FEBRUARY 24, 2020. BY STEPHANIE BOLTON, PhD.
reviewed by: Charlie Starr IV (Pest Control Advisor and Grower, Lodi CA), Dr. Akif Eskalen (UCCE Plant Pathologist), and Dr. Maher Al Rwahnih (UC Davis Virologist)
Across California, winegrape farmers are observing – much to their dismay – patches of grapevines mysteriously collapsing. Farmers, pest control advisors, extension personnel, and scientists have studied these dying vines extensively in Lodi since around 2010. By 2018, the Lodi Winegrape Commission began to organize this endeavor in the form of case study interviews and consistent vineyard testing. Thanks to the efforts of a team of growers and scientists, we are learning that viruses are likely involved in what we now call the “sudden vine collapse” and we can offer some management recommendations.
THE BEGINNING OF A COLLAPSE
During the growing season, a farmer will begin to notice that there are a few dead vines near each other. Vines die for many reasons – diseases, tractor injury, rot, severe stress, etc. – so the grower is not too alarmed. The grower will either ignore or remove these few vines without really knowing why they died. The same scenario may occur over the next two-three years with vines dying and possibly getting removed. By the third or fourth year, these dying vines are now one larger patch of missing, stunted, dying, and dead vines which are much more noticeable and frightening than before. Replants in this area may also begin to collapse. At this point, the grower is concerned about the spread of this dying patch of vines but is not sure what to test for or how to protect the rest of the vineyard. These collapsing patches can be up to acres in size and are viewable simply by looking at the satellite view in Google Maps or Google Earth.
In this sudden vine collapse example as viewed with Google Earth, the grower started seeing a single vine collapse here and there in 2014 or 2015 in his 23 acre block. He thought maybe it was oak root fungus. Look at the growth of the collapsing patch by May 2017 (right) and the difference from June 2013 (left). There are many examples just like this one. Some growers have seen their collapsing patch grow by 30% over one year.
THE HISTORY IN LODI
Charlie Starr and Mark Shimozaki, local independent pest control advisors, and Paul Verdegaal, retired UCCE Farm Advisor, brought in dozens of scientists between 2010-2019 to study collapsing vines in different vineyards. Unfortunately, for many years no one was able to pin down a cause that made sense. Each expert could usually find the pathogen(s) that they study in the collapsing patch of vines, but the pathogen or disease found was inconsistent across vineyard sites, did not match the pattern of spread, or could not be attributed to the death of the grapevines. The only consistencies in the earlier days were that the collapse was typically occurring in mature vineyards (aged 15-20 years) on Freedom rootstock and when tested for common viruses, leafroll virus showed up. Freedom rootstock is very popular in Lodi so it was hard to tell if the rootstock was a causal factor or just a coincidence.
Leafroll virus is known to inhibit ripening, decrease yield, reduce quality, and decline a vineyard’s lifespan, but the team did not think that this virus alone could cause a mature vine to collapse. Once the collapse was observed on CDFA-certified virus tested replants within a patch, the team realized that the age of a vineyard was no longer a causal factor. Grape scion variety also does not seem to be relevant, with collapsing vines occurring in Cabernet Sauvignon, Pinot noir, Chardonnay, and other varieties.
Many, many theories were tested – from Phylloxera to esca to Phytophthora to lightning strikes. By 2018, the working hypothesis was that a combination of certain rootstocks (including Freedom), leafroll virus, and a third stress (possibly trunk disease, vitiviruses, water stress, etc.) created a disease complex leading to the collapse. Intrigued by the mystery, UC Plant Pathologist Dr. Akif Eskalen (UC Davis Plant Pathologist) joined in the efforts in 2019. The Lodi team was happy to have Akif on board because he was excited to help and more importantly, he was willing to work across scientific disciplines, building upon the work that preceded his involvement.
Two levels of stunted shoot growth, a typical symptom of the mysterious collapse, in July 2018 in a collapsing patch on Freedom rootstock in Lodi, California. Photo by Stephanie Bolton.
SYMPTOMS OF A COLLAPSING PATCH (based upon observations in Lodi):
- Vines may show stunted shoots, growing to less than half the size of healthy shoots.
