Phylogeography of the wide-host range panglobal plant pathogen Phytophthora cinnamomi.

Various hypotheses have been proposed regarding the origin of the plant pathogen Phytophthora cinnamomi. P. cinnamomi is a devastating, highly invasive soilborne pathogen associated with epidemics of agricultural, horticultural and forest plantations and native ecosystems worldwide. We conducted a phylogeographic analysis of populations of this pathogen sampled in Asia, Australia, Europe, southern and northern Africa, South America, and North America. Based on genotyping-by-sequencing, we observed the highest genotypic diversity in Taiwan and Vietnam, followed by Australia and South Africa. Mating type ratios were in equal proportions in Asia as expected for a sexual population. Simulations based on the index of association suggest a partially sexual, semi-clonal mode of reproduction for the Taiwanese and Vietnamese populations while populations outside of Asia are clonal. Ancestral area reconstruction provides new evidence supporting Taiwan as the ancestral area, given our sample, indicating that this region might be near or at the centre of origin for this pathogen as speculated previously. The Australian and South African populations appear to be a secondary centre of diversity following migration from Taiwan or Vietnam. Our work also identified two panglobal, clonal lineages PcG1-A2 and PcG2-A2 of A2 mating type found on all continents. Further surveys of natural forests across Southeast Asia are needed to definitively locate the actual centre of origin of this important plant pathogen.

BLIGHTSIM: A New Potato Late Blight Model Simulating the Response of Phytophthora infestans to Diurnal Temperature and Humidity Fluctuations in Relation to Climate Change.

Temperature response curves under diurnal oscillating temperatures differ from those under constant conditions for all stages of the Phytophthora infestans infection cycle on potatoes. We developed a mechanistic model (BLIGHTSIM) with an hourly time step to simulate late blight under fluctuating environmental conditions and predict late blight epidemics in potato fields. BLIGHTSIM is a modified susceptible (S), latent (L), infectious (I) and removed (R) compartmental model with hourly temperature and relative humidity as driving variables. The model was calibrated with growth chamber data covering one infection cycle and validated with field data from Ecuador. The model provided a good fit to all data sets evaluated. There was a significant interaction between average temperature and amplitude in their effects on the area under the disease progress curve (AUDPC) as predicted from growth chamber data on a single infection cycle. BLIGHTSIM can be incorporated in a potato growth model to study effects of diurnal temperature range on late blight impact under climate change scenarios.

Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen Phytophthora infestans.

The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high-coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid, as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3×). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of dominant clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby a higher copy number provides fitness, leading to replacement of prior clonal lineages.IMPORTANCE The plant pathogen implicated in the Irish potato famine, Phytophthora infestans, continues to reemerge globally. Understanding changes in the genome during emergence can provide insights useful for managing this pathogen. Previous work has relied on studying individuals from the United States, South America, Europe, and China reporting that these can occur as diploids, triploids, or tetraploids and are clonal. We studied variation in sexual populations at the pathogen's center of origin, in Mexico, where it has been reported to reproduce sexually as well as within clonally reproducing, dominant clones from the United States and Europe. Our results newly show that sexual populations at the center of origin are diploid, whereas populations elsewhere are more variable and show genome-wide variation in gene copy number. We propose a model of evolution whereby new pathogen clones emerge predominantly by increasing the gene copy number genome-wide.

Variation in Genetic Diversity of Phytophthora infestans Populations in Mexico from the Center of Origin Outwards.

The Toluca valley, located in central Mexico, is thought to be the center of origin of the potato late blight pathogen Phytophthora infestans. We characterized over 500 individuals of P. infestans sampled from populations with a geographical distance of more than 400 km in six regions adjacent to the Toluca valley in three states including Michoacán, Mexico, and Tlaxcala. Our sampling occurred on a predominant east to west gradient and showed significant genetic differentiation. The most western sampling location found in Michoacán was most differentiated from the other populations. Populations from San Gerónimo, Juchitepec, and Tlaxcala clustered together and appeared to be in linkage equilibrium. This work provides a finer understanding of gradients of genetic diversity in populations of P. infestans at the center of origin.