COMBINING TRADITIONAL, METABOLOMIC AND GENOMIC APPROACHES TO STUDY DISEASES LIMITING THE PROFITABILITY OF OHIO¿¿S ORNAMENTAL INDUSTRY

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 1020446
• Project Start Date: Oct 1, 2019
• Project End Date: Sep 30, 2024
• Program Code: [(N/A)]- (N/A)

Recipient Organization
OHIO STATE UNIVERSITY
1680 MADISON AVENUE
WOOSTER,OH 44691

Performing Department
Plant Pathology

Non Technical Summary
Ornamental crops represent the 4th largest crop commodity in the United States with a total value of sale of over $12 billion (NASS, 2017a). Across the nation, over 69,000 acres are in operations producing floriculture and bedding crops, and approximately 345,000 acres are dedicated to nursery crops (NASS, 2017a). Floriculture crops in Ohio accounted for $245 million in sales in 2017, while nursery stock accounted for $175 million, ranking the state 6th in the nation (NASS, 2017b).The sale of ornamental crops depends on a high-quality, nearly flawless product with a low threshold for disease tolerance. Growers suffer significant economic loss from disease outbreaks both from direct crop loss and disease management costs during the production of susceptible crops. To ensure that Ohio's ornamental industry remains competitive and sustainable, it is important to develop best management practices (BMPs) for disease management that are based on a thorough understanding of pathogen life cycles, disease epidemiology and pathogen-host interactions.In the last few years, the ornamental pathology lab at OSU has worked diligently to assist Ohio's stakeholders in addressing the disease problems affecting the industry. We have detected new pathogen outbreaks (Lin et al. 2017; Farinas et al. 2017; Lin et al. 2018a; Emanuel et al. 2019; Klass et al. 2019), shed light onto the etiology and epidemiology of emergent diseases (Lin et al. 2018b; Lin & Peduto Hand 2019a; Lin & Peduto Hand 2019b), and we have promptly communicated our findings to growers and green industry professionals to help them make informed decisions on production practices. However, in some cases, our studies have only scraped the surface of the problem revealing complex interactions between pathogens, hosts and environment, which need to be further investigated before comprehensive management strategies can be implemented by growers.In this project, we will use a combination of traditional, metabolomic and genomic approaches to studyemergent infectious diseases that are limiting the profitability of Ohio's ornamental industry with the ultimate goal of informing and modifying grower production practices based on improved knowledge of pathogen biology, epidemiology and genomics.

Animal Health Component

50%

Research Effort Categories

Basic

40%

Applied

50%

Developmental

10%

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
212	2110	1102	30%
212	2110	1170	20%
212	4020	1040	20%
212	4020	1070	10%
212	5220	1102	10%
216	5220	1170	10%

Knowledge Area
212 - Pathogens and Nematodes Affecting Plants; 216 - Integrated Pest Management Systems;

Subject Of Investigation
2110 - Ornamental trees and shrubs; 4020 - Fungi; 5220 - Pesticides;

Field Of Science
1040 - Molecular biology; 1070 - Ecology; 1102 - Mycology; 1170 - Epidemiology;

Keywords

ornamental plants

nursery crops

fungal pathogens

quiescent infections

fungal genomics

untargeted metabolomics

cultivar susceptibility

disease management

Goals / Objectives
In this project, we will use a combination of traditional, metabolomic and genomic approaches to studyemergent infectious diseases that are limiting the profitability of Ohio's ornamental industry with the ultimate goal of informing and modifying grower production practices based on improved knowledge of pathogen biology, epidemiology and genomics.The specific objectives of the project are:To understand pathogen-host interactions in the fruit rot disease of deciduous holly;To assess disease susceptibility of different Ilex verticillata cultivars and hybrids and determine their association with the production of antifungal compounds;To develop genomic resources to obtain insights into D. ilicicola's lifestyle;To evaluate the efficacy of plant protection products for disease management.

