Research Project: Mitigating High Consequence Domestic, Exotic, and Emerging Diseases of Fruits, Vegetables, and Ornamentals

Location: Subtropical Plant Pathology Research

2022 Annual Report

Objectives
1. Develop a risk-based index to analyze potential emerging pathogens/pests to identify those with greatest negative impact on agriculture to guide future research. 2. Characterize ecology, biology, epidemiology, genetics, and vector and host (crop and weed) interactions of exotic, newly emerging, re-emerging, and domestic pathogens. 2a. Characterize the basic biology, molecular biology and genetics of ‘Candidatus Liberibacter asiaticus (Las),’ the bacterium associated with citrus huanglongbing (HLB), and molecular mechanisms of host resistance/tolerance to Las infection. 2b. Characterize the basic biology, molecular biology, vector interactions and/or epidemiology of Tomato chlorotic spot virus (TCSV) and other tospoviruses, Squash vein yellowing virus (SqVYV), ilarviruses and other viruses of vegetables, ornamentals, and weeds, and Xanthomonas fragariae [causing angular leaf spot (ALS) on strawberry]. 2c. Characterize meteorological components affecting the epidemiology of Asiatic citrus canker (ACC), and the interactions of the Asian leaf miner with ACC, citrus black spot (CBS), the Asian citrus psyllid with HLB, the interaction of thrips with TSV. 3. Develop/refine and deliver rapid, sensitive reliable detection/sampling methods for high consequence/economic limiting pathogens, including but not limited to citrus canker, huanglongbing, black spot, plum pox virus, seedborne pathogens, and insect vectored viruses of vegetables and ornamentals. 3a. Develop improved detection methods for tospoviruses, Las and Xanthomonads on citrus and strawberry. 3b. Develop new and augment existing surveillance methods and protocols for HLB and the other newly introduced diseases such as CBS and PPV. 4. Develop or improve comprehensive integrated disease management strategies to rapidly find and delimit new disease introductions and develop quarantine and control/mitigation/eradication programs for exotic pathogens. 4a. Develop and use stochastic models to test various disease control strategies for citrus and prunus diseases caused by exotic pathogens. 4b.Develop and implement the most efficacious strategies for disease management of HLB, Xanthomonads of citrus and strawberry, CBS, PPV, and viruses of vegetables and ornamentals.

Approach
The overall approach is to thoroughly characterize plant pathogens causing domestic, exotic and emerging diseases at multiple levels: assessment and prioritization of economic, production and political risk; cellular, molecular and/or biochemical levels of host-pathogen-vector interaction; and traditional and newer stochastic epidemiological analysis at regional and plantation levels. New pathogens will be identified and characterized by biological and traditional cultural methods. Recombinant DNA and genomics technologies will be applied to study host-pathogen interactions. Resulting knowledge will be used to develop new detection and sampling methods, and management strategies, for these pathogens.

