WERA1007: Curtovirus Biology, Transmission, Ecology, and Management

(Multistate Research Coordinating Committee and Information Exchange Group)

Status: Active

WERA1007: Curtovirus Biology, Transmission, Ecology, and Management

Duration: 10/01/2021 to 09/30/2026

Administrative Advisor(s):


NIFA Reps:


Statement of Issues and Justification

Statement of Issues and Justification

Curtovirus spp. are the most widespread geminiviruses in the United States.  Curly top viruses, which are transmitted by the beet leafhopper, Circulifer (=Neoaliturus) tenellus Baker, have caused significant problems to irrigated agriculture in the western USA, including California, New Mexico, Idaho, Arizona, Colorado, Texas, and Washington since 1899 (Carsner and Stahl, 1924). The viruses infect a broad host range from many plant families and the leafhopper vector also feeds and breeds on an extensive range of plant hosts (Bennett, 1971).  The viruses cause economic damage to crops including tomato, pepper, dry beans, sugar beet, melons, and leafy greens in the western U.S.  In 2019, the virus also caused significant problems to hemp in Colorado. The impact of the disease is dependent on crop and location.

Curly top has a long history of major impacts on California agriculture starting in 1919 affecting sugar beet and to a lesser extent beans and melons. The state began a monitoring/management program for the beet leafhopper in 1943 and has continually followed the virus vector through this funded program since that time.  Curly top rarely impacted California processing tomatoes before the mid 1960’s, but as tomato production moved from directed seeded to transplants and from northern valleys to the Central Valley in the 1990’s, the risk for loss from BCTV greatly increased. In 2013, large leafhopper populations caused losses of more than 40% in many processing tomato fields, resulting in the loss of about one million short tons of fruit.

While the precise monetary losses to the tomato industry are not known, the costs associated with the monitoring/spray program (BCTV Control Program) are available.  Program income from grower assessments for fiscal years 2009/10-2013/14 was $1,544,051. Average annual Program expenses for the same fiscal years were $1,278,218. Since the outbreak in 2013, Program expenses have increased. For fiscal year 2014/15, which included the winter outbreak of 2015 when treatment and survey efforts greatly increased, expenditures were much higher than normal at $2,402,395, which included $905,000 in direct treatment costs (aerial spray contracts and pesticides).

During the 1920s and up to mid-1930s, curly top had the potential to eliminate the sugar beet crop in semi-arid areas of the western U.S. during years when large early beet leafhopper infestations occurred.  More recently, the Amalgamated sugar beet production area in Idaho, Oregon, and Washington estimated that 68,000 of its 174,000 acres of sugar beets were at high risk, another 68,000 acres were at medium risk and the remaining 38,000 were at low-low medium risk of curly top losses.  In Wyoming and Colorado, most of the 57,000 acres of sugar beets are at high risk.  Currently most commercial sugar beet cultivars have curly top resistance that can be described as low to intermediate.  In high risk areas the use of a neonicotinoid seed treatment with these cultivars will increase yield by 17% (Strausbaugh et al. 2006) annually.  Under medium risk conditions a neonicotinoid seed treatment will increase yields 11% annually.  With total value of the U.S. sugar beet crop ranging from 1.1 to 1.4 billion dollars from 2017 to 2019. (Natl. Ag Stat. Service) and approx. 35% of the production in the western U.S., the losses from curly top can be in the millions on an annual basis.  If we would lose the neonicotinoid seed treatments, the losses to curly top would lead to unsustainable production losses in the high risk areas.

Curly top affects peppers and tomatoes in New Mexico.  Losses to chile yields are variable, and have ranged from 50% in 2019 to 0.5% in 2012.  In Washington, curly top is also quite variable in dry beans with losses of 50-75% in large acreages (500-1,000 acres) in certain years.

