The role of the mealybug Phenacoccus aceris in the spread of Grapevine leafroll-associated virus −1 (GLRaV-1) in two French vineyards

Abstract

Spread patterns of a Grapevine leafrollassociated virus 1 (GLRaV-1) epidemic and a mealybug infestation survey over 10 year were recorded in two Burgundy French vineyards to investigate the relation between them. The temporal evolution of leafroll spread at both study sites was compared on disease incidence data with logistic regression models. We first tested if the spatial distribution of the disease and the mealybug were aggregated using permutation methods, then we tested the independence between the two spatial patterns by randomly shifting one pattern. In Bon-zon, an increase from 5 % to 86 % of leafroll prevalence was observed over an 8-year time span, whereas leafroll prevalence remained stable around 5 % in Marsannay-la-Côte during the same period. In Bonzon, the disease spread rapidly from older neighbouring vineyards in four main patches while no spread of the disease was recorded from infected vines in Marsannay-la-Côte. The mealybug Phenacoccus aceris was recorded on 74 % of vines in Bonzon throughout the study and only 6 % of vines in Marsannay-la-Côte. In the latter location, the disease was not associated with the presence of the mealybug, so that it may have arisen from infected plant material escaping the sanitary inspection. In Bonzon, the significant statistical correlation between the mealybug distribution and diseased plants suggests that P. aceris was responsible for the rapid spread of GLRaV-1 in the vineyard. This is the first report of GLRaV-1 natural spread in Europe.Keywords Epidemiology . Ampelovirus . Grapevine scale insects . Leafroll disease . Spatial statistics Abbreviations GLRaVGrapevine leafroll-associated virus GVA Grapevine virus A GVB Grapevine virus B DAS-ELISA Double-antibody sandwich enzyme-linked immunosorbent assay

Ecology and management of grapevine leafroll disease

“…citri (Cabaleiro and Segura, 1997b) linked mealybugs to the observed vineyard spread. GLD spread in established vineyards, 8–10 years after the initial planting, has been documented in Australia (Habili et al, 1995;Habili and Nutter, 1997), California-USA (Golino et al, 2008), and France (Le Maguet et al, 2013). The rate of spread was similar in these studies, close to 10% increase per year once GLD infections were identified as being present, and newly infected vines were spatially aggregated, indicating vine-to-vine spread.…”

“…In addition, better information should assist nurseries and others producing plant material, particularly those using mass selection, to adopt procedures aimed at producing virus-clean grapevines. Moreover, a recent French study showed the risk to neighboring vineyards posed by leafroll-infected and scale insect-infested plots (Le Maguet et al, 2013). Therefore, a new plantation should take into account the sanitary status of neighbors and the possible spread of vectors from older to younger plots.…”

“…Finally, the wide variety of GLD epidemiological scenarios in France (e.g.,Le Maguet et al, 2013) and the difficulty to define any damage thresholds hamper determining recommendations on how best to manage virus-infected and/or vector-infested vineyards. There is a crucial need for deeper knowledge of epidemiology, including determinant factors such as infection intensity, sensitivity of cultivars, virus and vector species present, and landscape structure.…”

A complex virome unveiled by deep sequencing analysis of RNAs from a French Pinot Noir grapevine exhibiting strong leafroll symptoms.

“…However, in the Northern French vineyards (Champagne, Burgundy and Alsace), GLRaV-1 is the most prominent species causing GLD (Le Maguet et al 2013 and unpublished data). Furthermore, the rapid spread of GLRaV-1 by the mealybug Phenacoccus aceris has been demonstrated in a vineyard in Bonzon (Burgundy, France) with an increase in prevalence from 5% to 86% in an eight-year span [35]. While a partial GLRaV-1 genome from Australia was published in 2000 (12 394 nts) [16], the first full-length sequence of GLRaV-1 from the Canadian isolate 1050 (GenBank JQ023131, 18 659 nts), was only released eleven years later.…”

Gone with the wind: Aerial dispersal of Parthenolecanium corni crawlers in a newly planted grapevine plot

“…Moreover, these piercing‐sucking insects are known to transmit three grapevine‐infecting viruses associated to “rugose wood complex”: Grapevine virus A (GVA), GVB and GVE (Herrbach et al, ), assigned to the genus Vitivirus . It has been demonstrated that, although scale species are unable to fly (except adult males which do not feed and therefore are not vectors), some mealybug species are able to rapidly spread the disease within plots and from infected plots to new plantations (Cabaleiro et al, ; Golino, Weber, Sim, & Rowhani, ; Le Maguet et al, , ). In addition to mealybugs, a few soft scale species: Ceroplastes rusci (L.), Neopulvinaria innumerabilis (Rathvon), Parthenolecanium corni (Bouché) and Pulvinaria vitis (L.) are also known to transmit GLD viruses (Belli, Fortusini, Belli, Bianco, & Prati, ; Ciampolini & Guarnone, ; Fortusini, Scattini, Prati, Cinquanta, & Belli, ; Hommay, Komar, Lemaire, & Herrbach, ; Mahfoudhi, Digiaro, & Dhouibi, ; Sforza, Boudon‐Padieu, & Greif, ; Zorloni, Prati, Bianco, & Belli, ), but their dispersal and ability to spread viruses in the vineyard has not been documented.…”