Ecology and management of grapevine leafroll disease

Grapevine leafroll disease (GLD) is caused by a complex of vector-borne virus species in the family Closteroviridae. GLD is present in all grape-growing regions of the world, primarily affecting wine grape varieties. The disease has emerged in the last two decades as one of the major factors affecting grape fruit quality, leading to research efforts aimed at reducing its economic impact. Most research has focused on the pathogens themselves, such as improved detection protocols, with limited work directed toward disease ecology and the development of management practices. Here we discuss the ecology and management of GLD, focusing primarily on Grapevine leafroll-associated virus 3, the most important virus species within the complex. We contextualize research done on this system within an ecological framework that forms the backbone of the discussion regarding current and potential GLD management strategies. To reach this goal, we introduce various aspects of GLD biology and ecology, followed by disease management case studies from four different countries and continents (South Africa, New Zealand, California-USA, and France). We review ongoing regional efforts that serve as models for improved strategies to control this economically important and worldwide disease, highlighting scientific gaps that must be filled for the development of knowledge-based sustainable GLD management practices.

[1]  Marcela González,et al.  DINÁMICA POBLACIONAL DE PLANOCOCCUS FICUS SIGN. (HEMIPTERA - PSEUDOCOCCIDAE) EN VIÑEDOS. MENDOZA ( ARGENTINA) POPULATION DYNAMICS OF VINE MEALYBUG PLANOCOCCUS FICUS SIGN. (HEMIPTERA - PSEUDOCOCCIDAE) IN VINEYARDS. MENDOZA (ARGENTINA) , 2006 .

[2]  N. Katis,et al.  Complete genome analysis and immunodetection of a member of a novel virus species belonging to the genus Ampelovirus , 2008, Archives of Virology.

[3]  E. Weber,et al.  Leafroll disease is spreading rapidly in a Napa Valley vineyard , 2008 .

[4]  V. Walton,et al.  Pheromone-based mating disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in California vineyards. , 2006, Journal of economic entomology.

[5]  S. Higgs,et al.  Chikungunya virus emergence is constrained in Asia by lineage-specific adaptive landscapes , 2011, Proceedings of the National Academy of Sciences.

[6]  G. Kasdorf,et al.  Transmission of grapevine leafroll disease and associated closteroviruses by the vine mealybug, Planococcus ficus. , 1990 .

[7]  S. Duffy,et al.  Genetic diversity in the 3' terminal 4.7-kb region of grapevine leafroll-associated virus 3. , 2011, Phytopathology.

[8]  K. Krüger,et al.  Grapevine leafroll-associated Virus 3 (GLRaV-3) Transmission by Three Soft Scale Insect Species (Hemiptera: Coccidae) with Notes on Their Biology , 2013 .

[9]  C. Cabaleiro,et al.  Some characteristics of the transmission of grapevine leafroll associated virus 3 by Planococcus citri Risso , 1997, European Journal of Plant Pathology.

[10]  Andrew G. Glen,et al.  APPL , 2001 .

[11]  M. Barrasa,et al.  Spatial analysis of epidemics of Grapevine leafroll associated virus-3 , 2008, European Journal of Plant Pathology.

[12]  A. Lindén,et al.  Effect of grapevine leafroll virus on vine growth and fruit yield and quality , 1970 .

[13]  M. Fuchs,et al.  Diversity of ampeloviruses in mealybug and soft scale vectors and in grapevine hosts from leafroll-affected vineyards. , 2009, Phytopathology.

[14]  D. Bosco,et al.  Effect of Host Plant Tissue on the Vector Transmission of Grapevine Leafroll-Associated Virus 3 , 2011, Journal of economic entomology.

[15]  D. Golino,et al.  Mealybug transmission of Grapevine leafroll viruses: an analysis of virus-vector specificity. , 2010, Phytopathology.

[16]  Varvara I. Maliogka,et al.  TAXONOMIC REVISION OF THE FAMILY CLOSTEROVIRIDAE WITH SPECIAL REFERENCE TO THE GRAPEVINE LEAFROLL-ASSOCIATED MEMBERS OF THE GENUS AMPELOVIRUS AND THE PUTATIVE SPECIES UNASSIGNED TO THE FAMILY , 2012 .

[17]  O. Lemaire,et al.  Grapevine virus A transmission by larvae of Parthenolecanium corni , 2008, European Journal of Plant Pathology.