Progress Report
This is the final report for this project.Candidatus Liberibacter asiaticus (Las) in vitro culture was greatly improved with much more consistent results along with the development of semi-selective medium. Las was maintained and propagated in liquid medium for >2 years, and caused Huanglongbing (HLB) via psyllid feeding and citrus inoculation. Selections of citrus seedlings and bud sports were evaluated for HLB resistance/tolerance via graft-based and psyllid inoculations. Resistant/tolerant selections from greenhouse evaluations were further propagated, and planted in research and commercial grove for field trials where they have been evaluated for 3-4 years. The best new selections have gone through pathogen clean-up by the Florida Division of Plant Industry to be ready for future release. From Las pathogenesis standpoint, ARS scientists at Fort Pierce, Florida, demonstrated that Las 5315 effector induced extreme starch accumulation and chlorosis, typical symptoms of HLB, and revealed that host DEAD-box RNA helicase (DDX3) was targeted by Las5315, and that downregulation of host DDX3 gene was associated with leaf chlorosis. These findings facilitate our understanding of Las pathogenesis and HLB symptom development. Aspects of tissue colonization and population development in different citrus genotypes showed that Las populations peaked within 30 days of tissue colonization and did not increase significantly after this time. Calculations indicated that bacterial populations increased slowly in planta, with a very slow doubling time approaching 48 hours. Transmission of tospoviruses, ilarviruses and squash vein yellowing virus (SqVYV) is continuing to be elucidated. Production scale monitoring of tospoviruses and ilarviruses was investigated. Seeds of fruits from watermelon plants infected with SqVYV were collected for virus testing and seed transmission studies. A novel tobamovirus (Hoya chlorotic spot virus) was isolated from the ornamental crop, Hoya spp., and its biology, host range and genome were characterized. A second novel tobamovirus (Brugmansia latent virus) was identified in another ornamental crop, Brugmansia spp., and its genome was sequenced and characterized with host range ongoing. A viable-cell detection assay for specific detection of living cells of Xanthomonas fragariae (Xf), the cause of strawberry angular leaf spot (ALS) was developed. The assay was used to determine the survival of Xf on the surfaces of 11 materials stored at multiple temperatures and days after inoculation (DAI) to determine the likelihood of those materials serving as source of inoculum for disease. All materials harbored viable bacteria up to 7 DAI when stored at -4°C. Xf survived 270 DAI on cardboard at -4°C. At 20°C, cardboard, cotton balls, cotton t-shirt, and strawberry leaf tissue supported bacterial populations up to 14 DAI. Information from this study can be used to improve sanitation practices for ALS management in strawberry nurseries. In cooperation with industry partners, we are developing technology to identify and map regional distribution of crops on satellite imagery, and produce landscape-level risk maps of whitefly and whitefly-transmitted viruses. Initial testing in southwest Florida showed this to be a good predictor of crop type once the crop has grown sufficiently to be “seen” by the satellite. Once refined, landscape-level risk maps can be incorporated into an areawide pest management program for management of whitefly-transmitted viral epidemics. Plots to test the interaction of Asiatic citrus canker (ACC), leafminer, and windbreaks were established in Brazil. Results indicated that combinations of windbreaks and leafminer control are highly efficacious for canker mitigation. Fear of spread by hurricanes of both ACC in Texas and citrus black spot (CBS) in Florida led to the development of predictive models to estimate pathogen spread via hurricane events. We have further extended models to predict dispersal risk from major weather events, including tropical storms to improve targeted surveillance effort. These results are being used by state and federal regulatory agencies for early detection of critical pests. The long distance dispersal model via hurricanes are incorporated into recent multi-pest survey design in Florida and Texas. Model accuracy has been assessed for multiple hurricanes and will continue to be analyzed for future hurricane events. A stochastic simulation risk-based model for CBS spread by trade pathways has also been developed, and tested against trade pathway data sets, reviewed by collaborators, and is now completed. New sets of conventional reverse transcription-polymerase chain reaction (RT-PCR) and qRT-PCR primers for all three genomic RNAs of tomato chlorotic spot virus (TCSV), groundnut ringspot virus (GRSV) and tomato spotted wilt virus (TSWV) have been developed and validated. These primers were used for first detection of TCSV in soybean. Full genome sequence of TCSV isolate from peanut was determined. New detection methods based on two different biomarkers from host response to Candidatus Liberibacter asiaticus (CLas) infection were developed. Another new CLas detection method based on citrus leaf stiffness was developed in cooperation with ARS researchers in Wyndmoor, Pennsylvania, and industry scientists. Collectively, these new tests may significantly reduce diagnostic time and cost for Huanglongbing, and provide early and high throughput detection. A multi-pest surveillance method for statewide sweeps for Huanglongbing (HLB) and its vector and several other diseases including citrus black spot (CBS) has been very successful, is continuously adapted to new disease priorities and personnel/resource capacities as requested by USDA APHIS and California Department of Food and Agriculture (CDFA), and is re-deployed twice yearly with updated survey design. Risk-based residential and commercial survey methods for Asian citrus psyllid (ACP) and HLB are in the 10th year of deployment in California. Model validation indicated the models and linked surveillance are highly successful as they continually detect new introductions in southern California, which have now exceeded 3,600 as of April 2022. At request of CDFA, a spatiotemporal analysis of HLB detections resulted in a recommendation of delimiting surveys around new detections to be reduced to 250m with significant savings in personnel and fiscal resources; now routinely used by CDFA. A risk-based survey to detect plum pox virus (PPV) outbreaks in New York was integrated into the State/Federal New York PPV eradication program for 8 years, successfully eradicating PPV in New York. A risk-based model and survey to detect new PPV introduction were developed and are being deployed in Central California by California Department of Food and Agriculture. Regulatory agencies and commodity groups are implementing our risk-based survey models for multiple pathogens to predict new outbreak locations and target disease/vector hotspots. These are refined each year to optimize surveys to the changing disease/vector conditions, available manpower and resources, and will continue to be used for many years into the future. Models for >5 other diseases continue to be augmented and extended in unique ways to address specific regulatory issues as they arise, providing the foundation for future work. Solar thermotherapy reduces the titer of Candidatus Liberibacter asiaticus (Las) and enhances canopy growth by altering gene expression profiles in Huanglongbing- (HLB-) affected citrus plants. Despite the presence of Las in heat-treated commercial citrus, many trees produced abundant flush and grew vigorously for 2- to 3-years after treatment. Transcriptome analysis comparing healthy trees to HLB-affected citrus both before and after heat treatment demonstrated that post-treatment transcriptional expression patterns more closely resembled the expression patterns of healthy controls. In addition, thermotherapy significantly improved the quality of orange juice. Overall, these results indicate that solar thermotherapy can be an effective component of an integrated control strategy for HLB. An agent-based model has also been developed to examine the efficacy of ACP and HLB control strategies in select locations in California with consideration of social and economic perspectives, area-wide approaches and delimitation protocols. A census-travel model to predict introductions of pathogens from international travel has been integrated into HLB, CBS, PPV, and other surveys as an added risk factor and has recently been published as a stand-alone method. A Bayesian Belief Network model to assess phytosanitary health of seed commodities has been developed and validated for a tomato seed-borne disease and is currently being extended to other seed bacterial, viral and fungal pathosystems (e.g. cucumber green mottle mosaic virus of cucurbits, black leg of brassicas) and being incorporated into systems approaches for seed health management. A thermotherapeutic protocol that combined a conditioning thermal treatment with an eradicative thermal treatment was developed to manage several pathogens and pests on strawberry nursery stock. Subsequently, a commercial-scale precision thermotherapy unit for applying the thermal treatment was designed, built and tested. Several trials were conducted by ARS scientists at Fort Pierce, Florida, in cooperation with commercial nurseries to demonstrate the impact of thermotherapy on plant health and disease management. Some commercial nurseries have adopted the thermal treatment for use on their nursery stock.

