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California contains a diverse flora, and knowledge of the pathogens that threaten those plants is essential to managing their long-term health. To better understand threats to California plant health, a meta-analysis of Phytophthora detections within the state was conducted using publicly available sequences as a primary source of data rather than published records. Accessions of internal transcribed spacer (ITS) ribosomal DNA were cataloged from 800 Californian Phytophthora isolates, analyzed, and determined to correspond to 80 taxa, including several phylogenetically distinct provisional species. A number of Phytophthora taxa not previously reported from California were identified, including 20 described species. Pathways of introduction and spread were analyzed by categorizing isolates' origins, grouped by land-use: (i) agriculture, (ii) forests and other natural ecosystems, (iii) horticulture and nurseries, or (iv) restoration outplantings. The pooled Phytophthora metacommunities of the restoration outplantings and horticulture land-use categories were the most similar, whereas the communities pooled from forests and agriculture were least similar. Phytophthora cactorum, P. pini, P. pseudocryptogea, and P. syringae were identified in all four land-use categories, while 13 species were found in three. P. gonapodyides was the most common species by number of ITS accessions and exhibited the greatest diversity of ITS haplotypes. P. cactorum, P. ramorum, and P. nicotianae were associated with the greatest number of host genera. In this analysis, the Phytophthora spp. most prevalent in California differ from those compiled from the scientific literature.
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Ecossistema , Phytophthora , Phytophthora/genética , Florestas , Plantas , Agricultura , Horticultura , DNA Intergênico , CaliforniaRESUMO
A collection of 30 Phytophthora cactorum and 12 P. pseudotsugae (subclade 1a) strains isolated from several recent surveys across California was phylogenetically compared to a worldwide collection of 112 conspecific strains using sequences from three barcoding loci. The surveys baited P. cactorum from soil and water across a wide variety of forested ecosystems with a geographic range of more than 1000 km. Two cosmopolitan lineages were identified within the widespread P. cactorum, one being mainly associated with strawberry production and the other more closely associated with apple orchards, oaks and ornamental trees. Two other well-sampled P. cactorum lineages, including one that dominated Californian restoration outplantings, were only found in the western United States, while a third was only found in Japan. Coastal California forest isolates of both Phytophthora species exhibited considerable diversity, suggesting both may be indigenous to the state. Many isolates with sequence accessions deposited as P. cactorum were determined to be P. hedraiandra and P. ×serendipita, with one hybrid lineage appearing relatively common across Europe and Asia. This study contains the first report of P. pseudotsugae from the state of California and one of the only reports of that species since its original description.
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Mega-fires of unprecedented size, intensity and socio-economic impacts have surged globally due to climate change, fire suppression and development. Soil microbiomes are critical for post-fire plant regeneration and nutrient cycling, yet how mega-fires impact the soil microbiome remains unclear. We had a serendipitous opportunity to obtain pre- and post-fire soils from the same sampling locations after the 2016 Soberanes mega-fire burned with high severity throughout several of our established redwood-tanoak plots. This makes our study the first to examine microbial fire response in redwood-tanoak forests. We re-sampled soils immediately post-fire from two burned plots and one unburned plot to elucidate the effect of mega-fire on soil microbiomes. We used Illumina MiSeq sequencing of 16S and ITS1 sequences to determine that bacterial and fungal richness were reduced by 38%-70% in burned plots, with richness unchanged in the unburned plot. Fire altered composition by 27% for bacteria and 24% for fungi, whereas the unburned plots experienced no change in fungal and negligible change in bacterial composition. Pyrophilous taxa that responded positively to fire were phylogenetically conserved, suggesting shared evolutionary traits. For bacteria, fire selected for increased Firmicutes and Actinobacteria. For fungi, fire selected for the Ascomycota classes Pezizomycetes and Eurotiomycetes and for a Basidiomycota class of heat-resistant Geminibasidiomycete yeasts. We build from Grime's competitor-stress tolerator-ruderal (C-S-R) framework and its recent microbial applications to show how our results might fit into a trait-based conceptual model to help predict generalizable microbial responses to fire.
