Caterina Villari
Ohio State University
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Publication
Featured researches published by Caterina Villari.
New Phytologist | 2016
Caterina Villari; Daniel A. Herms; Justin G. A. Whitehill; Don Cipollini; Pierluigi Bonello
We review the literature on host resistance of ash to emerald ash borer (EAB, Agrilus planipennis), an invasive species that causes widespread mortality of ash. Manchurian ash (Fraxinus mandshurica), which coevolved with EAB, is more resistant than evolutionarily naïve North American and European congeners. Manchurian ash was less preferred for adult feeding and oviposition than susceptible hosts, more resistant to larval feeding, had higher constitutive concentrations of bark lignans, coumarins, proline, tyramine and defensive proteins, and was characterized by faster oxidation of phenolics. Consistent with EAB being a secondary colonizer of coevolved hosts, drought stress decreased the resistance of Manchurian ash, but had no effect on constitutive bark phenolics, suggesting that they do not contribute to increased susceptibility in response to drought stress. The induced resistance of North American species to EAB in response to the exogenous application of methyl jasmonate was associated with increased bark concentrations of verbascoside, lignin and/or trypsin inhibitors, which decreased larval survival and/or growth in bioassays. This finding suggests that these inherently susceptible species possess latent defenses that are not induced naturally by larval colonization, perhaps because they fail to recognize larval cues or respond quickly enough. Finally, we propose future research directions that would address some critical knowledge gaps.
Tree Physiology | 2014
Caterina Villari; Massimo Faccoli; Andrea Battisti; Pierluigi Bonello; Lorenzo Marini
Plants protect themselves from pathogens and herbivores through fine-tuned resource allocation, including trade-offs among resource investments to support constitutive and inducible defences. However, empirical research, especially concerning conifers growing under natural conditions, is still scarce. We investigated the complexity of constitutive and induced defences in a natural Scots pine (Pinus sylvestris L.) stand under growth-limiting conditions typical of alpine environments. Phenotypic trade-offs at three hierarchical levels were tested by investigating the behaviour of phenolic compounds and terpenoids of outer bark and phloem. We tested resource-derived phenotypic correlations between (i) constitutive and inducible defences vs tree ring growth, (ii) different constitutive defence metabolites and (iii) constitutive concentration and inducible variation of individual metabolites. Tree ring growth was positively correlated only with constitutive concentration of total terpenoids, and no overall phenotypic trade-offs between different constitutive defensive metabolites were found. At the lowest hierarchical level tested, i.e., at the level of relationship between constitutive and inducible variation of individual metabolites, we found that different compounds displayed different behaviours; we identified five different defensive metabolite response types, based on direction and strength of the response, regardless of tree age and growth rate. Therefore, under growth-limiting field conditions, Scots pine appears to utilize varied and complex outer bark and phloem defence chemistry, in which only part of the constitutive specialized metabolism is influenced by tree growth, and individual components do not appear to be expressed in a mutually exclusive manner in either constitutive or inducible metabolism.
Applied and Environmental Microbiology | 2013
Caterina Villari; Jennifer A. Tomlinson; Andrea Battisti; N. Boonham; Paolo Capretti; Massimo Faccoli
ABSTRACT Loop-mediated isothermal amplification (LAMP) is an alternative amplification technology which is highly sensitive and less time-consuming than conventional PCR-based methods. Three LAMP assays were developed, two for detection of species of symbiotic blue stain fungi associated with Ips acuminatus, a bark beetle infesting Scots pine (Pinus sylvestris), and an additional assay specific to I. acuminatus itself for use as a control. In common with most bark beetles, I. acuminatus is associated with phytopathogenic blue stain fungi involved in the process of exhausting tree defenses, which is a necessary step for the colonization of the plant by the insect. However, the identity of the main blue stain fungus vectored by I. acuminatus was still uncertain, as well as its frequency of association with I. acuminatus under outbreak and non-outbreak conditions. In this study, we employed LAMP technology to survey six populations of I. acuminatus sampled from the Southern Alps. Ophiostoma clavatum was detected at all sampling sites, while Ophiostoma brunneo-ciliatum, reported in part of the literature as the main blue stain fungus associated with I. acuminatus, was not detected on any of the samples. These results are consistent with the hypothesis that O. clavatum is the main blue stain fungus associated with I. acuminatus in the Southern Alps. The method developed in the course of this work provides a molecular tool by which it will be easy to screen populations and derive important data regarding the ecology of the species involved.