Project Methods
Objective 1: To understand pathogen-host interactions in the fruit rot disease of deciduous hollyWe will use a combination of traditional and metabolomic approaches to understand the interactions between Diaporthe ilicicola and Ilex fruit and to identify the conducive environment for disease development.We will track the presence and abundance of total phenolic and sugar compounds within Ilex verticillata 'Sparkleberry' fruits inoculated and non-inoculated with D. ilicicola throughout the growing season to identify correlations between these two target metabolites and disease incidence. Two field plots will be set up at Snyder (Wooster, OH) and Waterman (Columbus, OH) Farms using a Randomized Complete Block Design (RCBD) including six blocks. Each block will contain two treatments (inoculated and non-inoculated), and each treatment will be composed of 4 potted plants constituting a single experimental unit, to allow for sufficient fruit to complete sampling throughout the season. Starting two weeks post-inoculation, sampling will occur either monthly (June-July), biweekly (August-September), or weekly (October-November). Time intervals between sampling times will be recorded in days post-inoculation (DPI). At each sampling time, 5 cm3 of fruit tissue will be collected randomly from each experimental unit inside a falcon tube; these samples will be assessed for disease and then flash frozen to be used for metabolite analysis. Flash frozen samples will be ground into a fine powder in liquid nitrogen and then lyophilized for 24 h before being stored in ultra-low temperatures until metabolic analysis are performed. Total sugar content will be determined using the phenol-sulfuric acid method described by Neilson (2005), while total phenol content will be determined using Folin-Ciocalteau's phenol reagent (Do et al., 2014; Singleton et al., 1999).We will also use an untargeted metabolomics workflow to identify antifungal compounds within the fruit that inhibit D. ilicicola colonization. A well-plate toxicity bioassay (Roy et al., 2018) will be used to test the ability of fruit extracts taken from different points during the growing season to inhibit D. ilicicola spore germination. Samples that are able to inhibit and those that are not will be coupled into separate groupings and used for comparative LC-MS analysis using untargeted metabolomics to identify unique peaks. These peaks will be analyzed further to identify compounds. Thin Layer Chromatography (TLC) will then be used to separate different components of individual fruit extracts.Objective 2: To assess disease susceptibility of different Ilex verticillata cultivars and hybrids and determine their association with the production of antifungal compounds An RCBD field plot with 6 blocks will be set up at Waterman Farms in Columbus, OH. Treatments will consist of 10 different Ilex verticillata hybrids and cultivars that will be chosen among the most popularly used in the industry. All treatments will be artificially inoculated with D. ilicicola spores during bloom and disease incidence and severity will be monitored throughout the growing season. Fruit samples from each cultivar will also be taken throughout the growing season to be assessed for the ability to inhibit D. ilicicola growth using the well-plate toxicity assays previously described. Concentrations of previously identified antifungal compounds can be determined using targeted LC-MS to correlate differences in susceptibility to variety-dependent concentrations of known fungal-inhibiting secondary metabolites.Objective 3: To develop genomic resources to obtain insights into D. ilicicola's lifestyleWe will generate fluorescently labeled D. ilicicola isolates as tools to visualize fruit colonization in vivo and further study pathogen behavior. Isolates will be transformed with plasmid pBHt2_sGFP(S65t), containing green fluorescent protein (GFP) under the control of a constitutive ToxA promoter, which will allow the transformed fungi to be seen within infected fruit tissue using an epifluorescence microscope. The plasmid will also contain a hygromycin resistance gene, allowing for selection of successfully transformed D. ilicicola isolates on PDA supplemented with hygromycin B. Plasmid isolation will be achieved using a QIAprep™ spin column plasmid miniprep kit, and confirmed by PCR amplification of the sGFP(S65t) fluorescence gene using the primers 5'-TAGGCCATGGTGAGCAAGGGC-3' and 5'-GCGGCCGCTTTACTTGTACAG-3' (Zhang et al., 2001). The plasmid will also be sequenced at the Genomics Shared Resource Center at the Ohio State University's Comprehensive Cancer Center to confirm the plasmid identity. The protoplast isolation and transformation protocol, adapted from Zhang et al. (2018), will be used to insert the pBHt2_sGFP(S65t) plasmid into D. ilicicola. Successfully transformed isolates will be stored at -20oC in filter paper stocks until further use.Additionally, we will sequence and annotate the genome of the D. ilicicola type strain as a resource for understanding the genetic basis of pathogen responses to host and environmental conditions. This genome will serve as a reference for future gene expression work and enable prediction of genes and metabolic pathways involved in the release of quiescence. DNA will be isolated using the DNeasy Plant kit (Qiagen), and a dual-sequencing strategy will be employed. Paired-end 150bp reads will be generated on the HiSeq X Ten platform (Illumina) to a coverage of 100X, and variable length long-reads will be generated from unsheared DNA extracts using MinION (Oxford Nanopore Technologies) to a coverage of 10X. Hybrid genome assembly will be performed using SPAdes v.3.12.0 (Antipov et al. 2015), and the high quality draft genome will be annotated using an iterative MAKER v.2.31.9 (Cantarel et al. 2008) pipeline trained with Diaporthe ampelina UCDDA912 protein models and RNAseq data from Phomopsis longicolla and five other Diaporthales species, and using SNAP v2013-02-16 (Korf 2004) and Augustus v3.3 (Stanke et al. 2008) gene predictors. Gene functions will be assigned using EGGNOG, EMAPPER, and INTERPROSCAN. Metabolic gene clusters involved in the production and degradation of secondary metabolites will be predicted with antiSMASH v.5.0 (Blin et al. 2015) and custom perl scripts (Gluck-Thaler and Slot 2018) using resources of the Ohio Supercomputer Center.Objective 4: To evaluate the efficacy of plant protection products for disease managementSeveral plant protection products that are indicated as safe for use on pollinators will be tested for their ability to control D. iliciola infections. Potted Ilex verticillata 'Sparkleberry' plants will be arranged in an RCBD field plot design with 6 blocks at Waterman Farms in Columbus, OH. Fungicide treatments containing different chemistries, along with one non-treated control group, will be randomly assigned to experimental units within each block. Ilex flowers will be sprayed with fungicides at rates in accordance with their labels or manufacturer protocols at flower bloom. Following fungicide application, flowers will be inoculated with D. ilicicola spores at a concentration of 105 spores/mL. Disease incidence and severity will be assessed at least weekly following inoculation and data will be analyzed by ANOVA or non-parametric methods as appropriate.

