DELIVERING BREEDING AND MANAGEMENT SOLUTIONS TO PREVENT LOSSES TO EMERGING AND EXPANDING DISEASE THREATS IN STRAWBERRY

• Sponsoring Institution: National Institute of Food and Agriculture
• Project Status: ACTIVE
• Funding Source: OTHER GRANTS
• Reporting Frequency: Annual
• Accession No.: 1029186
• Grant No.: 2022-51181-38328
• Cumulative Award Amt.: $6,242,957.00
• Proposal No.: 2022-05304
• Project Start Date: Sep 15, 2022
• Project End Date: Sep 14, 2026
• Grant Year: 2022
• Program Code: [SCRI]- Specialty Crop Research Initiative

Recipient Organization
UNIVERSITY OF CALIFORNIA, DAVIS
410 MRAK HALL
DAVIS,CA 95616-8671

Performing Department
(N/A)

Non Technical Summary
US farmers unfailingly deliver a high quality supply of fresh strawberries to consumers year round, an accomplishment enabled by immense productivity gains over the last half century or more. With a 10-fold increase in US production since 1960, strawberries have become one of the most widely consumed fruits, having surpassed oranges as a source of vitamin C in the American diet. The medical community has discovered that strawberries have diverse preventive and therapeutic health benefits beyond basic nutrition. Our research initiative, although geographically broad in scope and impact, places an emphasis on finding solutions to the most common and debilitating disease problems facing growers in California and Florida where 94-96% of domestic strawberries are produced. The phenomenal growth of the strawberry industry has been achieved by the development and introduction of progressively higher yielding cultivars and widespread adoption of chemically intensive production practices. The sustainability of those chemically intensive practices, however, are threatened by adverse environmental impacts and increased regulation of chemicals (gaseous fumigants) historically used to control diseases caused by soil-borne pathogens. Moreover, the demand for foods produced with environmentally friendly and organic production practices have been increasing in the US. Since 2005 when a global treaty banned the application of gaseous fumigant methyl bromide as a chemical for controlling soil-borne pathogens, the incidence of the diseases they cause increased. The four most serious diseases, and the primary focus of our research, are Fusarium wilt, Verticillium wilt, Macrophomina, and Phytophthora crown rot. We have shown that a significant fraction of the cultivars grown today are highly susceptible to one or more of these diseases, which reduce plant health and frequently cause plant death. Our research initiative seeks to identify and deliver plant breeding and field management solutions that prevent pandemics, minimize economic losses to diseases, and increase the sustainability of strawberry production in the US. One of the most important outcomes of our research will be the development of cultivars that are naturally resistant to Fusarium wilt, Verticillium wilt, Macrophomina, Phytophthora crown rot, and Neopestalotiopsis, a completely new above-ground fungal disease that threatens US strawberry production. We are using natural sources of resistance and modern genetic approaches to identify and deliver solutions to these disease problems. Our research includes studies to better understand methods for minimizing losses to diseases through improved disease diagnosis, prevention, and management. We work closely with growers and stakeholders to transfer technology from the laboratory to the field. Our initiative engages and benefits stakeholders across the supply chain and strives to improve the lives of farmers and rural communities and society as a whole by protecting growers and the environment, ensuring a steady supply of fresh strawberries year round, and increasing the sustainability of production.

Animal Health Component

50%

Research Effort Categories

Basic

50%

Applied

50%

Developmental

(N/A)

Classification

Knowledge Area (KA)	Subject of Investigation (SOI)	Field of Science (FOS)	Percent
201	1122	1081	60%
212	1122	1160	30%
601	1122	3010	10%

Knowledge Area
601 - Economics of Agricultural Production and Farm Management; 212 - Pathogens and Nematodes Affecting Plants; 201 - Plant Genome, Genetics, and Genetic Mechanisms;

Subject Of Investigation
1122 - Strawberry;

Field Of Science
1160 - Pathology; 1081 - Breeding; 3010 - Economics;

Keywords

climate change

disease resistance

genomic selection

marker-assisted selection

plant pathogen

Goals / Objectives
Despite more than a half century of steady growth and commercial success, strawberry growers and other industry stakeholders face strong headwinds from changes in soil fumigation practices, soaring production costs, increased incidence and severity of diseases caused by soil-borne pathogens (especially Macrophomina phaseolina and Fusarium oxysporum f.sp. fragariae), and the emergence of foliar and fruit diseases caused by Neopestalotiopsis species that could potentially cripple strawberry production in FL and beyond. The elimination of methyl bromide (MeBr) as a soil fumigant, while critical for sustainability and planetary health, has profoundly changed production practices in the annual production systems that supply 96-98% of the strawberries produced in the US. Since the MeBr phase out, losses caused by Fusarium wilt and Macrophomina have sharply increased. Moreover, the soil fumigants that replaced MeBr are less effective and, as our stakeholders have warned, on the verge of being heavily restricted and possibly banned. These changes are profoundly changing strawberry production practices and economic realities in the US.The proposed initiative is urgently needed to create a more sustainable path forward for our industry, brace growers for imminent changes in production practices, and protect the environment and human health. Our SCRI-, California Strawberry Commission (CSC)-, and Florida Strawberry Growers Association (FSGA)-funded research studies have shown that decades of scientific neglect and reliance on soil fumigation have meant that a high percentage of cultivars and genetic resources worldwide are susceptible to one or more diseases. The genetic gains for yield in the US (10-fold since 1960 when MeBr was introduced) were achieved largely because MeBr effectively eliminated losses to diseases caused by soil-borne pathogens. The introduction of MeBr, once hailed as one of the greatest technical achievements of the twentieth century, had profound consequences, including inattention to disease resistance breeding and widespread cultivation of disease susceptible cultivars, e.g., our analyses show that, over the last 15 years, 50-80% of the cultivars grown in CA were Fusarium wilt susceptible and 60-70% of cultivars grown in FL were Phytophthora crown rot susceptible. Our stakeholders have reprioritized disease resistance breeding and pathology research and stressed the importance of developing cultivars resistant to the broadest possible spectrum of diseases affecting strawberry. They have strongly endorsed our proposal and stressed the importance of pushing the envelope of genomic and genome-editing technologies to solve problems facing the industry. Our initiative, while not geographically limited, emphasizes solutions to the most debilitating disease problems in CA and FL and strives to increase the sustainability of production by delivering cultivars resistant to a broad spectrum of diseases, while reducing chemical inputs and improving the environment.We expect the proposed initiative to improve the lives of farmers and rural communities by preventing losses to diseases that adversely affect strawberry production. The solutions we deliver are expected to reduce production risk, improve disease diagnosis, prevention, and management, decrease pesticide usage, facilitate the transition from fumigant-dependent to alternative production systems, and enable the expansion of organic production. One of the goals of this SCRI will be the development and deployment of cultivars with unmatched resistance to a broad spectrum of diseases.One of our goals is to train the next-generation of problem solvers. Our trainees include undergraduate and graduate students and postdoctoral scholars in horticulture, plant breeding, genomics, bioinformatics, molecular biology, and plant pathology. Trainees will have the opportunity to extend knowledge and interact with diverse stakeholder communities through field days, workshops, on-farm research, cooperative extension and scientific meetings, and one-on-one and small group activities.The proposed initiative directly benefits strawberry breeding and plant pathology research in the public and private sectors in the US and abroad by providing enabling information critical for implementing marker-assisted selection and genomic selection, understanding pathogen diversity, biology, and evolution, and diagnosing, preventing, and managing diseases. Our goals include advancing genome-editing solutions to disease resistance breeding problems, improving transformation and genome-editing platforms, and delivering a DNA-free genome editing platform.Objective #1: Empower Predictive Breeding. To expand our understanding of genetic mechanisms underlying resistance to the most important diseases of strawberry and empower predictive breeding approaches, we are proposing to: (A) identify sources of resistance and elucidate the genetic basis of resistance to Pestalotia leaf spot and fruit rot; (B) identify race-specific Fusarium wilt resistance genes and develop a deeper understanding of the underlying host-pathogen interactions); (C) deploy and cross-validate the effects of favorable quantitative trait locus (QTL) alleles previously shown to substantially increase resistance to Macrophomina, Fusarium wilt, and Phytophthora crown rot; and (D) utilize established plant transformation and genome editing approaches to modify susceptibility genes hypothesized to increase resistance to filamentous fungi (e.g., Fusarium oxysporum) and develop an efficient DNA-free genome editing platform.Objective #2: Deliver a New Generation of Disease Resistant Cultivars. To deliver cultivars resistant to a broad spectrum of diseases, we are proposing to: (A) develop, validate, and deliver cost-effective, high-throughput, turnkey genotyping solutions to facilitate the application of genomic selection on a large scale; (B) stack favorable alleles for resistance to Fusarium wilt, Macrophomina, Verticillium wilt, and Phytophthora crown rot in California-adapted populations and deliver cultivars with enhanced disease resistance; and (C) stack favorable alleles for resistance to Macrophomina, Pestalotia, and Phytophthora crown rot in Florida-adapted populations and deliver cultivars with enhanced disease resistance.Objective #3: Improve Disease Management, Monitoring, & Identification. To improve disease management and detection, we are proposing to: (A) characterize pathogen genomic diversity, assess the durability of pathogen resistance, and improve the specificity of molecular methods for pathogen identification and (B) elucidate environmental variables and cultivar-by-environment interactions that are conducive to disease and identify strategies to mitigate these effects.Objective #4: Enhance the Sustainability of Production Through Outreach and Extension. To increase the sustainability of production and extend knowledge, we are proposing to: (A) translate technical advances and innovations from the laboratory to the field through diverse outreach activities; (B) shed light on economic factors affecting the sustainability of strawberry production; and (C) increase public awareness of the safety, benefits, and limitations of genome-editing for solving strawberry production problems.

