UNDERSTANDING THE EMERGENCE OF DESTRUCTIVE PLANT PATHOGENS: EVOLUTION, MIGRATION, AND POPULATION BIOLOGY OF PHYTOPHTHORA

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: COMPLETE
• Funding Source: HATCH
• Reporting Frequency: Annual
• Accession No.: 0233038
• Project Start Date: Mar 1, 2013
• Project End Date: Mar 1, 2018
• Program Code: [(N/A)]- (N/A)

Recipient Organization
UNIVERSITY OF FLORIDA
G022 MCCARTY HALL
GAINESVILLE,FL 32611

Performing Department
Plant Pathology

Non Technical Summary
Phytophthora plant pathogens include some of the most destructive plant pathogens affecting both agricultural crops and native ecosystems. These pathogens cause costly diseases of staple crops, vegetables, high value specialty crops, and timber trees. Late blight of potato, caused by P. infestans, is infamous for the Irish potato famine and is still a major disease of this important crop, costing more than $3 billion per year to worldwide potato production and threatening food security. This species also causes late blight on tomatoes on a nearly annual basis in Florida. Phytophthora species cause the most serious soilborne diseases of citrus in Florida, causing damping-off of seedings, and tree-decline and yield loss in mature trees. Phytophthora diseases affect other Florida crops including strawberries, bell pepper, squash, watermelon, and ornamentals including palms, orchids, and Anthurium. Thus, Phytophthora pathogens are costly to growers across Florida. Several Phytophthora species have been studied for many years, yet we still have much to learn about the biology of these pathogens. For example, P. infestans has been studied for over 150 years, but the series of events that led to the emergence of this species as a global pathogen are debated and new strains are appearing in the US from unknown sources. In contrast, the research community has scrambled to study P. ramorum, which is a relatively new species that is destroying oak and tanoak woodlands in coastal California and larch plantations in the UK, and threatens the Appalachian ecosystem. P. ramorum has a broad host range, including many ornamental plants, and regulations implemented as a result of the introduction of this aggressive pathogen have been costly to the nursery industry. Likewise, many new Phytophthora species are being discovered in forest environments about which little to nothing is known. While regulations, improved crop breeding, and disease management may control the damage from Phytophthora pathogens in the short-term, managing these pathogens in the long-term will require more extensive knowledge about the global movement of these pathogens, how and why some Phytophthora emerge as damaging pathogens, and the biology of this group in their native ecosystems, which is essentially unknown. The benefit of this research will be in the prevention of future losses from new introductions, early identification of introduced species for rapid management, and the early detection or prevention of emergent virulent lineages of existing pathogens.

Animal Health Component

(N/A)

Research Effort Categories

Basic

(N/A)

Applied

(N/A)

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
212	4020	1060	40%
212	4020	1080	40%
212	4020	1102	20%

Knowledge Area
212 - Pathogens and Nematodes Affecting Plants;

Subject Of Investigation
4020 - Fungi;

Field Of Science
1060 - Biology (whole systems); 1102 - Mycology; 1080 - Genetics;

Keywords

phytophthora

plant pathogen

emergence

global migration

evolution

hybridization

diversity

florida forests

exotic pathogen

population genetics

Goals / Objectives
The objectives of the project are to: (1) Identify centers of diversity and global migration pathways of successful and widely distributed Phytophthora plant pathogens. (2) Investigate the role of hybridization in generating novel evolutionary lineages of Phytophthora pathogens. (3) Evaluate the diversity of Phytophthora in Florida natural areas and use population genetic variation to generate hypotheses of endemism or recent introduction.

Project Methods
The project will employ gene and genome sequencing, genotyping, sampling of natural communities, and population genetic analysis using both traditional and modern coalescent-based approaches. Knowledge in my field will be advanced by presenting the results of this research in the scientific literature, at professional meetings, and through hands-on workshops. The outputs will be evaluated using the number of publications resulting from this project and their impact on other research through numbers of citations.

Progress 03/01/13 to 03/01/18

Outputs
Target Audience:Scientists in plant pathology and high school science teachers. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A PhD student completed her degreeand undergraduates participated in lab and field research activities. How have the results been disseminated to communities of interest?Middle and high school teacher training workshops were conducted on the topic "Plants get sick too!" What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? We elucidated the origin and movement of Phytophthora infestans and P. palmivora, examined nuclear DNAcontent and developeda high resolution melting PCRtest to advance knowledge ofPhytophthora hybrids, and conducted novel sampling of Phytophthora and Pythium in Florida. The work that has not been published provides preliminary data and foundational work for future projects on these organisms.