Curly top caused significant losses or greater than 90% to hemp fields in western Colorado in 2019. Hemp grown for CBD in Colorado averages more than $50,000 per acre. The lack of pesticides registered for use on the crop and the need for organic production, has limited the management options for curly top.

Curly top epidemiology in the western U.S. is dependent on area, climate, plant diversity and distribution, and cropping cycles (Bennett, 1971).  Generally, the beet leafhoppers overwinters on weed hosts, acquires virus from the weeds, and migrates into agricultural areas to feed on (and infect) crops and weeds.  In some areas of California, leafhoppers migrate back to the overwintering areas in the fall (Cook, 1967). 

Curly top viruses are monopartite viruses in the family Geminiviridae, genus Curtovirus, which are characterized by a circular ssDNA genome within twin spherical particles.  Molecular characterization of curtoviruses in sugar beet in the 1980s, demonstrated that the viruses existed as three strains and variants of these strains (Stenger and McMahon, 1997), which were later determined to be distinct species.  New curtovirus strains have been identified in New Mexico (Creamer et al, 2005; Lam et al, 2009), Idaho (Strausbaugh et al., 2017), California (Chen et al., 2010, Chen and Gilbertson, 2016), and Mexico (Chen et al., 2011).

Due to the ability of the virus to infect a large diversity of weeds and the ability of its insect vector to survive on a similarly large and diverse group of weeds, as well as migrate considerable distances, Curtovirus spp. are endemic in the western U.S.  Management of this viral pathogen and its leafhopper vector has proven difficult.

Use of a variety of insecticides with different active ingredients registered on a crop has been used in an attempt to control curly top.  However, since the vector needs only a brief feeding interval in which to introduce the virus into a healthy plant, insecticides will not block virus transmission.  Soil treatments with the systemic insecticide, imidicloprid, can reduce virus incidence on sugar beets (Wang et al., 1999).  In Idaho, control of curly top with a first-generation neonicotinoid seed treatment such as imidacloprid proved to be unacceptable since control only lasts about 30 days and yield increases were marginal (Strausbaugh et al. 2006). However, planting sugar beet seed treated with a second-generation neonicotinoid (control lasts for at least 77 days) such as Poncho Beta, yields can be increased 11 to 17% with commercial sugar beet cultivars (Strausbaugh et al., 2006, 2012).  This extended early season control with the second-generation neonicotinoids, provides the plants with protection when they are small.  A larger sugar beet plant develops considerably better host resistance and can with stand late season curly top pressure with only minor to in significant yield losses.  Sugar beets are also effective breeding hosts for the leafhopper.  However, chile and tomato are not breeding hosts of the insect, like sugar beets, and the leafhopper spends very little time on the plants (Hudson et al., 2010), so that even the use of systemic insecticides on chile and tomatoes have not proved efficacious in preventing curtovirus spread or infection.  Even in crops such as sugar beet, where insecticide use has been effective, the industry perceives their use as a temporary solution since the leafhoppers may develop resistance in time and environmental concerns may eliminate their use.  

California has long used an industry-funded pesticide spray program to control the leafhopper using organophosphate sprays to uncultivated foothill breeding areas (Clark, 1995), although that program has not always been effective.  The BCTV Control Program sprayed about 24,700 acres in 2012, 52,330 acres in 2013, 49,000 acres in 2014, and 89,250 acres in 2015. The spray program utilized both ground and air spraying in the San Joaquin and Coastal Valleys of California based on sweep net counts in leafhopper breeding areas. An aggressive spray program was implemented in 2015 that combined spraying in winter, as well as spring, instead of sprays in spring and fall because of the early large sweep net counts in the breeding areas.

Knowledge of when and where to spray for most effective control of the leafhoppers in CA has also proven somewhat difficult. Timing of BLH outbreaks is highly variable and unpredictable because they are strongly dependent upon particular weather patterns. Historically they tended to happen about once every 6-10 years. Droughts in CA have impacted the BLH so that surveys identify BLH much further north and east than historically observed.

