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Disease Progression of Vector-Mediated Grapevine Leafroll-Associated Virus 3 Infection of Mature Plants Under Commercial Vineyard Conditions

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Disease Progression of Vector-Mediated Grapevine Leafroll-Associated Virus 3 Infection of Mature Plants Under Commercial Vineyard Conditions UC Berkeley UC Berkeley Previously Published Works Title Disease progression of vector-mediated Grapevine leafroll-associated virus 3 infection of mature plants under commercial vineyard conditions Permalink https://escholarship.org/uc/item/7dp9s67t Journal European Journal of Plant Pathology, 146(1) ISSN 0929-1873 Authors Blaisdell, GK Cooper, ML Kuhn, EJ et al. Publication Date 2016-09-01 DOI 10.1007/s10658-016-0896-8 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Eur J Plant Pathol (2016) 146:105–116 DOI 10.1007/s10658-016-0896-8 Disease progression of vector-mediated Grapevine leafroll-associated virus 3 infection of mature plants under commercial vineyard conditions G. Kai Blaisdell & Monica L. Cooper & Emily J. Kuhn & Katey A. Taylor & Kent M. Daane & Rodrigo P. P. Almeida Accepted: 24 February 2016 /Published online: 2 March 2016 # Koninklijke Nederlandse Planteziektenkundige Vereniging 2016 Abstract Grapevine leafroll-associated virus 3 newly symptomatic vines in commercial vineyards (GLRaV-3) is associated with the economically damag- probably became infected during the previous growing ing grapevine leafroll disease, and is transmitted in a season, and a decline in berry quality can be expected semi-persistent manner by several mealybug species. during the same year in which symptoms appear. We performed the first controlled field study of vector- mediated inoculations with GLRaV-3 in a commercial Keywords Grapevine leafroll-associated virus-3 . vineyard with previously asymptomatic vines, and mon- Grapevine leafroll disease . Incubation time . itored the vines during four growing seasons. We then Pseudococcusmaritimus . Semi-persistent transmission . compared the outcome of vector-mediated inoculations Vitis vinifera in the field study to an analogous laboratory study. In the vineyard, about half of all inoculated plants became Abbreviations infected with GLRaV-3, fewer than in the controlled ANOVA Analysis of Variance laboratory inoculations. Mealybugs had lower settling GLRaV-3 Grapevine leafroll-associated virus-3 and feeding success in the field than in the laboratory RNA ribonucleic acid inoculations. Our study suggests that laboratory studies RT-PCR reverse transcription and polymerase may overestimate transmission efficiency. All success- chain reaction fully inoculated vineyard plants first became symptom- atic one growing season after inoculations, and berry quality declined within one year after inoculations. Introduction Vineyard plants were effective virus sources one year after inoculations. Our findings generally indicate that More than three quarters of all plant viruses are trans- mitted by insects (Hogenhout et al. 2008), and informa- G. K. Blaisdell : K. M. Daane : R. P. P. Almeida (*) tion regarding key biological traits of vector-borne path- Department of Environmental Science, Policy, and Management, ogens is needed to inform effective control strategies. University of California, Berkeley, CA 94720, USA For example, knowledge of transmission efficiency can e-mail: [email protected] aid in predicting rates of pathogen spread (Purcell M. L. Cooper : E. J. Kuhn 1981). Another key parameter in estimating the rate of UC Cooperative Extension, 1710 Soscol Avenue, Suite 4, Napa, appearance of newly diseased hosts is the pathogen CA 94559, USA incubation period, the time between initial infection K. A. Taylor and when symptoms become evident. Despite the im- Constellation Brands, Inc., 1358 Walnut Drive, Oakville, CA portance of transmission efficiency and incubation peri- 94562, USA od with respect to the development of disease 106 Eur J Plant Pathol (2016) 146:105–116 management strategies, data are often not available and, subsequent disease progression under commercial vine- when available, are usually derived from research per- yard conditions. We performed a controlled GLRaV-3 formed under artificial conditions such as greenhouse transmission study into mature V. vinifera cv. Cabernet environments. franc vines in Napa Valley, CA USA. We used first Grapevine leafroll-associated virus 3 (GLRaV-3), in instars of the vector Pseudococcus maritimus the genus Ampelovirus,familyClosteroviridae,isthe (Ehrhorn), a mealybug species that is a common vine- primary virus species associated with grapevine leafroll yard pest and native to North America (Daane et al. disease in vineyards of wine growing regions worldwide 2012). We performed a concurrent laboratory study, (reviewed in Almeida et al. 2013). GLRaV-3 can cause with identical experimental design, to compare patho- interveinal reddening and