Publications

• Type: Conference Papers and Presentations Status: Accepted Year Published: 2018 Citation: Ratti M, Goss EM, Evaluation of High Resolution Melting Analysis to discriminate between parental and hybrid Phytophthora species, International Congress of Plant Pathology 2018, Boston, MA, August 2018. Contributed poster.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Ratti MF G, MS Ascunce P, JJ Landivar, EM Goss (2018) Pineapple heart rot isolates from Ecuador reveal a new genotype of Phytophthora nicotianae, Plant Pathology, https://doi.org/10.1111/ppa.12885
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Mideros MF, DA Turissini, N Guayaz�n, H Ibarra-Avila, G Danies, M C�rdenas, K Myers, J Tabima, EM Goss, A Bernal, LE Lagos, A Grajales, LN Gonzalez, DEL Cooke, WE Fry, N Gr�nwald, DR Matute, S Restrepo (2018) Phytophthora betacei, a new species within Phytophthora clade 1c causing late blight on Solanum betaceum in Colombia. Persoonia - Molecular Phylogeny and Evolution of Fungi 41: 39-55.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Ascunce MS P, JC Huguet-Tapia p, A Ortiz-Urquiza p, NO Keyhani, EL Braun, EM Goss (2017) Phylogenomic analysis supports multiple instances of polyphyly in the oomycete peronosporalean lineage. Molecular Phylogenetics and Evolution 114: 199-211.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: 8. Wang J G, SP Fern�ndez-Pav�a, MM Larsen, E Garay-Serrano, R Gregorio-Cipriano, G Rodr�guez-Alvarado, NJ Gr�nwald, EM Goss (2017) High levels of diversity and population structure in the potato late blight pathogen at the Mexico center of origin. Molecular Ecology 26(4): 1091-1107.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2017 Citation: Goss EM, Global movement, local consequences: Using population genomics to understand the changing landscape of plant pathogens,  Plenary session of the Annual Meeting of the American Phytopathological Society, San Antonio, TX, August 2017.
• Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ratti M, A new genetic group of Phytophthora nicotianae found in isolates from pineapple heart rot disease, American Phytopathological Society Annual Meeting, San Antonio, TX, August 2017.

Progress 10/01/17 to 03/01/18

Outputs
Target Audience: Nothing Reported Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One graduate student, one undergraduate, and one visiting scholar are involved in the project. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? (1) Identify centers of diversity and global migration pathways of successful and widely distributed Phytophthora plant pathogens: First paper on Phytophthora nicotianae was published. This is a common, wide-host range pathogen that is understudied in the tropics and sub-tropics, and host specialization is not well understood. (2) Investigate the role of hybridization in generating novel evolutionary lineages of Phytophthora pathogens: Paper describing the diversification of putative hybrid P. betacei was published. Work on our PCR test for differentiating two hybrid Phytophthora from their parental species was submitted for presentation at the International Congress of Plant Pathology. (3) Evaluate the diversity of Phytophthora in Florida natural areas and use population genetic variation to generate hypotheses of endemism or recent introduction: Samples from the UF/IFAS Ordway-Swisher Biological Station continue to be processed.?

Publications

• Type: Journal Articles Status: Published Year Published: 2018 Citation: Ratti MF, MS Ascunce, JJ Landivar, EM Goss (2018) Pineapple heart rot isolates from Ecuador reveal a new genotype of Phytophthora nicotianae, Plant Pathology 67: 18031813.
• Type: Journal Articles Status: Published Year Published: 2018 Citation: Mideros MF, DA Turissini, N Guayaz�n, H Ibarra-Avila, G Danies, M C�rdenas, K Myers, J Tabima, EM Goss, A Bernal, LE Lagos, A Grajales, LN Gonzalez, DEL Cooke, WE Fry, N Gr�nwald, DR Matute, S Restrepo (2018) Phytophthora betacei, a new species within Phytophthora clade 1c causing late blight on Solanum betaceum in Colombia. Persoonia - Molecular Phylogeny and Evolution of Fungi 41: 39-55.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2018 Citation: Ratti M, Evaluation of High Resolution Melting Analysis to discriminate between parental and hybrid Phytophthora species, International Congress of Plant Pathology 2018, Boston, MA, August 2018.

Progress 10/01/16 to 09/30/17

Outputs
Target Audience:My graduate student and I gave research talks at the American Phytopathological Society, a national meeting for scientists in plant pathology. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two graduate students, one undergraduate and a visiting scholar are involved in the project. How have the results been disseminated to communities of interest?Phytophthora infestans was one of the pathogens discussed in two high school science teacher training workshops held in the UF/IFAS Department of Plant Pathology to introduce Florida teachers to plant diseases. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? (1) Identify centers of diversity and global migration pathways of successful and widely distributed Phytophthora plant pathogens: P. infestans results were published in Molecular Ecology. (2) Investigate the role of hybridization in generating novel evolutionary lineages of Phytophthora pathogens: PCR tests to differentiate two hybrid Phytophthora from parental species are in development. (3) Evaluate the diversity of Phytophthora in Florida natural areas and use population genetic variation to generate hypotheses of endemism or recent introduction: Sampling was conducted in natural areas in the UF/IFAS Ordway-Swisher Biological Station in Melrose, FL.