Progress 10/01/19 to 09/30/20

Outputs
Target Audience:Individuals that were reached by our efforts during the reporting period included the following: Greenhouse and nursery producers; Landscapers/Arborists; Homeowners; Master Gardener Volunteers; Ohio State University Extension personnel, educators and assistants; Undergraduate students Graduate students Changes/Problems:Due to COVID-19 shutdown of all on farm research activities during Spring 2020, the field component of this project is currently delayed. What opportunities for training and professional development has the project provided? Nothing Reported How have the results been disseminated to communities of interest?In addition to the scientific conferences listed in the Publication section of this report, results of this project have been presented as a 2-hour webinar to Winterberry Nursery Growers on 2/25/2020 What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period we will continue the development of genomic resources to study host-pathogen interactions in the Diaporthe ilicicola-winterberry pathosystem. The genome we sequenced this yearwill be annotated and serve as reference for future gene expression work (Obj. 3). If field season is not further impacted by the COVID-19 pandemic, we will set-up and conduct the cultivar susceptibility and/or fungicide trials (Obj. 2 and 4) Metaboloimic analyses will be conducted with fruit extracts collected during the growing season (Obj. 1)

Impacts
What was accomplished under these goals? Activities for this reporting period have focused on objective 1 and 3. Due to shutdown of all on farm research activities during Spring 2020, the field component of this project is currently delayed. Objective 1: To understand pathogen-host interactions in the fruit rot disease of deciduous holly Effects of temperature on spore germination and hyphal growth of fungi associated with latent fruit rot in deciduous holly (Ilex spp.) Isolates of Diaporthe ilicicola (FPH2015-598; FPH2016-671; FPH2016-702), Alternaria alternata (FPH2015-597), Epicoccum nigrum (FPH2015-417) and Colletotrichum fioriniae (FPH2016-462) representative of different Ilex cultivars and geographical locations of isolation, were grown on PDA at room temperature with a 14h photoperiod for three weeks. Hyphal growth assay. 4mm mycelium plugs were excised from the three-week-old plates and transferred to fresh PDA. Plates were then placed in incubators set at 5, 10, 15, 20, 25, 30 and 35?C in a split-plot randomized complete block design with three blocks in each plot (temperature treatment). The diameter of the fungal colony was measured from the edge of the mycelium plug in each plate by averaging the length of two perpendicular cross sections twice a week for three weeks. The experiment was conducted twice. Spore germination assay. Spores were collected from the three-week-old plates and suspended in sterile water at a concentration of 105 spores/ml. Three 5??L drops were placed on a PDA plate and incubated at temperature treatments 5, 10, 15, 20, 25, 30 and 35?C. Germination and hyphal growth was halted at 2, 4, 8, 12 and 24 h following plating by flooding plates with lactophenol aniline blue. Percent germinated spores was calculated by counting the number of germinated spores out of 50 randomly selected spores. Spores were considered germinated when the germination hyphae length reached 1x the spore length. The experiment was conducted twice. Data Analysis. The area under the hyphal growth and spore germination progress curves were calculated in Microsoft Excel (Madden & Nutter, 1995). Temperature treatment effects were analyzed by ANOVA and means separation was done using Tukey's HSD (??