Microclimate Impacts Survival and Prevalence of Phytophthora ramorum in Umbellularia californica,a Key Reservoir Host of Sudden Oak Death in Northern California Forests

Phytophthora ramorum, an invasive pathogen and the causal agent of Sudden Oak Death, has become established in mixed-evergreen and redwood forests in coastal northern California. While oak and tanoak mortality is the most visible indication of P. ramorum’s presence, epidemics are largely driven by the presence of bay laurel (Umbellularia californica), a reservoir host that supports both prolific sporulation in the winter wet season and survival during the summer dry season. In order to better understand how over-summer survival of the pathogen contributes to variability in the severity of annual epidemics, we monitored the viability of P. ramorum leaf infections over three years along with coincident microclimate. The proportion of symptomatic bay laurel leaves that contained viable infections decreased during the first summer dry season and remained low for the following two years, likely due to the absence of conducive wet season weather during the study period. Over-summer survival of P. ramorum was positively correlated with high percent canopy cover, less negative bay leaf water potential and few days exceeding 30°C but was not significantly different between mixed-evergreen and redwood forest ecosystems. Decreased summer survival of P. ramorum in exposed locations and during unusually hot summers likely contributes to the observed spatiotemporal heterogeneity of P. ramorum epidemics.     

Common Factors Drive Disease and Coarse Woody Debris Dynamics in Forests Impacted by Sudden Oak Death

Disease ecology has made important steps in describing how epidemiological processes control the impact of pathogens on populations and communities but fewer field or theoretical studies address disease effects at the ecosystem level. We demonstrate that the same epidemiological mechanisms drive disease intensity and coarse woody debris (CWD) dynamics in natural forest ecosystems impacted by an emerging disease. Sudden oak death (causal agent, Phytophthora ramorum) has caused mortality of tanoak (Notholithocarpus densiflorus) on a spatial scale and rate comparable to other major North American forest diseases caused by invasive pathogens. In pathogen invaded stands, mean CWD masses were 22.4 Mg ha⁻¹ of standing dead tanoak (snags) and 11.5 Mg ha⁻¹ in logs compared to 0.27 and 1.16 Mg ha⁻¹ of snags and logs in an uninvaded stand. Within invaded stands variation in CWD mass and accumulation rates were largely driven by the distribution of pre-disease tanoak biomass and the densities of infected tanoak and California bay laurel (Umbellularia californica) which jointly determine P. ramorum sporulation and disease emergence rates. In a narrow range of community and host characteristics sudden oak death can result in woody debris dynamics similar to discrete disturbances such as fire and forest harvest but it is more common to have lower maximum amounts with slower rates of accumulation than these better studied disturbances. Our results indicate that models of CWD dynamics need to integrate epidemiological processes to predict realistic ecosystem impacts and lead to management applications for forest pathogens.     

Litter Chemistry,Community Shift,and Non-additive Effects Drive Litter Decomposition Changes Following Invasion by a Generalist Pathogen

Forest pathogens have strong potential to shape ecosystem function by altering litterfall, microclimate, and changing community structure. We quantified changes in litter decomposition from a set of distinct diseases caused by Phytophthora ramorum, an exotic generalist pathogen. Phytophthora ramorum causes leaf blight and increased litterfall %N, but no mortality on California bay laurel (Umbellularia californica), a common overstory tree that accumulates high levels of infection. Lethal twig and bole cankers on tanoak (Notholithocarpus densiflorus) lead to the disease sudden oak death which creates canopy openings and alters litterfall in mixed-species forests dominated by redwood (Sequoia sempervirens) which is minimally susceptible. Species identity had the greatest effect on mass loss and N dynamics with the most rapid rates in bay laurel, slowest in redwood, and intermediate in tanoak. Decomposing litter from infected sources had increased N accumulation, and although these changes were of lower magnitude relative to species identity, the region-scale invasion of P. ramorum suggests that this effect could occur over an extensive area. Canopy mortality was a significant and slowing influence on litter N dynamics in all species and also dampened non-additive effects within mixed litter bags. Redwood—the lowest quality litter—demonstrated non-additive interactions with consistently lower C:N when decomposed in mixed litter bags, but this effect did not alter the entire mixture. Mortality and subsequent changes in community composition have the greatest magnitude effects on litter decomposition for sudden oak death, but our study implies that different and sometimes cryptic mechanisms will drive decomposition changes for other forest diseases.     

