Ecological speciation within the Phytophthora genus

Over the past few years, symptoms akin to late blight disease have been reported on a variety of crop plants in South America. Despite the economic importance of these crops, the causal agents of the diseases belonging to the genus Phytophthora have not been completely characterized. In this study, we used an integrative approach that leveraged morphological, ecological, and genetic approaches to explore cryptic speciation within P. infestans sensu lato. We described a new Phytophthora species collected in Colombia from tree tomato (Solanum betaceum), a semi-domesticated fruit. All morphological traits and population genetic analyses, using microsatellite data and a reduced representation of single nucleotide polymorphism (SNP) data, support the description of the new species, Phytophthora betacei sp. nov. We have demonstrated that ecological differences are important in the persistence of P. infestans and P. betacei as genetically isolated units across an overlapping area in the northern Andes.

[1]  P. Rojas,et al.  Novel microsatellite markers for the analysis of Phytophthora capsici populations and Host Resistance for Management of Phytophthora Blight of Pepper , 2017 .

[2]  G. Forbes,et al.  Identification of an A2 population of Phythophthora andina attacking tree tomato in Peru indicates a risk of sexual reproduction in this pathosystem. , 2016 .

[3]  Robert E. Boyles,et al.  Rebuttal to letter to the editor , 2016, The Journal of manual & manipulative therapy.

[4]  Mark N. Puttick,et al.  Size is not everything: rates of genome size evolution, not C-value, correlate with speciation in angiosperms , 2015, Proceedings of the Royal Society B: Biological Sciences.

[5]  Nathan Wales,et al.  Genomic Characterization of a South American Phytophthora Hybrid Mandates Reassessment of the Geographic Origins of Phytophthora infestans , 2015, Molecular biology and evolution.

[6]  J. Otte,et al.  Coalescent-Based Species Delimitation Approach Uncovers High Cryptic Diversity in the Cosmopolitan Lichen-Forming Fungal Genus Protoparmelia (Lecanorales, Ascomycota) , 2015, PloS one.

[7]  C. Nusbaum,et al.  Mitochondrial genome sequences reveal evolutionary relationships of the Phytophthora 1c clade species , 2015, Current Genetics.

[8]  C. Muir,et al.  The Limited Contribution of Reciprocal Gene Loss to Increased Speciation Rates Following Whole-Genome Duplication , 2014, The American Naturalist.

[9]  Javier F. Tabima,et al.  Speciation in fungal and oomycete plant pathogens. , 2014, Annual review of phytopathology.

[10]  William E. Fry,et al.  The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes , 2014, Proceedings of the National Academy of Sciences.

[11]  M. Coffey,et al.  A combined mitochondrial and nuclear multilocus phylogeny of the genus Phytophthora. , 2014, Fungal genetics and biology : FG & B.

[12]  E. Stukenbrock.  Evolution, selection and isolation: a genomic view of speciation in fungal plant pathogens. , 2013, The New phytologist.

[13]  Marco Thines,et al.  The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine , 2013, eLife.

[14]  L. Bachmann,et al.  Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach , 2013, Nucleic acids research.

[15]  Heng Li.  Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[16]  Pascal Frey,et al.  Phylogenetic species recognition reveals host-specific lineages among poplar rust fungi. , 2013, Molecular phylogenetics and evolution.

[17]  Alexandra M. E. Jones,et al.  The Irish Potato Famine Pathogen Phytophthora infestans Translocates the CRN8 Kinase into Host Plant Cells , 2012, PLoS pathogens.

[18]  Z. Abad,et al.  Identification and Detection of Phytophthora: Reviewing Our Progress, Identifying Our Needs. , 2012, Plant disease.

[19]  Javier F. Tabima,et al.  Defining species boundaries in the genus Phytophthora: the case of Phytophthora andina A response to ‘Phytophthora andina sp. nov., a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands’ (Oliva et al., 2010) , 2012 .

[20]  F. Govers,et al.  The genus Phytophthora anno 2012. , 2012, Phytopathology.