=0.05) using R v. 3.6.3. The strong negative correlation between temperature and symptoms development observed by Ilex growers and in research field trials between 2016-2019 prompted these experiments, which investigated the effect of cold temperature on the fungi causing latent fruit rot in deciduous holly (Lin et al., 2019; Emanuel & Peduto Hand, unpublished data). Results indicate that Diaporthe ilicicola spore germination and hyphal growth rates are significantly decreased below 15°C and almost completely inhibited at 5°C. Compared to the Diaporthe ilicicola isolates, the other fungi in the complex are faster to germinate and grow at most of the temperature treatments, but are also significantly inhibited at temperatures at and below 15°C, with a few notable exceptions: Colletotrichum fioriniae has an optimal hyphal growth temperature range of 15-30°C and Epicoccum nigrum has an optimal germination temperature and hyphal growth range of 10-35°C, respectively. Based on these results, Epicoccum nigrum has the potential to take advantage of drops in field temperatures, but the other fungi do not share this innate psychrotrophic characteristic. Published work on this system indicate that Diaporthe ilicicola and Alternaria alternata are key players in the development of this disease so the decreased ability of these pathogens to grow at temperatures below 15°C suggest that temperature alone is not responsible for late-season symptoms development. Objective 3.To develop genomic resources to obtain insights into D. ilicicola's lifestyle Transformation of Diaporthe ilicicola (FPH2015-598) with tdTomato Agrobacterium tumefaciens containing a pBH plasmid with tdTomato was grown in LB + rifampicin (50 ug/mL) + gentamicin (15 ug/mL) + kanamycin (50 ug/mL) for two days at 28C.The bacterium was washed and resuspended in LB to an OD600 of 0.2. Acetosyringone was added to the bacterial suspension to a final concentration of 200uM and bacteria were incubated on a shaking apparatus at 150rpm at 28C for 5 hours. Following incubation, spores of D. ilicicola isolate FPH2015-598 were collected and suspended in sterile water to a concentration of ~106 spores/mL. 100uL of bacterial suspension was combined with 100uL of spore suspension and the co-culture was centrifuged at 2500 xg for 5 minutes to create a pellet. Supernatant was removed until ~50uL remained. The pellet was resuspended in the supernatant and all 50uL were plated atop a sterile cellophane circle placed on 0.1x PDA amended with acetosyringone (200uM). Plates were incubated at room temperature under ambient light for 2-5 days until mycelia could be seen growing on the cellophane. Cellophane containing the co-culture was removed and cut into four equal sized pieces using sterile scissors and forceps. Sections of cellophane were then placed on fresh PDA containing hygromycin B (25-50 ug/mL)+ Cephalexin (25ug/mL). Plates were incubated at room temperature under ambient light until hyphae could be seen growing from the cellophane into the selective media. Hyphal tips were sub-cultured onto PDA + hygromycin B (25-50ug/mL) and grown for 3-5 days. Sub-cultured isolates were screened for red fluorescence using an epifluorescent microscope. Genome assembly Diaporthe ilicicola (FPH2015-502) was sequenced using Illumina MiSeq (long reads) and minION (short reads) and assembled on the Ohio Super Computer (OSC). Read quality was checked using fastQC and sequences were trimmed using trimmomatic. Assemblies were created using SPAdes and the quality of full genome assemblies were checked against a reference genome of Diaporthe helianthe(retrieved from the NCBI database) using QUAST.

