Flavescence dorée: incurable phytoplasma meets Langhe grit

Progress notwithstanding, winegrowers face continued pressure from a multitude of pests and diseases. Some can be prevented, treated and managed by winegrowers; meanwhile, others resist all effort, proving more virulent and problematic. Among these, the grapevine yellow, flavescence dorée, a phytoplasma—a type of obligate intracellular parasite—is transmitted by the leafhopper vector Scaphoideus titanus. Symptoms include delayed or no bud break, golden yellow or reddish patches on curling leaves, rubbery shoots which fail to lignify, black pustules near the bases of nodes, necrotic growing points, and shrivelled and falling flower and fruit clusters. Symptoms usually appear the year after infection and worsen until the vine dies. In some cases, symptoms disappear in an apparent recovery. Though the phytoplasma strain responsible is native to Europe, the vector likely “hitchhiked” to Europe from North America on rootstocks imported to tackle phylloxera. Experts have reported epidemics in Langhe since 1999; from 2003 to 2018, the ‘settlement areas’ increased from a restricted zone of one province to almost 25% of the whole region. Though Nebbiolo has proved reasonably resistant, Barbera’s genetic make-up renders it particularly susceptible. To date, flavescence has resisted all attempts at treatment. Moreover, studying the disease has proven impossible, given that it cannot be reproduced outside of its host. Both Barbera and Dolcetto are crucial to Langhe winegrowers. Quicker to market than Nebbiolo, both varieties benefit cash flow, not to mention their increasing standalone quality. Impact notwithstanding, many winegrowers remain ill-equipped to combat the disease. This article examines flavescence’s arrival and spread in Langhe, assesses identification and response strategies, outlines areas for future research, and calls for more collective action and strict controls.

Flavescence dorée (FD) is a phytoplasma—a type of obligate intracellular parasite transmitted to plants by insect vectors, grafting, or dodder bridges established between the infected donor and the recipient plant only. Phytoplasmas are tiny wall-less organisms that are recalcitrant to in vitro cultivation and very difficult to purify from their hosts because of their fragility—they survive only a short period in extracts—and low titres. Grapevine FD phytoplasma (FDP) belongs to the elm yellows group and is specifically transmitted by the leafhopper species Scaphoideus titanus Ball. The leafhopper feeds on grapevines for its whole life and can acquire FD as a nymph and an adult. However, acquisition of FD by nymph allows the vector to transmit the phytoplasma for an extended period, whilst acquisition by adults, due to the long incubation period in the vector, results in a short period of infectivity, if any.

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The INRA reports that the phytoplasma strain responsible for FD is native to Europe, having existed in wild plants. However, the leafhopper Scaphoideus titanus—which transmits FD to grapevines—was introduced to Europe a few decades ago on American rootstocks brought over to contend with phylloxera. FD epidemics have been reported in Langhe since 1999, particularly in Monferrato, though prime vineyard sites in Barolo are also affected. From 2003 to 2018, the ‘FD-settlement areas’ increased from a zone of one province (Alessandria) to almost 25% of the region. Silvia Altare notes that her father, Elio, reports having observed FD much earlier; however, FD can be confused with several other diseases. So, without PCR/DNA analysis, earlier prevalence is difficult to confirm. 

No grapevine genetic resistance to FD is known, and all grapevine cultivars are susceptible to infection, although to different degrees. Moreover, cultivars with diverse susceptibility support varying pathogen loads, meaning the presence of susceptible cultivars may improve vector transmission efficiency. In Langhe, traditional cultivars are planted almost exclusively—the most common of these, namely Barbera, Dolcetto, Cortese, and Nebbiolo—show distinct susceptibility to infection.  Studies have shown FD titre is always higher in Barbera than in Nebbiolo. Published literature strongly suggests that grapevine genotype is likely to influence several aspects of FD epidemiology, namely vector acquisition efficiency, phytoplasma multiplication, and symptom expression. For Nebbiolo, most proteins modulated during infection belong to the ‘cell rescue, defence and virulence’ class.

On the other hand, preliminary studies on Barbera show a lower presence of proteins of the ‘defence’ category when compared to the total identified proteins. Perhaps counterintuitively, even poorly susceptible varieties like Timorasso and Moscato can host a relatively high phytoplasma load, making them a potential solid source for spread by vector. Thus, plant genetics and environmental conditions remain the most critical factors determining FD’s success in host colonisation.

Why Langhe?