Accomplishments
1. Plant pathogen detector dogs provide a new management tool. Detector dog development and deployment provide early detection and rapid response to offer the possibility to mitigate plant pathogens before they become epidemic. ARS researchers in Fort Pierce, Florida, and industry cooperators, have initiated a program for detector dog training to sample transplant trays for squash vein yellowing virus (cause of viral watermelon vine decline) in watermelon, rather than relying on traditional field scouting. Sampling transplant trays is far more efficient than sampling fields. Canines can sample thousands of plants in transplant trays far quicker than when these same transplants are planted in the field. Moreover, canines are more focused and less prone to exhaustion when plants are densely packed rather than being spaced 2 to 6 feet apart in the field. This development has led to consultation and initial plans with a major strawberry producer in California for use of canines for pest detection in strawberry nursery production. Initial detector dog research was recognized with a regional technology transfer award from the Federal Laboratory Consortium in late 2021.

2. Risk model and risked-based surveys improve Huanglongbing management decisions. Risk model and resulting risk-based surveys continue to direct California program to combat Huanglongbing (HLB). The overall project goal is early detection before the disease becomes established/endemic in California and improving evidence-based decision-making for successful HLB management. Development of risk-based survey protocols by ARS researchers at Fort Pierce, Florida, is critical for slowing the spread and optimizing mitigation measures. Background data and risk factors that change as the epidemic evolves were assessed and updated with data up to 12/31/2021. The dooryard citrus estimate for southern California has also been improved for using land parcel and U.S. census data. At present, California has about 40 surveyors dedicated to state-wide surveys but they cannot reach all commercial and residential properties. ARS researchers in Fort Pierce, Florida, have continued developing a risk-model that uses 10 risk criteria to rank every square mile in California and validation has indicated the high success rate of the predictive model. ARS researchers in Fort Pierce, Florida, have also designed a 2-cycle survey based on the risk model to survey across the entire state twice per year to capture the seasonality of disease development. The risk-based residential and commercial survey methods for Asian citrus psyllid and HLB are in the 10th year of deployment in California and has become the mainstay of the large-scale statewide survey in California. The survey continually detects new infections in southern California, which have now exceeded 3,600 as of April 2022. These detections are immediately removed and result in a quarantine surrounding the detection source with delimiting response protocols initiated. At present, the survey is done visually with PCR confirmation of suspicious trees; however, canine detection will likely be integrated soon.