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Ascomicetos , Incêndios , Sequoia , Bactérias/genética , Ecossistema , Florestas , SoloRESUMO
Since species vary in abundance and host competence (i.e., ability to get infected and transmit a pathogen), changes in species composition caused by biodiversity loss impacts disease dynamics. Forecasting effects of species composition on disease depends on community (dis)assembly, processes determining how species are added to (or lost from) communities. We simulated community assembly by planting mesocosms, nested along a richness gradient, and tested how relationships between richness, species assembly order, and overall density affect disease risk. Mesocosms with up to six crop species of varying competence were inoculated with a soilborne fungal pathogen, Rhizoctonia solani. Disease was measured as species-level prevalence, community-level prevalence, and total number of diseased plants. Regardless of metric, richness limited disease when species assembly order negatively correlated with competence and total density remained unchanged with richness. When density increased with richness or species assembled randomly, richness primarily correlated positively or weakly with disease. Our results align with theoretical expectations and represent the first empirical study to test the influence of species densities, assembly order, and competence on diversity-disease relationships.
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Biodiversidade , PlantasRESUMO
One Health is a transdisciplinary approach used to address complex concerns related to human, animal, plant, and ecosystem health. One Health frameworks and operational tools are available to support countries and communities, particularly for the prevention and control of zoonotic diseases and antimicrobial resistance and the protection of food safety. However, One Health has yet to be implemented in a manner that fully considers the complexities and interconnectedness of the diverse influences that have impacts at a larger system level. This lack of consideration can undermine the sustainability of any positive outcomes. To ensure the One Health approach can function effectively within the new global context of converging and escalating health, social, economic, and ecological crises, it must evolve and expand in three overlapping dimensions: (1) Scope: the partners, knowledge, and knowledge systems included, (2) Approach: the techniques, methodologies, and scholarship considered, and (3) Worldview inclusivity: the interweaving of other worldviews together with the mainstream scientific worldview that currently predominates. Diverse partners and knowledge from outside the mainstream health and scientific sectors, including Indigenous peoples and representatives of local communities, and traditionally generated knowledge, must be included. These systems of knowledge can then be braided together with mainstream science to comprise a holistic framework for decision-making. Scholarship and methodologies being applied in other fields and contexts to solve complex challenges and manage uncertainty, such as collaborative governance, social-ecologic systems theory, and complexity science, must be recognized and incorporated. The spectrum of considered worldviews must also expand to authentically integrate the expanded scope and approach into action and sustainable impact. By increasing community and social engagement and by recognizing and entwining different worldviews, the plurality of disciplines, and traditional and scientific ways of knowing to address community concerns in the contexts in which they exist, we can ensure that One Health remains effective and true to its paradigm in our rapidly changing and complex world.
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Ecossistema , Saúde Única , Humanos , Animais , ZoonosesRESUMO
Understanding why diversity sometimes limits disease is essential for managing outbreaks; however, mechanisms underlying this 'dilution effect' remain poorly understood. Negative diversity-disease relationships have previously been detected in plant communities impacted by an emerging forest disease, sudden oak death. We used this focal system to empirically evaluate whether these relationships were driven by dilution mechanisms that reduce transmission risk for individuals or from the fact that disease was averaged across the host community. We integrated laboratory competence measurements with plant community and symptom data from a large forest monitoring network. Richness increased disease risk for bay laurel trees, dismissing possible dilution mechanisms. Nonetheless, richness was negatively associated with community-level disease prevalence because the disease was aggregated among hosts that vary in disease susceptibility. Aggregating observations (which is surprisingly common in other dilution effect studies) can lead to misinterpretations of dilution mechanisms and bias towards a negative diversity-disease relationship.
