogens. Here we investigated the repertoire of MPs in 46 stramenopile species including 37 oomycetes, 5 diatoms, and 4 brown algae. Screening their complete proteomes using hidden Markov models (HMMs) trained for MP detection resulted in over 4,000 MPs, with most species having between 65 and 100 putative MPs. Classification in clans and families according to the MEROPS database showed a highly diverse MP repertoire in each species. Analyses of domain composition, orthologous groups, distribution, and abundance within the stramenopile lineage revealed a few oomycete‐specific MPs and MPs potentially related to lifestyle. In‐depth analyses of MPs in the plant pathogen Phytophthora infestans revealed 91 MPs, divided over 21 protein families, including 25 MPs with a predicted signal peptide or signal anchor. Expression profiling showed different patterns of MP gene expression during pre‐infection and infection stages. When expressed in leaves of Nicotiana benthamiana, 12 MPs changed the sizes of lesions caused by inoculation with P. infestans; with 9 MPs the lesions were larger, suggesting a positive effect on the virulence of P. infestans, while 3 MPs had a negative effect, resulting in smaller lesions. To the best of our knowledge, this is the first systematic inventory of MPs in oomycetes and the first study pinpointing MPs as potential pathogenicity factors in Phytophthora., Proteome mining and comparative analyses uncovered a large variety of metalloproteases (MPs) in oomycetes. Functional in planta assays pinpointed 12 MPs as potential pathogenicity factors in Phytophthora infestans.

Published
2021

49. Internuclear gene silencing in Phytophthora infestans is established through chromatin remodelling

Author

van West, Pieter, Shepherd, Samantha J., Walker, Claire A., Li, Shuang, Appiah, Alex A., Grenville-Briggs, Laura J., Govers, Francine, and Gow, Neil A.R.

Subjects
Pathogenic microorganisms -- Genetic aspects, Gene silencing -- Physiological aspects, Chromatin -- Genetic aspects, Biological sciences
Abstract

In the plant pathogen Phytophthora infestans, nuclear integration of inf1 transgenic DNA sequences results in internuclear gene silencing of inf1. Although silencing is regulated at the transcriptional level, it also affects transcription from other nuclei within heterokaryotic cells of the mycelium. Here we report experiments exploring the mechanism of internuclear gene silencing in P. infestans. The DNA methylation inhibitor 5-azacytidine induced reversion of the inf1-silenced state. Also, the histone deacetylase inhibitor trichostatin-A was able to reverse inf1 silencing. inf1-expression levels returned to the silenced state when the inhibitors were removed except in non-transgenic inf1-silenced strains that were generated via internuclear gene silencing, where inf1 expression was restored permanently. Therefore, inf1-transgenic sequences are required to maintain the silenced state. Prolonged culture of non-transgenic inf1-silenced strains resulted in gradual reactivation of inf1 gene expression. Nuclease digestion of inf1-silenced and non-silenced nuclei showed that inf1 sequences in silenced nuclei were less rapidly degraded than non-silenced inf1 sequences. Bisulfite sequencing of the endogenous inf1 locus did not result in detection of any cytosine methylation. Our findings suggest that the inf1-silenced state is based on chromatin remodelling.

Published
2008

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