3. Hurricane modeling improves surveys for key citrus diseases. Epidemiological models predict the spread of Asiatic citrus canker (ACC) and citrus black spot (CBS), two serious diseases that are not only causing economic damage but are severe impediments to international trade of citrus as a commodity. ACC, caused by a bacterium, and CBS, caused by a fungus, are both dispersed by rain splash. In the presence of hurricanes, such rain splash can be spread hundreds of miles. Multiple hurricane events, Harvey, Imelda, Beta and Hanna in southeast Texas, and Irma in southwest Florida potentially spread ACC and CBS, respectively. ARS researchers in Fort Pierce, Florida, extended the modeling approach by incorporating advanced spatial interpolation procedures with consideration of hurricane/storm features, inoculum population dynamic at source locations, risk dispersal patterns, and improved model flexibility to consider other plant pests and diseases at different scales. Results of these model predictions were integrated to a multi-pest survey design for improved decision-making by regulatory agencies and science advisory committees. As a result, Texas and Florida state regulatory agencies in collaboration with USDA, Animal and Plant Health Inspection Service have deployed the surveys for early detection of potential spread of these diseases in both states. There are ongoing analyses of the recent/future hurricane events to refine survey design for disease management.

4. New management tools for whitefly-transmitted viruses provide growers more options. Areawide pest management (AWPM) is an alternative for whitefly-transmitted virus management in vegetable crops. A number of whitefly-transmitted viruses, particularly tomato yellow leaf curl virus (TYLCV) in tomato and squash vein yellowing virus in watermelon, have severely impacted vegetable production in Florida and the southeastern U.S. for several decades. Current strategies for management focus on farm-centric tactics that rely mainly on strategic insecticide application for whitefly vector control, use of virus-resistant cultivars, rogueing infected plants and various cultural controls. With the exception of resistant cultivars, these approaches have had limited success for controlling both virus and whitefly. Recent research characterizing the spatial and temporal dynamics of TYLCV and its whitefly vector revealed that AWPM may be a viable alternative for managing TYLCV and likely other whitefly-transmitted viruses of vegetables. ARS researchers at Fort Pierce, Florida, worked with local crop consultants and an agricultural technology company to develop the tools for real-time mapping and a system for information delivery to foster development of AWPM as a new strategy for managing whitefly-transmitted virus epidemics in Florida and the southeast U.S. In addition, ARS researchers worked with a high-resolution satellite-image provider to develop an algorithm to classify the landscape by crop type and planting stage. Having the ability to fully characterize the landscape in real time (new satellite images are available every 3-5 days) allow us to identify areas of the landscape that may serve as sources or reservoirs for pests and pathogens, and subsequently use this information for areawide management. Canine detection of whitefly-transmitted vegetable viruses is currently being developed.

5. Latent class analysis offers improved means to evaluate bacterial viability assays. A latent class analysis (LCA) was conducted to evaluate the performance of a viable-cell quantitative PCR (qPCR) detection assay developed by ARS researchers against a simple plant bioassay and a standard qPCR assay for detection of Xanthomonas fragariae, the causal agent of angular leaf spot of strawberry. For any detection assay, calculation of error rates is essential for determining its diagnostic capabilities and its suitability for practical applications, particularly when evaluating competing assays or tests. A collection of contaminated samples was obtained, and the plant bioassay was used to split the sample population into ‘case’ and ‘control’ populations. The case population was the population of samples that contained living bacteria, and the control population contained samples with only non-viable bacteria (presumed dead) and produced no symptoms on inoculated leaves. A receiver operating characteristic (ROC) curve analysis was first conducted using the case and control populations to identify optimal qPCR threshold values for both qPCR assays to facilitate splitting the test results for use in LCA. Using these thresholds, estimated error rates were calculated for the viable-cell and standard qPCR assays, as well as for the bioassay. The analyses showed that the viable-cell detection assay outperformed the standard qPCR assay for detection of viable cells. Viability testing is extremely useful in certification and disease management applications, and with the information on test performance generated by LCA, the test can be put to practical use to design sampling strategies to account for the errors in testing.