Project Methods
The primary efforts associated with our initiative include the delivery of science-based knowledge through: (a) formal classroom and laboratory instruction; (b) informal laboratory and field research and development activities: (c) experiment design and planning, field experiment preparation, maintenance, and management; (d) greenhouse and laboratory experiment design and analysis; (e) workshops on genome-informed breeding and genome-editing; and (f) grower education, extension, and outreach programs.One of the primary methods for evaluating the impact of our work on growers (one of the intended audiences) will be the adoption of disease resistant cultivars, e.g., with over half of the acres in California planted to Fusarium wilt susceptible cultivars, we can directly estimate how our work increases the acreage planted to Fusarium wilt resistant cultivars from industry planting surveys. Similar metrics will be collected for the other diseases we are investigating.Our impact on the scientific community (one of the other intended audiences) will be evaluated by documenting: (a) the number and impact of peer-reviewed publications (measured by accesses and citations); (b) the quality and quantity of open-source data deposited in public databases and downloads from open-source data repositories; (c) direct feedback at scientific meetings and workshops; and (d) direct interactions with scientists in the broader scientific community.

Progress 09/15/23 to 09/14/24

Outputs
Target Audience:The target audiences for this research are: (a) private and public sector strawberry breeders, plant pathologists, scientists, and extension specialists; (b) strawberry growers, shippers, and packers and others engaged in producing and marketing strawberries; (c) academic scientists engaged in breeding and genomics of other species in the Rosaceae and other asexually propagated species; (d) graduate students, postdoctoral researchers, and academic scientists engaged in economics, sociology, plant pathology, horticulture, breeding, genetics, and genomics research. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?UC Davis (Feldmann, Knapp, Coaker, Bjornson):This USDA SCRI project has directly supported Marta Bjorson (project scientist)who recently submitted her first USDA AFRI proposal as PI), Alicia Sillers (PhD Candidate) who advanced to candidacy in October 2024, Mishi Vachev (PhD Candidate, coadvised by Knapp, Feldmann, Coaker) who is set to graduate in January 2025. Paul Skillin (PhD Candidate)and Caitlyn Morgan (Master's student) have been able to take advantage of the resources, specifically genotyped plant material, funded by USDA SCRI, to kick start their own dissertation and thesis research. Adrianna Ng (Masters student) joined the lab in September 2024 (Feldmann, Debernardi). Ryan Chiang (undergraduate, advised by Feldmann, Bjornson) has been working on a research project testing transient gene editing in fruit, and is preparing a poster for spring 2025 undergraduate research conference.Feldmann, Bjornson, and Vachev attended PAG in 2024.Feldmann, Bjornson, and Sillers will be attending the Plant and Animal Genome in January 2025. Madison Lalico (PhD student) is rotating with Feldmann and Bjornson working on fine mapping resistance loci against fusarium wilt. UC Davis (Debernardi):At Transformation Facility, we are training an SRA (Lucero Jimenez) on strawberry transformation using agrobacterium. Lucero has leaded the development of the agrobacterium transformation platform for modern cultivars and the evaluation of CRISPR cassettes, and she currently manages the strawberry transformation service at our Facility. In addition, in collaboration with Prof. Feldmann, we are co-mentoring a Master student (Adrianna Ng), who is being trained in protoplast isolation, encapsulation and regeneration protocols. Adrianna is leading the work to establish an efficient protoplast-based editing platform. She will be also working on optimizing a Cas12 cassette for agrobacterium-based editing. U Florida:PhD student Elissar Alam published two papers (see above) and successfully defended her dissertation. PhD student Lis Porto presented at the Annual meeting of the Phytopathological Society. A postdoc (Antt Wai) presented research result (see above) at the In Vitro Biology conference.Our postdoc presented research at the In Vitro Biology Meeting, while graduate students attended the Plant and Animal Genome (PAG) meeting, the In Vitro Biology Meeting, and various workshops and seminars at local and statewide levels. Additionally, the postdoc and students participate annually in the Strawberry Field Day and AgExpo events. USDA:Four undergraduate students from California State University, Monterey Bay (CSUMB) were trained in microbiology and molecular biology techniques as part of this grant, with total FTE of 100%. CSUMB is a Hispanic Serving Institution and all four undergraduate students are part of demographic groups that are underrepresented in STEM. Cal Poly:Aug 8, 2024: Joseph Ramirez presented his research results on 'Susceptibility to Macrophomina root rot and Verticillium wilt in 63 cultivars and advanced breeding lines' at the Cal Poly Strawberry Center's annual field day (620 attendees). Aug 8, 2024: Marina Guitierrez presented her research results on 'Effect of abiotic stresses on Macrophomina root rot development in California strawberry.' at the Cal Poly Strawberry Center's annual field day (620 attendees). Aug 12-16, 2023: Joseph Ramirez presented his host plant resistance results to the Small Fruits Working Group at Plant Health 2024 Conference (APS Annual meeting) in Memphis, TN. How have the results been disseminated to communities of interest?UC Davis (Feldmann, Knapp, Coaker, Bjornson):Feldmann, Bjornson, Vachev, and Sillers attend PAG to disseminate research findings to the global strawberry community. Feldmann, Knapp, Bjornson attend the scientific advisory committee meetings to update the CA strawberry industry on research findings. Knapp and Feldmann held 4 field day events for the UC Davis Strawberry Breeding program, reaching 30-50 attendees at each event. Feldmann and Pincot presented and had postersat NAPB. Results of the research were also presented at the Cal Poly Strawberry Center Field Day (~600 attendees). UC Davis (Debernardi):Our group has participated in discussions with collaborators from academia and industry about the challenge and benefits of genome editing technology for strawberry. U Florida:At the UF breeding program field day in Dover, FL on January 10, 2024, 75 strawberry growers and nurserymen were provided preliminary data on a new Neopestalotiopsis breeding selection being considered for release. Results from the field trials for evaluation of the disease models were also presented at the field day Dover. In addition, results from the model trials were presented to around 100 growers at the Agritech meeting in Plant City on May, 2024, for about 30 growers at the Driscolls pre-plant meeting in Tampa on September 2024. Results of DNA markers and application for improving varieties were presented at the annual Field Day and in various extension workshops.Results have been shared through both oral and poster presentations at national and international professional conferences. Additionally, findings are presented at the annual Field Day and in various extension workshops to engage and inform the community directly. USDA:The results were communicated to academic audiences at the American Phytopathological Society's Pacific Division and national (=Plant Health 2024) meetings and the Conference on Soilborne Plant Pathogens. Results were communicated to industry at the California Strawberry Commission's Research Committee meeting in December 2023 and at the Strawberry Center Field Day at California Polytechnic University, San Luis Obispo. Cal Poly:Cal Poly: Aug 8, 2024: HostedCal Poly Strawberry Center's annual field day (620 attendees), including representatives from UC Davis, Driscoll's, Plant Sciences Inc, California Berry Cultivars, Planasa, Lassen Canyon, GoodFarms, Crown Nursery, Cedar Point Nursery, NatureRipe, California Giant, Mar Vista, Sorrento Berries, Blazer Wilkinson Gee, the California Strawberry Commission, and many other members of the California strawberry industry. What do you plan to do during the next reporting period to accomplish the goals?UC Davis (Feldmann, Knapp, Coaker, Bjornson):Bjornson and Picnotwill complete our fine mapping experiments for Fusarium wilt race 1 (specifically for the FW4 and FW5 QTL). Feldmann, Knapp, Bjornson, and Vachevwill publish our work identifying FW6 and FW7, which segregate in the Earliglow cultivar. Mishi Vachev will graduate with her PhD in Plant Biology from UC Davis.We will establish field trials in early Nov, 2024 to trial potential cultivars againstMacrophomina phaseolina, Fusarium oxysporum, Verticillium dahliae, and Phytophthora cactorum. We will establish field trials in Florida and CA in Nov 2024 to screen germplasm against Neopestalotiopsis for a second year in collaboration with the University of Florida Strawberry Breeding Program. We will hold our midpoint team meeting in Davis, CA, in early 2025, with the topics to start discussing opportunities for a 3rd submission to Specialty Crop Research Initiative in 2026-2027,and plan our 4th year meeting in early 2026 to confirm our plans for resubmission and need for no-cost extension. UC Davis (Debernardi):1. We will continue working to establishing a protoplast-based platform. We will evaluate parameters for optimal regeneration of whole plants. We will also perform protoplast transfection and editing using Cas9 Ribonucleoprotein complexes (RNPs) assembled in vitro. We have previously developed a protoplast-based system for grape, and we have already gained considerable experience on RNPs transfection parameters. Therefore, we think that it will be relatively simple to incorporate RNP transfection. 2. We will continue working to improve our agrobacterium-based editing platform. Having successfully validated Cas9-based vectors, we are now shifting our focus to developing efficient vectors using alternative nucleases and editing methods. Currently, we are working on vectors based on Cas12, which has been shown to outperform Cas9 in certain CRISPR applications, such as promoter editing and targeted gene insertion. Our goal is to establish a robust and versatile platform that facilitates various types of editing to support strawberry research and breeding programs. U Florida:We will continue efforts to (1) characterize the resistance allele RPc2-H2 for Phytophthora resistance, (2) identify candidate genes associated with the major QTL RNp2 for Neopestalotiopsis resistance, and (3) validate CRISPR-edited strawberry lines for enhanced resistance to multiple diseases. USDA:We plan to complete revisions until acceptance of the paper describing population genomics of Macrophomina spp. We also plan to continue supporting efforts characterizing the impacts of salt and water deficit stresses on disease severity by M. phaseolina. We are researching the molecular mechanisms of host specialization on strawberry and expect to identify genetic correlates of this trait. Cal Poly:We will establish field trials in early Nov, 2024; produce Macrophomina phaseolina inoculum for experiments in Ventura and San Luis Obispo.?

