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Fungi in the grapevine, that’s rotten!

“Grapevine trunk disease” is an increasingly common problem in the vineyard that causes a yield reduction and the dead of grapevines. It is a collective name for various diseases of the trunk, of which the fungal diseases Eutypa dieback, Phomopsis dieback, Botryosphaeria dieback and the esca complex are the most important. In recent years a lot of research has been done into wood fungi in the vineyard, and many new fungi have been identified. However, due to the use of multiple disease names and new disease definitions, there is often uncertainty about the name and course of fungal diseases in the grapevine. This article provides an overview based on the latest insights.

It often takes several years for the symptoms of fungal diseases of the trunk to become visible. This makes it difficult to detect and treat fungal infections in time. The spores of the fungi infect the vine especially through pruning wounds, but other damage to the grapevine can also form a gateway. The fungi grow inside the trunk and slowly kill and digest the wood. In general, the place where the fungus has invaded the trunk is visible on the outside of the wood in the form of “cankers”. These are dead deeper lying pieces of the trunk that are (partially) overgrown by the surrounding bark. In addition, a cross-section of the infected wood often shows discolored or necrotic parts that are located centrally or in a wedge-shaped zone of the wood. The fungi cause a reduced sap flow, and / or release of toxic substances (phytotoxins)1-5 causing the shoots and leaves to discolor, grow to a reduced extent, or even to die6,7. The symptoms can vary per grape variety8,9, and because a vine is often infected with multiple fungi species, the symptoms of several fungal diseases can occur simultaneously3,10.

FUNGAL DISEASES AND THEIR SYMPTOMS

The most important fungal diseases of the vine that fall under “grapevine trunk disease” are Eutypa dieback, Phomopsis dieback, Botryosphaeria dieback and the esca complex. The term “dieback” points to the characterizing course of disease caused by these fungi. First the young shoots are affected and gradually the disease spreads, and makes a receding movement towards the increasingly older parts of the plant. The “esca complex” is a combination of multiple diseases that can cause shoots and parts of the vine to die. In the following sections, a detailed description of the symptoms will be given for each disease.

Eutypa dieback and Phomopsis dieback

“Dead arm disease” is an old term used when a part of the grapevine died due to a wood fungus while black necrotic spots were visible on the shoots. In the 1970s, it appeared that the symptoms of dead arm disease were actually a combination of two fungal diseases caused by the fungi Eutypalata and Phomopsis viticola11. A redefinition took place in which Eutypa lata causes Eutypa dieback. When the grapevine is infected with this fungus, the shoots grow later and slower, are shorter and have shorter internodes. In addition, the leaves of the infected plant are smaller, withered and chlorotic with torn edges. The affected shoots often die during the season12. When a cross-section of the infected wood is made, a wedge-shaped zone of discolored and dead vasculature in the wood can be seen that is caused by the Eutypa lata infection5. The other fungus, Phomopsis viticola, was held responsible for “Phomopsis cane and leaf spot”, the black necrotic spots on the first internodes of young shoots13. On the older shoot these spots are transformed into brown-black crusts with a corky appearance. Recently it came to light that Phomopsis viticola not only causes these black spots, but can also – just like Eutypa lata – cause the vascular discoloration of the wood, and the death of part of the vine11. Again a redefinition took place, and the fungal disease Phomopsis dieback was born.

Symptoms of Eutypa dieback and Phomopsis dieback.
Symptoms of Eutypa dieback and Phomopsis dieback. A wedge-shaped discoloration of the wood by Eutypa lata (A). Shortened shoots with small chlorotic leaves (B). The necrotic black spots on the 1-year shoots typical for an infection by Phomopsis viticola (C).
Figures adapted from Andolfi, 2011 via CC BY-3.0 (A + B) and Pinzid via Public domain (C).