Phytophthora ramorum: a pathogen with a remarkably wide host range causing sudden oak death on oaks and ramorum blight on woody ornamentals

Phytophthora ramorum is an oomycete plant pathogen classified in the kingdom Stramenopila. P. ramorum is the causal agent of sudden oak death on coast live oak and tanoak as well as ramorum blight on woody ornamental and forest understorey plants. It causes stem cankers on trees, and leaf blight or stem dieback on ornamentals and understorey forest species. This pathogen is managed in the USA and Europe by eradication where feasible, by containment elsewhere and by quarantine in many parts of the world. Genomic resources provide information on genes of interest to disease management and have improved tremendously since sequencing the genome in 2004. This review provides a current overview of the pathogenicity, population genetics, evolution and genomics of P. ramorum. Taxonomy: Phytophthora ramorum (Werres, De Cock & Man in't Veld): kingdom Stramenopila; phylum Oomycota; class Peronosporomycetidae; order Pythiales; family Pythiaceae; genus Phytophthora. Host range: The host range is very large and the list of known hosts continues to expand at the time of writing. Coast live oak and tanoak are ecologically, economically and culturally important forest hosts in the USA. Rhododendron, Viburnum, Pieris, Syringa and Camellia are key ornamental hosts on which P. ramorum has been found repeatedly, some of which have been involved in moving the pathogen via nursery shipments. Disease symptoms: P. ramorum causes two different diseases with differing symptoms: sudden oak death (bleeding lesions, stem cankers) on oaks and ramorum blight (twig dieback and/or foliar lesions) on tree and woody ornamental hosts. Useful websites: http://nature.berkeley.edu/comtf/ , http://rapra.csl.gov.uk/ , http://www.aphis.usda.gov/plant_health/plant_pest_info/pram/index.shtml , http://genome.jgi‐psf.org/Phyra1_1/Phyra1_1.home.html , http://pamgo.vbi.vt.edu/ , http://pmgn.vbi.vt.edu/ , http://vmd.vbi.vt.edu./ , http://web.science.oregonstate.edu/bpp/labs/grunwald/resources.htm , http://www.defra.gov.uk/planth/pramorum.htm , http://www.invasive.org/browse/subject.cfm?sub=4603 , http://www.forestry.gov.uk/forestry/WCAS‐4Z5JLL     

Impact of sudden oak death on tree mortality in the Big Sur ecoregion of California

The Big Sur ecoregion in coastal California is a botanically and ecologically diverse area that has recently experienced substantial mortality of oak (Quercus spp.) and tanoak (Lithocarpus densiflorus) trees due to the emerging forest disease sudden oak death, caused by the invasive pathogen Phytophthora ramorum. In response to the urgent need to examine environmental impacts and create management response strategies, we quantified the impact of P. ramorum invasion on tree mortality across the Big Sur ecoregion using high-resolution aircraft imagery and field data. Using the imagery, we mapped all detectable oak and tanoak trees possibly killed by P. ramorum infection within redwood-tanoak forests and mixed oak woodlands. To validate and improve our remote assessment, we quantified the number, size, and infection status of host trees in 77 field plots (0.25 ha). The field data showed that our remote assessment underestimated mortality due to the occurrence of dead trees in the forest understory. For each forest type, we developed regression models that adjusted our remote assessments of tree mortality in relation to field observations of mortality and local habitat variables. The models significantly improved remote assessment of oak mortality, but relationships were stronger for mixed oak woodlands (r ² = 0.77) than redwood-tanoak forests (r ² = 0.66). Using the field data, we also modeled the amount of dead tree basal area (m²) in relation to the density of mapped dead trees in mixed oak woodlands (r ² = 0.73) and redwood-tanoak forests (r ² = 0.54). Application of the regression models in a GIS estimated 235,678 standing dead trees in 2005 and 12,650 m² of tree basal area removed from the ecoregion, with 63% of mortality occurring in redwood-tanoak forests and 37% in mixed oak woodlands. Integration of the remote assessment with population estimates of host abundance, obtained from an independent network of 175 field plots (0.05 ha each), indicated similar prevalence of mortality in redwood-tanoak forests (20.0%) and mixed oak woodlands (20.5%) at this time. This is the first study to quantify a realistic number of dead trees impacted by P. ramorum over a defined ecological region. Ecosystem impacts of such widespread mortality will likely be significant.