Impacts
What was accomplished under these goals? UC Davis (Feldmann, Knapp, Coaker, Bjornson): Obj 1A. We have finished the first year of 2, multi-year field trials to evaluate Neopestalotiopsis (NPT) leaf spot and fruit rot in collaboration with UF PIs. These experiments are to evaluate 434 strawberry hybrids for leaf spot in FL and fruit rot in CA. We have planted the second year of planned field experiments. PI Peres and Whitaker shared germplasm for screening and supported out methods development and APHIS permits and UC Davis biological use permits, which we were successful in maintaining. This work also allowed PD Feldmann to develop a collaborative project (USDA NIFA AFRI) with Dr Daniel Runcie (UC Davis) and Barbara Blanco-Ulate (UC Davis) to support research on Strawberry Anthracnose, Grey Mold, and Angular Leaf Spot. Obj 1B. We have identified two new resistance QTL from the cultivar Earliglow through a combination of kmer GWAS and bulk segregant analysis. The graduate student leading this work is preparing her dissertation and publications. Similarly, we have identified two very strong candidate genes underlying the primary FW1 resistance locus using de novo transcriptomics and differential gene expression analysis, and are currently conducting the co-expression assays in tobacco to demonstrate a causal relationship. We have also designed and are producing KO lines in collaboration with Juan Debernardi, co-PI. Obj 1C. We have genotyped 36,000 seedlings for multiple Fusarium QTL (4), Phytophthora (1), and Macrophomina (10) and applied selection at the pre-transplant stage to increase the frequency of favorable alleles. Obj 1D. We have designed and are producing KO lines in collaboration with Juan Debernardi, co-PI. We expect to assess these plants for resistance/susceptibility in 2025. Obj 2A. We have designed and tested three medium density genotyping platforms, aqnd are focusing our attention on the ThermoFisher technology in collaboration with PI Whitaker's lab. Current prices have us genotyping 1,650 markers for $12. We, in collaboration with PI Whitaker's group, are working on a publication to support this new platform, which is being tested by Driscoll's and Plant Sciences Inc. Obj 2B. See Obj 1C. We have not applied genomic prediction at the pre-transplant stage as we have not had a genotyping platform meet the cost requirements to genotype 16,000-18,000 plants per year. Obj 4A. We have participated in field days targeting growers in CA central coast and the central valley, where growers are primarily Hmong and Mien. These growers in the central valley are mostly small acre and typically grow older genetics, even though new genetics are more disease resistance and provide many favorable characteristics. We, in collaboration with PI Lloyd, have handed out ~12,000 plants to these growers to hopefully seed excitement and fuel adoption. Obj 4C. We have given presentations at the North American Strawberry Growers Association meeting and to the California Strawberry Commission to increase the awareness and education of the CA and North American strawberry growers on gene editing technology. PD Feldmann has spoked at the midway California Seed Association meeting on gene editing. UC Davis (Debernardi): We have optimized efficient protocols for protoplast isolation using leaf tissue and calli as starting explants. We tested different enzymes concentrations in order to get an efficient cell wall digestion. Our results indicated that leaf tissue is not the best material for protoplast isolation; calli material yielded better quality protoplast. We have also evaluated parameters for protoplast encapsulation in alginate beads, and we have induced protoplast division. We have continued working on optimizing an agrobacterium-based transformation protocol and tissue culture method. We have tested the incorporation of a GRF-GIF cassette to improve regeneration frequency. We found that GRF-GIF doubles the transformation efficiency and reduces the time needed to obtain transgenic plants by half. We have worked on optimizing a CRISPR-Cas9 cassette for efficient genome editing using agrobacterium-based transformations. The best CRISPR cassette was incorporated into a binary vector that allows easy cloning of gRNAs, and Prof. Feldmann's lab is currently using that vector to perform editing in candidate genes in UC cultivars. Our transformation facility has already completed 12 transformation orders, and 21 additional orders are in progress for Prof. Feldmann's group. U Florida: Objective 1A. A field trial was continued for a second year to screen GWAS populations for NPT resistance. Phenotypes were integrated with DNA markers in a GWAS analysis that revealed a moderate-effect locus conferring resistance. Marker development for the locus is ongoing. Objective 1C. DNA markers were developed for charcoal resistance loci Mp2 and Mp3 for the high-throughput marker-assisted selection. Using transcriptome data analysis, candidate genes for Mp2 and Mp3 were identified and functional markers were developed. To develop markers for the resistant haplotype H2 for Pc2 (Phytophthora resistance locus), a breeding population was developed and tested under field conditions to Phytophthora crown rot. For NPT resistance, two QTLs, RNp1 and RNp2, were identified, and DNA markers were developed to support resistance breeding through marker-assisted selection. Additionally, we identified a susceptibility gene for NPT and are pursuing CRISPR gene editing applications to further enhance resistance. Objective 1D. A candidate gene (OCP3) for NPT resistance was identified and cloned for CRISPR gene editing. Tissue culture condition was optimized for the CRISPR gene editing in several commercial varieties. Objective 2A. A 1650 locus SNP custom panel was developed and initially validated with clean DNA in ~2,000 UF strawberry seedlings. Validation with crude DNA extracts ongoing. Objective 2C. Parent selection was conducted via genomic prediciton for multiple disease targets, and in 2,000 seedlings genotyped as in 2A above. Pyramiding Mp1,Mp2, and Mp3 in 800 seedlings was conducted using newly developed markers for each locus. Objective 3A. We have added to our collection and have now over 500 isolates of NPT. Two isolates with different virulence to strawberry were selected for chromosome-scale genome sequencing. Additional 120 isolates were sequenced and data used for the development of new molecular primers for identification of aggressive NPT. Objective 3B. A second year of field trials with a highly susceptible and a moderately susceptible cultivar were set up to evaluate different thresholds of the disease infection and spore germination models previously developed. Model-based applications were triggered 8 to 10 times compared to 16 times for the calendar sprays. Disease control and yield were similar among the treatments, indicating model applications can help to reduce the number of fungicide sprays. USDA ARS: A study was completed on Macrophomina spp. isolates from all major strawberry production regions. This study found evidence for host specialization on strawberry: only a single clade was virulent on strawberry. This was the first report of host specialization in this species and it aids breeding by indicating isolates that should be used for host resistance screening and aids management by showing molecular identification should target specific genotypes of M. phaseolina, not the species as a whole. This work also traced the global spread of this pathogen on strawberry, finding that trade of plant material is associated with dispersal. We completed an in-depth analysis of the geographic constraints on strawberry production in CA, and found that disease caused by M. phaseolina tended to increase in frequency as the distance from the ocean increased. This demonstrated that higher temperatures were a major factor in promoting disease caused by M. phaseolina.