Tree Physiology | 2012
Caterina Villari; Andrea Battisti; Sourav Chakraborty; Marco Michelozzi; Pierluigi Bonello; Massimo Faccoli
Conifer bark beetles are often associated with fungal complexes whose components have different ecological roles. Some associated species are nutritionally obligate fungi, serving as nourishment to the larvae, whereas others are pathogenic blue-stain fungi known to be involved in the interaction with host defenses. In this study we characterized the local and systemic defense responses of Scots pine (Pinus sylvestris L.) against Ophiostoma brunneo-ciliatum Math. (a blue-stain pathogen) and Hyalorhinocladiella macrospora (Franke-Grosm.) Harr. (a nutritional fungus). These fungi are the principal associates of the pine engraver beetle, Ips acuminatus (Gyll.). Host responses were studied following inoculation with the fungi, singly and as a fungal complex, and by identifying and quantifying terpenoids, phenolic compounds and lignin. Although the length of the necrotic lesions differed between control (wound) and fungal treatments, only two compounds (pinosylvin monomethyl ether and (+)-α-pinene) were significantly affected by the presence of the fungi, indicating that Scots pine has a generic, rather than specific, induced response. The fact that both nutritional and blue-stain fungi triggered comparable induced defense responses suggests that even a non-pathogenic fungus may participate in exhausting host plant defenses, indirectly assisting in the beetle establishment process. Our findings contribute to the further development of current theory on the role of associated fungal complexes in bark beetle ecology.
Plant Cell and Environment | 2017
Kenneth F. Raffa; Charles J. Mason; Pieruluigi Bonello; Stephen P. Cook; Nadir Erbilgin; Ken Keefover-Ring; Jennifer G. Klutsch; Caterina Villari; Philip A. Townsend
Warming climate is allowing tree-killing bark beetles to expand their ranges and access naïve and semi-naïve conifers. Conifers respond to attack using complex mixtures of chemical defences that can impede beetle success, but beetles exploit some compounds for host location and communication. Outcomes of changing relationships will depend on concentrations and compositions of multiple host compounds, which are largely unknown. We analysed constitutive and induced chemistries of Dendroctonus ponderosaes primary historical host, Pinus contorta, and Pinus albicaulis, a high-elevation species whose encounters with this beetle are transitioning from intermittent to continuous. We quantified multiple classes of terpenes, phenolics, carbohydrates and minerals. Pinus contorta had higher constitutive allocation to, and generally stronger inducibility of, compounds that resist these beetle-fungal complexes. Pinus albicaulis contained higher proportions of specific monoterpenes that enhance pheromone communication, and lower induction of pheromone inhibitors. Induced P. contorta increased insecticidal and fungicidal compounds simultaneously, whereas P. albicaulis responses against these agents were inverse. Induced terpene accumulation was accompanied by decreased non-structural carbohydrates, primarily sugars, in P. contorta, but not P. albicaulis, which contained primarily starches. These results show some host species with continuous exposure to bark beetles have more thoroughly integrated defence syndromes than less-continuously exposed host species.