Botryosphaeria dieback

There are more than twenty different fungi from the Botryosphaeria family that are known to cause Botryosphaeria dieback8. The symptoms of Botryosphaeria dieback show similarities with the symptoms of Eutypa dieback and “grapevine leaf stripe disease” (see below). Like Eutypa dieback, a cross-section of the wood shows a wedge-shaped discoloration.  In addition, an orange-brown discoloration is visible under the bark and in the longitudinal direction of the trunk (which is also a symptom of grapevine leaf stripe disease)14. The leaves of the grapevine get yellow-orange and red discolorations between the veins and at the edges of the leaf (for white and red varieties, respectively). These discolorations become necrotic, so that at a later stage the leaf is discolored around the green veins, and the edges of the leaf and the middle parts between the veins are dead and brown3,8,14. These symptoms have also been reproduced by manually infecting green shoots of the grapevine with fungi from the Botryospaeria family15. In addition to the discoloration of the leaves, other symptoms are falling off of the leaves and drying and rotting of the clusters. As with Eutypa dieback, it is possible that at the start of the season the shoots have a growth retardation and chlorotic leaves, and die later during the growing season3,14.

Symptoms of Botryosphaeria dieback.
Symptoms of Botryosphaeria dieback. Starting (A) and advanced leaf discoloration including necrotic parts between the veins and at the edge (B). Orange-brown discoloration on the trunk under the bark (C). Two wedge-shaped discolorations in a section of the trunk (D) and shortened shoots with chlorotic leaves (E).
Figures adapted from Larignon, 2001 via CC BY-4.0 (A-C) and Andolfi, 2011 via CC BY-3.0 (D, E).

Esca complex

Esca is in name possibly the most famous and notorious fungal disease. However, the old idea that “esca” leads to wood rot, a tiger stripe patern on the leaves and apoplexy in extreme cases, has been replaced by a complex of five fungal diseases. Each of these diseases is responsible for some of the symptoms typical for the old definition of “esca”. The five fungal disease that now together form the “esca complex3,10,16 are:

1. Dark wood streaking,
2. Petri disease,
3. Grapevine leaf stripe disease,
4. White rot, and
5. Esca proper

A number of these diseases are caused by the same fungi, but depending on the age of the vine and the duration of the infection they cause different symptoms. In short, the Phaeoacremonium minimum and Phaeomoniella chlamydospora fungi cause Dark wood streaking, Petri disease, and Grapevine leaf stripe disease, causing necrosis and discoloration of the wood (shown in cross-sections). This affected wood is then an ideal substrate for white rot that is caused by fungi such as Fomitiporia spp. and other fungi from the Basidiomycota family that digest the wood. “Esca proper” is ultimately the final stage in which multiple types of fungi are present, and the wood is affected in an advanced stage. The precise composition of fungi present in the wood is often different, which makes that the associated symptoms can differ. It is therefore difficult, but not impossible, to make a correct diagnosis of the disease(s). In addition, an acute esca variant can occur in which apoplexy occurs. In this case, healthy-looking green shoots and leaves will dry out and die within a few days without any specific leaf symptoms occurring. This often happens when a wet period is followed by hot and dry weather. It is not yet entirely clear how this is caused. It is thought that it is due to a sudden rise and activity of the phytotoxins secreted by the fungi, in combination with the extra evaporation due to the dry weather3,6,16,17.
In the next three paragraphs the chronic symptoms of the esca complex will be discussed in young and old vines.

Young planting

Dark wood streaking and Petri disease occur in young vines and are caused by the fungi Phaeoacremonium minimum and Phaeomoniella chlamydospora, and Petri disease also by Cadophora luteo-olivacea10. If brown vasculature is observed (when making a cross-section) in very young plants (<2 years), then this is defined as dark wood streaking. This is often a sign that the grapevines are grafted with contaminated wood. The leaves do not yet show any symptoms of the fungal disease. Petri disease occurs in slightly older, but still young plantings (<7 years), that also show the discolored vasculature. With both diseases it is possible that tar-like black droplets are observed when cutting the discolored wood. With Petri disease, the leaves may also show chlorosis and wither, and the vine can even die in its entirety10,16.