Publications

• Type: Peer Reviewed Journal Articles Status: Awaiting Publication Year Published: 2024 Citation: Qin C, Goldman PH, Leap J, Henry PM. in press. Cover cropping attenuates population growth of Macrophomina phaseolina by limiting weed biomass, despite asymptomatic colonization of cover crops. Plant Disease. DOI:10/1094/PDIS-05-24-0951-RE
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Ramos G, Goldman P, Sharrett J, Sacher GO, Pennerman KK, Dilla-Ermita CJ, Jaime JH, Steele ME, Hewavitharana SS, Holmes GJ, Waterhouse H, Dundore-Arias JP, Henry PM. 2024. Geospatial analysis of California strawberry fields reveals regional differences in crop rotation patterns and the potential for lengthened rotations at current levels of production. Frontiers in Sustainable Food Systems. 8:1341782. DOI: 10.3389/fsus.2024.1341782.
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Dilla-Ermita CJ, Goldman P, Anchieta A, Feldmann MJ, Pincot DDA, Famula RA, Vachev M, Cole GS, Knapp SJ, Klosterman SJ, and Henry PM. 2024. Secreted in xylem 6 (SIX6) mediates Fusarium oxysporum f.sp. fragariae race 1 avirulence on FW1-resistant strawberry cultivars. Molecular Plant Microbe Interactions 37:530-541. DOI: 10.1094/MPMI-02-24-0012-R
• Type: Peer Reviewed Journal Articles Status: Under Review Year Published: 2024 Citation: K.K. Pennerman, P. Goldman, C.J. Dilla-Ermita, G. Ramos, J.H. Jaime, J. Lopez-Hernandez, J. Ramos, M. Aviles, C. Borrero, A.O. Gomez, J.M. Neal, M. Chilvers, V. Ortiz, E.H. Stukenbrock, G.H. Goldman, A. Mengitsu, H.D. Lopez-Nicora, G.O. Sacher, N. Vaghefi, L. Kiss, J.P. Benz, A.R. Machado, T.E. Seijo, N.A. Peres, F.N. Martin, J.C. Broome, K. Ivors, G. Cole, S. Knapp, D.J. McFarlane, S.W. Mattner, M. Gambardella, P.M. Henry. (under review). Population genomics of Macrophomina spp. reveals cryptic host specialization and evidence for meiotic recombination. bioRxiv 2024.09.03.609457; doi: https://doi.org/10.1101/2024.09.03.609457
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Vondracek Kaitlyn , Altpeter Fredy , Liu Tie , Lee Seonghee. 2024. Advances in genomics and genome editing for improving strawberry (Fragaria �ananassa). Frontiers in Genetics. DOI=10.3389/fgene.2024.1382445
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Yoon Jeong Jang, Taehoon Kim, Makou Lin, Jeongim Kim, Kevin Begcy, Zhongchi Liu, Seonghee Lee. 2024. Genome-wide gene network uncover temporal and spatial changes of genes in auxin homeostasis during fruit development in strawberry (F.?�?ananassa). BMC Plant Biology 24:876
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Jang, Y. J., Oh, Y., Verma, S., Porter, M. E., Dalid, C., Yoo, C. M., & Lee, S. (2024). Updates on Strawberry DNA Testing and Marker-Assisted Breeding at the University of Florida. International Journal of Fruit Science, 24(1), 219 -228. https://doi.org/10.1080/15538362.2024.2365683
• Type: Other Journal Articles Status: Accepted Year Published: 2024 Citation: Ronald Tapia, Won Suk Lee, Vance M. Whitaker and Seonghee Lee. 2024. Multiple Methods for Predicting Strawberry Powdery Mildew Severity from Field Canopy Reflectance Data. PhytoFrontiers.
• Type: Other Journal Articles Status: Accepted Year Published: 2024 Citation: Jin-Hee Kim, Vance M. Whitaker, and Seonghee Lee. 2024. A Haplotype-Phased Genome Characterizes the Genomic Architecture and Causal Variants for RXf1 Conferring Resistance to Xanthomonas fragariae in Strawberry (F. �ananassa). BMC Genomics.
• Type: Other Journal Articles Status: Accepted Year Published: 2024 Citation: Hyeondae Han, Natalia Salinas, Christopher R Barbey, Yoon Jeong Jang, Zhen Fan, Sujeet Verma, Vance M. Whitaker and Seonghee Lee. 2024. A Telomere-To-Telomere Phased Genome of an Octoploid Strawberry Reveals a Receptor Kinase Conferring Anthracnose Resistance. GigaScience
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Hyeondae Han, Yoon Jeong Jang, Youngjae Oh, Marcus Vinicius Marin, Jose Huguet-Tapia, Natalia A. Peres, Seonghee Lee. Chromosome-Scale Genome Sequence Resource for Two Neopestalotiopsis spp. Isolates with Di?erent Virulence in Strawberry (Fragaria � ananassa). Phytofrontiers 4:422-426.
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Alam, E., S. Lee, N. Peres and V.M. Whitaker. 2024. Marker-assisted pyramiding of charcoal rot resistance loci in strawberry. 59:1328-1334.
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Alam, E., C. Moyer, S. Verma, N.A. Peres and V.M. Whitaker. 2024. Exploring the genetic basis of resistance to Neopestalotiopsis in strawberry. The Plant Genome https://doi.org/10.1002/tpg2.20477.
• Type: Other Journal Articles Status: Submitted Year Published: 2025 Citation: Jin-Hee Kim, Cheol-Min Yoo, Chi Dinh Nguyen, Man Bo Lee, Heqiang Huo, and Seonghee Lee. Optimization of Shoot Regeneration and Agrobacterium-Mediated Transformation in Strawberry (Fragaria � ananassa). Journal of American Horticultural Science.
• Type: Other Journal Articles Status: Accepted Year Published: 2024 Citation: Holmes, G.J. 2024. The California strawberry industry: current trends and future prospects. International Journal of Fruit Science 24:115-129. https://doi.org/10.1080/15538362.2024.2342900
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Hassani, M-A., Gonzalez, O., Hunter, S.S., Holmes, G., Hewavitharana, S., Ivors, K. and Lazcano C. 2023. Microbiome network connectivity and composition linked to disease resistance in strawberry plants. Phytobiomes 7:298-311. https://doi.org/10.1094/PBIOMES-10-22-0069-R
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Steven J Knapp, Glenn S Cole, Dominique D A Pincot, Christine Jade Dilla-Ermita, Marta Bjornson, Randi A Famula, Thomas R Gordon, Julia M Harshman, Peter M Henry, Mitchell J Feldmann, Transgressive segregation, hopeful monsters, and phenotypic selection drove rapid genetic gains and breakthroughs in predictive breeding for quantitative resistance to Macrophomina in strawberry, Horticulture Research, Volume 11, Issue 2, February 2024, uhad289, https://doi.org/10.1093/hr/uhad289
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Feldmann, M. J., Pincot, D. D. A., Vachev, M. V., Famula, R. A., Cole, G. S., & Knapp, S. J. (2024). Accelerating genetic gains for quantitative resistance to verticillium wilt through predictive breeding in strawberry. The Plant Genome, 17, e20405. https://doi.org/10.1002/tpg2.20405
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Feldmann, M.J., Pincot, D.D.A., Cole, G.S. et al. Genetic gains underpinning a little-known strawberry Green Revolution. Nat Commun 15, 2468 (2024). https://doi.org/10.1038/s41467-024-46421-6
• Type: Peer Reviewed Journal Articles Status: Published Year Published: 2024 Citation: Mitchell J Feldmann, Dominique D A Pincot, Danelle K Seymour, Randi A Famula, Nicol�s P Jim�nez, Cindy M L�pez, Glenn S Cole, Steven J Knapp, A dominance hypothesis argument for historical genetic gains and the fixation of heterosis in octoploid strawberry, Genetics, 2024;, iyae159, https://doi.org/10.1093/genetics/iyae159
• Type: Other Journal Articles Status: Accepted Year Published: 2024 Citation: Fangyi Wang, Mitchell J Feldmann, Daniel E Runcie. Why is usefulness rarely useful? G3.