Discovery of a fourth evolutionary lineage of Phytophthora ramorum: EU2

Phytophthora ramorum is a recently introduced, aggressive Phytophthora species that has caused extensive mortality of oak and tanoak trees in the western USA and Japanese larch trees in the UK. P. ramorum is also present on Rhododendron, Camellia, and Viburnum in the nursery industry, which is thought to have been the pathway for its spread into new geographic regions including forests and natural ecosystems. Three lineages of P. ramorum have been described, informally designated EU1, NA1, and NA2, and each lineage is believed to originate from an as yet unknown exotic centre of origin. Preliminary SSR and sequence analysis of isolates from a UK P. ramorum survey revealed seven isolates with profiles that did not match the previously known lineages. Detailed SSR and multilocus sequence analysis of these isolates are presented, allowing us to assign these isolates to a new P. ramorum lineage, designated EU2. Although the known geographical origin of these isolates is currently limited to Northern Ireland and western Scotland, the EU2 lineage isolates have been obtained from four different host plants, including Japanese larch. All isolates are of A1 compatibility type, which implies that this finding does not increase the risk of outcrossing with the EU1 lineage isolates already present in the UK. The oldest EU2 strain was isolated in 2007 but no SSR-based intraEU2 lineage genotypic diversity was detected. The combination of these elements points to a recent introduction, despite emergency phytosanitary measures to control introduction and spread. A PCR-RFLP method for the rapid identification of EU2 lineage isolates is presented.     

Evolution of RXLR-Class Effectors in the Oomycete Plant Pathogen Phytophthora ramorum

Phytophthora plant pathogens contain many hundreds of effectors potentially involved in infection of host plants. Comparative genomic analyses have shown that these effectors evolve rapidly and have been subject to recent expansions. We examined the recent sequence evolution of RXLR-class effector gene families in the sudden oak death pathogen, P. ramorum. We found that P. ramorum RXLR effectors have taken multiple evolutionary paths, including loss or gain of repeated domains, recombination or gene conversion among paralogs, and selection on point mutations. Sequencing of homologs from two subfamilies in P. ramorum’s closest known relatives revealed repeated gene duplication and divergence since speciation with P. lateralis. One family showed strong signatures of recombination while the other family has evolved primarily by point mutation. Comparison of a small number of the hundreds of RXLR-class effectors across three clonal lineages of P. ramorum shows striking divergence in alleles among lineages, suggesting the potential for functional differences between lineages. Our results suggest future avenues for examination of rapidly evolving effectors in P. ramorum, including investigation of the functional and coevolutionary significance of the patterns of sequence evolution that we observed.     

Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode

During pathogen attack, the host plant induces genes to ward off the pathogen while the pathogen often produces effector proteins to increase susceptibility of the host. Gene expression studies of syncytia formed in soybean root by soybean cyst nematode (Heterodera glycines) identified many genes altered in expression in resistant and susceptible roots. However, it is difficult to assess the role and impact of these genes on resistance using gene expression patterns alone. We selected 100 soybean genes from published microarray studies and individually overexpressed them in soybean roots to determine their impact on cyst nematode development. Nine genes reduced the number of mature females by more than 50 % when overexpressed, including genes encoding ascorbate peroxidase, β-1,4-endoglucanase, short chain dehydrogenase, lipase, DREPP membrane protein, calmodulin, and three proteins of unknown function. One gene encoding a serine hydroxymethyltransferase decreased the number of mature cyst nematode females by 45 % and is located at the Rhg4 locus. Four genes increased the number of mature cyst nematode females by more than 200 %, while thirteen others increased the number of mature cyst nematode females by more than 150 %. Our data support a role for auxin and ethylene in susceptibility of soybean to cyst nematodes. These studies highlight the contrasting gene sets induced by host and nematode during infection and provide new insights into the interactions between host and pathogen at the molecular level. Overexpression of some of these genes result in a greater decrease in the number of cysts formed than recognized soybean cyst nematode resistance loci.     

Genetics of tan spot resistance in wheat

Tan spot is a devastating foliar disease of wheat caused by the necrotrophic fungal pathogen Pyrenophora tritici-repentis. Much has been learned during the past two decades about the genetics of wheat–P. tritici-repentis interactions. Research has shown that the fungus produces at least three host-selective toxins (HSTs), known as Ptr ToxA, Ptr ToxB, and Ptr ToxC, that interact directly or indirectly with the products of the dominant host genes Tsn1, Tsc2, and Tsc1, respectively. The recent cloning and characterization of Tsn1 provided strong evidence that the pathogen utilizes HSTs to subvert host resistance mechanisms to cause disease. However, in addition to host–HST interactions, broad-spectrum, race non-specific resistance QTLs and recessively inherited qualitative ‘resistance’ genes have been identified. Molecular markers suitable for marker-assisted selection against HST sensitivity genes and for race non-specific resistance QTLs have been developed and used to generate adapted germplasm with good levels of tan spot resistance. Future research is needed to identify novel HSTs and corresponding host sensitivity genes, determine if the recessively inherited resistance genes are HST insensitivities, extend the current race classification system to account for new HSTs, and determine the molecular basis of race non-specific resistance QTLs and their relationships with host–HST interactions at the molecular level. Necrotrophic pathogens such as P. tritici-repentis are likely to become increasingly significant under a changing global climate making it imperative to further characterize the wheat–P. tritici-repentis pathosystem and develop tan spot resistant wheat varieties.     

Evidence of statistical epistasis between DISC1, CIT and NDEL1 impacting risk for schizophrenia: biological validation with functional neuroimaging

The etiology of schizophrenia likely involves genetic interactions. DISC1, a promising candidate susceptibility gene, encodes a protein which interacts with many other proteins, including CIT, NDEL1, NDE1, FEZ1 and PAFAH1B1, some of which also have been associated with psychosis. We tested for epistasis between these genes in a schizophrenia case–control study using machine learning algorithms (MLAs: random forest, generalized boosted regression and Monte Carlo logic regression). Convergence of MLAs revealed a subset of seven SNPs that were subjected to 2-SNP interaction modeling using likelihood ratio tests for nested unconditional logistic regression models. Of the ⁷C₂ = 21 interactions, four were significant at the α = 0.05 level: DISC1 rs1411771–CIT rs10744743 OR = 3.07 (1.37, 6.98) p = 0.007; CIT rs3847960–CIT rs203332 OR = 2.90 (1.45, 5.79) p = 0.003; CIT rs3847960–CIT rs440299 OR = 2.16 (1.04, 4.46) p = 0.038; one survived Bonferroni correction (NDEL1 rs4791707–CIT rs10744743 OR = 4.44 (2.22, 8.88) p = 0.00013). Three of four interactions were validated via functional magnetic resonance imaging (fMRI) in an independent sample of healthy controls; risk associated alleles at both SNPs predicted prefrontal cortical inefficiency during the N-back task, a schizophrenia-linked intermediate biological phenotype: rs3847960–rs440299; rs1411771–rs10744743, rs4791707–rs10744743 (SPM5 p < 0.05, corrected), although we were unable to statistically replicate the interactions in other clinical samples. Interestingly, the CIT SNPs are proximal to exons that encode the DISC1 interaction domain. In addition, the 3′ UTR DISC1 rs1411771 is predicted to be an exonic splicing enhancer and the NDEL1 SNP is ~3,000 bp from the exon encoding the region of NDEL1 that interacts with the DISC1 protein, giving a plausible biological basis for epistasis signals validated by fMRI.     