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Árvores , Umbellularia , Suscetibilidade a Doenças , Humanos , Doenças das Plantas , PrevalênciaRESUMO
Although healthy plants are vital to human and animal health, plant health is often overlooked in the One Health literature. Plants provide over 80% of the food consumed by humans and are the primary source of nutrition for livestock. However, plant diseases and pests often threaten the availability and safety of plants for human and animal consumption. Global yield losses of important staple crops can range up to 30% and hundreds of billions of dollars in lost food production. To demonstrate the complex interrelationships between plants and public health, we present four case studies on plant health issues directly tied to food safety and/or security, and how a One Health approach influences the perception and mitigation of these issues. Plant pathogens affect food availability and consequently food security through reductions in yield and plant mortality as shown through the first case study of banana Xanthomonas wilt in East and Central Africa. Case studies 2, 3 and 4 highlight ways in which the safety of plant-based foods can also be compromised. Case study 2 describes the role of mycotoxin-producing plant-colonizing fungi in human and animal disease and examines lessons learned from outbreaks of aflatoxicosis in Kenya. Plants may also serve as vectors of human pathogens as seen in case study 3, with an example of Escherichia coli (E. coli) contamination of lettuce in North America. Finally, case study 4 focuses on the use of pesticides in Suriname, a complex issue intimately tied to food security though protection of crops from diseases and pests, while also a food safety issue through misuse. These cases from around the world in low to high income countries point to the need for interdisciplinary teams to solve complex plant health problems. Through these case studies, we examine challenges and opportunities moving forward for mitigating negative public health consequences and ensuring health equity. Advances in surveillance technology and functional and streamlined workflow, from data collection, analyses, risk assessment, reporting, and information sharing are needed to improve the response to emergence and spread of plant-related pathogens and pests. Our case studies point to the importance of collaboration in responses to plant health issues that may become public health emergencies and the value of the One Health approach in ensuring food safety and food security for the global population.
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Sudden oak death (SOD), caused by the generalist pathogen Phytophthora ramorum, has profoundly impacted California coastal ecosystems. SOD has largely been treated as a two-host system, with Umbellularia californica as the most transmissive host, Notholithocarpus densiflorus less so, and remaining species as epidemiologically unimportant. However, this understanding of transmission potential primarily stems from observational field studies rather than direct measurements on the diverse assemblage of plant species. Here, we formally quantify the sporulation potential of common plant species inhabiting SOD-endemic ecosystems on the California coast in the Big Sur region. This study allows us to better understand the pathogen's basic biology, trajectory of SOD in a changing environment, and how the entire host community contributes to disease risk. Leaves were inoculated in a controlled laboratory environment and assessed for production of sporangia and chlamydospores, the infectious and resistant propagules, respectively. P. ramorum was capable of infecting every species in our study and almost all species produced spores to some extent. Sporangia production was greatest in N. densiflorus and U. californica and the difference was insignificant. Even though other species produced much less, quantities were nonzero. Thus, additional species may play a previously unrecognized role in local transmission. Chlamydospore production was highest in Acer macrophyllum and Ceanothus oliganthus, raising questions about the role they play in pathogen persistence. Lesion size did not consistently correlate with the production of either sporangia or chlamydospores. Overall, we achieved an empirical foundation to better understand how community composition affects transmission of P. ramorum.
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Phytophthora , Ecossistema , Doenças das Plantas , Folhas de Planta , UmbellulariaRESUMO
It is commonly assumed that asexual lineages are short-lived evolutionarily, yet many asexual organisms can generate genetic and phenotypic variation, providing an avenue for further evolution. Previous work on the asexual plant pathogen Phytophthora ramorum NA1 revealed considerable genetic variation in the form of Structural Variants (SVs). To better understand how SVs arise and their significance to the California NA1 population, we studied the evolutionary histories of SVs and the forest conditions associated with their emergence. Ancestral state reconstruction suggests that SVs arose by somatic mutations among multiple independent lineages, rather than by recombination. We asked if this unusual phenomenon of parallel evolution between isolated populations is transmitted to extant lineages and found that SVs persist longer in a population if their genetic background had a lower mutation load. Genetic parallelism was also found in geographically distant demes where forest conditions such as host density, solar radiation, and temperature, were similar. Parallel SVs overlap with genes involved in pathogenicity such as RXLRs and have the potential to change the course of an epidemic. By combining genomics and environmental data, we identified an unexpected pattern of repeated evolution in an asexual population and identified environmental factors potentially driving this phenomenon.