Plant resistance has been or is being developed for impacted crops.  While curly top resistant sugar beet cultivars have been developed, resistance is still only low to intermediate in the commercial sugar beet crop. However, all commercially grown chile pepper and tomato varieties are susceptible to the virus (Sedano et al., 2012). Cultural control in chile has relied primarily on overseeding the crop or removing infected plants. Biocontrol, including releasing imported egg parasitoids to control the leafhopper vector was evaluated in California.  Predictive models of disease have been developed for specific areas and crops, such as chile in southern New Mexico (Lehnhoff and Creamer, 2020), but do not eliminate the disease.

A sustainable management program is needed for this difficult pest/pathogen combination. Since leafhoppers migrate across state (and country) lines, management requires a coordinated effort between the different affected areas.  Any approach to management requires an understanding of the genetic variability of the pathogen and vector among the different crop hosts of curtoviruses to be successful.  Knowledge of the viral distribution within the region in wild and cultivated host plants, and the proximity of these virus reservoirs to commercial production fields is essential to reduce viral disease incidence. Since an integrated approach is necessary, significant progress in management of this viral disease will be possible only when individuals with different areas of expertise work together.

We propose the continuation of the WERA1007 group to address these problems.  This committee will continue to meet to discuss, assess, and prioritize required research into curtovirus genetics, vector biology and genetics, weed ecology, and disease management.  Individuals will share their best practices for management, which is the greatest benefit for active participation in the group, as rated by the current and past members. The committee will coordinate action plans to determine who will accomplish which aspects of the research, including who will work together to seek funding for the highest priority research.  The group will also coordinate research to provide preliminary information needed to secure grant funding.

Related, Current, and Previous Work

There are no other related ongoing regional projects that address this topic.  This project has been ongoing since 2004, first as a Western Region IPM working group and then as WERA 1007. Accomplishments of the group and of specific project members toward curly top management are listed below.

The largest impact of the WERA 1007 group has been development of sustainable collaborations among group members and sharing of information.  For example, studies on strain emergence involve several laboratories in the group including the Wintermantel Lab, Karasev Lab, and Carl Strausbaugh (Idaho). The Nachappa and Creamer lab are involved in studying the ecology, epidemiology and disease mitigation strategies for BCTV in hemp. This project is recently funded by FFAR (Foundation for Food and Agriculture Research).

Member accomplishments include development of infectious clones for specific strains by the Karasev lab that has allowed for specific testing of sugar beet cultivars for resistance, screening for resistance in beans the Miklas lab, and identification and characterization of curly top strains in sugar beets from the Strausbaugh group (Strausbaugh et al., 2017).

The Creamer lab has identified a bacterial endosymbiont of the beet leafhopper and shown that it produces GroEL-like compounds that bind to curtovirus capsid protein. The lab also determined the temperature and moisture requirements for Kochia, which is a key host for the virus and insect vector in southern New Mexico. A beet leafhopper prediction model for southern New Mexico based on fall rainfall was published that will help chile growers plan for disease (Lehnhoff and Creamer, 2020).

Previous accomplishments in Idaho include the demonstration of the effectiveness of Poncho Beta, Cruiser, and NipsIt, neonicotinoid insecticide seed treatments, for control of BCTV in sugar beet, followed by foliar applied pyrethroids (Strausbaugh et al., 2006, 2012, 2014, 2016).  The Idaho group also released a sugar beet line, KDH13, for the industry to use for improving resistance in commercial cultivars (Eujayl et al., 2018).  The Idaho group has also established to BCTV strains present in sugar beet production areas in the western U.S. (Strausbaugh et al. 2008).  The Idaho group also documented a reduction in the Severe strain of BCTV in Idaho with the introduction of the neonicotinoid seed treatments (Strausbaugh et al.,2017).  The Idaho group also collaborated with the Karasev lab to help them establish an immunodetection system for BCTV (Durrin et al. 2010).