- Vines may collapse at any time during the year.
- Many vines push out fruit before they collapse.
- Collapsed vines lack feeder roots (smaller roots closer to the surface).
- The entire vine goes from having green shoots to being completely dried up rather quickly (typically in 2-6 weeks).
- The symptoms look similar to Eutypa dieback, but vine death is more rapid and without cankers.
- In many cases, the graft union in particular appears rotten and when you saw through the trunk at this junction, you can see dark, necrotic tissue.
- The scion tissue directly above the graft union may appear swollen or engorged.
- The patch of collapse tends to spread in the direction of the wind.
- The patch itself appears as a rough circular shape (resembling a soil-borne disease) which can be viewed in Google Maps once it gets large enough.
GETTING CLOSER TO SOLVING THE MYSTERY
With leafroll virus likely involved, the team enlisted the help of Dr. Maher Al Rwahnih (UC Davis Plant Virologist). In July 2019, Akif and Maher, along with Starr and others, took samples of collapsing and healthy vines from four affected vineyards in Lodi which had been monitored for this issue for several years. Rootstock and scion samples were thoroughly tested for fungal and viral pathogens by Akif and Maher, respectively. The Lodi Winegrape Commission helped to fund fungal testing and Maher generously donated highly accurate virus testing (high throughput sequencing and PCR). Maher tested for leafroll viruses (of which there are several types – designated by numbers such as leafroll 3 virus), vitiviruses (another group of viruses with several types – designated by letters such as grapevine virus A), and even unknown viruses, which can be picked up by the high throughput sequencing. Maher was familiar with research studies conducted by Dr. Deborah Golino (UC Davis Plant Virologist) where a combination of a leafroll virus and a vitivirus led to vine decline, both at the time of grafting and later on in a vine’s life (with infection occurring post-planting).
Every collapsing vine from each of these four vineyards tested positive for both a leafroll virus and a vitivirus. Trunk disease pathogens were isolated from each sample, but not the same ones. So far, multiple case studies from California vineyards have provided evidence to support the current hypothesis that a combination of a leafroll virus-sensitive rootstock, a leafroll virus, a vitivirus, and another stress (possibly trunk pathogens, crop or water stress, etc.) leads to the collapse. Collapse symptoms and positive test results for both a leafroll virus and a vitivirus have been confirmed on Freedom, O39-16, and 101-14 Mtg rootstocks, but there are likely more affected rootstocks. We continue to collect case studies to investigate the potential role of viruses and rootstock types in the collapse disease complex. Thus far, leafroll 3 virus and the vitiviruses grapevine virus A and F appear to be the most common pathogen culprits in the disease complex leading to the collapse.
By October 2019, the team of growers and scientists studying the Sudden Vine Collapse were ready to present their preliminary data to the Lodi winegrowing industry. Thanks to various presentations and a new grapevine virus email list-serve created by the Lodi Grapevine Virus Focus Group, people across California knew that the Lodi Winegrape Commission was actively trying to solve the mystery of the collapse. On October 1, 2019, during harvest, about 140 people showed up at a Lodi breakfast meeting to hear Stephanie, Akif, and Maher talk about the collapse and announce the potential involvement of a combination of a leafroll virus and a vitivirus. The high number of attendees from both near and far (and during harvest!) showed just how widespread and economically devastating the issue had become. Journalist Ted Rieger attended the meeting and wrote an article about the collapse for Wine Business Monthly, which was the #1 read article for 30 days on winebusiness.com (Rieger 2019).
THE DANGEROUS LEAFROLL VIRUS & VITIVIRUS COMBINATION
The Lodi Grapevine Virus Research Focus Group studied fanleaf virus, red blotch virus, and leafroll virus. Most of the members had heard about vitiviruses, but we figured that vitiviruses were one of the many grapevine viruses which existed but that we didn’t really have to worry about. We were wrong, and we have Maher to thank for educating us. In combination with a leafroll virus, vitiviruses can actually be quite harmful to grapevines – especially those on leafroll-sensitive rootstocks. Most growers in California have probably never heard of vitiviruses. Vitiviruses are a group of viruses with letter names – grapevine virus A, grapevine virus B, grapevine virus F, etc. Alone, vitivirus infections may cause the rugose wood disease symptoms of stem grooving or corky bark, along with differences in rootstock and scion diameter. Like leafroll viruses, vitiviruses are spread (or vectored) by mealybugs and scale insects. There is research to suggest that together, a co-infection of a leafroll virus and a vitivirus worsens any disease effect on grapevines (Rowhani et al 2018).
