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2. Scaling up from greenhouse resistance to fitness in the field for a host of an emerging forest disease

Author

Hayden, Katherine J, Garbelotto, Matteo, Dodd, Richard, and Wright, Jessica W

Subjects
Good Health and Well Being, forest management, generalized linear mixed models, host-parasite interactions, invasive species, natural selection and contemporary evolution, quantitative genetics, sudden oak death, survival analysis, host–parasite interactions, Medicinal and Biomolecular Chemistry, Evolutionary Biology, Genetics
Abstract

Forest systems are increasingly threatened by emergent, exotic diseases, yet management strategies for forest trees may be hindered by long generation times and scant background knowledge. We tested whether nursery disease resistance and growth traits have predictive value for the conservation of Notholithocarpus densiflorus, the host most susceptible to sudden oak death. We established three experimental populations to assess nursery growth and resistance to Phytophthora ramorum, and correlations between nursery-derived breeding values with seedling survival in a field disease trial. Estimates of nursery traits' heritability were low to moderate, with lowest estimates for resistance traits. Within the field trial, survival likelihood was increased in larger seedlings and decreased with the development of disease symptoms. The seed-parent family wide likelihood of survival was likewise correlated with family predictors for size and resistance to disease in 2nd year laboratory assays, though not resistance in 1st year leaf assays. We identified traits and seedling families with increased survivorship in planted tanoaks, and a framework to further identify seed parents favored for restoration. The additive genetic variation and seedling disease dynamics we describe hold promise to refine current disease models and expand the understanding of evolutionary dynamics of emergent infectious diseases in highly susceptible hosts.

Published
2013

8. Variation and heritability of host susceptibility to the introduced pathogen Phytophthora ramorum in tanoak (Lithocarpus densiflorus, proposed name Notholithocarpus densiflorus) populations

Author

Hayden, Katherine J.

Subjects
Ecology, Forestry, evolutionary ecology, forest pathology, host-pathogen interactions
Abstract

This dissertation presents a body of work collected from the very beginning of the outbreak of the introduced forest pathogen Phytophthora ramorum. The first data were collected the same year that P. ramorum was identified as the causal pathogen of the disease in California. The research, aimed at gathering the scientific knowledge necessary for an understanding and informed response to a new problem, placed an emphasis on bridging evolutionary ecological theory and management practice. First, my colleagues and I outline two quantitative polymerase chain reaction (qPCR) diagnostic assays for P. ramorum and their use as part of a widespread survey screening California plants for the pathogen. In Chapter 3, my colleagues and I report the first surveys of variation in susceptibility to P. ramorum on detached leaves of field-collected tanoak trees. We found low but non-zero heritability of susceptibility, and that the structure of phenotypic variation in this measure of susceptibility echoed that of neutral genetic markers. Finally, I describe the establishment of a greenhouse common garden population of tanoak seedlings concurrently with a field test garden in an infested natural area. Using these study populations, we calculated the heritability of susceptibility in detached leaves with much greater precision, and expanded the assay techniques and types of host resistance we measured. In so doing we discovered highly variable responses of seedling families to intact-seedling tip inoculations, the majority of which variation was due to genetic factors. With the qPCR detection techniques described in Chapter 2, we confirmed seedlings' infection within the first 7 months of the field test garden's establishment, with disease incidence rising over the course of the study. We found that both P. ramorum infection status and family origin have significant effects on tanoak survival in natural disease conditions. Together with the laboratory assays, our findings show that tanoak does possess some forms of genetic resistance to P. ramorum. The gardens we established provide the infrastructure necessary to determine if this resistance affects survival under natural conditions, to further investigate its inheritance and action, and to test the effect of varying environment and host genotype on its expression.

Published
2010

12. Evolution of morphological but not aggressiveness‐related traits following a major resistance breakdown in the poplar rust fungus, Melampsora larici‐populina.

Author

Maupetit, Agathe, Fabre, Bénédicte, Pétrowski, Jérémy, Andrieux, Axelle, De Mita, Stéphane, Frey, Pascal, Halkett, Fabien, and Hayden, Katherine J.