Symptoms of dark wood streaking and petri disease.
Symptoms of dark wood streaking and petri disease. Two sections with vascular discoloration and “tar droplets” in dark wood streaking (A, B). Petri disease with vascular discoloration in a 9 year old trunk as a result of a pruning wound (C). Vascular discoloration 14 months after a pruning wound was manually infected with Phaeomoniella chlamydospora (D).
Figures adapted from Rumbou, 2001 via CC BY-4.0 (A) and Mostert, 2006 via CC BY-4.0 (B-D).

In new and old vineyards

Grapevine leaf stripe disease is also mainly caused by Phaeoacremonium minimum and Phaeomoniella chlamydospora and can occur in both young and old vines. The characteristic feature of this fungal disease is the tiger stripe pattern on the leaves. This pattern develops between the veins of the leaf where first dark red or yellow stripes are formed, for red and white grape varieties respectively. Later on, the leaves also show necrotic stripes between the veins, and also the red varieties can now show a yellow stripe between the green and red / necrotic part of the leaf3,10,18. Because the yellow discoloration in red varieties shows often only in a later stage of the disease, it can be easily confused with Botryosphaeria dieback (see above). However, the discoloration of Botryosphaeria dieback occurs earlier in the season, from May to June, and not from the end of June to the beginning of July as with grapevine leaf stripe disease8. Other characteristics of grapevine leaf stripe disease are small necrotic spots on the grapes (“black measles”), possibly together with cracks in the grapes, and an orange-brown discoloration in the longitudinal direction of the trunk that becomes visible when the bark is removed. This discoloration originates from the canker, the site of infection. Also with grapevine leaf stripe disease, parts of the vine may suddenly wilt and die during the growing season10.

Symptoms of grapevine leaf stripe disease.
Symptoms of grapevine leaf stripe disease. Development of leaf discoloration for the white grape Trebbiano d’Abruzzo (A-C) and blue grape Cabernet Sauvignon (D-F). Multi-leaf shoot with typical tiger stripe pattern (G). Cracked grapes with necrotic spots (H). Orange-brown discoloration on the trunk under the bark (I).
Figures adapted from Calzarano, 2014 via CC BY-4.0 (A-C, G), Lecomte, 2012 via public domain (D-F, I) and Cloete, 2015 via CC BY-4.0 (H).

In old(er) vineyards

White rot and esca proper are diseases that occur in old vineyards. White rot is caused by fungi (Formitiporia spp.) that break down lignin in the wood, leaving long white cellulose fibers and making the trunk brittle and fragile. Esca takes its name from these cellulose fibers. The dry cellulose can be used as tinder wood to make a fire and is called “esca” in Latin / Italian6,19. White rot shows no external symptoms and is only perceptible when a cross-section of the wood is made10,16. Esca proper is – in the new definition of esca – the combination of all fungi and symptoms that fall within the esca complex10,16. With esca proper the trunk shows a discoloration of the wood as described for dark wood streaking and petri disease, but also shows parts of the wood that are affected by white rot. This damage to the wood spreads from the point where the first infection occurred, usually recognizable by a canker and an orange-brown discoloration on the trunk. The infection is almost never lower than the graft, and never affects the root system6. The grapevines that are infected with esca proper show the characteristic tiger stripe pattern on the leaves and the necrotic spots on the grapes, as is also evident with grapevine leaf stripe disease16.

