<i>Phytophthora</i>:an ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation

The considerable economic and social impact of the oomycete genus Phytophthora is well known. In response to evidence that all downy mildews (DMs) reside phylogenetically within Phytophthora, rendering Phytophthora paraphyletic, a proposal has been made to split the genus into multiple new genera. We have reviewed the status of the genus and its relationship to the DMs. Despite a substantial increase in the number of described species and improvements in molecular phylogeny the Phytophthora clade structure has remained stable since first demonstrated in 2000. Currently some 200 species are distributed across twelve major clades in a relatively tight monophyletic cluster. In our assessment of 196 species for twenty morphological and behavioural criteria the clades show good biological cohesion. Saprotrophy, necrotrophy and hemi-biotrophy of woody and non-woody roots, stems and foliage occurs across the clades. Phylogenetically less related clades often show strong phenotypic and behavioural similarities and no one clade or group of clades shows the synapomorphies that might justify a unique generic status. We propose the clades arose from the migration and worldwide radiation ~ 140 Mya (million years ago) of an ancestral Gondwanan Phytophthora population, resulting in geographic isolation and clade divergence through drift on the diverging continents combined with adaptation to local hosts, climatic zones and habitats. The extraordinary flexibility of the genus may account for its global ‘success’. The 20 genera of the obligately biotrophic, angiosperm-foliage specialised DMs evolved from Phytophthora at least twice via convergent evolution, making the DMs as a group polyphyletic and Phytophthora paraphyletic in cladistic terms. The long phylogenetic branches of the DMs indicate this occurred rather rapidly, via paraphyletic evolutionary ‘jumps’. Such paraphyly is common in successful organisms. The proposal to divide Phytophthora appears more a device to address the issue of the convergent evolution of the DMs than the structure of Phytophthora per se. We consider it non-Darwinian, putting the emphasis on the emergent groups (the DMs) rather than the progenitor (Phytophthora) and ignoring the evolutionary processes that gave rise to the divergence. Further, the generic concept currently applied to the DMs is narrower than that between some closely related Phytophthora species. Considering the biological and structural cohesion of Phytophthora, its historic and social impacts and its importance in scientific communication and biosecurity protocol, we recommend that the current broad generic concept is retained by the scientific community. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s43008-022-00097-z

Increasing forest loss worldwide from invasive pests requires new trade regulations

Loss of forests due to non-native invasive pests (including insects, nematodes, and pathogens) is a global phenomenon with profound population, community, ecosystem, and economic impacts. We review the magnitude of pest-associated forest loss worldwide and discuss the major ecological and evolutionary causes and consequences of these invasions. After compiling and analyzing a dataset of pest invasions from 21 countries, we show that the number of forest pest invasions recorded for a given country has a significant positive relationship with trade (as indicated by gross domestic product) and is not associated with the amount of forested land within that country. We recommend revisions to existing international protocols for preventing pest entry and proliferation, including prohibiting shipments of non-essential plants and plant products unless quarantined. Because invasions often originate from taxa that are scientifically described only after their introduction, current phytosanitary regulations – which target specific, already named organisms – are ineffective

Complexities underlying the breeding and deployment of Dutch elm disease resistant elms

Dutch elm disease (DED) is a vascular wilt disease caused by the pathogens Ophiostoma ulmi and Ophiostoma novo-ulmi with multiple ecological phases including pathogenic (xylem), saprotrophic (bark) and vector (beetle flight and beetle feeding wound) phases. Due to the two DED pandemics during the twentieth century the use of elms in landscape and forest restoration has declined significantly. However new initiatives for elm breeding and restoration are now underway in Europe and North America. Here we discuss complexities in the DED 'system' that can lead to unintended consequences during elm breeding and some of the wider options for obtaining durability or 'field resistance' in released material, including (1) the phenotypic plasticity of disease levels in resistant cultivars infected by O. novo-ulmi; (2) shortcomings in test methods when selecting for resistance; (3) the implications of rapid evolutionary changes in current O. novo-ulmi populations for the choice of pathogen inoculum when screening; (4) the possibility of using active resistance to the pathogen in the beetle feeding wound, and low attractiveness of elm cultivars to feeding beetles, in addition to resistance in the xylem; (5) the risk that genes from susceptible and exotic elms be introgressed into resistant cultivars; (6) risks posed by unintentional changes in the host microbiome; and (7) the biosecurity risks posed by resistant elm deployment. In addition, attention needs to be paid to the disease pressures within which resistant elms will be released. In the future, biotechnology may further enhance our understanding of the various resistance processes in elms and our potential to deploy trees with highly durable resistance in elm restoration. Hopefully the different elm resistance processes will prove to be largely under durable, additive, multigenic control. Elm breeding programmes cannot afford to get into the host-pathogen arms races that characterise some agricultural host-pathogen systems

Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum

BackgroundAneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.ResultsWe show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.ConclusionThis work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival

Mitotic Recombination and Rapid Genome Evolution in the Invasive Forest Pathogen Phytophthora ramorum

Invasive alien species often have reduced genetic diversity and must adapt to new environments. Given the success of many invasions, this is sometimes called the genetic paradox of invasion. Phytophthora ramorum is invasive, limited to asexual reproduction within four lineages, and presumed clonal. It is responsible for sudden oak death in the United States, sudden larch death in Europe, and ramorum blight in North America and Europe. We sequenced the genomes of 107 isolates to determine how this pathogen can overcome the invasion paradox. Mitotic recombination (MR) associated with transposons and low gene density has generated runs of homozygosity (ROH) affecting 2,698 genes, resulting in novel genotypic diversity within the lineages. One ROH enriched in effectors was fixed in the NA1 lineage. An independent ROH affected the same scaffold in the EU1 lineage, suggesting an MR hot spot and a selection target. Differences in host infection between EU1 isolates with and without the ROH suggest that they may differ in aggressiveness. Non-core regions (not shared by all lineages) had signatures of accelerated evolution and were enriched in putative pathogenicity genes and transposons. There was a striking pattern of gene loss, including all effectors, in the non-core EU2 genome. Positive selection was observed in 8.0% of RxLR and 18.8% of Crinkler effector genes compared with 0.9% of the core eukaryotic gene set. We conclude that the P. ramorum lineages are diverging via a rapidly evolving non-core genome and that the invasive asexual lineages are not clonal, but display genotypic diversity caused by MR