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Grapevine Leafroll Disease in the East: How big a threat does it pose to the eastern wine grape industry?

Grapevine leafroll disease (GLRD) is nothing new to most of the world and has had the attention of scientists and grapegrowers for a long time. As early as 1853, the disease was observed in French vineyards and was called rougeau (red leaf), for obvious reasons. By 1936, the causal organism was thought to be viral in nature. (2) However, the disease is relatively new to the grape and wine industry in the northeastern United States, partly because vinifera grapevines, the species most dramatically affected, were not widely planted in the region. As the acreage of vinifera in Pennsylvania continues to expand and become a larger part of the "bottom line," encounters and frustrations with GLRD will likely increase.

The symptoms and causes of GLRD

The most obvious symptoms of the disease consist of cupping and loss of chlorophyll in the leaves during late summer and fall. For example, on red-fruited varieties such as Cabernet Franc, leaves of infected vines can display a distinct red coloration of the interveinal tissue, while veins remain green. (11) On whitefruited vinifera varieties like Chardonnay, symptoms are less noticeable and leaves are cupped and tend to look yellowish in the interveinal tissue. (5) Discoloration generally affects older leaves first. (2) These symptoms are not necessarily diagnostic of the disease, as they may be due to other causes such as nutrient deficiencies, water stress and even crown gall, which many growers in Pennsylvania have become familiar with since the very cold winters of 2014 and 2015.

More significant, and perhaps less recognized, are the detrimental effects of GLRD on yield and fruit quality in the region. Compared to healthy vines, those affected by GLRD are known to have reduced yield, vegetative growth and even lower cold hardiness, which is a factor of critical importance for varieties grown in the region. GLRD can also delay fruit maturity, negatively affect grape chemistry at harvest (lower soluble solids, higher titratable acidity) and reduce color development in red vinifera grapes--all factors that may adversely impact perceived wine quality.

GLRD is caused by viruses in the family Closteroviridae, which have relatively long (as viruses go), rod-shaped particles that can be viewed with transmission electron microscopy. Currently, there are about five distinct species of grapevine leafroll-associated viruses (GLRaVs) found in cultivated grapes: GLRaV-1, 3, 4 in the genus Ampelovirus; -2 in the genus Closterovirus, and -7 in the genus Velarivirus (International Committee on Taxonomy of Viruses (ICTV), 2016). Grapevine leafroll associated viruses-5, 6, 9,10 and 11 are also reported in the literature, but the phylogeny clusters them as close relatives of GLRaV-4.

The most common species found in grapes is GLRaV-3, which is thought to be endemic to North America. (2) The severity of the GLRD effects can vary from one season to the next and is dependent on a number of factors including grapevine variety, scion/rootstock combination, virus strain, climate, soil, cultural practices, stress factors, etc.

The effects of these viruses on hybrid grape varieties and Vitis labrusca are generally considered to be less serious than those on vinifera, but the effects are also less well-known and studied on those species. As the symptoms of GLRD can mimic other maladies of the vine, analysis of grapevine tissues in the laboratory is the only way to confirm the presence (or absence) of these viruses.

Infection by GLRaVs is limited to the phloem, (11) and results in the degeneration of primary phloem tissues in shoots, leaves, and clusters. The phloem, the thin layer of tissue between the outer bark and the cambium, conducts the products of photosynthesis (primarily sugars) from green tissues (mainly leaves) to the rest of the vine. The degeneration of this tissue can have profound effects on grapevine health and productivity.