Publications

• Type: Journal Articles Status: Published Year Published: 2020 Citation: Farinas, C, Jourdan, P, Paul, PA, Slot, JC, Daughtrey, ML, Devi Ganeshan, V, Baysal-Gurel, F, Peduto Hand, F. (2020). "Phlox species show quantitative and qualitative resistance to a population of powdery mildew isolates from the Eastern United States". PHYTOPATHOLOGY 110(8): 14101418
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Wolff, P. B., Nielsen, M. L., Slot, J. C., Andersen, L. N., Petersen, L. M., Isbrandt, T., ... & Hoof, J. B. (2020). Acurin A, a novel hybrid compound, biosynthesized by individually translated PKS-and NRPS-encoding genes in Aspergillus aculeatus. Fungal Genetics and Biology, 103378.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Baysal-Gurel, F, Farinas, C, Peduto Hand, F, Avin, F. (2020). First report of powdery mildew of Phlox caused by Golovinomyces magnicellulatus in Tennessee. PLANT DISEASE 104(8): 2294-2294
• Type: Journal Articles Status: Published Year Published: 2020 Citation: South, KA, Peduto Hand, F, Jones, ML. (2020). "Beneficial bacteria identified for the control of Botrytis cinerea in petunia greenhouse production". PLANT DISEASE 104(6): 1801-1810.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Farinas, C, Henderson E, Peduto Hand, F. (2020). Evaluation of foliar fungicides in a preventative or curative program for control of powdery mildew on garden Phlox, 2019. PLANT DISEASE MANAGEMENT REPORTS. Vol. 14, OT009.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Peduto Hand, F. (2020). Evaluation of directed fungicide spray applications for control of Rhizoctonia crown rot on impatiens, 2019. PLANT DISEASE MANAGEMENT REPORTS. Vol. 14, OT011.
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Wang, Y. W., Hess, J., Slot, J. C., & Pringle, A. (2020). De novo gene birth, horizontal gene transfer and gene duplication as sources of new gene families associated with the origin of symbiosis in Amanita. Genome Biology and Evolution, evaa193, https://doi.org/10.1093/gbe/evaa193
• Type: Journal Articles Status: Published Year Published: 2020 Citation: Gluck-Thaler, E., Cerutti, A., Quintero, A. P., Butchacas, J., Roman-Reyna, V., Madhaven, V. N., ... & Lang, J. M. (2020). Repeated gain and loss of a single gene modulates the evolution of vascular pathogen lifestyles. Science Advances, EABC4516. https://advances.sciencemag.org/content/6/46/eabc4516
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Klass, TL, Long, JJ, Summers, JA, Roman-Reyna, V, Koebnik, R, Jacobs, JM, Peduto Hand, F. (2019). First report of bacterial blight of peony caused by Xanthomonas hortorum in Ohio. PLANT DISEASE 103(11): 2940.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Emanuel, I, Farinas, C, Lin, S, Pyerzynski, J, Crouch, JA, Peduto Hand, F. (2019). "Occurrence of boxwood blight caused by Calonectria pseudonaviculata in Ohio landscapes". PLANT DISEASE 103(10): 2670.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Olarte, R. A., Menke, J., Zhang, Y., Sullivan, S., Slot, J. C., Huang, Y., ... & Bushley, K. E. (2019). Chromosome rearrangements shape the diversification of secondary metabolism in the cyclosporin producing fungus Tolypocladium inflatum. BMC genomics, 20(1), 1-23.
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Ewing, C. J., Hausman, C. E., Pogacnik, J., Slot, J., & Bonello, P. (2019). Beech leaf disease: An emerging forest epidemic. Forest Pathology, 49(2), e12488.