Progress 09/15/22 to 09/14/23

Outputs
Target Audience:The target audiences for this research are: (a) private and public sector strawberry breeders, plant pathologists, scientists, and extension specialists; (b) strawberry growers, shippers, and packers and others engaged in producing and marketing strawberries; (c) academic scientists engaged in breeding and genomics of other species in the Rosaceae and other asexually propagated species; (d) graduate students, postdoctoral researchers, and academic scientists engaged in economics, sociology, plant pathology, horticulture, breeding, genetics, and genomics research. Changes/Problems:One of our cooperators, Andreas Biscaro left UCCE but is now back with UCCE and will contribute to experiments on the effect of moisture, salt and temperature stress on Macrophomina root rot. What opportunities for training and professional development has the project provided?Co-PI Coaker has co-mentored two scientists, Marta Bjornson and Mishi Vachev. She has provided training for interviewing in industry and academic jobs as well as feedback on scientific presentations. She meets every two weeks with Mishi Vachev to discuss research progress and provide feedback. Mishi Vachev presented her work at the Phytopathology conference. Marta Bjornson presented her work at PAG 2023. PI Knapp and Feldmann have co-mentored 7 scientists, Marta Bjornson, Dominique Pincot, Mishi Vachev, Nicolas Jimenez, Alicia Sillers, Paul Skillin, and Caitlyn Morgan, who have all conducted USDA NIFA SCRI-focused research on disease resistance in strawberry. Nicolas and Mishi have both presented at important conferences in 2023. Alicia, Paul, and Caitlyn are new students working on S gene identification, Neopestalotiopsis resistance, and Fusarium wilt resistance, respectively. PI Feldmann, Knapp, and Bjornson co-mentor 4 undergraduate research associates at University of California Davis. Master's student Joseph Ramirez completed his first year of field studies and presented results at a field day and grower's meeting. Gerardo Ramos and Jose Jaime (technicians) both presented research to the Conference on Soilborne Plant Pathogens (~100 attendees)/ Kayla Pennerman (post-doc) presented research at the International Congress of Plant Pathology to an audience of ~100 plant pathology researchers from around the globe. She also volunteered to help run a Data Carpentry workshop on Unix, Python, and R scripting. Kayla started a USDA-ARS fungal bioinformatics working group that has members from across the country and has organized several journal clubs to discuss papers of interest. PhD student Elissar Alam conducted Np phenotyping and GWAS analysis, along with Mp population development. PhD student Lis Porto conducted phenotyping studies for isolates of Neopestalotiopsis spp. from different genetic clades At Transformation Facility, we are training an SRA (Lucero Jimenez) on strawberry transformation using Agrobacterium. Lucero has leaded the evaluation of agrobacterium transformation of modern cultivars and the evaluation of different CRISPR-Cas9 cassettes. She is currently testing the incorporations of developmental regulators to improve transformation protocol. Hiring a MSc student to be co-advised by Dr Feldmann. Joseph Ramirez presented his research results on 'Susceptibility to Macrophomina root rot and Verticillium wilt in 63 cultivars and advanced breeding lines' at the Cal Poly Strawberry Center's annual field day (450 attendees). Colin Koubek presented his research results on 'Effect of plastic mulch color and number of drip lines on incidence of Macrophomina root rot' at the Cal Poly Strawberry Center's annual field day (450 attendees). Joseph Ramirez presented his host plant resistance results to the Small Fruits Working Group at Plant Health 2023 Conference (APS Annual meeting) in Denver, CO. Joseph Ramirez presented Macrophomina and Verticillium susceptibility in strawberry at the 22nd Annual Strawberry Production Meeting in Ventura County Shashika Hewavitharana presented on 'Sequential crop termination and bed fumigation and cultivar resistance as tools for Verticillium wilt management in strawberries' in strawberry at the 22nd Annual Strawberry Production Meeting in Ventura County How have the results been disseminated to communities of interest?The results have been disseminated at three strawberry grower extension meetings, each with ~100 attendees, and at the Cal Poly Field day, with ~450 attendees. Multiple presentations at three different national or international meetings disseminated the results to the scientific community. At the UF breeding program field day in Dover, FL on January 11, 2023, 50 strawberry growers were provided preliminary data on a new Neopestalotiopsis breeding selection being considered for release. Results for the field modeling studies to time fungicide applications were also presented. UCD breeding program has held 3 field days since Septemeber 2022 with ~50 strawberry growers attending each. Disease resistance results were provided on fusarium, Macrophomina, phytophthora, and verticillium. Similarly, variety release docuements are being prepared for submission to HortScience that describe the disease resistance packages of the 5 new cultivars from UCD. We have participated in the SCRI Project Meeting and in the North American Strawberry Symposium (NASS), where we discussed our results and progress with other researchers. We have also participated in discussions with collaborators from academia and industry about the challenges and benefits of incorporating genome editing technology into strawberry breeding and research. We will establish field trials in early Nov, 2023; produce Macrophomina phaseolina inoculum for experiments in Ventura and San Luis Obispo. What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we plan to guide molecular biology experiments to enable verification of the FW1 Fusarium resistance gene and guide the selection and cloning of genome editing constructs for strawberry transformation. We will complete our preliminary work on PMR4 S-gene and produce gene edit plants for evaluation. We will complete the first year of joint NPT GWAS analysis between UF and UCD and prepare plant propagation for a second year. We expect that all of the new genotyping platforms will be available publicly through their respective third-party vendors by the end of the next reporting cycle. During the next reporting period, we will test the pathogenicity of strawberry-pathogenic isolates on other crops to determine if they are host-specific rather than host-specialized. We will also evaluate if cultivar resistance to Macrophomina depends on which strawberry-pathogenic isolate is used. We will conduct laboratory tests supporting experiments in Ventura to evaluate the impact of salt and water stress on Macrophomina disease development. We will continue working on establishing the protoplast-based platform. We will evaluate parameters for protoplast encapsulation in alginate beads. We will test protoplast division and microcalli colony formation using different media compositions. If successful, we will test the regeneration of whole plants. We have previously developed a protoplast-based system for grape, and using that system, we have already gained considerable experience on DNA-free editing, which includes the assembly of Ribonucleoprotein complexes(RNPs) in vitro and protoplast transfection parameters. Therefore, once we have a regeneration protocol working on strawberry protoplast, we think that it will be relatively simple to incorporate RNP transfection. We will continue working on improving the efficiency of our agrobacterium-based transformation. We expect that the delivery of some developmental regulator will help to reduce the regeneration bottleneck we have observed in different cultivars.