Rieger, T. 2019. “Sudden Vine Collapse May Be Associated with Combination of Virus Pathogens.” October 7. Wine Business. winebusiness.com/news/?go=getArticle&dataId=220522
Rowhani, A, Daubert, S, Arnold, K, Al Rwahnih, M, Klassen, V, Golino, D, and JK Uyemoto. 2018. “Synergy between grapevine vitiviruses and grapevine leafroll viruses.” European Journal of Plant Pathology. 151: 919-925. link.springer.com/article/10.1007%2Fs10658-018-1426-7
ROOTSTOCKS & VIRUS SENSITIVITY
Thus far, most of the observed collapsing vines have been on Freedom rootstock, with verified symptoms/positive virus test results also discovered on O39-16 and 101-14 Mtg rootstocks. Additionally, the team knows of unconfirmed reports of collapse happening on 110R, 1103 Paulsen, Harmony, and others.
In a blog post on lodigrowers.com published on October 7, 2016, Stan Grant (Viticulturist, Progressive Viticulture) warned growers that when it comes to viruses, vines on Freedom, 3309 Courderc, and Kober 5BB rootstocks “commonly display more severe disease symptoms than vines on other rootstocks” (Grant 2016).
From Chapter 13 of the textbook Grapevine Viruses: Molecular Biology, Diagnostics and Management (Rowhani et al 2017) and a Cornell handout called “Grape leafroll disease” (Cieniewicz and Fuchs 2015):
- The following rootstocks have shown some level of graft incompatibility with a leafroll virus in the scientific literature: Kober 5BB, 1103 Paulsen, 5C Teleki, 3309 Courderc, 1616 Courderc, 3306 Courderc, 101-14 Mtg, Harmony, and Freedom.
- When both leafroll virus 2 and the vitivirus grapevine virus B were present, the rootstocks Freedom, Harmony, Kober 5BB, and 3309 Courderc experienced virus-induced young vine decline.
- Studies showed graft incompatibility or vine decline when scions infected with leafroll virus 1 and the vitivirus grapevine virus A were grafted onto 3309 Couderc, 101-14 Mtg, Freedom, and 420A Mgt.
The Lodi team is currently reviewing scientific studies from all over the world to have a more comprehensive list of rootstocks which may be a risk factor for this collapse.
Cieniewicz, E, and M Fuchs. 2015. “Grape leafroll disease.” Cornell University and the New York State IPM Program. hdl.handle.net/1813/43103
Grant, S. 2016. “Selecting a Rootstock for a Winegrape Vineyard.” Lodi Growers Viticulture Coffee Shop Blog. October 7. lodigrowers.com/selecting-a-rootstock-for-a-winegrape-vineyard/
Rowhani, A, Uyemoto, JK, Golino, DA, Daubert, SD, and M Al Rwahnih. 2017. Chapter 13: “Viruses Involved in Graft Incompatibility and Decline.” In Grapevine Viruses: Molecular Biology, Diagnostics and Management. Eds. Meng, B, Martelli, GP, Golino, DA, and M Fuchs.
COLLAPSING VINE PHYSIOLOGY
The combination of a rootstock that is very sensitive to leafroll virus (such as Freedom) + a leafroll virus + a vitivirus may lead to a sudden vine collapse, which can happen in patches in a vineyard block or a region due to the presence of an efficient and prolific virus vector, the vine mealybug.
The virus and rootstock combination mentioned above is likely the primary cause of this collapse, where:
- A scion becomes infected with virus(es) in the vineyard.
- The virus-sensitive rootstock is rejecting the virus-infected scion in an effort to save itself from infection (which is ultimately a terrible move).
- The movement of starches from the scion to the rootstock is inhibited, causing a buildup of free starch around the graft union and a swelling of tissue above the graft union.