downward rolling in red ber- gen transmission efficiency under controlled laboratory ried grape varieties (Vitis vinifera L.), inhibits photosyn- and field conditions. In the field study, we estimated thesis, decreases vine lifespan, and reduces fruit yield transmission efficiency and monitored time to GLRaV-3 and quality (Almeida et al. 2013). GLRaV-3 is one of detection via molecular diagnostics, appearance of the most common and detrimental viruses of grapevines, symptoms, and effects of disease on berry quality. Our and has led to economic losses of 25 % or more (Atallah findings are key to informing sound management prac- et al. 2012; Cabaleiro et al. 2013; Ricketts et al. 2015). tices with respect to understanding spread and progres- Spread of GLRaV-3 in vineyards and vector-borne sion of disease in a commercial vineyard. Furthermore, transmission in controlled laboratory studies were first we provide a previously missing link between con- documented in South Africa (Engelbrecht and Kasdorf trolled laboratory studies and realistic vineyard 1990), and since then GLRaV-3 spread in vineyards and conditions. transmission by several mealybug species have been documented in wine growing regions worldwide (Cabaleiro and Segura 1997; Charles et al. 2009; Materials and methods Golino et al. 2008;Habili1995;LeMaguetetal. 2012;Tsaietal.2008). Virus, plant, and insect materials Although multiple grape-colonizing mealybug spe- cies transmit GLRaV-3, estimates of vector transmission Virus-infected dormant cuttings of V. vinifera cv efficiency vary both among and within mealybug spe- Cabernet Sauvignon were used as source of GLRaV-3 cies (Almeida et al. 2013). GLRaV-3 is transmitted in a in our transmission experiments. Foundation Plant semi-persistent manner with no latent period required Services at the University of California, Davis provided between acquisition and inoculation by vectors; trans- accession LV89-01 from their Virus Source Vineyard, mission can occur after access periods of as little as one which is known to be infected with genetic variant hour, and reaches a maximum after access periods of group III of GLRaV-3, Grapevine virus B (GVB), and 24 hours (Tsai et al. 2008). First instar mealybugs are the Grapevine fleck virus (GFkV). This accession was cho- most efficient vectors, and mealybugs lose the ability to sen because genetic variant group III of GLRaV-3 is transmit GLRaV-3 four days after being removed from common in Napa Valley (Sharma et al. 2011). Plant an infected source (Le Maguet et al. 2012; Petersen and cuttings were cut to three buds each, treated with Charles 1997;Tsaietal.2008). There is no evidence of RootBoost (GardenTech, Lexington, KY) rooting hor- GLRaV-3 transovarial passage (Tsai et al. 2008). While mone, planted in 1:1 vermiculite: perlite, and kept on a laboratory-based transmission studies have been infor- mist bench for 6 weeks, until a few leaves were pro- mative, there is still a need for field-based transmission duced and roots were approximately 2.5 cm long. experiments to accurately estimate expected vector Cuttings were then removed from the mist bench and transmission efficiency and disease incubation time transplanted to 10 cm pots with a growth medium within the host. Information is lacking regarding how consisting of 2:1:1 SuperSoil: perlite: sand (Rod soon disease symptoms will appear after vector-borne McClellan Company, Elk Grove, CA), and kept in the infections are initiated, or how soon crop quality will be greenhouse until used as virus sources in transmission affected. experiments. GLRaV-3 infection was confirmed by mo- The goal of our study was to obtain information lecular diagnostics prior to use for source material in about vector-borne transmission of GLRaV-3 and transmission studies. Virus-free dormant V. vinifera cv Eur J Plant Pathol (2016) 146:105–116 107 Pinot noir cuttings were also provided by Foundation testing (described below). The block consisted of 8315 Plant Services, collected during winter dormancy 2011, vines planted at 588 vines per hectare. Row spacing was and propagated in the same manner as the virus-infected 1.8 m, and vine spacing was 1.5 m, with a vertical shoot source cuttings. positioning trellis system and bilateral pruning. Row We used Ps. maritimus as the mealybug vector, direction was northwest-southeast. Drip irrigation was which is difficult to maintain in insect colonies; there- provided using one 3.8 - L·h–1 emitter every 1.5 m. A fore we relied on field collections for experimental minimum of five buffer vines were left untreated at each inoculations. To obtain virus-free first instar Ps. end of the rows. Experimental vines were spaced every maritimus mealybugs, third instar females were collect- third vine, and treatments were fully randomized. The ed from a vineyard in Pope Valley, CA in May 2011, and three treatments included inoculations with no leaf allowed
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