Tree Physiology | 2015
Patrick Sherwood; Caterina Villari; Paolo Capretti; Pierluigi Bonello
Plants experiencing drought stress are frequently more susceptible to pathogens, likely via alterations in physiology that create favorable conditions for pathogens. Common plant responses to drought include the production of reactive oxygen species (ROS) and the accumulation of free amino acids (AAs), particularly proline. These same phenomena also frequently occur during pathogenic attack. Therefore, drought-induced perturbations in AA and ROS metabolism could potentially contribute to the observed enhanced susceptibility. Furthermore, nitrogen (N) availability can influence AA accumulation and affect plant resistance, but its contributions to drought-induced susceptibility are largely unexplored. Here we show that drought induces accumulation of hydrogen peroxide (H2O2) in Austrian pine (Pinus nigra Arnold) shoots, but that shoot infection by the blight and canker pathogen Diplodia sapinea (Fr.) Fuckel leads to large reductions in H2O2 levels in droughted plants. In in vitro assays, H2O2 was toxic to D. sapinea, and the fungus responded to this oxidative stress by increasing catalase and peroxidase activities, resulting in substantial H2O2 degradation. Proline increased in response to drought and infection when examined independently, but unlike all other AAs, proline further increased in infected shoots of droughted trees. In the same tissues, the proline precursor, glutamate, decreased significantly. Proline was found to protect D. sapinea from H2O2 damage, while also serving as a preferred N source in vitro. Fertilization increased constitutive and drought-induced levels of some AAs, but did not affect plant resistance. A new model integrating interactions of proline and H2O2 metabolism with drought and fungal infection of plants is proposed.
Functional Ecology | 2017
Charles J. Mason; Caterina Villari; Ken Keefover-Ring; Stephanie M Jagemann; Jun Zhu; Pierluigi Bonello; Kenneth F. Raffa
Plants defend against herbivores and pathogens through integrated constitutive and induced defenses. Induced responses may be expressed locally or tissue/plant-wide, i.e. systemically, and may also be primed for subsequent attack. Although the elicitation and efficacy of induced responses are increasingly well-characterized, we have little understanding of how timing and within-plant spatial patterns of induced defenses relate to different herbivore behaviors and selective pressures. We used interactions between pines and their major mortality agents, native bark beetle-fungal complexes, to explore this dimension. We analyzed concentrations of multiple terpenoid and phenolic classes, and lesion formation, to provide a comprehensive profile of specialized metabolites and histological responses in red pine (Pinus resinosa) phloem. We examined these profiles in constitutive tissue and following simulated attack, sampling both at the point of challenge and away from the attack site, and following a second simulated attack. Terpenoid concentrations increased by > 100-fold at the site of simulated attack. In contrast, systemic induction of terpenoids was absent or weak, with most exhibiting no change and others increasing only 1.5–2 fold. Previous elicitation did not influence terpenoid concentrations, either locally or tissue-wide, when trees were challenged a second time. Phenolics had mixed responses in localized tissues, with some compounds increasing and others decreasing. Like terpenoids, phenolics did not show substantial systemic, tissue-wide changes, and likewise showed no evidence of priming. Collectively, these results indicate that red pine employs a strategy of maximizing its response at each point of attack by bark beetles. Pines have been shown to express systemic induced resistance against several canker fungi, so the absence of these responses suggests agent-specific reactions, rather than inherent incapability. Rapid local induction seems to be a better strategy in this instance because when a bark beetle succeeds in entering and producing pheromones from a host, the resulting mass attack rapidly covers the entire circumference and kills the tree. These results highlight how plant defense syndromes can modulate the spatial and temporal dynamics of induced responses, in addition to the chemical and morphological traits deployed. This article is protected by copyright. All rights reserved.