Impacts
What was accomplished under these goals? Objective 1A. A field trial was conducted to screen GWAS populations for Neopestalotiopsis resistance. Phenotypes were integrated with DNA markers in a GWAS analysis that revealed a moderate-effect locus conferring resistance. Marker development for the locus was initiated. A large population was propagated in high elevation nurseries (Crown Nursery) to conduct a joint GWAS experiment for Neopestalotiopsis resistance between UF and UCD. Phenotypes will be integrated with DNA markers in a GWAS analysis to discover genetic loci associated with fruit rot symptoms, foliar symptoms, and their covariance. Objective 1B. narrowed down candidate resistance genes for FW1 conferring Fusarium resistance in strawberry. Two genes are promising targets and a strategy for testing them in conjunction with the AvrFW1 effector has been developed. Constructs are in the process of being synthesized for testing. Identified promising targets for genome editing to confer broad-spectrum fungal resistance in strawberry. Constructs are being cloned for transformation. Objective 1C. The genomic regions of three charcoal rot resistant loci (Mp1, Mp2, Mp3) were fine-mapped and DNA markers were developed for Mp1 for the high-throughput marker-assisted selection. A new mapping population for identifying another resistance source for Phytophthora crown rot was developed. Completed and published a study of phytophthora resistance in strawberry. Validating the RPc2 locus discovered by PI Whitaker and Lee. Developed new DNA markers for deployment in UCD breeding program. Completed and published a study of verticillium wilt resistance in strawberry. Verticillium wilt has a complex genetic architecture and can be improved using genomic prediction. Completed and submitted a multi-year study on Macrophomina resistance and have uncovered Mp1-3 (validation of work by PI Whitaker) and an additional 7 moderate effect loci. Marker development is complete and these are being deployed in breeding populations at UCD. Objective 1D. A candidate susceptibility gene, OCP3, to Neopestalotiopsis disease was discovered, and functionally validated the gene function by RNAi-mediated transient knockdown assay in two UF varieties. Two genes (published Lee et al 2023) were identified for enhancing resistance to Botrytis grey mold. CRISPR-edited lines has been developed for further test. Candidate susceptibility genetics, PMR4, have been identified by homology in the octoploid strawberry genome. CRISPR-edited lines will be created in the next reported cycle and screened for induced resistance. Our efforts during the first year were focused on developing an efficient protoplast isolation protocol. We found that published protocols yielded very low quantity and low quality of protoplasts. We also found that strawberry materials were recalcitrant to cellulase digestions, and we evaluated different enzymes concentrations in order to get an efficient cell wall digestion. We have now identified an optimal protocol for protoplast isolation from leaf sections, and we are starting to test protoplast encapsulation and regeneration. In parallel to the work on protoplasts, we have continued working on optimizing an agrobacterium-based transformation protocol and tissue culture method that our group developed. We are testing the incorporation of developmental regulators into the T-DNA region of binary vectors to improve regeneration frequency, which seems to be a big bottleneck in current protocols. In addition, we have evaluated transformation efficiency of modern UC strawberry cultivars, which will allow to perform genome editing approach on relevant materials. We have worked on optimizing a CRISPR cassette for efficient genome editing using agrobacterium-based transformations. We have tested different promoters and Cas9 versions and have identified a combination with high editing activity. This CRIPSR cassette was incorporated into a binary vector that allows easy cloning of gRNAs. Prof. Knapp and Feldmann labs are currently using that vector to perform editing in candidate genes in UC cultivars. Objective 2A. Multiple genotyping platforms have been created and tested by UCD and UF, including a 5,000 SNP platform offered by RAPID Genomics (FlexSeq), a 5,000 SNP platform offered by ThermoFisher (AgriSeq), and a 5,000 and 3,000 SNP platform offered by Diversity Arrays Technology (DArTag). The DArTag platform was accepted for publication in 2023 and is already available and being used by the USDA Breeding Insights group. We have confirmed that these platforms all accurately capture genomic relatedness and should provide accurate results for genomic prediction and parentage assessment. Additionally, two 500 SNP genotyping platforms (subsets from the 5K platforms) were tested on UF strawberry seedlings, one each from Agriplex and Rapid Genomics (LGC). In total approximately 2,600 seedlings were tested, with leaf tissue submitted, data received and determined usable. Objective 2B. Using the developed platforms, we have genotyped and phenotyped 4,000 seedlings to test and validate genomic prediction for verticillium wilt and phytophthora. Individuals with high predicted GEBVs are being crossed to validate GEBV accuracy against progeny tested GCA estimates. Objective 2C. Using the genomic selection models from 2A, 465 seedlings predicted to have increased Neopestalotipsis resistance were selected for field testing and multiplied in the UF breeding program's summer nursery. Also, backcross populations with Macrophomina resistance locus Mp3 were inoculated in field screening trials and resistant parents retained. These were used as parents for pyramiding Mp1,Mp2, and Mp3 resulting in 6 pyramiding crosses totaling 436 seedlings that were multiplied in the summer nursery. Objective 3A. Ninety isolates of Neopestalotiopsis from strawberry were collected during this first year of the project, making the total number of isolates in the collection close to 400. Of these, 129 isolates were sequenced, which includes isolates from strawberry and other hosts. Six isolates from two genetic clusters were inoculated in two cultivars with different susceptibility levels, but none of the cultivars was considered resistant and thus no differences were observed. Whole genome sequences were generated for ~400 isolates of Macrophomina spp. Admixture, maximum likelihood phylogeny, and reticulate phylogeny support the delineation of M. phaseolina into eight clades. Equal mating type ratios in multiple clades and admixed isolates suggest there is an ongoing sexual cycle in wild M. phaseolina populations. One clade contained almost all M. phaseolina isolates from strawberry. Replicated experiments with forty isolates spanning the diversity of M. phaseolina showed only isolates in this strawberry-associated clade were highly virulent on strawberry. Some isolates from other clades are known to be virulent on other cultivars than were tested in this experiment. Overall, the results show that M. phaseolina is highly diverse, has on-going meiotic recombination, and contains a clade that is specialized for virulence on strawberry. These results overturn the dogma that M. phaseolina is a generalist, broad host range pathogen with no sexual cycle. Objective 3B. Two field trials were set, one with a highly susceptible and one with a moderately susceptible cultivar, to evaluate different thresholds of the disease infection and spore germination models previously developed. Following the model recommendations, 8 or 9 fungicide applications were made, which provided the same level of control as a calendar based program with 20 applications. Objective 4. Multiple field days have been held by UCD, UF, Cal Poly, and UCCE reaching approximately 750 attendees. At the NASS meeting in March 2023, our research team UF and UCD held an open forum on the new SCRI award, and discussed the potential impacts and value that can be created by gene editing in strawberry.