Previous accomplishments in Washington include the establishment of a beet leafhopper monitoring network that spans the entire Columbia Basin irrigated production region (700,000 acres). This provides growers (650 current subscribers) with an early warning, through pest alerts, about potential beet leafhopper-related problems (Wohleb, unpublished).  Rondin et al. (2016) characterized curly top strains in leafhoppers in Oregon.

The biggest impact of the California USDA effort involves work to develop biotech-based control strategies BCTV and collaboration with the Gilbertson lab sequence the leafhopper vector.

The biggest accomplishments for the California Curly Top Program are improved communication to growers to alert them of potential devastation (throughout the year) by testing numerous samples of beet leafhoppers and host plants all year long and giving them info on pest pressure and virus pressure in real time, and increased educational outreach to growers, PCA’s, UC extension farm advisors, to teach them how to identify a beet leafhopper versus other non-target leafhoppers. Communication and education have had a tremendous positive impact for the tomato industry in CA.  

Objectives

  1. 1. Continue assessing the current status of curly top and setting priorities for integrated research on curly top disease.
  2. 2. Characterization of curtovirus strains including virus genetic diversity, new virus strains and virus in new hosts.
  3. 3. Organize research on the biology and ecology of the leafhopper, virus transmission, and the role of weed hosts in curly top in the western US.
  4. 4. Organize research to improve virus and vector management.
  5. 5. Provide a national platform for education on curly top disease, virus/insect/plant ecology and management, collaboration among scientists involved in these activities, and extension of research-based information for producers.

Procedures and Activities

Procedures and Activities

  1. Assess the current status of curly top and set priorities for integrated research on curly top disease.

Individuals working on different aspects of curly top in the western US come together annually to improve communication among different disciplines. Those that have met with the group in the past include virologists, weed scientists, entomologists, plant breeders, and extension scientists from New Mexico, Arizona, California, Colorado, Idaho, and Washington.  The group has been approximately 25% each AES researchers, CES scientists, USDA scientists, and growers/industry representatives.  Regional stakeholders with a commitment to the working group and its research include the New Mexico Chile Commission, New Mexico Chile Association, the New Mexico Farmers Marketing Association, the California Beet Sugar Association, California Tomato Research Institute (Fresno, CA), the Beet Sugar Development Foundation (Kimberly, ID), Curry Seed Co (Pearce, AZ), and the California Department of Food and Agriculture Curly Top Control Program, the Amalgamated Sugar Co. (Boise, ID). The coordinating committee will meet yearly to discuss the status of curly top in the western US and present the latest developments in curly top research. At the annual meetings, the group will also discuss gaps in the knowledge of the disease and set priorities for research.

The group met on July 14, 2020 virtually due to the on-going covid pandemic. There were 30 participants including post-docs and students. The group discussed the following as research priorities for the next 5 years:

  1. Alternatives to neonicitinoid seed treatments
  2. Novel sources of disease resistance
  3. A centralized database for leafhopper trapping results
  4. Better understanding of overwintering and weed hosts and leafhopper movement in the landscape
  5. Improved disease prediction model, including within season spread in all locations and to test and refine the model in each major cropping area that is affected by the disease.

 