[18]  J. G. Charles,et al.  Transmission of grapevine leafroll-associated closteroviruses by Pseudococcus longispinus and P. calceolariae. , 1997 .

[19]  M. Gifford,et al.  Grapevine leafroll virus—history and anatomic effects , 1967 .

[20]  J. G. Charles,et al.  A review of the ecology of grapevine leafroll associated virus type 3 (GLRaV-3) , 2006 .

[21]  S. Duffy,et al.  A divergent variant of Grapevine leafroll-associated virus 3 is present in California , 2012, Virology Journal.

[22]  Walton,et al.  Vineyard managers and researchers seek sustainable solutions for mealybugs, a changing pest complex , 2008 .

[23]  M. Cooper,et al.  Development of a Multiplex PCR for Identification of Vineyard Mealybugs , 2011, Environmental entomology.

[24]  E. Koonin,et al.  Genomic and biological analysis of Grapevine leafroll-associated virus 7 reveals a possible new genus within the family Closteroviridae. , 2012, Virus research.

[25]  D. G. James,et al.  Movement of grape mealybug, Pseudococcus maritimus, on and between host plants , 2008 .

[26]  Nuredin Habili,et al.  Temporal and Spatial Analysis of Grapevine Leafroll-Associated Virus 3 in Pinot Noir Grapevines in Australia. , 1997, Plant disease.

[27]  P. Bianco,et al.  TRANSMISSION OF GRAPEVINE VIRUS A AND GRAPEVINE LEAFROLL-ASSOCIATED VIRUS 3 BY HELIOCOCCUS BOHEMICUS , 2006 .

[28]  R. Lathe Phd by thesis , 1988, Nature.

[29]  Alison G. Power,et al.  Competition between Viruses in a Complex Plant‐‐Pathogen System , 1996 .

[30]  R. Almeida,et al.  Biology and Management of Mealybugs in Vineyards , 2012 .

[31]  V. Walton,et al.  Pheromone-Based Mating Disruption of Planococcus ficus (Hemiptera: Pseudococcidae) in California Vineyards , 2006 .

[32]  N. Bertazzon,et al.  Genetic variability and pathological properties of Grapevine Leafroll-associated Virus 2 isolates , 2010, European Journal of Plant Pathology.

[33]  C. W. Tsaia,et al.  Seasonal dynamics and virus translocation of Grapevine leafroll-associated virus 3 in grapevine cultivars , 2012 .

[34]  A. Babini,et al.  Effects of Virus and Virus-Like Infections on Growth, Yield, and Fruit Quality of Albana and Trebbiano Romagnolo Grapevines , 1997 .

[35]  G. Kasdorf,et al.  Association of a closterovirus with grapevines indexing positive for grapevine leafroll disease and evidence for its natural spread in grapevine. , 1985 .

[36]  P. Jerie,et al.  Aerial dispersal of first- and second-instar longtailed mealybug, Pseudococcus longispinus (Targioni Tozzetti) (Pseudococcidae: Hemiptera). , 1994 .

[37]  S. Duffy,et al.  Occurrence of Grapevine Leafroll-Associated Virus Complex in Napa Valley , 2011, PloS one.

[38]  M. Digiaro,et al.  Transmission of Grapevine Leafroll Viruses by Planococcus ficus (Hemiptera: Pseudococcidae) and Ceroplastes rusci (Hemiptera: Coccidae). , 2009, Plant disease.

[39]  O. Lemaire,et al.  The role of the mealybug Phenacoccus aceris in the spread of Grapevine leafroll-associated virus −1 (GLRaV-1) in two French vineyards , 2012, European journal of plant pathology.

[40]  M. Roossinck The good viruses: viral mutualistic symbioses , 2011, Nature Reviews Microbiology.

[41]  D. Golino,et al.  Pathogen testing and certification of Vitis and Prunus species. , 2005, Annual review of phytopathology.

[42]  G. Belli,et al.  Transmission of a grapevine leafroll associated closterovirus by the scale insect Pulvinaria vitis L. , 1994 .

[43]  S. E. McGregor,et al.  GRAPEVINE LEAFROLL-ASSOCIATED VIRUS 3 PERSISTENCE IN VITIS VINIFERA REMNANT ROOTS , 2009 .

[44]  Gerhard Pietersen,et al.  Control of Grapevine Leafroll Disease Spread at a Commercial Wine Estate in South Africa: A Case Study , 2013, American Journal of Enology and Viticulture.

[45]  D. Golino,et al.  The origins of the grape program at Foundation plant materials service , 2001 .