[21]  S. Restrepo,et al.  The Plant Pathogen Phytophthora andina Emerged via Hybridization of an Unknown Phytophthora Species and the Irish Potato Famine Pathogen, P. infestans , 2011, PloS one.

[22]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[23]  T. Wetzel.  Phytophthora: Identifying Species by Morphology and DNA Fingerprints , 2011 .

[24]  Mark A. Miller,et al.  Creating the CIPRES Science Gateway for inference of large phylogenetic trees , 2010, 2010 Gateway Computing Environments Workshop (GCE).

[25]  B. Langmead,et al.  Aligning Short Sequencing Reads with Bowtie , 2010, Current protocols in bioinformatics.

[26]  Amanda D. Roe,et al.  Multilocus species identification and fungal DNA barcoding: insights from blue stain fungal symbionts of the mountain pine beetle , 2010, Molecular ecology resources.

[27]  M. DePristo,et al.  The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. , 2010, Genome research.

[28]  J. Ristaino,et al.  Phytophthora andina sp nov., a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands , 2010 .

[29]  Jonathan D. G. Jones,et al.  Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans , 2009, Nature.

[30]  Itay Mayrose,et al.  The frequency of polyploid speciation in vascular plants , 2009, Proceedings of the National Academy of Sciences.

[31]  R. Visser,et al.  Applied Biotechnology to Combat Late Blight in Potato Caused by Phytophthora Infestans , 2009, Potato Research.

[32]  Chia-Hui Hu,et al.  Phylogenetic relationships of Phytophthora andina, a new species from the highlands of Ecuador that is closely related to the Irish potato famine pathogen Phytophthora infestans , 2008, Mycologia.

[33]  A. J. Haverkort,et al.  Societal Costs of Late Blight in Potato and Prospects of Durable Resistance Through Cisgenic Modification , 2008, Potato Research.

[34]  W. Fry,et al.  Phytophthora infestans: the plant (and R gene) destroyer. , 2008, Molecular plant pathology.

[35]  D. Geiser,et al.  A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. , 2008, Fungal genetics and biology : FG & B.

[36]  Bryan C. Carstens,et al.  Delimiting species without monophyletic gene trees. , 2007, Systematic biology.

[37]  H. Shaffer,et al.  Delimiting species in recent radiations. , 2007, Systematic biology.

[38]  N. Talbot,et al.  Insights from Sequencing Fungal and Oomycete Genomes: What Can We Learn about Plant Disease and the Evolution of Pathogenicity? , 2007, The Plant Cell Online.

[39]  Ignazio Carbone,et al.  An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies , 2007, Proceedings of the National Academy of Sciences.

[40]  A. Stamatakis.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[41]  C. Moritz,et al.  DNA barcoding will often fail to discover new animal species over broad parameter space. , 2006, Systematic biology.

[42]  G. Forbes,et al.  Genetic Structure of the Population of Phytophthora infestans Attacking Solanum ochranthum in the Highlands of Ecuador , 2006, European Journal of Plant Pathology.

[43]  D. S. Shaw,et al.  Novel microsatellite markers for the analysis of Phytophthora infestans populations , 2006 .

[44]  P. Kindlmann,et al.  Temporal differentiation and spatial coexistence of sexual and facultative asexual lineages of an aphid species at mating sites , 2006, Journal of evolutionary biology.

[45]  P. Smouse,et al.  genalex 6: genetic analysis in Excel. Population genetic software for teaching and research , 2006 .

[46]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[47]  R. Poulin.  Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization , 2004, Parasitology.

[48]  N. Grünwald,et al.  First Report of Blight on Ipomoea purpurea Caused by Phytophthora ipomoeae. , 2004, Plant disease.

[49]  F. Bakker,et al.  Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. , 2004, Fungal genetics and biology : FG & B.

[50]  G. Forbes,et al.  Genetic Diversity of Phytophthora infestans sensu lato in Ecuador Provides New Insight Into the Origin of This Important Plant Pathogen. , 2004, Phytopathology.