  1. Characterization of curtovirus strains including virus genetic diversity, new virus strains and virus in new hosts.

The ability to manage a virus disease requires an understanding of which virus is causing the disease. Committee members have demonstrated that viral genetic diversity is present in a variety of plant hosts and that new curtoviruses appear regularly. Within cooperating western states, there are efforts underway to study the virus incidence and diversity, for example in sugarbeets in Idaho and Wyoming, in peppers in New Mexico, and in tomatoes in California. More recently, BCTV was reported for the first time on hemp in Colorado.  The Nachappa lab confirmed the virus in over 150 hemp samples from 9 counties in Colorado, with several fields reporting disease incidence levels above 50%. This led to diminished crop yield, including low quality of the flower and overall stunted growth. Interestingly, only Co and Wor strains were found to be infecting hemp. There is concern among hemp growers that BCTV maybe seed transmitted in hemp. These reports show that genetic diversity within curtoviruses is very high and will require a concerted effort to identify the tremendous virus diversity throughout the western US. The group will continue to share information on viral genetic diversity and encourage attempts to gain funding to study virus genetic diversity throughout the region by sequencing the genome of curtovirus isolates collected from different crops, weeds, and states. The compilation of this information is also essential for effective development of technology-based management systems.

  1. Organize research on the biology and ecology of the leafhopper, virus transmission, and the role of weed hosts in curly top in the western US.

While much research has been done to determine the leafhopper host range, the biology and ecology of the leafhopper in specific locations differs with cropping patterns and weed populations. Research to assess how the leafhoppers are overwintering has been done for some states, but not others and similarly, leafhopper flight patterns have been studied in some areas and not others. These research questions need to be expanded to additional areas in the western US.

Preliminary information suggests that beet leafhopper populations from different states vary genetically according to analysis of the mitochondrial DNA. The group will encourage leafhopper collections from diverse populations to assess the vector leafhopper genetic variability. Leafhopper populations from the different breeding areas may be geographically isolated or interbreeding populations. If they are reproductively isolated, then there may be important differences in adaptation to local host plants, host range and preferences, and virus strain-vector specificity. If they are interbreeding populations that exhibit a similar phenotype, then it may be possible to devise broadly based disease control strategies.   One member of the committee has begun to obtain the nucleic acid sequence of the beet leafhopper.  We hope to use this resource to analyze other genes from the leafhopper that may be useful for differentiating between populations.

There are many reports on the weeds hosts of BCTV and its leafhopper vector. However, many of these reports are historical, and the weed populations have changed significantly in the last 50 to 80 years since the reports were published. Virus incidence in weeds has been reported for California and New Mexico. Similarly, overwintering and key weed hosts have been studied in the two states. California is now beginning to use the methods developed in New Mexico to study the leafhopper population movements. The group will also encourage combining data for the leafhoppers and viruses into GIS mapping studies for each primary vector breeding area. Data on the movement of leafhoppers from weeds to crop plants will be incorporated into predictive models.

 

  1. Organize research to improve virus and vector management.

Curly top has proved very difficult to control. Project members have studied a variety of methods to manage the disease including biocontrol of the leafhopper vector, impact of insecticide sprays, use of anti-transpirants to deter leafhopper feeding, effectiveness of trap crops, row covers to deter insects, identification of plant resistance to virus and leafhoppers, engineered resistance, and predictive modeling to determine the likelihood of curly top in the next growing season and timing of leafhopper flights. All areas where curly top occurs are very interested in adapting curly top prediction models for their locations, specific weed populations, and environmental conditions. The group will continue to coordinate management tests in more than one location. The group will continue to help distribute management tools and products, such as resistant varieties and predictive models.  Management tools developed in one crop can be easily transferred into a new crop.  For example, the Nachappa and Creamer lab will monitor BLH movement in New Mexico and Colorado to developing predictions models of leafhopper population and virus dynamics in hemp. This project is recently funded by FFAR (Foundation for Food and Agriculture Research). Previous work by the Creamer lab helped the CA Curly top Program develop a trapping method to help growers and sparked a research project for testing the effectiveness of kaolin clay on organically grown tomatoes in CA. This has led to changes in the methods used for enumerating leafhoppers. In addition, we anticipate that information about the genetics of the virus and vector may lead to novel management strategies applicable to many locations. An example of a request from the tomato industry for help in management is for a BCTV rapid detection kit for in field detection.  This sort of tool could be used by growers in a variety of crops impacted by curly top.

