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Botryosphaeria canker and dieback of grapevines
Introduction
In recent years it has become evident that several species of Botryosphaeria have wide host ranges and geographic distributions. Disease symptoms vary from leaf spots to cankers, dieback, and various other shoot and trunk diseases. Many of these species have also been reported from grapevines, where they are associated with a wide variety of diseases and symptoms (Phillips, 2001). Inconsistent literature reports, however, have led to confusion regarding the various Botryosphaeria species occurring on vines. It is therefore presently unclear which species of Botryosphaeria pose the biggest threat to grapevine cultivation (Phillips, 2001). A further problem concerning the diagnosis of Botryosphaeria diseases is that field symptoms closely resemble that of other diseases such as cane and leaf spot (caused by Phomopsis viticola) and Eutypa dieback (caused by Eutypa lata) (Castillo-Pando et al., 2001). Accurate identification of the causal organism is also difficult since Botryosphaeria spp. do not readily form fruiting structures in artificial media under laboratory conditions (Denman et al., 2000).
Botryosphaeria diseases: a global perspective
Although the importance of the various Botryosphaeria species occurring on grapevines has not yet been clarified, various symptoms and diseases have been associated with Botryosphaeria species occurring on this host worldwide. These are summarised below:
Excoriose
This disease is present wherever grapevines are grown and severe damage occurs when wet weather is encountered early in the season. Symptoms associated with this disease are bud mortality, leading to reduction in yield losses, breakage of branches and shoot dieback. The disease does not develop rapidly, but it builds up in a vineyard and leads to a gradual decline in vigour and yield (Phillips, 1998). This aspect is probably the reason why the most severe losses due to this disease occur in vines that are eight years and older (Larignon & Dubos, 2001).
The fungus invades the young shoots of vines early in the season and causes elongated black lesions on the internodes. The infected branches become swollen at the base, and the blackened cortex may rupture. These branches are consequently very brittle and can easily collapse under their own weight. Some of the branches, which do not break, may die back. Later in the season, after harvest, the black lesions turn grey or white with black fruiting structures immersed in the host tissue. These symptoms are seen as typical excoriose symptoms, while bud necrosis may also occur (Phillips, 1998).
Grapevine decline syndrome
Between 1996 and 1999, AJL Phillips conducted a survey of grapevines in Portugal to determine which species of Botryosphaeria were associated with grapevines. Isolations were made from five different symptoms. Together these five symptom types were called grapevine decline syndrome. One or all of these symptoms may occur on an infected vine.
The first symptom was trunk dieback, with a dark brown discolouration of the wood, which started at large pruning wounds, spreading down the trunk. From this symptom Botryosphaeria parva was readily isolated. In some cases brown streaking of the wood was also encountered with a dark brown discolouration of the trunk. This streaking had the appearance of small black spots when looking at the branch in cross section. This symptom appeared similar to the symptom found in trunks and arms affected by Petri disease (= Black Goo), which is caused by Phaeomoniella chlamydospora. The symptom differs from Petri disease in that the spots are more diffuse and in the case of Petri disease, a black tarry substance oozes from the spots which is not the case with the spots caused by Botryosphaeria. From these spots, B. parva and sometimes B. obtusa and B. stevensii were readily isolated (Castillo-Pando et al., 2001; Phillips, 2001).
In cases where isolations were made from young plants where the graft union failed, P. chlamydospora was mostly isolated, but in some cases B. parva, B. obtusa and B. dothidea were also isolated. Bud necrosis was also encountered on some vines and isolations made from the dead tissue around the buds yielded mainly B. stevensii and sometimes B. parva. Another type of Botryosphaeria symptom is the typical bleaching of dormant canes seen during winter, and which is normally associated with excoriose or Phomopsis cane blight. Isolations from this symptom yielded B. parva and B. lutea, with B. obtusa also encountered in some isolations (Phillips, 2001).