Publications

• Type: Journal Articles Status: Published Year Published: 2023 Citation: Pincot DDA, Feldmann MJ, Hardigan MA, Vachev MV, Henry PM, Gordon TR, Bjornson M, Rodriguez A, Cobo N, Famula RA, Cole GS, Coaker G, Knapp SJ. (2022) Novel Fusarium wilt resistance uncovered in natural and cultivated strawberry populations are found on three non-homoeologous chromosomes. Theoretical and Applied Genetics, 135, 2121-2145 doi: 10-1007/s00122-022-04102-2
• Type: Journal Articles Status: Awaiting Publication Year Published: 2023 Citation: Pennerman KK, Dilla-Ermita CJ, Henry PM. 2023. Exaggerated plurivory of Macrophomina phaseolina: An accounting of the large host range claim and the shifting of scientific language. Phytopathology. Accepted for publication on August 2, 2023. DOI: 10.1094/PHYTO-05-23-0154-R
• Type: Journal Articles Status: Published Year Published: 2023 Citation: Dilla-Ermita CJ, Goldman P, Jaime JH, Ramos G, Pennerman KK, Henry PM. 2023. First report of Fusarium oxysporum f. sp. fragariae race 2 causing Fusarium wilt of strawberry (Fragaria � ananassa) in California. Plant Disease 107:2849. DOI: 10.1094/PDIS-02-23- 0217-PDN
• Type: Journal Articles Status: Published Year Published: 2023 Citation: Henry PM, Dilla-Ermita CJ, Goldman P, Jaime J, Ramos G. 2023. Sporodochia formed by Fusarium oxysporum f. sp. fragariae produce airborne conidia and are ubiquitous on diseased strawberry plants in California. Phytopathology 113:1399-1404. DOI: 10.1094/PHYTO-10-22-0375-SC
• Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Dilla-Ermita CJ, Goldman P, Anchieta A, Feldmann MJ, Vachev MV, Pincot DDA, Famula RA, Cole GS, Knapp SJ, Klosterman SJ, Henry PM. In review. Secreted in xylem 6 (SIX6) mediates Fusarium oxysporum f. sp. fragariae race 1 avirulence on FW1-resistant strawberry cultivars. Submitted to Molecular Plant Microbe Interactions in August, 2023.
• Type: Journal Articles Status: Published Year Published: 2023 Citation: Lee, M. B., Han, H. and Lee, S. 2023. The role of WRKY transcription factors, FaWRKY29 and FaWRKY64, for regulating Botrytis fruit rot resistance in strawberry (Fragaria?�?ananassa Duch.). BMC Plant Biology.~ 23:420
• Type: Journal Articles Status: Awaiting Publication Year Published: 2023 Citation: Hassani, M-A., Gonzalez, O., Hunter, S. S., Holmes, G., Hewavitharana, S., Ivors, K. and Lazcano C. 2023. Microbiome network connectivity and composition linked to disease resistance in strawberry plants. Phytobiomes XX:XXX-XXX. https://doi.org/10.1094/PBIOMES-10-22-0069-R
• Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Wang, Y-C., Hewavitharana, S. S. and Holmes, G. J. Effect of cultivar and, soil and air temperature on disease development of strawberry Macrophomina root rot in Strawberry. Plant Health Progress.
• Type: Journal Articles Status: Submitted Year Published: 2024 Citation: Koster, J. T., Ding, S., Holmes, G. J., Robinson, E. A. and Hewavitharana, S. S. Effect of sequential crop termination and bed fumigation on Verticillium dahliae soil and plant density in strawberry. International Journal of Fruit Science
• Type: Journal Articles Status: Published Year Published: 2023 Citation: Jim�nez, N. P., Feldmann, M. J., Famula, R. A., Pincot, D. D., Bjornson, M., Cole, G. S., & Knapp, S. J. (2023). Harnessing underutilized gene bank diversity and genomic prediction of cross usefulness to enhance resistance to Phytophthora cactorum in strawberry. The Plant Genome, 16(1), e20275.
• Type: Journal Articles Status: Published Year Published: 2023 Citation: Feldmann, M. J., Covarrubias-Pazaran, G., & Piepho, H. P. (2023). Complex traits and candidate genes: estimation of genetic variance components across multiple genetic architectures. G3: Genes, Genomes, Genetics, 13(9), jkad148.
• Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Feldmann, M. J., Pincot, D. D., Cole, G. S., & Knapp, S. J. Genetic Gains Underpinning a Strawberry Green Revolution. Nature Communications.
• Type: Journal Articles Status: Under Review Year Published: 2024 Citation: Knapp SJ, Cole GS, Pincot DDA, Dilla-Ermita CJ, Bjornson M, Famula RA, Gordon TR, Harshman JM, Henry PM, Feldmann MJ. Transgressive Segregation, Hopeful Monsters, and Phenotypic Selection Drove Rapid Genetic Gains and Breakthroughs in Predictive Breeding for Quantitative Resistance to Macrophomina in Strawberry. Horticulture Research.
• Type: Journal Articles Status: Awaiting Publication Year Published: 2023 Citation: Hardigan MA, Feldmann MJ, Carling J, Zhu A, Kilian A, Famula RA, Cole GS, Knapp SJ. A medium-density genotyping platform for cultivated strawberry using DArTag technology. The Plant Genome.