How GLRaVs are spread

As is the case with so many plant pathogens, GLRaVs have been distributed across the world through increased trade and movement of plant material and other products. (2) In fact, infected nursery stock appears to be the prime method of transmission. The viruses can spread through the graft union; but thankfully, they do not appear to be transmissible from one plant to another via pruning or contact, since their concentration, or titer, in the phloem is very low. (11)

A nationwide study conducted in Canada in 1994-95 raised the possibility that GLRaV-3 may be endemic to North America, as it was most commonly found in non-vinifera grapevines that had been cultivated on the continent for a long time. On the other hand, the fact that GLRaV-1 was found most often in vinifera varieties (whose arrival in Canada is much more recent) provided evidence that it was imported with vines from Europe and Asia. (11)

Once in the vineyard, GRLD can be spread short distances, from vine to vine, by phloem-feeding insects such as mealybugs and scale insects. The grape mealybug (Pseudococcus maritimus) is thought to be the primary vector species, (3,15) together with Planococcus ficus and P longispinus, but its presence and distribution in Pennsylvania has never been studied. Interestingly, no vector has yet been found for GLRaV-2 and -7 (.15)

Resistance to GLRaVs

There are no known sources of resistance to GLRaVs among Vitis species, and these viruses have been found in many cultivated grape varieties from labrusca to interspecific hybrids and vinifera. As mentioned earlier, labrusca varieties such as Concord and Niagara can also become infected with GLRaVs, but the infections appear to remain latent or dormant (1) and do not result in visual symptoms of the disease. (19)

Vinifera varieties, however, make up a growing sector of the eastern wine grape industry and are severely affected by GLRaVs. Where infected labrusca vineyards border on areas of wine grape production, there is a real concern that these viruses will be vectored by insects into healthy wine grape vineyards.

Management of GLRD

For new vineyards, planting only certified virusfree stock is the first line of defense. Infection by aLRaVs is permanent; there is no way to rid vines 3f these viruses once they become infected. To nanage and reduce the effects of the disease jnce in the vineyard, infected vines must be -ogued and replaced by certified healthy vines.

The National Clean Plant Network (nationalcleanplantnetwork.org) has a list of national clean plant centers that can be contacted for certified material. When a symptomatic vine has been identified as positive for GLRD, removal of each adjacent vine within the row is also recommended, as it may take from one to three years for the visible symptoms to be expressed. Inspection of vineyards should be done annually between veraison and harvest, when symptoms are most vividly displayed, especially in red varieties. (12)

Since certain species of phloem feeding insects can vector these viruses, insecticides that target mealybugs and soft scales can prevent vine-to-vine spread within the vineyard (grapevine leafroll disease fact sheet). (2) Studies have shown that applications of insecticides such as spirotetramat (Movento) can significantly reduce mealybug counts and can help to control spread. (10,16)

Grape mealybug overwinters on the vine and first instar crawlers are thought to be the most mobile life stage, and hence most apt to spread the virus. Since this insect can have two generations per season, there are two crawler stages that need to be targeted for management. (3,18) Studies in New York showed that insecticide applications should target overwintered and early season mealybug crawlers by combining delayed dormant applications of horticultural oils, applied in late April, before green tissue, followed by acetamiprid in early July, when the first of the new summer generation of crawlers was observed, or by applications of spirotetramat after bud break and again in early July.

Among the systemic insecticides, spirotetramat appeared to outperform acetamiprid and helped slow the spread of GLRD. (16) Once a block has been identified as positive for GLRD, it will be important to minimize populations of the potential vectors to reduce spread within the block and to adjacent blocks. Scouting for mealybugs in vineyards with GLRD can be important to reducing its spread.

Unfortunately, to our knowledge, recommendations regarding insecticide spray programs for slowing the spread of GLRD have not yet been optimized. Insect vectors can also "hitchhike" from infected areas to clean areas or blocks via human activity (by vineyard workers and equipment), suggesting appropriate measures be taken to minimize this method of spread. (12)

Lastly, a study with grape phylloxera (Daktulosphaira vitifoliae), a phloem feeder and potential vector of these viruses, showed that phylloxera can acquire GLRaVs in greenhouse transmission experiments, but this was not observed in the field. However, there was no evidence that phylloxera can transmit GLRaV1, 2, 3, or 4 to healthy vines. (20)

Surveys for the presence of GLRaVs

Interest in GLRD and the extent of its effects has been growing in the northeastern U.S. and Canada over the past 20 years. This concern has resulted in a number of surveys in some prominent grapegrowing states that have confirmed the presence of GLRaVs in commercial vineyards and yielded important information necessary to the management of grapevine leafroll disease. As a result, academic institutions have developed research programs around this important group of pathogens and created a growing body of information that will be essential for vineyard managers.