In sugarbeets, neonicotinoid seed treatments are effective against beet leafhopper for 50 to 55 days after planting (Strausbaugh et al., 2012). However, there are reports of neonicotinoid resistance in numerous insect pests and this neurotoxin insecticide is also harmful to non-target insects including natural enemies (Szczepaniec et al., 2011) and pollinators (Pisa et al., 2015). Moreover, the state of Colorado is planning to ban neonicotinoids as early as next year. If the legislation is successful Colorado would join Maryland, Connecticut, and Vermont that have limited neonicotinoid use. Hence, it is critical explore alternates to neonicotinoids in sugarbeets. The Nachappa lab is currently evaluating insecticide resistance to pyrethroids and Poncho-Beta in BLH and hopes to screen populations of BLH from other states.

 

  1. Provide a national platform for education on curly top disease, virus/insect/plant ecology and management, collaboration among scientists involved in these activities, and extension of research-based information for producers.

The group has accumulated much information on various aspects of curly top and has actively disseminated the information as it has been generated.  Much of the information has been disseminated through peer-reviewed publications and at grower meetings and field days; however, general practical information on the disease and its management is not available in a usable format in a single location.  Often, the information that is available is specific to a particular crop or location. The extensive industry interaction within the group has made the gaps in information availability more obvious.  The committee, with directed input from the industry members, will develop best practices management recommendations, both general and specific, for each crop impacted by curly top.

The group will develop a website to house information on facts about curly top and the best practices recommendations developed by the group. Just as important, the group plans to add new information as it becomes available, keeping the information current.  For example, one member of the group, William Wintermantel, has produced a webinar on curly top that could be added to the site.

The website will also be a repository for K-12 teaching modules related to curly top, its vector, weed hosts, and monitoring and predicting disease.  Several modules have already been developed for middle school students for working with leafhoppers; additional modules will be developed dealing with ecology and epidemiology of diseases.  Other modules will be added as needed.

The meetings of the group will continue to provide an opportunity for undergraduates and graduate students working on curly top to present their research and to meet industry representatives and established researchers. Indeed, at this year’s virtual WERA meeting there were 6 students and post-docs including one undergraduate student. The importance of these meetings for students has not been acknowledged, but the small group format has generally provided an ideal opportunity for graduate students to present their research, with an average of two graduate student presentations each year.

Outputs:

The implementation of this proposal will result in continued annual meetings of the WERA 1007. At meetings, research progress reports will be presented, graduate students will present their research, and priorities for needed research into curly top will be identified. An annual action plan will be developed to determine which components of the group will accomplish which aspects of the needed work. Subgroups of the participants will be formed to work on specific projects throughout the year including educational materials, presentations, and reference sheets.

It is expected that preliminary research will be coordinated to obtain information needed to secure grant funding. Several members of the group will focus on submitting a large grant such as SCRI (Specialty Crop Research Initiative), CAP (Coordinated Agriculture Projects) or AFRI SAS (Sustainable Agricultural Systems) grant for one of the crops that is a problem for curly top, such as peppers, tomatoes, beans or other specialty crops.

A transcript of all meeting discussions will be made available to all committee members and interested individuals. Best practices management recommendations, both general and specific by crop will be developed. K-12 modules addressing aspects of curly top will be developed. A website will be established to house the information.

Expected Outcomes and Impacts

  • • Research will be coordinated at a regional and national level (among researchers at different locations) and become more interdisciplinary (among researchers from different disciplines).
  • • Information on new, emerging strains of BCTV and new hosts will be shared among the group.
  • • Information about BLH captures and movement within a specific location and overwintering hosts will be shared and housed in an online repository/website.
  • • Management strategies and products, such as resistant plant varieties and predictive models, information on insecticide resistance will be extended to new locations.
  • • The agricultural industry will be able to influence the direction of the research.
  • • Information about curly top will be more widely disseminated, bringing attention to the disease and its control.