[51]  D. Jacobson,et al.  A MULTILOCUS GENEALOGICAL APPROACH TO PHYLOGENETIC SPECIES RECOGNITION IN THE MODEL EUKARYOTE NEUROSPORA , 2003, Evolution; international journal of organic evolution.

[52]  D. J. Funk,et al.  Species-Level Paraphyly and Polyphyly: Frequency, Causes, and Consequences, with Insights from Animal Mitochondrial DNA , 2003 .

[53]  R. H. Kushler,et al.  Statistical Computing: An Introduction to Data Analysis Using S-PLUS , 2003, Technometrics.

[54]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[55]  Christina Gloeckner,et al.  Modern Applied Statistics With S , 2003 .

[56]  G. Forbes,et al.  The Andean fruit crop, pear melon (Solanum muricatum) is a common host for A1 and A2 strains of Phytophthora infestans in Ecuador. , 2002 .

[57]  U. Gisi,et al.  Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland , 2002 .

[58]  W. Fry,et al.  Diversity in and evidence for selection on the mitochondrial genome of Phytophthora infestans , 2002, Mycologia.

[59]  N. Grünwald,et al.  Phytophthora ipomoeae sp. nov., a new homothallic species causing leaf blight on Ipomoea longipedunculata in the Toluca Valley of central Mexico , 2002 .

[60]  T. Harrington,et al.  Species Delimitation and Host Specialization of Ceratocystis laricicola and C. polonica to Larch and Spruce. , 2002, Plant disease.

[61]  J. Duncan,et al.  A molecular phylogeny of Phytophthora and related oomycetes. , 2000, Fungal genetics and biology : FG & B.

[62]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[63]  C. Smart,et al.  A Novel Population of Phytophthora, Similar to P. infestans, Attacks Wild Solanum Species in Ecuador. , 2000, Phytopathology.

[64]  O. K. Ribeiro,et al.  Phytophthora diseases worldwide , 1998 .

[65]  D. S. Shaw,et al.  Polymorphisms in Phytophthora infestans: Four Mitochondrial Haplotypes Are Detected after PCR Amplification of DNA from Pure Cultures or from Host Lesions , 1998, Applied and Environmental Microbiology.

[66]  Alfonso,et al.  AFLP Linkage Map of the Oomycete Phytophthora infestans , 1997, Fungal genetics and biology : FG & B.

[67]  Michael J. Crawley,et al.  GLIM for Ecologists , 1994 .

[68]  S. B. Goodwin,et al.  Cloning and genetic analyses of two highly polymorphic, moderately repetitive nuclear DNAs from Phytophthora infestans , 1992, Current Genetics.

[69]  E. G. Strauss,et al.  Molecular phylogeny , 1992, Current Biology.

[70]  D. S. Shaw,et al.  Restriction fragment length polymorphisms of mitochondrial DNA of Phytophthora infestans , 1990 .

[71]  R. Thaxter.  A New American Phytophthora , 1889, Botanical Gazette.

[72]  T. Pohlert.  The Pairwise Multiple Comparison of Mean Ranks Package (PMCMR) , 2016 .

[73]  K. Lamour.  Phytophthora: a global perspective. , 2013 .

[74]  G. A. Forbesa,et al.  Letter to the Editor A rebuttal to the letter to the editor concerning ‘Defining species boundaries in the genus Phytophthora : the case of Phytophthora andina ’ , 2012 .

[75]  R. Olivaa,et al.  Phytophthora andina sp . nov . , a newly identified heterothallic pathogen of solanaceous hosts in the Andean highlands , 2010 .

[76]  J. de la Fuente,et al.  BMC Evolutionary Biology BioMed Central , 2009 .

[77]  Alejandro Rojas,et al.  Characterization of Phytophthora infestans populations in Colombia: first report of the A2 mating type. , 2009, Phytopathology.

[78]  D. Rizzo,et al.  Defining Species in the Fungi , 1999 .

[79]  H. Hohl,et al.  Phytophthora mirabilis, a new species of Phytophthora , 1985 .