For example, surveys conducted in New York, Ohio and Virginia have revealed the presence of GLRaVs in commercial vineyards in those states. (5,8,9) However, no extensive surveys have been conducted in Pennsylvania vineyards. Based on the fact that some Pennsylvania vines were found infected by GLRaVs, (6) and that GLRD is a common disease in every vine-growing region in the world, we believed a survey of Pennsylvania wine grape vineyards was an important and necessary step toward determining the impact of GLRaVs and their associated disease. Only then will we be able to address the effects of these viruses on grapevine productivity and fruit quality, develop measures to reduce their spread and impact, and provide management information that will contribute to the growth and improvement of the wine grape industry in Pennsylvania.

Sampling

Over the years, different research teams have devised their own sampling methods in vineyard blocks of their respective states. The types of tissues to collect and timing of the sample are based on the biology of the virus in the plant. Since these viruses are limited to the phloem tissue in grapevines, tissue samples have involved the collection of woody cane sections (for scrapings of the cambium) during the dormant period, or leaf petioles during the growing season.

The concentration of plant viruses typically changes over the course of a year, and GLRaVs are no exception. (4,13,14,17) The most recent evidence seems to show that these viruses are generally most easily detected in petiole or dormant cane samples collected between August and February in California, when the concentration of the virus (titer) was highest in grape phloem tissues. It would also appear that distribution of the virus in different phloem tissues varies among GLRaV viruses. (13)

Pennsylvania survey for GLRaV-1 and 3

Is this disease a problem in Pennsylvania vineyards, and if so, what can be done about it? Researchers at Penn State University are in the process of answering those questions, and the first step was taken in August 2017. The Penn State grape team delivered a questionnaire to the listserv of wine grape growers, asking them if they have observed symptoms of the disease in their vineyards, and if they would like to participate in a statewide, confidential survey that would include an assessment of their vineyard blocks for the presence of grapevine leafroll-associated viruses. The project then would follow up with tissue sampling from participating symptomatic and non-symptomatic vineyards throughout the state, and serological analysis (ELISA) to determine the presence of GLRaV -1 and -3, the most common of the leafroll viruses in commercial vineyards in Pennsylvania. The collection of vineyard samples across the state will continue over two or more seasons and will provide a map of the geographical distribution of these viruses on vinifera and hybrid varieties. Labrusca samples will not be collected, at least initially.

While vineyards were selected from all parts of Pennsylvania, the number of locations favors northwestern and southeastern Pennsylvania, where the majority of vineyards are located. So far, leaf petiole samples collected from vineyards in Berks, Erie, Snyder and Wyoming counties have been analyzed with serological methods for GLRaV-1 and 3. Samples from Bedford, Chester, Cumberland, Delaware, Lancaster, Lehigh, Northampton, Schuylkill and York counties will be collected in 2018. The results will be made available to growers at various meetings throughout the next several years.

Results in 2017

Penn State researchers collected samples of four commonly grown vinifera varieties--Cabernet Franc, Pinot Noir, Chardonnay and Riesling--and one hybrid variety, Chambourcin, in 34 vineyard blocks in 2017. Of those that have been analyzed thus far, 53% of the vinifera vineyard blocks tested positive, with at least one vine with one of the viruses in a block, while 25% of the Chambourcin blocks tested positive.

Overall, the percentage of vines testing positive for the viruses ranged from 12% to 34% for the vitiifera blocks, and only 2.5% for Chambourcin. Early results show a range of infection: Some farms sampled showed no evidence of GLRaV-1 and 3, while other farms were heavily infected with them. This is just a quick snapshot of the results to date, and further analysis may change or modify this picture somewhat.

As expected, many of the vines that tested positive for viruses displayed leaf symptoms of the disease. However, a few symptomatic vines turned up with negative test results for the GLRaV-1 and 3. It should be noted that these symptoms are not necessarily diagnostic of the presence of these two viruses, and symptoms may be due to other causes such as additional viruses or low virus titer. Again, only tissue analysis in the laboratory can confirm the presence of GLRaVs.