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Emanuel, IB., Peduto Hand, F. (2020). Effects of temperature on spore germination and hyphal growth of fungi associated with latent fruit rot in deciduous holly (Ilex spp.). Global One Health Day 2020 Conference, Columbus, OH (Nov 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Olmos, C, Cohen, SP, Koebnik, R, Peduto Hand, F, Jacobs, JM. (2020). Insights into the?pathogenicity of?Xanthomonas?hyacinthi, the causal agent of yellow disease?on?Hyacinthus?spp. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Roman-Reyna, V, Dupas, E, Cesbron, S, Marchi, G, Hansen MA, Bush, E, Rotondo, F, Lewis Ivey, ML, Miller, SA, Peduto Hand, F, Jacques, M, Jacobs, JM. (2020). Metagenomic sequencing as a diagnostic tool for Xylella fastidiosa diseases such as olive quick decline syndrome and Pierces disease of grapes. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Farinas, C, Wooten, A, Peduto Hand, F, Bonello, E. (2020). Assessment of American Sycamores resistance to canker pathogens. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Farinas, C, Jourdan, P, Slot, JC, Peduto Hand, F. (2020). Shedding light on the evolutionary strategies of obligate biotrophic pathogens: the example of Phlox powdery mildew. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Emanuel, IB., Peduto Hand, F. (2020). Determining the stage in the fruit maturation process when detached fruits of Ilex serrata � I. verticillata become susceptible to colonization by Diaporthe ilicicola. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Klein, J. M., Wu, T., Delgado, J., Peduto Hand, F., Baysal-Gurel, F., Hirsch, R. L., Friesen, T. L., Donofrio, N. M. (2020). The current status of plant-related outreach across the United States and what APS is doing to help. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Journal Articles Status: Published Year Published: 2019 Citation: Slot, J. C., & Gluck-Thaler, E. (2019). Metabolic gene clusters, fungal diversity, and the generation of accessory functions. Current Opinion in Genetics & Development, 58, 17-24.
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Castroagudin, VL, Weiland, J, Baysal-Gurel, F, Cubeta, M, Daughtrey, M, Gauthier, N, LaMondia, J, Luster, D, Peduto Hand, F, Shishkoff, N, Woodward-Williams, J, Zhang, X, LeBlanc, N, Crouch, JA. (2020). Genetic structure of contemporary populations of the boxwood blight pathogen in the U.S. American Phytopathological Society Annual Meeting (Aug 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2020 Citation: Peduto Hand, F. Necessity or luxury? Defining the value of ornamental plants and of collaborative research in ornamental plant pathology. Ohio State University Plant Sciences Symposium, Columbus, OH (July 2020)
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Lopez-Nicora, H. D., Gluck-Thaler, E., Ralston, T. I., Ganeshan, V. D., Ocampos, C. G., Dorrance, A. E., ... & Niblack, T. L. (2019). Deciphering the pangenome of Macrophomina phaseolina populations from Ohio and Paraguay. Plant Health 2019.
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Cerutti, A., Jauneau, A., Auriac, M. C., Butchacas, J., Gluck-Thaler, E., Slot, J., ... & Jacobs, J. M. (2019, July). A single cellobiosidase is required for barley hydathode and xylem colonization by Xanthomonas translucens. In 2019 IS-MPMI XVIII Congress. ISMPMI.
• Type: Conference Papers and Presentations Status: Other Year Published: 2019 Citation: Gluck-Thaler, E., Cerutti, A., Quintero, A. L. P., Pesce, C., Jauneau, A., Vancheva, T., ... & Szurek, B. (2019). Ebb and flow of vascular pathogenesis through repeated gain and loss of a molecular switch. Molecular Plant-Microbe Interactions, 32(Suppl. 10).
• Type: Theses/Dissertations Status: Published Year Published: 2020 Citation: Farins, C. (2020). Understanding the powdery mildew disease of the ornamental plant Phlox: combining applied and basic research. The Ohio State University