Review Publications
Wang, Q., Xu, Y., Yang, X., Jia, J., Zhou, J., Duan, Y., Hartung, J.S., Ding, F. 2021. Novel insight into the distribution and dissemination of Candidatus Liberibacter asiaticus, the causal agent ofcitrus Huanglongbing. Plant Biotechnology Journal. 20(2):247–249. https://doi.org/10.1111/pbi.13753.
Latora, A.G., Codod, C.B., Lagarrea, S., Dutta, B., Kemerait, R.C., Adkins, S.T., Turechek, W., Coolong, T., Ribeiro Da Silva, A.B., Srinivasan, R. 2022. Combining cultural tactics and insecticides for the management of sweetpotato whitefly, Bemisia tabaci MEAM1, and viruses in yellow squash. Horticulturae. 8:341. https://doi.org/10.3390/horticulturae8040341.
Kuhn, J.H., Adkins, S.T., Alkhovsky, S.V., Avšic-Županc, T., Et Al. 2021. 2021 Taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology. https://doi.org/10.1007%2Fs00705-021-05143-6.
Herbert, A., Wang, H., Saski, C., Turechek, W. 2021. Draft genome sequence resource for two Xanthomonas fragariae strains. Microbiology Resource Announcements. 10:e00138-21. https://doi.org/10.1128/MRA.00138-21.
Dey, K., Vilez-Climent, M., Soria, P., Batuman, O., Mavrodieva, V., Wei, G., Zhou, J., Adkins, S.T., Mcvay, J. 2021. First Report of Tomato brown rugose fruit virus (ToBRFV) Infecting Tomato in Florida, U.S.A. New Disease Reports. 44:e12028. https://doi.org/10.1002/ndr2.12028.
Kuhn, J.H., Adkins, S.T., Alioto, D., Alkhovsky, S.V., et al. 2020. 2020 Taxonomic update for Phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Archives of Virology. https://doi.org/10.1007/s00705-020-04731-2.
Gottwald, T.R., Taylor, E.L., Amorim, L., Bergamin-Filho, A., Bassanezi, R.B., Silva Jr., G.J., Fogliata, G., Fourie, P.H., Graham, J.H., Hattingh, V., Kriss, A.B., Luo, W., Magarey, R.D., Schutte, G.C., Sposito, M.B. 2020. Probabilistic risk-based model for the assessment of Phyllosticta citricarpa-infected citrus fruit and illicit plant material as pathways for pathogen introduction and establishment. Crop Protection. 142(2021) 105521. https://doi.org/10.1016/j.cropro.2020.105521.
Turechek, W., Myhrene, O., Slovin, J.P., Peres, N. 2020. The use of aerated steam as a heat treatment for managing angular leaf spot in strawberry nursery production and its effect on plant yield. PhytoFrontiers. 1:104-119. https://doi.org/10.1094/PHYTOFR-08-20-0012-R.
Funderburk, J., Martini, X., Freeman, J., Strzyzewski, I., Traczyk, E., Skarlinsky, T., Adkins, S.T. 2019. Sampling for estimating Frankliniella species flower thrips and orius species predators in field experiments. Journal of Visualized Experiments. (149), e59869. https://doi.org/10.3791/59869.
Gilbertson, R.L., Batuman, O., Webster, C.G., Adkins, S.T. 2015. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. . 2:67-93. https://doi.org/10.1146/annurev-virology-031413-085410.
Milne, A., van den Bosch, F., Gottwald, T.R., Parnell, S.R., Chavez, V.A. 2020. What makes or breaks an effective disease control campaign? PLoS Computational Biology. 16(2):e1007570. https://doi.org/10.1371/journal.pcbi.1007570.
Bourhis, Y., Gottwald, T.R., Van Den Bosch, F. 2019. Translating surveillance data into incidence estimates. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 374:20180262. https://doi.org/10.1098/rstb.2018.0262.
Gottwald, Timothy, Luo, Weiqi, McRoberts, Neil. 2017. Risk-based HLB surveys: for southern California, statewide and targeted - an analysis of the increasing risk of HLB over the last five years. Citrograph. 9(1):38-43.