未来气候变化下栎树猝死病菌在中国的适生性分析

基于中国国家有害生物检疫信息平台的有关记录和文献以及WoldClim网站,获取栎树猝死病菌的地理分布数据及气候数据,并用SPSS软件和刀切法筛选主导环境变量。利用MaxEnt生态位模型和ArcGIS软件,对栎树猝死病菌现代和未来情景下在我国的潜在适生区进行预测,并计算和绘制栎树猝死病菌高风险区质心转移轨迹。通过不同年份和不同气候情况下的受试者工作特征曲线(ROC)的训练集和测试集受试者工作特征曲线下面积(AUC)值均大于0.91,说明MaxEnt模型准确并适用于预测栎树猝死病菌在我国的潜在分布,同时结合其主要寄主植物的地理分布进一步增强预测模型的可信度。预测结果表明,最冷季度降水量、最冷季度平均温度、最干季度平均温度和年均降水量是影响栎树猝死病菌分布的主要环境变量。而2030s(2021—2040年)、2050s(2041—2060年)和2070s(2061—2080年)在3种气候情景下(SSP1-2.6、SSP2-4.5、SSP5-8.5),栎树猝死病菌的潜在适生区相较于现代情景下都有所增加。此外,高风险区面积在3个年代3种情景下的面积增长率均高于45%。高风险区质心变化的预测结果表...     

Examining the strength and possible causes of the relationship between fire history and Sudden Oak Death

Fire can be a dominant process in the ecology of forest vegetation and can also affect forest disease dynamics. Little is known about the relationship between fire and an emerging disease epidemic called Sudden Oak Death, which is caused by a new pathogen, Phytophthora ramorum. This disease has spread across a large, fire-prone portion of California, killing great numbers of oaks and tanoaks and infecting most associated woody plants. Suitable hosts cover a much broader geographic range, raising concern over where the disease may spread. To understand the strength and potential sensitivities of a fire–disease relationship, we examined geographic patterns of confirmed P. ramorum infections in relation to past fire history. We found these infections to be extremely rare within the perimeter of any area burned since 1950. This finding is not caused by spatial bias in sampling for the disease, and is robust to variation in host abundance scenarios and to aggregation of closely spaced sampling locations. We therefore investigated known fire-related factors that could result in significantly lower incidence of the disease in relatively recently burned landscapes. Chemical trends in post-fire environments can influence the success of pathogens like P. ramorum, either by increasing plant nutrient stress or by reducing the occurrence of chemicals antagonistic to Phytophthoras. Succession in the absence of fire leads to greater abundance of host species, which will provide increased habitat for P. ramorum; this will also increase intraspecific competition where these trees are abundant, and other density-dependent effects (e.g. shading) can reduce resource allocation to defenses. Despite these findings about a fire–disease relationship, a much deeper understanding is necessary before fire can be actively used as a tool in slowing the epidemic.     

Screening Trichoderma species for biological control activity against Phytophthora ramorum in soil