The last symptom type found in association with Botryosphaeria is a V-shaped necrotic sector that can be seen in the stem of the vine in cross section. In the field this symptom was also found in association with brown wood streaking. These symptoms resemble Eutypa dieback, but can be distinguished by the absence of poor shoot development and small, yellow, malformed leaves (Castillo-Pando et al., 2001). From this symptom, B. obtusa was readily isolated. In Australia, B. obtusa was also found to be the causal organism of dieback of Semillon grapevines in New South Wales (Castillo-Pando et al., 2001). Botryosphaeria obtusa occurs on a wide variety of woody hosts and can live saprophytically on dead wood and bark (Castillo-Pando et al., 2001). It has been recognised as a wound pathogen and can cause dieback symptoms as well as cankers. In Portugal, B. obtusa was found associated with reduced growth, reduced bud burst and death of arms (Phillips, 2001). In Australia and California, B. rhodina was also isolated from this V-shaped symptom (Pascoe, 1998a; 1998b).
In Australia, B. stevensii was also isolated from vines showing decline symptoms (Pascoe, 1998a), as was the case in Hungary (Lehoczky, 1974). Because B. ribis was mostly associated with fruit rot in Australian vineyards, it was concluded that it might not be a pathogen of shoots or canes in this country (Pascoe, 1998a).
Black Dead Arm
Since 1974, B. stevensii has been associated with black dead arm disease of grapevines in Hungary. This disease is characterised by mild chlorosis appearing on the leaves, depending on how far the fungus has invaded the vascular tissue. Wilting of the leaves may occur if water transport becomes insufficient due to infection. Infection of berries does not occur generally, but severe berry and cluster rot have been reported from White Hanepoot and Red Hanepoot cultivars in South Africa (Lehoczky, 1974; 1994). The infection occurs near ripening and the berries become dark brown, shrivelled and dry out. Losses in yield can range between 25 to 30%. In the spurs, arms and trunks narrow black streaks develop in the xylem. This streaking expands towards the pith, as well as longitudinally and laterally. The discoloured tissue becomes necrotic and dysfunctional, with the bark over the infected tissue also dying (Lehoczky, 1974; 1994). The association of B. stevensii with this symptom of thin, black streaks also corresponds with the findings of Phillips (2001).
Macrophoma rot
In the USA, B. dothidea is regarded as the causal organism of Macrophoma rot of Muscadine grapes. This disease is characterised by one or more round, sunken lesions developing on infected berries as they mature. The lesions are black with small brownish centres in which the fruiting bodies (pycnidia) of the fungus are embedded. These affected berries later drop from the vine and dry up with pyncnidia covering the entire surface. This disease develops optimally at 28oC and overwinters as pycnidia on dried-out berries on the vineyard floor (Kummuang et al., 1996a; 1996b; Milholland, 1991; 1994). Botryosphaeria ribis is also reported to occur in the USA, though little is known about its relative importance (http://www.nt.ars-grin.gov).
Diplodia Cane Dieback and Bunch Rot
The causal organism of Diplodia cane dieback (Fig 4) and bunch rot is regarded to be B. rhodina. This disease begins in the summer season with shoots dying back from the tip toward the base. The dead parts turn brown to grey and are speckled with pycnidia. Cankers also develop on the shoots and may spread in any direction along the shoot. Black pycnidia can be seen in the bark of infected parts of the vine. Spurs or portions of spurs and arms may die and in the summer the pycnidia erupt through newly formed bark.
When berries become infected, they at first appear water-soaked and as the rot develops the skin cracks and the berries become covered in a white mass of mycelium. The berries eventually dry out and become mummified with black pycnidia emerging on the surface of the dried-out berries. These berries are seldom seen due to the fact that the berries become infected with secondary fungi and yeasts that cause the cluster to turn into a rotten mass, known as summer bunch rot (Hewitt, 1994).
In the vineyard, the fungus overwinters inside diseased parts of the vine or in the soil. In spring, when temperature starts to increase and the vine becomes active again, the propagules of B. rhodina also revive. The fungus can become soil-borne from prunings lying on the vineyard floor. The disease is spread by windblown fungal spores (conidia) or splash dispersed in water droplets from rain or sprinkle irrigation. Infection of shoots occurs when shoots touch wet soil or are covered with soil during cultivation. The fungus then spreads along the shoot and may grow into arms and spurs of the plant and kill tissues as it grows. Berry infection occurs during or shortly after bloom from windblown conidia.
Botryosphaeria diseases in South Africa
In South Africa, Botryosphaeria was shown to be one of the more important pathogens of grapevines, as it was isolated from approximately 9% of all diseased plants received at the diagnostic clinic at ARC Infruitec-Nietvoorbij (Fourie & Halleen, 2001). According to Crous et al. (2000), only three Botryosphaeria species occur on grapevines in South Africa, namely B. obtusa, B. dothidea and B. ribis.