Subjects
RUST fungi, ADAPTIVE testing, CULTIVARS, AGRICULTURAL productivity, PHYTOPATHOGENIC microorganisms, POPLARS
Abstract

Crop varieties carrying qualitative resistance to targeted pathogens lead to strong selection pressure on parasites, often resulting in resistance breakdown. It is well known that qualitative resistance breakdowns modify pathogen population structure but few studies have analyzed the consequences on their quantitative aggressiveness‐related traits. The aim of this study was to characterize the evolution of these traits following a resistance breakdown in the poplar rust fungus, Melampsora larici‐populina. We based our experiment on three temporal populations sampled just before the breakdown event, immediately after and four years later. First, we quantified phenotypic differences among populations for a set of aggressiveness traits on a universally susceptible cultivar (infection efficiency, latent period, lesion size, mycelium quantity, and sporulation rate) and one morphological trait (mean spore volume). Then, we estimated heritability to establish which traits could be subjected to adaptive evolution and tested for evidence of selection. Our results revealed significant changes in the morphological trait but no variation in aggressiveness traits. By contrast, recent works have demonstrated that quantitative resistance (initially assumed more durable) could be eroded and lead to increased aggressiveness. Hence, this study is one example suggesting that the use of qualitative resistance may be revealed to be less detrimental to long‐term sustainable crop production. [ABSTRACT FROM AUTHOR]

Published
2021
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19. Sudden Oak Death: Interactions of the Exotic Oomycete Phytophthora ramorumwith Naïve North American Hosts

Author

Garbelotto, Matteo and Hayden, Katherine J.

Abstract

ABSTRACTTen years after a threatening and previously unknown disease of oaks and tanoaks appeared in coastal California, a significant amount of progress has been made toward the understanding of its causal agent Phytophthora ramorumand of the novel pathosystems associated with this exotic organism. However, a complete understanding of the ecology and epidemiology of this species still eludes us. In part, our inability to fully understand this organism is due to its phylogenetic, phylogeographic, phenotypic, and epidemiological complexities, all reviewed in this paper. Most lines of evidence suggest that the high degree of disease severity reported in California is not simply due to a generalized lack of resistance or tolerance in naïve hosts but also to an innate ability of the pathogen to survive in unfavorable climatic conditions and to reproduce rapidly when conditions become once again favorable.

Published
2012
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20. Dual Transcriptome Analysis Reveals Insights into Innate and Phosphite-Induced Resistance of Tanoak to Phytophthora ramorum.

Author

Takao Kasuga, Matteo Garbelotto, Eyre, Catherine A., Croucher, Peter J. P., Schechter, Shannon, Hayden, Katherine J., and Wright, Jessica W.

Subjects
DISEASE resistance of plants, PLANT defenses, MEMBRANE transport proteins, VITAMIN B6, PHYTOPHTHORA, GENETIC regulation
Abstract

Phosphites have been used in the control of sudden oak death, however, the precise mode of action of these compounds is not fully understood. In order to study the action of phosphites in the context of naturally occurring host resistance, we designed an inoculation experiment on four open-pollinated tanoak families, previously defined as partially resistant. Stems of treatmentindividuals were sprayed with phosphite, and 7 days later, distal leaves were inoculated with the sudden oak death pathogen, Phytophthora ramorum. Leaves from treated and untreated control plants were harvested for RNA extraction before and 7 days after inoculation, and transcriptomes of both host and pathogen were analyzed. We found that tanoak families differed in the presence of innate resistance and in the response to phosphite treatment. Sets of genes associated with innate resistance and with phosphite-induced resistance showed little overlap among tree families. However, sets of genes associated with innate resistance and with phosphite-induced resistance largely overlapped within a more susceptible but phosphite-treatment responsive tanoak family, supporting the hypothesis that phosphite treatment increases the resistance of susceptible host plants to Phytophthora infection. In addition, our dual RNA-Seq enabled us to monitor gene regulation of the pathogen in planta. Genes for energy generation such as those in the TCA cycle and genes for amino acid membrane transporters were upregulated, whereas elicitin genes were downregulated when comparing genic expression of P. ramorum in tanoak leaves relative to genic expression of P. ramorum mycelium in culture. We also found that genes of the pathogen involved in detoxification, such as ATP-binding cassette (ABC) transporters and vitamin B6 biosynthesis genes, were upregulated in phosphite-treated plants, but not in untreated plants. Upregulation of these genes has been observed for axenic culture of P. cinnamomi in the presence of phosphite, indicating these genes responded to the direct toxicity of phosphite. In summary, our dual RNA-Seq supports a dual mode of action of phosphite compounds, including a direct toxic effect on P. ramorum and an indirect enhancement of resistance in the tanoak host. [ABSTRACT FROM AUTHOR]

Published
2020

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