Symptoms of white rot and esca proper.
Symptoms of white rot and esca proper. Esca proper shows wood discoloration and white rot, central in the trunk (A), or on the side in a wedge shape (B). External characteristics of esca proper that correspond to grapevine leaf stripe disease; tiger stripe pattern (C), necrotic spots on the grapes (D) and an orange-brown stripe on the trunk under the bark (E).
Figures adapted from Cloete, 2015 via CC BY-4.0 (A-D) and Lecomte, 2012 via public domain (E).
FUNGAL DISEASESYNONYMSCAUSING FUNGIREF
Eutypa diebackDead arm diseas / Eutypa dead arm / EutypioseEutypa lata5, 11
Phomopsis diebackDead arm disease / Phomopsis cane and leaf spot / excoriosePhomopsis viticola11,13
Botryosphaeria dieback Botryosphaeria canker / black dead arm / slow strokeMore than 20 different fungi species from the Botryosphaeria family, and other fungi such as Lasiodiplodia theobromaeNeofusicoccum parvumDiplodia mutila 3, 4, 5, 8, 14, 15
Esca complex esca3, 5, 6, 10, 16, 18
1. Dark wood streaking Brown wood streaking / black goo Phaeoacremonium minimumPhaeomoniella chlamydospora
2. Petri disease Young vine declinePhaeoacremonium minimum (and other spp.), Phaeomoniella chlamydosporaCadophora luteo-olivacea
3. Grapevine leaf stripe disease Black measlesPhaeoacremonium spp., Phaeomoniella chlamydospora
4. White rotFormitiporia spp. (e.g. mediterranea en australiensis), and other fungi species from the Basidiomycota family
5. Esca properPhaeoacremonium spp. (e.g. minimum and aleophilum), Phaeomoniella chlamydospora, Formitiporia spp. (e.g. mediterranea and australiensis)

MISDIAGNOSIS

Nutrient deficiencies can also lead to leaf discoloration and necrosis, and are often confused with the symptoms of fungal diseases. For example, a magnesium deficiency causes chlorosis followed by necrosis of parts of the leaf which resembles the symptoms of esca complex. However, the difference is that with magnesium deficiency, the discoloration is more even and ends in green points18. To choose the right treatment, it is therefore important to map out the symptoms very accurately and, when in doubt, to perform extra tests such as a soil test.

Magnesium deficiency symptoms visible on the leaf.
Magnesium deficiency symptoms visible on the leaf. Typical: the leaf green ends in points towards the edge of the leaf.
Figure adapted from Calzarano, 2014 via CC BY-4.0.

PREVENTION AND TREATMENT

Since the ban on carcinogenic sodium arsenate, there are no curative products on the market that can effectively combat the various wood fungi8. When the symptoms occur, it is already too late and the vines have been infected for a long time8. Healthy plants with a good immune system are therefore an important condition for the absence of diseases. Strengthening agents for the grapevine such as biofungicides20 and treatment with cysteine21 or other chemicals22 are for that reason fully tested to make the vines more resistant to fungal infections. In addition, there are also a number of preventive measures that can be applied in vineyard management. These measures start already when planting new grapevines. Stress factors such as poor drainage, insufficient or an abundance of nutrients, or poor planting of the rootstocks promote the development of fungal diseases23. Further, once the vineyard is planted, infection and spread of fungal diseases can often be prevented by the following methods and measures:

1. the Simonit & Sirch pruning method
2. Wound paste to seal large wounds in (older) wood
3. Decontamination of the secateurs between different vines
4. Not pruning in wet weather
5. Cutting the shoots diagonally so that no water remains on the wound
6. Removing contaminated wood from the vineyard (and burn or bury it)

A number of these preventive methods – such as disinfecting the secateurs and not pruning in wet weather – are good in theory, but not always practicable in larger vineyards. Cutting at an angle and removing contaminated wood, on the other hand, is possible to prevent the fungi from spreading. Of the above methods, the Simonit & Sirch pruning method is likely to have the greatest effect on the prevention of fungal diseases, and is also applicable in larger vineyards. A characteristic of this pruning method is that it prevents large wounds from forming in old wood. These wounds do not heal, or very slowly, and are therefore a gateway for fungal spores. Treatment with wound paste can prevent spores from penetrating into these wounds. However, it is a lot of work to (continue to) treat all wounds and it is not a complete guarantee for the absence of infection. Until a curative product comes on the market, it is important to timely signal the symptoms of fungal diseases – as described above. Removing the infected (part of the) grapevines, and ensuring that the other grapevines are as healthy as possible, is currently the only way to prevent the spread of wood fungi in the vineyard.

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