It is not wholly clear why FD has spread with such ferocity in Langhe, agronomist and researcher Martina Tarditi proposes several hypotheses, albeit with a caveat of uncertainty. Martina notes that varieties particularly susceptible to FD are planted extensively in Langhe, most notably Barbera and Dolcetto, which usually occupy whole hillsides, usually those deemed less than ideal for Nebbiolo. In the past, Barbera commanded a less viable price than it does today, leading many winegrowers to abandon whole vineyards. These vineyards have, in many cases, lay dormant uncultivated for many years. With no response to infection or mandatory insecticide treatment, Scaphoideus titanus thrived. Because of its peripatetic nature, Scaphoideus titanus may have emigrated from these dormant vineyards to nearby woods and forest—where the vector thrives—and then to cultivated vineyards elsewhere.

flavescence-dorée-langhe

Environmental factors notwithstanding, Langhe winegrowers have, until recently, been fragmented and uncooperative, much more so than Burgundy, where FD has control has been much more effective. This distinctly uncooperative spirit meant winegrowers failed to leverage the value of shared experience, thus hampering FD response. Further, nurseries had long been unaware of their role in spreading FD, and so it is possible that winegrowers planted batches of infected plants simultaneously, amounting to ‘super spread’ events. Today, the percentage of infected plants coming from nurseries is low. Finally, warmer autumns may well mean that leafhoppers survive until late October, increasing the time they can spread the disease. In short, FD may have encountered the ‘perform storm’ in Langhe. A set of circumstances and environmental factors congruent to its flourishing. 

Signs, symptoms, infection and identification

FD phytoplasma moves and multiplies in the phloem sieve tubes of plants and the body of their insect vector. Infected vector nymphs remain inoculative for the rest of their life, able to infect a plant on each feeding or probing event. Infection of grapevine with FDP by Scaphoideus titanus may occur from the beginning of June (young larvae) until late September (old adults). The severity of the disease does not depend on the date of inoculation. Incubation of the phytoplasma takes place from the moment of inoculation until symptom expression. Symptoms will typically develop in the following year. Infected plant material used for vegetative propagation is infected definitively and is a source for long-distance disease transportation unless recovery occurs. Yellows diseases attributed to phytoplasmas induce symptoms on plants’ vegetative and reproductive organs, indicating that host nutrient circulation, hormonal balance and sugar flow are affected. Symptoms of flavescence dorée are typical of these disturbances.

flavescence-dorée-symptoms

Symptoms of FD first appear in early summer and increase in incidence and severity until harvest. During the first year of expression, symptoms are usually limited to only a few shoots. Early season symptoms can be observed on inflorescence, which partially or totally withers or on aborted bunches. If berries form, summer symptoms will include drying of berry peduncles and consecutive shrivelling or drying of berries, leaf discolouration (yellowing), backward curling of laminae, and shoots becoming rubbery and failing to lignify. Characteristic black spots and blemishes may be seen in longitudinal rows near the bases of shoots, extending radially in the vineyard. The leaves have golden yellow or reddish patches and curl downward. Growing points become necrotic, and flower and fruit clusters shrivel up and fall. Finally, plants lack structural integrity and will bend to the ground in a striking ‘weeping’ posture to the tree, manifested even when vines are not attached.

Management today and a strategy for the future

Although no treatment has proven successful in curing FD-infected vines, management and mitigation strategies have proven reasonably effective in reducing spread within and between vines, decreasing inoculum density and controlling the vector. Greater awareness, enhanced collaboration and investment, and strengthening and diversifying these strategies represent a significant opportunity to further limit spread—plus its associated risks—dramatically reducing producer’s economic burden and future susceptibility. Common FD management strategies, points for further consideration and opportunities for improvement and future research are outlined henceforth.

flavescence-dorée

Early intervention is crucial to managing flavescence dorée; however, intervention relies wholly on effective and swift identification. Unfortunately, many winemakers remain ill-equipped to recognise early symptoms, whether due to lack of resources—physically checking vines requires intensive observation—or inability to identify signs at varying growth stages correctly. A more comprehensive and intuitive identification protocol as well as resource sharing in ’at risk’ areas—these should be identified objectively—may prove helpful in limiting the impact of FD. Attribute studies may help identify shortfalls in identification skills, followed by training and upskilling of vineyard workers. Shared mobile applications and big data may help record and track incidence while also benchmarking best practices.

Further, researchers are studying methods to improve and automate identification capability, exploring using UAV’s and Deep Learning to develop models designed to automatically detect FD-like symptoms so that winegrowers can isolate samples for laboratory testing. Initial studies demonstrate success, with positive rates as high as 98.4% in Chardonnay, though success varies by variety. Albeit more primitive, Barbaresco winemaker Luca Paitin positions traps transversal to the vineyards from one end to the other, measuring where the vector is most prevalent. The traps colour attracts the vector, which becomes stuck upon impact, helping mitigate the spread and inform behaviours and areas of concern. Accessible and practicable solutions like these may prove effective in the mid-term.