Publications

• Type: Journal Articles Status: Published Year Published: 2017 Citation: Wang J, SP Fern�ndez-Pav�a, MM Larsen, E Garay-Serrano, R Gregorio-Cipriano, G Rodr�guez-Alvarado, NJ Gr�nwald, EM Goss (2017) High levels of diversity and population structure in the potato late blight pathogen at the Mexico center of origin. Molecular Ecology 26(4): 1091-1107.
• Type: Journal Articles Status: Published Year Published: 2017 Citation: Ascunce MS, JC Huguet-Tapia, A Ortiz-Urquiza, NO Keyhani, EL Braun, EM Goss (2017) Phylogenomic analysis supports multiple instances of polyphyly in the oomycete peronosporalean lineage. Molecular Phylogenetics and Evolution 114: 199-211.
• Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Ratti M, A new genetic group of Phytophthora nicotianae found in isolates from pineapple heart rot disease, American Phytopathological Society Annual Meeting, San Antonio, TX, August 2017
• Type: Conference Papers and Presentations Status: Published Year Published: 2017 Citation: Goss EM, Pathways and populations in Phytophthora  a legacy of destruction, Annual Meeting of the American Phytopathological Society, San Antonio, TX, August 2017.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2017 Citation: Goss EM, Global movement, local consequences: Using population genomics to understand the changing landscape of plant pathogens, Plenary session of the Annual Meeting of the American Phytopathological Society, San Antonio, TX, August 2017.

Progress 10/01/15 to 09/30/16

Outputs
Target Audience:My students and I presented results to scientists working in Plant Pathology, Oomycete Genetics, and Plant Genetics at national and international meetings. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Two graduate students and one undergraduate are involved in the project. How have the results been disseminated to communities of interest?A presentation was made on plant pathogen virulence evolutionto Florida Title I school teachers participating in a UF trainingprogram. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? (1) Identify centers of diversity and global migration pathways of successful and widely distributed Phytophthora plant pathogens: Preliminary results forP. palmivora were presented at conferences. A manuscript reporting the P. infestans results is in preparation (2) Investigate the role of hybridization in generating novel evolutionary lineages of Phytophthora pathogens: Results for P. andina were published. (3) Evaluate the diversity of Phytophthora in Florida natural areas and use population genetic variation to generate hypotheses of endemism or recent introduction: No activities conducted.

Publications

• Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Wang J, JW Presser, and EM Goss (2016) Nuclear DNA content of the hybrid plant pathogen Phytophthora andina determined by flow cytometry. Mycologia 108: 899-904.
• Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Ali SS, I Amoako-Attah, RA Bailey, MD Strem, M Schmidt, AY Akrofi, S Surujdeo-Maharaj, OO Kolawole, BAD Begoude, GM ten Hoopen, EM Goss, W Phillips-Mora, LW Meinhardt, BA Bailey (2016). PCR-based identification of cacao black pod causal agents and identification of biological factors possibly contributing to Phytophthora megakarya⿿s field dominance in West Africa. Plant Pathology 65(7): 1095-1108
• Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Ascunce MS, JC Huguet-Tapia, EL Braun, A Ortiz-Urquiza, NO Keyhani, and EM Goss (2016) Whole genome sequence of the emerging oomycete pathogen Pythium insidiosum strain CDC-B5653 isolated from an infected human in the USA. Genomics Data 7, 60-61.
• Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Patel JS, A Vitoreli, AJ Palmateer, A El-Sayed, D Norman, EM Goss, MS Brennan and GS Ali (2016) Characterization of Phytophthora spp. Isolated from ornamental plants in Florida. Plant Disease 100(2): 500-509
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Wang, Coffey, Goss. Model for the geographic origin and spread of the globally distributed pathogen Phytophthora palmivora, American Phytopathological Society Annual Meeting, Tampa, FL, August 2016.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Ratti M, Oomycete species richness in cacao soil assessed by massive amplicon sequencing of the cytochrome oxidase II gene, American Phytopathological Society Annual Meeting, Tampa, FL, August 2016
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Goss EM, ⿿Genome-enabled analysis of pathogen migration and evolution,⿝ Plant and Animal Genome XXIV Conference, San Diego, California, January 2016.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2016 Citation: Wang J, M Coffey, EM Goss, ⿿Phylogeography of the tropical oomycete Phytophthora palmivora,⿝ Oomycete Molecular Genetics Network Annual Meeting, Asilomar, CA, March 2016.