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Invasive forest pathogens can harm cultural, economic, and ecological resources. Here, we demonstrate the potential of endemic tree pathogen resistance in forest disease management using Phytophthora ramorum, cause of sudden oak death, in the context of management of tanoak (Notholithocarpus densiflorus), an ecologically unique and highly valued tree within Native American communities of northern California and southern Oregon in the United States. We surveyed resistance to P. ramorum on the Hoopa Valley Indian Reservation and Yurok Indian Reservation in a set of study sites with variable management intensities. Variation in resistance was found at all sites with similar mean and variation across stands, and resistance tended to have a random spatial distribution within stands but was not associated with previous stand management (thinning or prescribed fire) or structural characteristics such as tree density, basal area, or pairwise relatedness among study trees. These results did not suggest host, genetic, management, or environment interactions that could be easily leveraged into treatments to increase the prevalence of resistant trees. We applied epidemiological models to assess the potential application of endemic resistance in this system and to examine our assumption that in planta differences in lesion size-our measure of resistance-reflect linkages between mortality and transmission (resistance) versus reduced mortality with no change in transmission (tolerance). This assumption strongly influenced infection dynamics but changes in host populations-our conservation focus-was dependent on community-level variation in transmission. For P. ramorum, slowing mortality rates (whether by resistance or tolerance) conserves host resources when a second source of inoculum is present; these results are likely generalizable to pathogens with a broader host range. However, when the focal host is the sole source of inoculum, increasing tolerant individuals led to the greatest stand-level pathogen accumulation in our model. When seeking to use variation in mortality rates to affect conservation strategies, it is important to understand how these traits are linked with transmission because tolerance will be more useful for management in mixed-host stands that are already invaded, compared with single-host stands with low or no pathogen presence, where resistance will have the greatest conservation benefits.
Assuntos
Fagaceae/microbiologia , Phytophthora/patogenicidade , Doenças das Plantas/microbiologia , California , Conservação dos Recursos Naturais , Resistência à Doença , Oregon , Árvores/microbiologiaRESUMO
Human-altered ecological disturbances may challenge system resilience and disrupt biological legacies maintaining ecosystem recovery. Yet, the extent to which novel regimes challenge these legacies varies. This may be partially explained by differences in the vulnerability of life history strategies to disturbance characteristics. In the fire-prone, resprouter-dominated coast redwood forests of California, the introduced disease sudden oak death (SOD) alters fuel profiles, fire behavior, and aboveground tree mortality; however, this system is dominated by resprouting trees that are well-adapted to aboveground damage, and belowground survival of individuals may represent the principal biological legacy connecting pre- and post-fire communities. Much of the research exploring altered disturbances and forest recovery has focused on legacies determined by seed dispersal and aboveground survival of adults. In this work, we use pre- and post-fire data from a long-term monitoring network to assess the impacts of novel disturbance interactions between wildfire and SOD on the belowground survival and vegetative reproduction of resprouters. We found that increasing accumulation of coarse woody surface fuels from SOD-killed hosts decreased the likelihood of belowground survival for resprouting tanoak trees, but not for redwoods. Tanoaks' belowground survival was negatively related to substrate burn severity, which increased with the volume of surface fuels from hosts, suggesting heat damage as a possible mechanism influencing altered patterns of resprouter mortality. These impacts increased with decreasing tree size. By contrast, redwood and tanoak trees that survived both disturbances resprouted more vigorously, regardless of post-fire infection by P. ramorum, and generated similar recruitment at the stand level. Our results demonstrate that disease-fire interactions can narrow recruitment filters for resprouters, which could impact long-term population and demographic structure; yet, compounded disturbance may also reduce stand density and disease pressure, allowing competitive release of survivors. Resprouters displayed vulnerabilities to altered disturbance, but our research suggests that legacies maintained by resprouting may be more resilient to certain compounded disturbances, compared to seed-obligate species, because of high rates of individual survival under increasingly severe events. These trends have important implications for conservation of declining tree species in SOD-impacted forests, as well as predictions of human impacts in other disturbance-prone systems where resprouters are present.