The 112 isolates of Botryosphaeria used in this study were obtained from different sources. Some of the isolates were isolated from asymptomatic nursery plants, a few isolates came from asymptomatic mother material and many came from plants received at the diagnostic clinic at ARC Infruitec-Nietvoorbij. Isolates were also obtained from grapevine material collected from vineyard floors in the Stellenbosch area. The twigs were incubated under moist conditions for one week and single spore isolations were made of the Botryosphaeria species that sporulated on the grapevine material. A number of reference isolates were also obtained from co-workers in Argentina and Portugal.
A DNA molecular study was conducted to characterise the various Botryosphaeria species present on grapevines. Preliminary results from this study indicated that at least ten different species of Botryosphaeria occur on grapevines, eight of which occur in South Africa. Several of these species have either not been reported from South Africa, or appear to be new to science. Of the three species reported to occur on vines in South Africa (Crous et al., 2000), only B. obtusa was confirmed in this study. The possibility exists, however, that B. dothidea and B. ribis do in fact occur on vines locally, but that they were simply not isolated in the survey done during the study. A further possibility could be that they occur in areas other than the Western Cape Province, which was the area most intensively sampled for Botryosphaeria.
Isolates obtained from ARC Infruitec-Nietvoorbij were also correlated with the various symptom types from which they were isolated. This was done in an attempt to correlate it with the study done by Phillips in Portugal (Phillips, 2001). Isolations were made from three different symptom types, as well as from asymptomatic mother material, and healthy nursery plants. Results indicated that several species of Botryosphaeria could be present in plant material, even though no disease was evident. As has been reported from other woody hosts, species of Botryosphaeria can therefore also survive as endophytes in apparently healthy vines, which confirms earlier findings of Mostert et al. (2000). From these asymptomatic plants, B. obtusa and another Botryosphaeria sp. were mainly isolated.
Several species of Botryosphaeria were found to be associated with V-shaped necrotic trunk lesions of vines examined in cross-section (Figs 1, 2). This symptom also closely resembles Eutypa dieback. The second symptom from which Botryosphaeria species were isolated, was typical half-moon lesions in grapevine trunks (cross-section) (Fig 3) and this symptom mainly yielded isolates of B. obtusa. The third symptom type commonly encountered were brown speckles that occurred in the trunks, and which resemble the black spots (Fig 2 & 3) usually associated with Petri disease (=Black Goo). From these speckles, B. obtusa and another Botryospheria sp. were isolated. The final symptom, which was commonly observed in the field, entailed a brown dieback of shoots. Some of the species encountered in this study were collected from dead plant material on the vineyard floor, showing that plant debris is an important source of new infections, as Botryosphaeria overwinters on the dead material, from where it sporulates, causing new infections.
Control of Botryosphaeria diseases on grapevines
The control of Botryosphaeria diseases is difficult, as information on disease control, especially chemical control, is very limited. In many instances the recommended control measures vary from one region to another, and even from one country to another (Milholland, 1991). Currently there are no fungicides registered for use against Botryosphaeria dieback in South Africa (Nel et al., 1999). France is one of the very few countries where a fungicide is registered for control of black dead arm that is caused by B. obtusa, B. dothidea and in some cases B. stevensii. Sodium arsenite is recommended and must be used under the same conditions as for the treatment of Esca disease (Larignon & Dubos, 2001; Lehoczky, 1974; 1994). In the USA, Macrophoma rot is controlled by the application of protective fungicides like maneb, which start after bloom and continues throughout the fruit-ripening period (Milholland, 1994).
Another control measure that is widely recommended for most diseases caused by the various Botryosphaeria species, is good sanitation practice. After pruning, the debris should be removed from the vineyard and preferably burnt, as this material can be a source of inoculum that can cause new infections. This practice is supported by the fact that in this study several Botryosphaeria species were isolated from pruning debris collected up from the vineyard floor.