Despite efforts of eradication and sanitation, Phytophthora ramorum persists in the United States and abroad. Fungicides have limited effectiveness, but there are concerns that they may only inhibit pathogen growth and hasten resistance development after repeated fungicide applications. Biological control is an active control measure that can work continuously as long as the agent is alive and active. The goal of this study was to examine whether Trichoderma spp. have the potential as a biological control agent against P. ramorum. Sixteen Trichoderma spp. isolates were screened for mycoparasitism of P. ramorum in a dual culture assay. The different Trichoderma spp. isolates demonstrated variable mycoparasitic activities with some isolates showing no activity while others completely eliminated the pathogen after 4 weeks. Seven isolates of T. asperellum were consistent among replicated trials in eliminating recovery of P. ramorum from the exposed agar plugs and preventing leaf disk necrosis. Further testing of six T. asperellum isolates against two different P. ramorum isolates (A1 and A2 mating types) resulted in the same high level of mycoparasitic activity. Soil assays involving P. ramorum-infested potting mix and selected Trichoderma spp. isolates demonstrated that two isolates (04-22 and 02-64) were consistent among the repetitions to eliminate P. ramorum propagules to non-detectable levels. Based on these results, specific T. asperellum isolates have the potential to remediate P. ramorum-infested soil and have the potential to be developed into a commercially-viable product.     

The effect of salinity on the survival,growth, sporulation and infection of Phytophthora ramorum

Phytophthora ramorum has been found in waterways outside infested nurseries, but little is known about its behavior in water. This study examined the effect of salinity on survival, growth, sporulation, and infection. P. ramorum survival and growth was negatively correlated with salt concentration (range of 0–45 g l⁻¹), but showed a level of tolerance even at 45 g l⁻¹. No sporangia were observed in cultures with higher than 20 g l⁻¹ of salt and zoospores were not released from sporangia above 14 g l⁻¹. Water sources with different salinity were used to understand the environment where P. ramorum can survive and infect host material. Water from natural bodies and water amended with different salt concentrations were added to P. ramorum-infested sand and baited with rhododendron leaf disks. Infection decreased with increasing salt concentration and increased with higher initial concentration of P. ramorum. This research helps to better understand the effects of water quality on survival and infectivity of P. ramorum, expanding the potential survey range.     

Genome-wide identification of laccase gene family in three Phytophthora species

Phytophthora spp. is a primary pathogen in oomycete, causing economically and environmentally devastating epidemics of plants. Laccases have been found in all domains of life but have not been reported in oomycte. In this paper, laccase genes of Phytophthora spp. were identified in three genomes (Phytophthora capsici, Phytophthora sojae and Phytophthora ramorum). 18 laccase genes were identified in total, including four in P. capsici genome, six in P. sojae genome and eight in P. ramorum genome. Most of the predicted gene models shared typical fungal laccase character, possessing three conserved positions with one cysteine and ten histidine residues at these positions. Phylogenetic analysis illustrated that laccases from Phytophthora clustered into four clades, while fungal laccases clustered together. The results provided the theoretical ground for new hypotheses about the roles laccases in oomycetes and may guide the future research of these enzymes.     

AFLPs detect low genetic diversity for Phytophthora nemorosa and P. pseudosyringae in the US and Europe

In California and Oregon, two recently described oomycete forest pathogens, Phytophthora nemorosa and P. pseudosyringae, overlap in their host and geographic ranges with the virulent P. ramorum, causal agent of “sudden oak death.” Epidemiological observations, namely broader geographic distribution and lack of landscape-level mortality, led to the hypothesis they are native to this region, whereas multiple lines of evidence indicate P. ramorum is exotic to North America. We used AFLP analysis to measure genetic variability in the homothallic P. nemorosa and P. pseudosyringae and to evaluate the hypothesis of endemism. We analysed 39 P. nemorosa and 48 P. pseudosyringae isolates (29 American and 19 European) from throughout their geographic and host ranges. In the US, both P. nemorosa and P. pseudosyringae have a dominant AFLP clone with several closely related variants. There is no evidence that genetic diversity is partitioned by host or location in P. nemorosa, but the US P. pseudosyringae clonal lineage is largely nested within a more genetically variable European group. Though the absence of highly variable sampled source populations does not allow us to determine whether each species is native or introduced in the western US with certainty, the results are most consistent with the hypothesis that both are introduced — P. pseudosyringae perhaps from Europe. Invasive Phytophthora species are increasingly being implicated in emergent forest diseases, highlighting the need to identify and characterize both native and previously unknown introduced forest Phytophthoras.