Assuntos
Incêndios , Árvores , California , Ecossistema , FlorestasRESUMO
BACKGROUND: Accumulating evidence suggests that genome plasticity allows filamentous plant pathogens to adapt to changing environments. Recently, the generalist plant pathogen Phytophthora ramorum has been documented to undergo irreversible phenotypic alterations accompanied by chromosomal aberrations when infecting trunks of mature oak trees (genus Quercus). In contrast, genomes and phenotypes of the pathogen derived from the foliage of California bay (Umbellularia californica) are usually stable. We define this phenomenon as host-induced phenotypic diversification (HIPD). P. ramorum also causes a severe foliar blight in some ornamental plants such as Rhododendron spp. and Viburnum spp., and isolates from these hosts occasionally show phenotypes resembling those from oak trunks that carry chromosomal aberrations. The aim of this study was to investigate variations in phenotypes and genomes of P. ramorum isolates from non-oak hosts and substrates to determine whether HIPD changes may be equivalent to those among isolates from oaks. RESULTS: We analyzed genomes of diverse non-oak isolates including those taken from foliage of Rhododendron and other ornamental plants, as well as from natural host species, soil, and water. Isolates recovered from artificially inoculated oak logs were also examined. We identified diverse chromosomal aberrations including copy neutral loss of heterozygosity (cnLOH) and aneuploidy in isolates from non-oak hosts. Most identified aberrations in non-oak hosts were also common among oak isolates; however, trisomy, a frequent type of chromosomal aberration in oak isolates was not observed in isolates from Rhododendron. CONCLUSION: This work cross-examined phenotypic variation and chromosomal aberrations in P. ramorum isolates from oak and non-oak hosts and substrates. The results suggest that HIPD comparable to that occurring in oak hosts occurs in non-oak environments such as in Rhododendron leaves. Rhododendron leaves are more easily available than mature oak stems and thus can potentially serve as a model host for the investigation of HIPD, the newly described plant-pathogen interaction.
Assuntos
Aberrações Cromossômicas , Genômica , Interações Hospedeiro-Parasita , Fenótipo , Phytophthora/genética , Variações do Número de Cópias de DNA , Haplótipos , Phytophthora/fisiologia , Umbellularia/parasitologiaRESUMO
Phylogenetic relationships between thirteen species of downy mildew and 103 species of Phytophthora (plant-pathogenic oomycetes) were investigated with two nuclear and four mitochondrial loci, using several likelihood-based approaches. Three Phytophthora taxa and all downy mildew taxa were excluded from the previously recognized subgeneric clades of Phytophthora, though all were strongly supported within the paraphyletic genus. Downy mildews appear to be polyphyletic, with graminicolous downy mildews (GDM), brassicolous downy mildews (BDM) and downy mildews with colored conidia (DMCC) forming a clade with the previously unplaced Phytophthora taxon totara; downy mildews with pyriform haustoria (DMPH) were placed in their own clade with affinities to the obligate biotrophic P. cyperi. Results suggest the recognition of four additional clades within Phytophthora, but few relationships between clades could be resolved. Trees containing all twenty extant downy mildew genera were produced by adding partial coverage of seventeen additional downy mildew taxa; these trees supported the monophyly of the BDMs, DMCCs and DMPHs but suggested that the GDMs are paraphyletic in respect to the BDMs or polyphyletic. Incongruence between nuclear-only and mitochondrial-only trees suggests introgression may have occurred between several clades, particularly those containing biotrophs, questioning whether obligate biotrophic parasitism and other traits with polyphyletic distributions arose independently or were horizontally transferred. Phylogenetic approaches may be limited in their ability to resolve some of the complex relationships between the "subgeneric" clades of Phytophthora, which include twenty downy mildew genera and hundreds of species.
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Peronospora/genética , Filogenia , Phytophthora/genética , Núcleo Celular/genética , Funções Verossimilhança , Mitocôndrias/genética , Doenças das Plantas/parasitologiaRESUMO
Phytophthora spp. are regularly recovered from streams but their ecology in aquatic environments is not well understood. Phytophthora ramorum, invasive in California forests, persists in streams at times when sporulation in the canopy is absent, suggesting that it reproduces in the water. Streams are also inhabited by resident, clade 6 Phytophthora spp., believed to be primarily saprotrophic. We conducted experiments to determine whether differences of trophic specialization exist between these two taxa, and investigated how this may affect their survival and competition on stream leaf litter. P. ramorum effectively colonized fresh (live) rhododendron leaves but not those killed by freezing or drying, whereas clade 6 species colonized all leaf types. However, both taxa were recovered from naturally occurring California bay leaf litter in streams. In stream experiments, P. ramorum colonized bay leaves rapidly at the onset; however, colonization was quickly succeeded by clade 6 species. Nevertheless, both taxa persisted in leaves over 16 weeks. Our results confirm that clade 6 Phytophthora spp. are competent saprotrophs and, though P. ramorum could not colonize dead tissue, early colonization of suitable litter allowed it to survive at a low level in decomposing leaves.