Progress 10/01/14 to 09/30/15

Outputs
Target Audience:Researchers and scientists in the field of plant pathology. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two PhD students are working under the project. How have the results been disseminated to communities of interest? Nothing Reported What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Publication of an invited review synthesized knowledge of plant pathogen migration. The take-home message is that international scientific cooperation is required to understand the movement and emergence of plant pathogens in a global context. (1) Identify centers of diversity and global migration pathways of successful and widely distributed Phytophthora plant pathogens: analyses of both P. infestans and P. palmivora dataare in progress. (2) Investigate the role of hybridization in generating novel evolutionary lineages of Phytophthora pathogens:Data collection and analysis are underway for hybrid P. andina. (3) Evaluate the diversity of Phytophthora in Florida natural areas and use population genetic variation to generate hypotheses of endemism or recent introduction: No activities conducted.

Publications

• Type: Journal Articles Status: Published Year Published: 2015 Citation: Goss EM (2015) Genome-enabled analysis of plant-pathogen migration. Annual Review of Phytopathology 53: 121-135.
• Type: Journal Articles Status: Published Year Published: 2015 Citation: Shakya SK G, EM Goss, NS Dufault, AHC van Bruggen (2015) Potential effects of diurnal temperature oscillations on potato late blight under climate change. Phytopathology 105(2): 230-238.
• Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Wang J, et al. Global population genetic diversity and phylogenetic analysis of Phytophthora palmivora, American Phytopathological Society Annual Meeting, Pasadena, CA, August 2015.
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2015 Citation: Wang J, Population genetic structure of the late blight pathogen, Phytophthora infestans, in Mexico, Florida Phytopathological Society, Gainesville, FL, May 2015.
• Type: Conference Papers and Presentations Status: Published Year Published: 2015 Citation: Kolawole OO, EM Goss, Three clonal lineages of the cocoa pathogen Phytophthora megakarya in Nigeria, Annual Meeting of the American Phytopathological Society, Pasadena, CA, August 2015.

Progress 10/01/13 to 09/30/14

Outputs
Target Audience: Other scientists and researchers for plantpathologyand biology Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? A graduate student was mentored under this project. A postdoc is also contributing to the project and gaining skills in pathogen genomics. A Borlaug LEAP fellow studying Phytophthora was also mentored. How have the results been disseminated to communities of interest? The University of Florida and collaborating universities prepared press releases on the publication. The story was covered on several websites and in grower publications. What do you plan to do during the next reporting period to accomplish the goals? Current activities will continue, including data analysis and publication of results. Funding to continue activities under objectives 1 and 2, and to advance objective 3 will be pursued.

Impacts
What was accomplished under these goals? A paper was published in PNAS on the first objective. Two manuscripts were also prepared under this objective and data collection continued. Data was obtained for the second objective as well as funding to support a portion of this objective.

Publications

• Type: Journal Articles Status: Published Year Published: 2014 Citation: 7. Goss EM, JF Tabimag, DEL Cooke, S Restrepo, WE Fry, GA Forbes, VJ Fieland, M Cardenas, and NJ Gr�nwald (2014) The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proceedings of the National Academy of Sciences USA 111(24): 8791-8796.
• Type: Conference Papers and Presentations Status: Published Year Published: 2014 Citation: Wang J, M Larsen, R Gregorio-Cipriano, G Rodr�guez-Alvarado, NJ Grunwald, SP Fernandez-Pavia, EM Goss (2014) Characterization of genetic structure in Mexico populations of Phytophthora infestans using single sequence repeats, Annual Meeting of the American Phytopathological Society, Minneapolis, August 2014.

Progress 03/01/13 to 09/30/13

Outputs
Target Audience: The target audience fo this reporting period was scientists working in the field of Plant Pathology. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? A graduate student, undergraduate, and high school intern have worked on the project. A postdoctoral associate joined the project and is developing her skills in analysis of genomic data. How have the results been disseminated to communities of interest? Research on these topics was presented in invited talks at two scientific meetings. Results generated under this project have not yet been disseminated. What do you plan to do during the next reporting period to accomplish the goals? Continue data collection and analysis of these data. The focus will be on goal 1 and aspects of goal 2.

Impacts
What was accomplished under these goals? In the first 6 months of this project, data were collected.

Publications

• Type: Conference Papers and Presentations Status: Accepted Year Published: 2013 Citation: Goss et al., 2013, Multilocus support for a Central Mexico center of origin for Phytophthora infestans, 10th International Congress of Plant Pathology, Beijing, China, August 25-30, 2013
• Type: Conference Papers and Presentations Status: Accepted Year Published: 2013 Citation: Goss, 2013, Migration and evolution of Phytophthora plant pathogens in the age of globalization, American Phytopathological Society 2013 Annual Meeting, Austin, Texas, August 10-14, 2013.