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Once identified, early intervention is paramount to limiting spread. Currently, FDP is a quarantine organism in the EU (Directive EEC 77/93); winegrowers must apply insecticides upon identification, while high-incidence vineyards must be grubbed up. The EU recently fined Biodynamic Emmanuel Giboulet for refusing to spray infected vines. This mandate leaves organic growers stuck between a rock and a hard place, though ultimately minimising spread is collectively favourable. However, treatment and management for organic winegrowers are limited. Silvia Altare has experimented with a range of organic solutions, though she admits it does not seem like anything has helped outside of spraying the vector. Silvia has experimented with nettle-soaked water, propolis liquid spray, echinacea liquid spray and tannin spray. Today she is testing a “mushroom” treatment, adding the compound to the soil and soaking every new rootstock, hoping it may stimulate a beneficial plant response. 

Luca Paitin notes that currently, the best approach, albeit costly, might be to constantly monitor the vineyards while working and immediately cut the smaller branches back when they show infection. However, this comes with risk; the vine may appear asymptomatic when pruned, though it remains a source of inoculum. Loss notwithstanding, the best response may be that once disease vines are identified, producers immediately prune back all stems and shoots (strip back to old wood), followed by grubbing up the vine. Producers in the region could establish a consortium—funded by contribution per hectare under management—which employed a full-time team tasked with tracking high-risk areas, scouring the vineyards and immediately removing sick vines. Rapid PCR testing of cuttings upon identification would also help improve response protocol and track high-risk areas. If producers refuse to remove diseased vines, the DOCG should impose severe penalties.

Control of the vector depends on insecticide treatments applied either against the eggs during winter or against larvae and adult leafhoppers during the growing season. Pruning wood that carries the eggs of Scaphoideus titanus should be burned. The number of viable eggs can be reduced by treating wood in March before budburst. There are usually three summer treatments; the first is generally in June and should not be done later than one month after the beginning of hatching; the delay is the period necessary for the first insects to become infective if they could feed on infected vines soon after hatching. The time of the second treatment depends on the stability of the compound used. Still, it is usually applied in combination with the second generation of grape berry moth control. Adult leafhoppers immigrating into the vineyards from surrounding areas are the target of a third treatment in August.

Mariacristina Oddero told WBI she believes eradicating diseased trunks is a fundamental and necessary practice to debilitate the disease. In addition, keeping the areas around the vineyard clean is essential. Dr Andrea Schubert at the University of Turin’s research centre has demonstrated that American rootstock or hybrids in abandoned vineyards are the primary cause of the pathogen’s transmission. Subsequently, the Consorzio Barbera d’Asti e Vini del Monferrato has developed a protocol for the destruction of wild vines. The onus to act, though, is on property owners. Removal of gone-wild Vitis surrounding the vineyard with a cultivar-specific approach must be made a collective priority.

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To date, no significant natural enemies of Scaphoideus titanus, either parasitoids or predators, have been identified. As the species originates from North America and has most probably been imported as eggs on dormant vine material, it is considered that it was transported without its natural enemies, if any. Thus, the latter should be searched for in the USA. Research is underway on the possible use of entomophagous fungi for biological control. Further research into sexual confusion and predator pests may help control the vector, as could bio-controls of dodder bridges. 

In France, all mother plots for propagation material must be treated with insecticides three times a year. In addition, all nurseries must be treated throughout the time when larval stages or adults of Scaphoideus titanus are likely to occur. Directives from the local authorities regulate the mandatory control of FD and its vector for areas where FD is present. They also restrict the obligate control of S. titanus by insecticides and the measures to be taken to reduce inoculum. Further, a curing method for nurseries involving soaking dormant material for 45 min in 50°C hot water has been shown to kill FDP in situ and ensure healthy material. This method should be applied to all planting material in FD regions, especially those inhabited by the leafhopper vector. 

Conclusion

Flavescence dorée represents a significant agricultural and economic risk to Langhe winegrowers. Akin in gravity to phylloxera, FD has spread across Europe at an alarming rate. Previously contained to smaller Langhe subzones, FD-settlement areas have expanded, with infected vines identified in Barbaresco and Barolo. Though mostly limited to Barbera and Dolcetto, higher inoculum density risks fostering selection pressures congruent with mutation. To date, no effective treatment nor any viable vector control has been identified. The disease cannot be tackled nor solved in isolation. Instead, it requires cooperation, investment and regulation. Led by a consortium or cooperative, shared research, resource, and future technologies could improve identification efficacy. Recording and recognition of at-risk areas may help proactively manage infection. Effective management and mitigation protocol combined with rapid testing and cleaning of dormant vineyards will limit spread and reduce the overall disease burden. Finally, further research funding must be made available. Identifying why some vines recover, which biological controls confuse or displace the vector, and seeking to isolate FDP in vitro will be crucial in ridding Langhe of FD. Flavescence dorée is a shared challenge, a burden bore by the entire region. The response must be systemic, collaborative and prompt.

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