- The root system becomes starved and feeder roots die off or the vine is unable to produce new feeder roots.
- The flow of nutrients and water within the vine is severely reduced.
- The vine struggles to grow, causing a stunting of shoots.
- A lack of water and nutrient flow leads to apoplexy (sudden death) in a matter of weeks.
A sample of scion (top) and rootstock taken for extensive testing, showing pitting and grooving of the rootstock just below the graft union. Photo by Maher Al Rwahnih.
Once an infected vine is completely dried up and dead, the virus-carrying, hungry vine mealybugs are forced to move to a live vine to obtain a new source of food – potentially exacerbating the spread of viruses contributing to a collapse.
IS YOUR VINEYARD AT RISK FOR THE COLLAPSE?
If you have a leafroll virus-sensitive rootstock and your vineyard is in a winegrowing region with mealybugs, leafroll viruses, and vitiviruses present, then you are at risk. Educate yourself. Talk with your pest control advisors and neighbors. Prevention is key as with any other disease. Both mealybugs and viruses may be present in your vineyard even though you cannot see them nor observe any symptoms (especially in white grape varieties).
MANAGEMENT OPTIONS FOR THE COLLAPSE
Now that there exists evidence to support the involvement of leafroll viruses and vitiviruses in the collapse, management options may be offered. The following advice is based upon intense study, via scientific articles and real-world experience, of grapevine viruses & mealybugs, how they spread, and their management. The California winegrape industry is still learning how to best manage for viruses and their vectors. Likewise, there is still a lot to learn about the sudden/mystery vine collapse. The information presented here is intended as sound advice only, in an effort to aide in the ultimate decision-making by the vineyard owner.
If you think you may be experiencing the collapse:
STEP ONE. Test your vineyard – both collapsing and healthy vines.
Choose a virus testing laboratory that you trust (you may want to send samples to one commercial laboratory plus Foundation Plant Services for extra confirmation when you begin virus testing). We suggest testing two composite samples. For composite sample 1, collect material from at least five non-adjacent collapsing vines in the patch (vines showing symptoms that are still alive). For composite sample 2, collect material from at least five non-adjacent healthy vines in the vineyard block, far away from the collapsing patch (but with similar soil, irrigation, etc.). Most laboratories will allow up to ten cane pieces per composite sample, which would mean one cane from each side of the vine for five vines. Usually when testing for leafroll and vitiviruses it is not necessary to sterilize your pruning shears between samples. However, since we are still studying the collapse, it is recommended to clean your shears between the diseased and healthy samples (or even better, begin your sampling in the healthy part of the vineyard).
Test the samples for:
- Leafroll virus 1, leafroll virus 2, leafroll virus 2RG, and leafroll 3 virus (common leafroll viruses in California)
- GVA, GVB, GVD, and GVF (common vitiviruses in California)
Testing in the fall (before the leaves senesce) is the best time of year to sample for these viruses because their amount within the grapevine is the highest. Plus, if you do have viruses, then the winter would be a good time of year to remove the infected grapevines because wet soil allows for the greatest removal of root material.
STEP TWO. Remove the co-infected vines.
Although it is painful, the most efficient way to reduce the spread of viruses in the field is to take out the infected vines. By rogueing or pulling out and destroying the vines, you are removing the source point of infection. Each situation should be considered individually and the decision on how many vines to remove is very personal. Any leafroll- or vitivirus-infected vines in a vineyard serve as a potential source of virus which could be transmitted to healthy vines via mealybugs, which are spread by wind, workers, equipment, ants, animals, etc.
How many vines to remove depends upon the virus-status of the rest of the vineyard, the value and marketability of the grapes, the risk to surrounding grapevines and neighboring vineyards, the age of the vineyard, the emotional attachment to the vines, the presence of mealybugs throughout the vineyard, and a grower’s financial situation. For nearly all growers, it will be too expensive to test each vine in and around the collapsing patch individually. If part of the vineyard is virus-free (confirmed with testing), growers will likely want to estimate the size of patch to be removed. Keep in mind that vines may be infected although the virus amount is not yet great enough to be detectable by commercial testing. In several cases, the team has found that an entire vineyard is infected with leafroll 3 virus and the collapsing patch is co-infected with leafroll 3 virus and a vitivirus.