• Type: Journal Articles Status: Awaiting Publication Year Published: 2023 Citation: Feldmann MJ, Pincot DDA, Vachev MV, Famula RA, Cole GS, Knapp SJ. Accelerating Genetic Gains for Quantitative Resistance to Verticillium Wilt Through Predictive Breeding in Strawberry. The Plant Genome.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Poster presented by Peter Henry et al. at the International Congress of Plant Pathology. Title: Fusarium oxysporum f. sp. fragariae race 2 in California did not evolve through a single mutation in the AvrFW1 avirulence gene.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Kayla Pennerman et al. at the International Congress of Plant Pathology. Title: " A broad genomic survey of Macrophomina spp. reveals host-genotype associations and evidence of on-going recombination"
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Peter Henry et al. at the 'Schroth Faces of the Future' symposium held at the Plant Health 2023 national plant pathology conference. Title: "Comparative genomics and literature review of Macrophomina phaseolina indicate that a re-interpretation of host range is necessary"
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Poster presented by Peter Henry et al. at the Plant Health 2023. Title: Revisiting the host range of Macrophomina phaseolina
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Poster presented by C. Jade Dilla-Ermita et al. at the Plant Health 2023 national plant pathology conference. Title: " Go in for the kill: the influence of temperature on necrotrophic growth of Macrophomina phaseolina on strawberry"
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Peter Henry et al. at the Fumigants and Alternatives Meeting & Annual Strawberry Production Research Meeting for Ventura County organized by Oleg Daugovish. Title: Updates on Fusarium oxysporum f. sp. fragariae race 2 in California.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Gerardo Ramos et al. at the Conference on Soilborne Plant Pathogens. Title: "Geospatial analysis of California strawberry fields reveals regional differences in crop rotation and vulnerability to a warming climate"
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Jose Jaime et al. at the Conference on Soilborne Plant Pathogens. Title: "Steam treatments for control of Macrophomina crown rot in summer-planted strawberry"
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Peter Henry et al. at the Conference on Soilborne Plant Pathogens. Title: Historic misunderstandings about the host range of Macrophomina phaseolina.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Peter Henry et al. at the Annual Strawberry Production Research Meeting organized by UCCE Advisor Mark Bolda. Title: Updates on Fusarium wilt research: Aerial dispersal and resistance- breaking strains.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Oral presentation by Peter Henry et al. at the North American Strawberry Symposium. Title: Genomic diversity in Fusarium oxysporum f. sp. fragariae; Implications for effective development of host resistance. EcoFarm. Title: Soil health and plant disease.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Porter, M., Song, X., Whitaker, V. M., Lee, S., Fan, Z. and Wang, Y. 2023. Genetic Investigation of Aroma Compounds in Strawberry. Annual Meeting of the American Society for Horticultural Science.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Porto, L.N.R., Marin, M.V., Acosta-Gonzalez, U., Rebollar-Alviter, A., and Peres, N.A. 2023. Exploring the phenotypic diversity of Neopestalotiopsis spp. isolates causing strawberry diseases. Plant Health annual meeting of the American Phytopathological Society.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Marin, M.V., Zuniga, A.I., and Peres, N.A. 2023. Evaluation of disease infection models to time fungicide applications for control of Neopestalotiopsis sp. on strawberry in Florida. Plant Health annual meeting of the American Phytopathological Society.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Verma, S., Osorio, L.F., and Whitaker, V.M. 2023. Genomic Selection in Strawberry: SNPs vs Haplotypes. Annual Meeting of the American Society for Horticultural Science.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Vondracek, K., Lee, S. and Liu, T. 2023. Effects of Exogenous Gibberellic Acid Application on Strawberry Development. 10th North American Strawberry Symposium.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Kim, J., Whitaker, V. M. and Lee, S. 2023. Genomic Characterization of the Locus Conferring Resistance to Bacterial Angular Leaf Spot in Strawberry (F. x ananassa). 10th North American Strawberry Symposium.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Porter, M., Song, X., Whitaker, V., Lee, S., Zhen, F. and Wang, Y. 2023. Strawberry Flavor Improvement Through Molecular Breeding. 10th North American Strawberry Symposium.
• Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Jang, Y. J., Oh, Y., Whitaker, V. M. and Lee, S. 2023. DNA Marker-Assisted Seedling Selections to Improve Strawberry Varieties. 10th North American Strawberry Symposium.
• Type: Journal Articles Status: Under Review Year Published: 2023 Citation: Knapp SJ, Cole GS, Pincot DDA, Lopez CM, Gonzalez-Benitez OA, Famula RA. UC Eclipse, a Photoperiod-Insensitive Cultivar Adapted to Summer Planting That Significantly Increases the Productivity of Strawberry in the Autumn Harvest Season. HortScience