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Phytophthora/fisiologia , Doenças das Plantas , Folhas de Planta/microbiologia , Rios , Umbellularia/microbiologia , Florestas , Phytophthora/classificação , Fatores de TempoRESUMO
Fungi in the genus Geosmithia (Ascomycota: Hypocreales) are frequent associates of bark beetles and woodborers that colonize hardwood and coniferous trees. One species, Geosmithia morbida, is an economically damaging invasive species. The authors surveyed the Geosmithia species of California and Colorado, USA, to (i) provide baseline data on taxonomy of Geosmithia and beetle vector specificity across the western USA; (ii) investigate the subcortical beetle fauna for alternative vectors of the invasive G. morbida; and (iii) interpret the community composition of this region within the emerging global biogeography of Geosmithia. Geosmithia was detected in 87% of 126 beetle samples obtained from 39 plant species. Twenty-nine species of Geosmithia were distinguished, of which 13 may be new species. Bark beetles from hardwoods, Cupressus, and Sequoia appear to be regular vectors, with Geosmithia present in all beetle gallery systems examined. Other subcortical insects appear to vector Geosmithia at lower frequencies. Overall, most Geosmithia have a distinct level of vector specificity (mostly high, sometimes low) enabling their separation to generalists and specialists. Plant pathogenic Geosmithia morbida was not found in association with any other beetle besides Pityophthorus juglandis. However, four additional Geosmithia species were found in P. juglandis galleries. When integrated with recent data from other continents, a global pattern of Geosmithia distribution across continents, latitudes, and vectors is emerging: of the 29 Geosmithia species found in the western USA, 12 have not been reported outside of the USA. The most frequently encountered species with the widest global distribution also had the broadest range of beetle vectors. Several Geosmithia spp. with very narrow vector ranges in Europe exhibited the similar degree of specialization in the USA. Such strong canalization in association could reflect an ancient origin of each individual association, or a recent origin and a subsequent diversification in North America.
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Biodiversidade , Besouros/microbiologia , Hypocreales/classificação , Insetos Vetores/microbiologia , Animais , California , Besouros/classificação , Colorado , DNA Fúngico/genética , Hypocreales/isolamento & purificação , Espécies Introduzidas , Fenótipo , Filogenia , Doenças das Plantas/microbiologia , Especificidade da Espécie , Árvores/microbiologiaRESUMO
Fire and forest disease have significant ecological impacts, but the interactions of these two disturbances are rarely studied. We measured soil C, N, Ca, P, and pH in forests of the Big Sur region of California impacted by the exotic pathogen Phytophthora ramorum, cause of sudden oak death, and the 2008 Basin wildfire complex. In Big Sur, overstory tree mortality following P. ramorum invasion has been extensive in redwood and mixed evergreen forests, where the pathogen kills true oaks and tanoak (Notholithocarpus densiflorus). Sampling was conducted across a full-factorial combination of disease/no disease and burned/unburned conditions in both forest types. Forest floor organic matter and associated nutrients were greater in unburned redwood compared to unburned mixed evergreen forests. Post-fire element pools were similar between forest types, but lower in burned-invaded compared to burned-uninvaded plots. We found evidence disease-generated fuels led to increased loss of forest floor C, N, Ca, and P. The same effects were associated with lower %C and higher PO4-P in the mineral soil. Fire-disease interactions were linear functions of pre-fire host mortality which was similar between the forest types. Our analysis suggests that these effects increased forest floor C loss by as much as 24.4 and 21.3 % in redwood and mixed evergreen forests, respectively, with similar maximum losses for the other forest floor elements. Accumulation of sudden oak death generated fuels has potential to increase fire-related loss of soil nutrients at the region-scale of this disease and similar patterns are likely in other forests, where fire and disease overlap.