When the disease has not spread throughout the whole plant, the diseased parts can be removed, which is the same practice used for the control of Eutypa dieback. Whole infected plants should be removed from the vineyard. To prevent the occurrence of Diplodia cane dieback (Fig 4) and bunch rot, it is important to prune and train vines in such a manner that the shoots do not touch the ground. It is also important to prevent unnecessary wounding of plants as most of the Botryosphaeria species, which occur on grapevines, are regarded as wound pathogens (Larignon & Dubos, 2001; Lehoczky, 1994; Milholland, 1991; 1994). Further research is presently underway to determine which of the Botryosphaeria spp. occurring on vines in South Africa are primary pathogens, and which diseases they cause. These findings will again lay the foundation for further research focused on control of specific Botryosphaeria diseases.
References
Castillo-Pando, M, Somers, A, Green, CD, Priest, M. & Sriskanthades, M. 2001. Fungi associated with dieback of Semillon grapevines in the Hunter Valley of New South Wales. Australian Plant Pathology 30: 59 - 63.
Crous, PW, Phillips, AJL & Baxter, AP. 2000. Phytopathogenic fungi from South Africa. University of Stellenbosch, Department of Plant Pathology Press, University of Stellenbosch Printers.
Denman, S, Crous, PW, Taylor, JE, Kang, J-C, Pascoe, I & Wingfield, MJ. 2000. An overview of the taxonomic history of Botryosphaeria, and re-evaluation of its anamorphs based on the morphology and ITS rDNA phylogeny. In: Molecules, morphology and classification: Towards monophyletic genera in the Ascomycetes. Studies in Mycology 45: 129 - 140.
Fourie, P & Halleen, F. 2001. Diagnosis of fungal diseases and their involvement in dieback diseases of young vines. Wineland December 2001.
Hewitt, WB. 1994. Diplodia cane dieback and bunch rot. In: Compendium of Grape Diseases. APS Press.
Kummuang, N, Diehl, SV, Smith, BJ & Graves, CH (Jr). 1996a. Muscadine grape berry rot diseases in Mississippi: Disease Epidemiology and Crop Reduction. Plant Disease 80: 244 - 247.
Kummuang, N, Diehl, SV, Smith, BJ & Graves, CH (Jr). 1996b. Muscadine Grape Berry Rot Diseases in Mississippi: Disease Identification and Incidence. Plant Disease 80: 238 - 243.
Larignon, P & Dubos, B. 2001. The villainy of Black Dead Arm. Wines and Vines 82(3): 86 - 89.
Lehoczky, J. 1974. Black Dead-arm Disease of grapevine caused by Botryosphaeria stevensii infection. Acta Phytopathologica Academiae Scientiarum Hungaricae 9: 319 - 327.
Lehoczky, J. 1994. Black Dead Arm. In: Compendium of Grape Diseases. APS Press.
Milholland, RD. 1991. Muscadine Grapes: Some important diseases and their control. Plant Disease 75: 113 - 117.
Milholland, RD. 1994. Macrophoma Rot. In: Compendium of Grape Diseases. APS Press.
Mostert, L, Crous, PW & Petrini, O. 2000. Endophytic fungi associated with shoots and leaves of Vitis vinifera, with specific reference to the Phomopsis viticola complex. Sydowia 52(1): 46 - 58.
NEL, A, KRAUSE, M, RAMAUTAR, N, & VAN ZYL, K. 1999. A guide for the control of plant diseases (1st ed.). National Department of Agriculture, Republic of South Africa.
Pascoe, I. 1998a. Grapevine trunk diseases in Australia: Diagnostics and taxonomy. Proceedings of the 1998 Seminar and Workshop on Black Goo: Symptoms & occurrence of grape declines. pp.56 - 77.
Pascoe, I. 1998b. Trunk diseases of grapevines - perspectives from a tour of California. Australian Grapegrower and Winemaker 417: 68 - 71.
Phillips, AJL. 1998. Botryosphaeria dothidea and other fungi associated with excoriose and dieback of grapevines in Portugal. Journal of Phytopathology 146: 327 - 332.
Phillips, AJL. 2000. Excoriose, cane blight and related diseases of grapevines: a taxonomic review of the pathogens. Phytopathologia Mediteranea 39: 341 - 356.
Phillips, AJL. 2002. Botryosphaeria species associated with diseases of grapevines in Portugal. Phytopathologia Mediteranea 41: 3 - 18.
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Jan van Niekerk1, Pedro Crous1, Paul Fourie2, Ewald Groenewald1 and Francois Halleen2
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