Sudden oak death caused by Phytophthora ramorum has been actively managed in Oregon since the early 2000’s. To date, this epidemic has been driven mostly by the NA1 clonal lineage of P. ramorum, but an outbreak of the EU1 lineage has recently emerged. Here we contrast the population dynamics of the NA1 outbreak first reported in 2001 to the outbreak of the EU1 lineage first detected in 2015. We tested if any of the lineages were introduced more than once. Infested regions of the forest were sampled between 2013-2018 (n = 903) and strains were genotyped at 15 microsatellite loci. Most genotypes observed were transient, with 272 of 358 unique genotypes emerging one year and disappearing the next. Diversity of EU1 was very low and isolates were spatially clustered (< 8 km apart), suggesting a single EU1 introduction. Some forest isolates are genetically similar to isolates collected from a local nursery in 2012, suggesting introduction of EU1 from this nursery or simultaneous introduction to both the nursery and latently into the forest. In contrast, the older NA1 populations were more polymorphic and spread over 30 km2. Principal component analysis supported two to four independent NA1 introductions. The NA1 and EU1 epidemics infest the same area but show disparate demographics owing to initial introductions of the lineages spaced 10 years apart. Comparing these epidemics provides novel insights into patterns of emergence of clonal pathogens in forest ecosystems.
Phytophthora species are notorious plant pathogens, with some causing devastating tree diseases that threaten the survival of their host species. One such example is Phytophthora agathidicida, the causal agent of kauri dieback – a root and trunk rot disease that kills the ancient, iconic and culturally significant tree species, Agathis australis (New Zealand kauri). A deeper understanding of how Phytophthora pathogens infect their hosts and cause disease is critical for the development of effective treatments. Such an understanding can be gained by interrogating pathogen genomes for effector genes, which are involved in virulence or pathogenicity. Although genome sequencing has become more affordable, the complete assembly of Phytophthora genomes has been problematic, particularly for those with a high abundance of repetitive sequences. Therefore, effector genes located in repetitive regions could be truncated or missed in a fragmented genome assembly. Using a combination of long-read PacBio sequences, chromatin conformation capture (Hi-C) and Illumina short reads, we assembled the P. agathidicida genome into ten complete chromosomes, with a genome size of 57 Mb including 34% repeats. This is the first Phytophthora genome assembled to chromosome level and it reveals a high level of syntenic conservation with the complete genome of Peronospora effusa, the only other completely assembled genome sequence of an oomycete. All P. agathidicida chromosomes have clearly defined centromeres and contain candidate effector genes such as RXLRs and CRNs, but in different proportions, reflecting the presence of gene family clusters. Candidate effector genes are predominantly found in gene-poor, repeat-rich regions of the genome, and in some cases showed a high degree of duplication. Analysis of candidate RXLR effector genes that occur in multicopy gene families indicated half of them were not expressed in planta. Candidate CRN effector gene families showed evidence of transposon-mediated recombination leading to new combinations of protein domains, both within and between chromosomes. Further analysis of this complete genome assembly will help inform new methods of disease control against P. agathidicida and other Phytophthora species, ultimately helping decipher how Phytophthora pathogens have evolved to shape their effector repertoires and how they might adapt in the future.
Invasive, exotic plant pathogens pose a major threat to native and agricultural ecosystems. Phytophthora × cambivora is an invasive, destructive pathogen of forest and fruit trees causing severe damage worldwide to chestnuts (Castanea), apricots, peaches, plums, almonds and cherries (Prunus), apples (Malus), oaks (Quercus), and beech (Fagus). It was one of the first damaging invasive Phytophthora species to be introduced to Europe and North America, although its origin is unknown. We determined its population genetic history in Europe, North and South America, Australia and East Asia (mainly Japan) using genotyping-by-sequencing. Populations in Europe and Australia appear clonal, those in North America are highly clonal yet show some degree of sexual reproduction, and those in East Asia are partially sexual. Two clonal lineages, each of opposite mating type, and a hybrid lineage derived from these two lineages, dominated the populations in Europe and were predominantly found on fagaceous forest hosts (Castanea, Quercus, Fagus). Isolates from fruit trees (Prunus and Malus) belonged to a separate lineage found in Australia, North America, Europe and East Asia, indicating the disease on fruit trees could be caused by a distinct lineage of P. × cambivora, which may potentially be a separate sister species and has likely been moved with live plants. The highest genetic diversity was found in Japan, suggesting that East Asia is the centre of origin of the pathogen. Further surveys in unsampled, temperate regions of East Asia are needed to more precisely identify the location and range of the centre of diversity.
Phytophthora plurivora is a recently described plant pathogen, formerly recognized as P. citricola. Recent sampling of Pacific Northwest nurseries frequently encountered this pathogen, and it has been shown to be among the most damaging Phytophthora pathogens on ornamentals. We characterized the population structure of P. plurivora in a survey of four Oregon nurseries across three different counties with focus on Rhododendron hosts. Isolates were identified to the species level by Sanger sequencing and/or a PCR-RFLP assay of the internal transcribed spacer (ITS) region. We used genotyping-by-sequencing to determine genetic diversity. Variants were called de novo, resulting in 284 high-quality variants for 61 isolates after stringent filtering. Based on Fst and AMOVA, populations were moderately differentiated among nurseries. Overall, population structure suggested presence of one dominant clonal lineage in all nurseries, as well as isolates of cryptic diversity mostly found in one nursery. Within the clonal lineage, there was a broad range of sensitivity to mefenoxam and phosphorous acid. Sensitivity of the two fungicides was correlated. P. plurivora was previously assumed to spread clonally, and the low genotypic diversity observed within and among isolates corroborated this hypothesis. The broad range of fungicide sensitivity within the P. plurivora population found in PNW nurseries has implications for managing disease caused by this important nursery pathogen. These findings provide the first perspective into P. plurivora population structure and phenotypic plasticity in Pacific Northwest nurseries.
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