Projected Participation

View Appendix E: Participation

Educational Plan

Educational Plan

All participants will be encouraged to disseminate information discussed at the meetings through grower and commodity board meetings as well as field days, pesticide applicator training, press releases, and extension and grower publications. Growers, crop consultants, processors, and extension personnel members of the group can help disseminate the information to their constituents and clientele. Transcripts of all meetings will be made available to all interested individuals upon request. Since the clientele has a large Hispanic base in New Mexico, Arizona, and Texas, and growers often conduct business in the US and Mexico, transcripts will also be translated into Spanish. To address the needs of smaller growers such as Native Americans or organic producers, relevant information will be distributed to representatives of these groups, such as the Federally Recognized Tribes Extension Program (FRTEP), who will also be encouraged to participate more actively in the coordinating committee.  A website will be developed to allow broad dissemination of information to clientele and the public not served through the extension meetings and publications.

K-12 teaching modules related to curly top, its vector, weed hosts and monitoring and predicting disease will be developed.  Several modules have already been developed for middle school students for working with leafhoppers and additional modules will be developed dealing with ecology and epidemiology of diseases.  Participants will be encouraged to develop educational modules based on current or past K-12 teaching and outreach related to curly top.

Organization/Governance

Organization/Governance

An Executive Committee made up of the chair, past chair, local arrangements chair, and secretary will serve as the governing board.  The committee will also help plan meetings and write relevant reports. The Chair position will rotate among members annually and will transition each year at the annual meeting.  Local arrangements chair for annual meetings will also be rotated among participants. Rebecca Creamer will initially serve as the secretary, keeping the email listing of participants, and maintaining all pertinent documentation.

Literature Cited

Literature Cited

Bennett, C. W.  1971.  The curly top disease of sugarbeet and other plants.  The Am. Phytopathol. Soc. Monogr. No. 7.

California Department of Food and Agriculture, 2019. Curly top Virus: Program Details.  https://www.cdfa.ca.gov/plant/ipc/curlytopvirus/ctv_hp.htm (accessed 28.05.2019).

Carsner, E. and Stahl, C. F.  1924.  Studies on curly-top disease of the sugar beet.  J. Agr. Res. 28:297-320.

Chen, L., Brannigan, K., Clark, R., Gilbertson, R. L. 2010.  Characterization of Curtoviruses associated with curly top disease of tomato in California and monitoring for these viruses in beet leafhoppers. Plant Dis. 94:99-108.

Chen, L.-F., Gilbertson, R.L., 2016.  Transmission of curtoviruses (Beet curly top virus) by the beet leafhopper (Circulifer tenellus). In: Brown, J.K. (Ed.), Vector Mediated Transmission of Plant Pathogens. American Phytopathological Society, St. Paul, MN, pp.243-262.

Chen, L.-F., Vivoda, E., and Gilbertson, R. L. 2011. Genetic diversity in curtoviruses: A highly divergent strain of Beet mild curly top virus associated with an outbreak of curly top disease in pepper in Mexico. Archives of Virology 156:547-555.

Clark, R. A.  1995.  Environmental assessment of curly top virus control in California: 1991-1995.  Cal. Dept. Food and Agr.  Sacramento, CA

Cook, W. C.  1967.  Life history, host plants, and migrations of the beet leafhopper in the western United States.  U.S.D.A. Tech. Bull. 1365. 122 p.

Creamer, R., Hubble, H., and A. Lewis.  2005.  Curtovirus infection of chile pepper in New Mexico.  Plant Disease 89:480-486.

Durrin, J.S., Nikolaeva, O.V., Strausbaugh, C.A., Karasev, A.V. 2010. Immunodetection of two curtoviruses infecting sugar beet. Plant Dis. 94:972-976.

Eujayl, I., Strausbaugh, C., Lu, C. 2018. Registration of sugarbeet doubled haploid line KDH13 with resistance to Beet curly top. J. Plant Registrations 12, 288. Doi:10.3198/jpr2015.09.0055crgs.er.