Interestingly, some asymptomatic vines tested positive for the presence of at least one of the two viruses. Results of this study will also be analyzed to test if a relationship exists between varieties, vine age and virus titer. Metadata collected from growers also will be used to tease apart the effect of rootstocks and scion, and to investigate the origin of the infected material. As Pennsylvania's wine grape industry continues to grow, the effects of grapevine leafroll viruses will probably become more evident in vineyards.

What does this mean? First of all, the project should be continued. It's obvious that leafroll viruses can be found in vineyards from one end of the state to the other, and the impact on the Pennsylvania wine grape industry should be determined. Once sampling is completed and the prevalence of the virus statewide is known, researchers should set up research plots in commercial vineyards to study the effects of the virus on parameters such as yield, vegetative growth, juice and wine composition, and cold hardiness, as well as mode and speed of virus spread and economical thresholds for disease management decisions.

As in other states, the study is targeted to help growers recognize the impact that the disease may be having on the Pennsylvania wine industry and to help them to address the effects of these viruses on productivity and fruit quality. The ultimate goal is to reduce the spread and impact of the viruses, and thereby improve the wine grape industry in Pennsylvania.

Grapegrowers in the northeastern United States need not feel they are the only ones with this disease-management challenge (as is the case with many fungal diseases of grapes). Grapevine leafroll-associated viruses are present in vineyards all over the world and may be an even bigger problem in those places that depend exclusively on vinifera grapes for their bread and butter, as vinifera appears to suffer most from infection by these viruses compared to hybrid and native grape varieties.

KEY POINTS

When individual grapevines start to display red leaves with green veins late in the summer and into the fall, it is a sign that grapevine leafroll disease (GLRD) has infected that plant. Other symptoms include cupped leaves and, on whitefruited varieties such as Chardonnay, leaves that are yellowish with green veins.

Grapevine leafroll disease is primarily caused by five species of grapevine leafroll-associated viruses; the most common species is known as grapevine leafroll-associated Virus-3, or GLRaV-3.

This disease is relatively new in Pennsylvania and other northeastern states, because until recently the grapes grown in the region were primarily labrusca or hybrid varieties. With more vinifera now being planted, growers are beginning to see more evidence of GLRD.

Researchers at Penn State University have started a study to determine the extent of GLRD n the state's vineyards and how it impacts vegatative growth and vineyard yields. The sampling study will continue so growers can recognize the disease and its impact on the wine industry, and ilso help them deal with the effects of the viuses on productivity and fruit quality.

Bryan Hed is a research technologist at the Lake Erie Grape Research and Extension Center In North East, Pa. Dr. Michela Centinari is assistant professor of viticulture, Dr. Cristina Rosa is assistant professor of plant virology, and Joseph Walls III is a Ph.D. candidate (advised by Dr. Rosa) at The Penn State College of Agricultural Sciences. They would like to thank the Pennsylvania Wine Marketing and Research Board for funding the Pennsylvania grapevine leafroll virus study.

The references for this article are available online at winesandvines.com/features

Please Note: Illustration(s) are not available due to copyright restrictions.

Caption: Red leaves with green veins are signs of infefction witrfgtapevine leafroll virus.

Caption: A vineyard row with healthy vines interspersed with vines with symptoms of grapevine leafroll virus.

Caption: Leaves with symptoms of grapevine leafroll virus with ripe grapes.

Caption: Adjacent vines, one with symptoms of grapevine leafroll virus and one with no sign of the disease.

Caption: A vineyard with several vines displaying the red leaves characteristic of grapevine leafroll virus.
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Title Annotation:GRAPEGROWING: WINE EAST
Comment:Grapevine Leafroll Disease in the East: How big a threat does it pose to the eastern wine grape industry?(GRAPEGROWING: WINE EAST)
Author:Hed, Bryan; Rosa, Cristina; Centinari, Michela; Walls, Joseph, III
Publication:Wines & Vines
Geographic Code:1U2PA
Date:Apr 1, 2018
Words:3003
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