Unfortunately, there is no cure for grapevine viruses now or in the foreseeable future. There is, however, financial assistance available to eligible growers who need to remove a vineyard infected with leafroll virus through the USDA Tree Assistance Program.
STEP THREE. Reduce the mealybug vectors.
Manage vine mealybugs to the best of your ability – this helps to protect your healthy vines as well as the vines of your neighbors and ultimately your region. Unfortunately, vine mealybugs are very sneaky insects and oftentimes growers do not realize they are in the vineyard until 1-2 years later, after they have infected vines with leafroll and/or vitiviruses.
STEP FOUR. Spread the word.
Due to the high numbers and great expanse of vine mealybugs and leafroll virus in California, there are a lot of vineyards at risk for this sudden vine collapse. Please help to spread the word and educate your friends and neighbors. There are many resources and videos available online at lodigrowers.com/growereducation/viruses/.
NOTE: Leafroll virus and vitiviruses are not only spread by mealybugs and scale insects, but they are also spread by planting material (through grafting or top-working). Therefore, grafting new material onto infected rootstock and collecting grafting material from an infected vineyard are highly discouraged.
THE MYSTERY CONTINUES…
Future research hopes to address the following questions:
- If the hypothesized disease complex risk factors (vine mealybugs, leafroll virus, vitiviruses, sensitive rootstocks) have been present for decades, then why are growers observing the collapse now? Wouldn’t growers have seen it earlier? Did the recent drought exacerbate the situation? Are there more mealybugs present now or are mealybugs and the viruses they vector distributed further across California than before?
- If the two main diseases in this complex are leafroll viruses and vitiviruses, both spread by mealybugs and scales, then why does the collapsing patch have a circular pattern? Mealybug-vectored diseases usually move down/across vineyard rows with a smaller amount of spread between rows.
- Which leafroll viruses are of concern? Which vitiviruses are of concern?
- Which rootstocks are more or less sensitive to leafroll virus, vitiviruses, and a combination of these viruses?
To learn more about real-world virus management in “grower language” please attend our Mealybug & Virus Outreach Meeting on April 9, 2020, at the Stockton Cabral Ag Center. There are videos and more posted to lodigrowers.com/growereducation/viruses/.
This California-based article was written for educational purposes only. Each person will ultimately manage for the sudden vine collapse on an individual basis according to what makes economic sense for them personally.
Featured Image: A typical sudden vine collapse site – in the collapsing “patch” are healthy vines, dead vines, recently collapsed vines, collapsing vines, and empty spaces where dead vines were removed. Taken July 2018 in Lodi, California. Photo by Stephanie Bolton.
VIRUS TESTING LABORATORIES
950 W Chiles Rd, Davis CA 95618 (sample delivery)
PO Box 285, Davis CA 95616 (mailing address)
Dr. Alan Wei | email@example.com
800.506.9852 | agri-analysis.com
USDA Tree Assistance Program (TAP)
USDA San Joaquin Co. Farm Service Agency
(Red Blotch Virus & *NEW* Leafroll Virus)
7585 S Longe St, Ste. 100, Stockton CA 95206
Joanne Gomez | firstname.lastname@example.org
209.337.2124 | fsa.usda.gov
LODI WINEGRAPE COMMISSION
You can always learn more about viruses and their vectors (like mealybugs) at our CD11 LODI PCA NETWORK BREAKFAST MEETINGS, held on the first Tuesday morning of every month from 8-9:30am at the Lodi Grape Festival Grounds, 413 E Lockeford St, Lodi, CA.
Everyone is welcome at these meetings! RSVP to email@example.com or 209.367.4727.
More information is available from the Lodi Winegrape Commission on these topics:
- Nursery Ordering 101: Viruses
- Mealybug Management
- Grapevine Virus Testing
- USDA Tree Assistance Program
- Rogueing Vines
Have something interesting to say? Consider writing a guest blog article!
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For more information on the wines of Lodi, visit the Lodi Winegrape Commission’s consumer website, lodiwine.com.