Hudson, A., Richman, D. B., Escobar, I., and Creamer, R.  2010.  Comparison of the feeding behavior and genetics of beet leafhopper (Circulifer tenellus, Baker) populations from California and New Mexico.  Southwestern Entomologist 35:241-250.

Lam, N., Creamer, R., Rascon, J., and Belfon, R. 2009.  Characterization of a new curtovirus, Pepper yellow dwarf virus, from chile pepper and distribution in weed hosts in New Mexico.  Archives of Virology 154:429-436.

Lehnhoff E, Creamer, R. 2020. Prediction of early season beet leafhopper populations in southern New Mexico. Plant Health Progress 21:71-76.

Pisa, L. W., Rogers, V. A., Belzunces, L. P., Bomatin, J. M. Downs, C. A., Goulson, D., Kreutzweiser, D. P. Krupke, C., Liess, M., McField, M., Morrissey, C. A., Noome, D. A., Settele, J., Simon-Delson, N., Stark, J. D., van der Sluijs, J. P., Van Dyck, H., and Wiemers, M. 2015.  Effects of neonicotinoids and fipronil on nontarget invertebrates. Environmental Sicence and Pollution Research 22:68-102.

Rondon, S.I., Roster,M.S., Hamlin, L.L., Green, K.J., Karasev, A.V., Crosslin, J.M. 2016.  Characterization of Beet curly top virus strains circulating in beet leafhoppers (Hemiptera:Cicadellidae) in northeastern Oregon. Plant Dis. 100:1586-1590.

Sedano, M., Lam, N., Escobar, I., Cross, T., Hanson, S. F., and Creamer, R.  2012.  Application of vascular puncture for evaluation of curtovirus resistance in chile pepper and tomato.  Journal of Phytopathology 160:120-128.

Stenger, D. C. and McMahon, C. L.  1997. Genotypic diversity of beet curly top virus populations in the western United States.  Phytopathology 87:737-744.

Strausbaugh, C. A., Eujayl, I. A., and Wintermantel, W. M. 2017. Beet curly top virus strains associated with sugar beet in Idaho, Oregon and a western U.S. collection. Plant Dis. 101:1373-1382.

Strausbaugh, C. A., Gillen, A. M., Gallian, J. J., Camp, S., and Stander, J. R. 2006. Influence of host resistance and insecticide seed treatments on curly top in sugar beets. Plant Dis. 90:1539-1544.

Strausbaugh, C. A., Wenninger, E. J., and Eujayl, I. A. 2012.  Management of severe curly top in sugar beet with insecticide.  Plant Dis. 96:1159-1164.

Strausbaugh, C. A., Wenninger, E. J., and Eujayl, I. A. 2016. Length of efficacy forcontrol of curly top in sugar beet with seed and foliar insecticides. Plant Dis.100:1364-1370

Strausbaugh, C. A., Wintermantel, W. M., Gillen, A. M., Eujayl, I. A. 2008. Curly top survey in the western United States. Phytopathology 98:1212- 1217.

Szczepanied, A., Creary, S. F., Laskowski, K. L., Nyrop, J. P., and Raupp, M. J. 2011. Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PlosOne doi.org/10.1371/journal.pone.0020018

Wang, H. Gurusinghe, P. de A., and Falk, B. W.  1999.  Systemic insecticides and plant age affect beet curly top virus transmission to selected host plants.  Plant Dis. 83:351-355.

Attachments

Land Grant Participating States/Institutions

CO, ID, NM, OR, WA

Non Land Grant Participating States/Institutions

California Department of Agriculture, California Tomato Research Institute , KWS Seeds, LLC, Pacific West Area, The Amalgamated Sugar Company LLC, USDA-ARS Temperate Tree Fruit and Vegetable Research Unit , USDA-ARS/Idaho, USDA-ARS/Washington
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