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Carbono , Solo , Incêndios , Florestas , Phytophthora , Doenças das Plantas , ÁrvoresRESUMO
Sudden oak death, caused by Phytophthora ramorum, has killed millions of oak and tanoak in California since its first detection in 1995. Despite some localized small-scale management, there has been no large-scale attempt to slow the spread of the pathogen in California. Here we use a stochastic spatially explicit model parameterized using data on the spread of P. ramorum to investigate whether and how the epidemic can be controlled. We find that slowing the spread of P. ramorum is now not possible, and has been impossible for a number of years. However, despite extensive cryptic (i.e., presymptomatic) infection and frequent long-range transmission, effective exclusion of the pathogen from large parts of the state could, in principle, have been possible were it to have been started by 2002. This is the approximate date by which sufficient knowledge of P. ramorum epidemiology had accumulated for large-scale management to be realistic. The necessary expenditure would have been very large, but could have been greatly reduced by optimizing the radius within which infected sites are treated and careful selection of sites to treat. In particular, we find that a dynamic strategy treating sites on the epidemic wave front leads to optimal performance. We also find that "front loading" the budget, that is, treating very heavily at the start of the management program, would greatly improve control. Our work introduces a framework for quantifying the likelihood of success and risks of failure of management that can be applied to invading pests and pathogens threatening forests worldwide.
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Florestas , Phytophthora , Doenças das Plantas/terapia , Quercus/parasitologia , California , Epidemias , Doenças das Plantas/prevenção & controle , Risco , Fatores de TempoRESUMO
BACKGROUND: Aneuploidy 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. RESULTS: We 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. CONCLUSION: This 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.
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Aneuploidia , Fenótipo , Phytophthora/genética , California , Variações do Número de Cópias de DNA , Elementos de DNA Transponíveis , Duplicação Gênica , Perfilação da Expressão Gênica , Ligação Genética , Genótipo , Perda de Heterozigosidade , Doenças das Plantas/microbiologia , Polimorfismo de Nucleotídeo Único , Quercus/microbiologia , TranscriptomaRESUMO
The challenges posed by observing host-pathogen-environment interactions across large geographic extents and over meaningful time scales limit our ability to understand and manage wildland epidemics. We conducted a landscape-scale, longitudinal study designed to analyze the dynamics of sudden oak death (an emerging forest disease caused by Phytophthora ramorum) across hierarchical levels of ecological interactions, from individual hosts up to the community and across the broader landscape. From 2004 to 2011, we annually assessed disease status of 732 coast live oak, 271 black oak, and 122 canyon live oak trees in 202 plots across a 275-km2 landscape in central California. The number of infected oak stems steadily increased during the eight-year study period. A survival analysis modeling framework was used to examine which level of ecological heterogeneity best predicted infection risk of susceptible oak species, considering variability at the level of individuals (species identity, stem size), the community (host density, inoculum load, and species richness), and the landscape (seasonal climate variability, habitat connectivity, and topographic gradients). After accounting for unobserved risk shared among oaks in the same plot, survival models incorporating heterogeneity across all three levels better predicted oak infection than did models focusing on only one level. We show that larger oak trees (especially coast live oak) were more susceptible, and that interannual variability in inoculum production by the highly infectious reservoir host, California bay laurel, more strongly influenced disease risk than simply the density of this important host. Concurrently, warmer and wetter rainy-season conditions in consecutive years intensified infection risk, presumably by creating a longer period of inoculum build-up and increased probability of pathogen spillover from bay laurel to oaks. Despite the presence of many alternate host species, we found evidence of pathogen dilution, where less competent hosts in species-rich communities reduce pathogen transmission and overall risk of oak infection. These results identify key parameters driving the dynamics of emerging infectious disease in California woodlands, while demonstrating how multiple levels of ecological heterogeneity jointly determine epidemic trajectories in wildland settings.
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Florestas , Phytophthora/fisiologia , Doenças das Plantas/microbiologia , Quercus/microbiologia , California , Fatores de TempoRESUMO
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.