[46]  D. Golino,et al.  Vitis californica and Vitis californica × Vitis vinifera Hybrids are Hosts for Grapevine leafroll-associated virus-2 and -3 and Grapevine virus A and B. , 2011, Plant disease.

[47]  A. Gutierrez,et al.  Prospective evaluation of the biological control of vine mealybug: refuge effects and climate , 2008 .

[48]  D. J. Allan,et al.  Mealybugs and the spread of grapevine leafroll-associated virus 3 (GLRaV-3) in a New Zealand vineyard , 2009, Australasian Plant Pathology.

[49]  M. Fuchs,et al.  Genomic analysis of grapevine leafroll associated virus-5 and related viruses. , 2012, Virus research.

[50]  D. Bosco,et al.  Transmission of grapevine leafroll-associated virus 3 by the vine mealybug (Planococcus ficus). , 2008, Phytopathology.

[51]  J. Eiras-Dias,et al.  Five phylogenetic groups identified in the coat protein gene of grapevine leafroll-associated virus 3 obtained from Portuguese grapevine varieties , 2011, Archives of Virology.

[52]  V. Dolja,et al.  The family Closteroviridae revised , 2002, Archives of Virology.

[53]  A. Karasev Genetic Diversity and Evolution of Closteroviruses. , 2000, Annual review of phytopathology.

[54]  R. Hamilton,et al.  Natural spread and molecular analysis of grapevine leafroll-associated virus 3 in Australia , 1995 .

[55]  Timothy E. Martinson,et al.  Economic Impact of Grapevine Leafroll Disease on Vitis vinifera cv. Cabernet franc in Finger Lakes Vineyards of New York , 2012, American Journal of Enology and Viticulture.

[56]  R. Sforza,et al.  New Mealybug Species Vectoring Grapevine Leafroll-Associated Viruses-1 and -3 (GLRaV-1 and -3) , 2003, European Journal of Plant Pathology.

[57]  C. Cabaleiro,et al.  Temporal Analysis of Grapevine leafroll associated virus 3 Epidemics , 2006, European Journal of Plant Pathology.

[58]  J. Burger,et al.  Distribution of grapevine leafroll associated virus-3 variants in South African vineyards , 2011, European Journal of Plant Pathology.

[59]  G. Martelli,et al.  Clonal and sanitary selection of the grapevine. 1. Effect of virus diseases on the crop and its quality. 2. Sanitary selection and diagnosis , 1997 .

[60]  R. Froissart,et al.  The virulence–transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  C. Cabaleiro,et al.  Field Transmission of Grapevine Leafroll Associated Virus 3 (GLRaV-3) by the Mealybug Planococcus citri. , 1997, Plant disease.

[62]  A. Purcell,et al.  Glassy-winged Sharpshooter , 2001 .

[63]  F. J. Pierce,et al.  The potential of spectral reflectance technique for the detection of Grapevine leafroll-associated virus-3 in two red-berried wine grape cultivars , 2009 .

[64]  K. Krüger,et al.  Transmission efficiency of Grapevine leafroll-associated virus 3 (GLRaV-3) by the mealybugs Planococcus ficus and Pseudococcus longispinus (Hemiptera: Pseudococcidae) , 2008, European Journal of Plant Pathology.

[65]  O. Lemaire,et al.  Transmission of six ampeloviruses and two vitiviruses to grapevine by Phenacoccus aceris. , 2012, Phytopathology.

[66]  A. Lindén,et al.  Virus diseases of grapevines in New Zealand , 1970 .

[67]  Y. Ben-Dov A systematic catalogue of the mealybugs of the world (Insecta: Homoptera: Coccoidea: Pseudococcidae and Putoidae) with data on geographical distribution, host plants, biology and economic importance , 1994 .

[68]  D. Bosco,et al.  Monitoring the spread of viruses after vineyard replanting with heat-treated clones of Vitis vinifera ‘Nebbiolo’ , 2009 .

[69]  J. G. Charles,et al.  Mealybugs (Hemiptera: Pseudococcidae) and their natural enemies in New Zealand vineyards from 1993-2009 , 2010 .

[70]  C. Geiger,et al.  Seasonal Movement and Distribution of the Grape Mealybug (Homoptera: Pseudococcidae): Developing a Sampling Program for San Joaquin Valley Vineyards , 2001, Journal of economic entomology.

[71]  William H. Swallow,et al.  Group testing for estimating infection rates and probabilities of disease transmission , 1985 .