Agricultural and Forest Entomology | 2018
David N. Showalter; Caterina Villari; Daniel A. Herms; Pierluigi Bonello
Emerald ash borer (Agrilus planipennis Fairmaire, EAB) is causing widespread ash (Fraxinus spp.) mortality as it invades North America and Eastern Europe. Resistance of its coevolved hosts, including Manchurian ash (Fraxinus mandshurica Rupr.), is considered to limit EAB outbreaks and ash mortality in its native Asia, although an understanding of resistance mechanisms is still developing. Such knowledge may facilitate breeding for resistance and management of EAB in its invaded ranges. In the present study, controlled egg inoculations were used to investigate resistance mechanisms impacting larval performance, as well as to characterize the effects of water and nutrient availability on inter‐ and intra‐specific variation in resistance phenotypes based on larval outcomes. Larval survival and growth rates were lower on coevolved Manchurian ash than on evolutionarily naïve white ash (Fraxinus americana L.). Water stress decreased tree growth and resistance of Manchurian ash to EAB, although it had little effect on resistance of the already highly susceptible white ash. High nutrient availability increased tree growth but had no effect on larval performance. These results show that the higher resistance of Manchurian ash to EAB is conferred by phloem traits that decrease larval performance, in addition to lower oviposition preference.
Plant Cell and Environment | 2018
Charles J. Mason; Ken Keefover-Ring; Caterina Villari; Jennifer G. Klutsch; Stephen P. Cook; Pierluigi Bonello; Nadir Erbilgin; Kenneth F. Raffa; Philip A. Townsend
Conifers possess chemical and anatomical defences against tree-killing bark beetles that feed in their phloem. Resins accumulating at attack sites can delay and entomb beetles while toxins reach lethal levels. Trees with high concentrations of metabolites active against bark beetle-microbial complexes, and more extensive resin ducts, achieve greater survival. It is unknown if and how conifers integrate chemical and anatomical components of defence or how these capabilities vary with historical exposure. We compared linkages between phloem chemistry and tree ring anatomy of two mountain pine beetle hosts. Lodgepole pine, a mid-elevation species, has had extensive, continual contact with this herbivore, whereas high-elevation whitebark pines have historically had intermittent exposure that is increasing with warming climate. Lodgepole pine had more and larger resin ducts. In both species, anatomical defences were positively related to tree growth and nutrients. Within-tree constitutive and induced concentrations of compounds bioactive against bark beetles and symbionts were largely unrelated to resin duct abundance and size. Fewer anatomical defences in the semi-naïve compared with the continually exposed host concurs with directional differences in chemical defences. Partially uncoupling chemical and morphological antiherbivore traits may enable trees to confront beetles with more diverse defence permutations that interact to resist attack.
Agricultural and Forest Entomology | 2018
Chad Michael Rigsby; Caterina Villari; Donnie L. Peterson; Daniel A. Herms; Pierluigi Bonello; Don Cipollini
In its native range in Asia, emerald ash borer (EAB; Agrilus planipennis Fairmaire) is a secondary colonizer of its coevolved hosts, including Manchurian ash (Fraxinus mandschurica Ruprecht). However, why larval performance is enhanced on stressed trees remains to be determined. We examined the mechanisms that may reduce the resistance of stressed Manchurian ashes. Trees in a common garden were girdled or left untreated as controls and both treatments were inoculated with EAB eggs. Larvae and bark tissue were harvested after feeding and larval performance so that the defensive mechanisms and nutritional quality of bark tissue could be assessed. Larval survival and mass was twice as high on girdled trees, although girdling had no effect on bark phenolics. The activity of two enzymes involved in wound repair and lignification (peroxidase and cinnamic alcohol dehydrogenase) was increased by girdling in bark tissue. Starch and total protein levels declined in girdled stems, although sugar content was unchanged. Total disulphide levels, a measure of protein oxidative damage, were increased by girdling, although no difference in lipid oxidative damage in ash phloem tissue was detected. Girdling ash increased larval performance even though it elevated some wound repair mechanisms and decreased some indices of plant nutritional quality. Other tree responses to girdling also were poor predictors of larval performance. It appears that mechanisms of stress‐induced variation in resistance of Manchurian ash to EAB differ from those that may explain interspecific variation in resistance.