Adams, M., Adkins, S.T., Bragard, C., Gilmer, D., Li, D., Macfarlane, S., Wong, S., Melcher, U., Ratti, C., Ryu, K. 2017. ICTV Virus Taxonomy Profile: Virgaviridae. Journal of General Virology. 98,1999-2000, 10.1099/JGV.0.000884.
Wente, R., Hutton, S., Adkins, S.T., Turechek, W., Funderburk, J. 2017. Tospovirus-resistant tomato varieties for southern Florida. Extension Digital Information Source (EDIS). HS-1311.
Dey, K., Melzer, M., Li, C., Xiaoan, S., Adkins, S.T. 2018. First report of Tuberose mild mottle virus infecting tuberose (Polianthes tuberosa) in the USA. Plant Disease. 102(2):461. https://doi.org/10.1094/PDIS-07-17-1024-PDN.
Adkins, S.T., Turechek, W., Roberts, P.D., Webb, S.E., Baker, C.A., Kousik, C.S. 2017. Squash vein yellowing virus. American Phytopathological Society. 2017:149-151.
Gadhave, K., Dutta, B., Coolong, T., Sparks, A., Adkins, S.T., Srinivasan, R. 2018. First report of Cucurbit yellow stunting disorder virus in cucurbits in Georgia, United States. Plant Health Progress. 19:9-10. http://dx.doi.org/10.1094/PHP-03-17-0016-BR.
Adrakey, H.K., Gibson, G.J., Streftaris, G., Gilligan, C.A., Cunniffe, N.J., Gottwald, T.R. 2017. Evidence-based controls for epidemics using spatio-temporal stochastic model as a Bayesian framwork. Journal of the Royal Society Interface. 14:20170386. http://dx.doi.org/10.1098/rsif.2017.0386.
Wang, H., Wagnon, R., Moreno, D., Timilsina, S., Jones, J., Vallad, G., Turechek, W. 2022. A long-amplicon viability-qPCR test for quantifying living pathogens of bacterial spot in tomato seed. Plant Disease. 106:1474-1485. https://doi.org/10.1094/PDIS-11-21-2509-RE.
Armstrong, C.M., Zhou, L., Luo, W., Batuman, O., Alabi, O., Duan, Y. 2022. Identification of a chromosomal deletion mutation and the dynamics of two major populations of Candidatus Liberibacter asiaticus in its hosts. Phytopathology. 112:81-88. https://doi.org/10.1094/PHYTO-08-21-0325-FI.
Kerry, R., Ingram, B., Garcia-Cela, E., Magan, N., Ortiz, B.V., Scully, B.T. 2021. Determining future aflatoxin contamination risk scenarios for corn in southern Georgia, USA using spatio-temporal modelling and future climate simulations. Nature Scientific Reports. 11:13522. https://doi.org/10.1038/s41598-021-92557-6.
Wu, B., Li, N., Deng, Z., Luo, F., Duan, Y. 2021. Selection and evaluation of a thornless and HLB-tolerant bud-sport of Pummelo citrus with an emphasis on molecular mechanisms. Horticulture Research. 12:739108. https://doi.org/10.3389/fpls.2021.739108.
Armstrong, C.M., Doud, M.S., Luo, W., Zhao, W., Plotto, A., Bai, J., Baldwin, L., Manthey, J.A., Raithore, S., Stover, E.W., Duan, Y. 2021. Beneficial horticultural responses from the application of solar thermotherapy to mature HLB-affected citrus trees. HortScience. https://doi.org/10.1016/j.hpj.2021.04.008.
Kousik, C.S., Vogel, G.M., Ikerd, J.L., Mandal, M.K., Mazourek, M., Smart, C.D., Turechek, W. 2021. New sources of resistance in winter squash (Cucurbita moschata) to phytophthora crown rot and their relationship to cultivated squash. Plant Health Progress. 22:323-331. https://doi.org/10.1094/PHP-02-21-0047-FI.
Rennberger G, Turechek WW, Keinath AP. Dynamics of the ascospore dispersal of Stagonosporopsis citrulli, a causal agent of gummy stem blight of cucurbits. Plant Pathol. 2021;00:1–12 https://doi. org/10.1111/ppa.13424
Pisani, C., Adkins, S.T., Turechek, W., Patel, P.C., Rosskopf, E.N. 2021. First report of Macrophomina phaseolina, Fusarium brachygibbosum, and Lasiodiplodia theobromae causing fungal watermelon vine decline in Southwest and West-Central Florida. Plant Health Progress. 22:544-551. https://doi.org/10.1094/PHP-09-20-0077-RS.