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Black foot disease of grapevine: Summary of research in South Africa
Francois Halleen1, Paul Fourie2 & Pedro Crous3
1 ARC Infruitec-Nietvoorbij, Stellenbosch
Abstract
Black foot disease of grapevine is a relatively new, and as yet poorly known disease affecting vines in various countries where grapevines are cultivated. Studies regarding the causal organisms, their distribution, associated symptoms, known epidemiology and possible management strategies have been the focus of attention in South Africa. Cylindrocarpon destructans, C. macrodidymum, Campylocarpon fasciculare and Campyl. pseudofasciculare have been identified as the causal organisms of this disease in South Africa. All four species have the ability to infect grafted grapevines in nursery soils. Hot water treatment of uprooted dormant nursery grapevines effectively reduced these infections.
Introduction
Over the last few years a drastic reduction has been noted in the survival rate of grafted grapevines in nurseries, as well as in young vineyards in the Western Cape Province of South Africa. The low average take percentages of young vines can be attributed to several factors, including fungal, bacterial and viral diseases, insect and nematode pests, abiotic factors, as well as nutritional deficiencies and toxicities. Cylindrocarpon spp., which causes black foot disease of grapevine, was found to be associated with the decline of young vines in South Africa. Results obtained from the diagnostic service at ARC Infruitec-Nietvoorbij (Plant Protection Division) showed that Cylindrocarpon spp. were isolated from 52%, 22% and 29% of diseased vines during 1999-2002, 2002-2003 and 2003-2004, respectively. However, it was unclear how and where these infections occurred. Very little information is available regarding the aetiology and epidemiology of the fungi believed to be involved in black foot disease. Diseased grapevines presented for diagnosis were typically less than 5 years old and in some instances symptoms even appeared during the first year of planting. Diseased plants display an array of decline symptoms. In vineyards, the first visible symptoms are usually delayed or absence of budding (Figure 1). Subsequently shoots develop abnormally (shortened internodes and small discoloured leaves) and may wilt and die during summer. When symptomatic plants are removed from the soil, inspection of the roots may reveal the presence of brown to black necrosis which ultimately leads to the underdevelopment of the entire root system. Further root abnormalities include the development of secondary root crowns with roots growing parallel to the soil surface. Internal symptoms include brown-black discolouration of xylem vessels originating from the base of the rootstock (Figure 2), brown-black discolouration in roots, and necrosis from the bark to the centre of roots (Figure 3) and rootstocks (Figure 4) (Fourie & Halleen, 2001).
The purpose of this communication is to provide a short overview of the results obtained from research conducted during the past 5 years. The primary aims of research have been (1) to conduct nursery surveys in order to determine which fungi are involved in the decline phenomenon, with special reference to the involvement of Cylindrocarpon spp., (2) to identify the organisms believed to be the causal organisms of black foot disease, and (3) the development of control and/or management strategies to prevent or eradicate Cylindrocarpon infections.
Nursery survey: Nursery grapevines that were sampled from 3 commercial nurseries in the Wellington area of the Western Cape province of South Africa were investigated during the 1999/2000 season by means of destructive sampling. The first isolations were made in September from callused cuttings prior to planting in nurseries. After planting, asymptomatic rooted cuttings were selected from nurseries after 3, 6 and 9 months. Isolations were made from the roots, rootstocks, graft unions and scions.
Identification of the causal organism: Cylindrocarpon-like isolates, obtained from the nursery survey, as well as from the grapevine diagnostic service at ARC Infruitec-Nietvoorbij, were collected for further investigation. Substantial variation in cultural and morphological characters was observed among these isolates. Morphological and phylogenetic studies were therefore conducted to identify these Cylindrocarpon spp. and to establish their association with black foot disease. Sequences of the partial nuclear large subunit ribosomal DNA (LSU rDNA), internal transcribed spacers 1 and 2 of the rDNA including the 5.8S rDNA gene (ITS), and partial beta-tubulin gene introns and exons were used for phylogenetic inference.
Control: Knowledge obtained pertaining to the infection period and site in the nursery survey suggested that any suitable control method will have to focus on preventing or eradicating infection of the basal ends of nursery cuttings. However, at present, no fungicides are registered for control of this disease in South African vineyards or nurseries. In vitro studies were conducted to evaluate the effectiveness of various fungicides. Benomyl, flusilazole and prochloraz manganese chloride were the most effective fungicides tested against these species in vitro. These fungicides, alone or in combination with a wax formulation or adjuvant, were included with biological and physical treatments in the semi-commercial field trials. These treatments were aimed at protecting the basal ends of rootstocks against infection. After callusing, the basal ends of grafted cuttings were dipped in various treatments prior to planting. Additional treatments involved soil amendments with Trichoderma formulations and hot water treatment of uprooted dormant nursery grapevines (30 min at 50øC). Nursery plants were uprooted after eight months. The trials were conducted at two field nurseries in Wellington during the 2002-2003 and 2003-2004 seasons.
Results and Discussion
Nursery survey: Isolation studies conducted in the nurseries clearly demonstrated that different Cylindrocarpon spp. infected cuttings from soil were once planted in the nurseries. These species rarely occurred in rootstock propagation material prior to planting. At the time of planting, the susceptible basal ends (especially the pith area) of most of the nursery cuttings are partly or even fully exposed. Callus roots also break during the planting process, resulting in small wounds susceptible to infection by soilborne pathogens. The isolation studies revealed that the first infections occurred in the roots, followed by infections of the rootstocks. Furthermore, these infections also increased progressively during the course of the growing season (Halleen et al., 2003).
Identification of the causal organism: Phylogenetic analyses confirmed the diversity observed among the isolates and four Cylindrocarpon-like species were identified. One of these groups was identified as Cylindrocarpon destructans. A second group was newly described in this study as Cylindrocarpon macrodidymum (Neonectria macrodidyma). The two remaining Cylindrocarpon-like species were placed in a new genus, Campylocarpon. The two species were named Campylocarpon fasciculare and Campylocarpon pseudofasciculare. Pathogenicity studies confirmed that all 4 species were able to reduce root and shoot mass significantly (Halleen et al., 2004).
Control: No Cylindrocarpon or Campylocarpon spp. was isolated from any of the control plants before planting in the nurseries. Isolations from uprooted grapevines at the end of the growing season revealed very low levels (4.1%) of Cylindrocarpon and Campylocarpon spp. in the roots of untreated control plants and no significant differences between treatments. However, infection levels in the basal ends were substantially higher and Cylindrocarpon and Campylocarpon spp. were isolated from 31.1% of untreated control plants. If all factors are taken into consideration (percentage fungal infection, take percentages, root- and shoot mass), none of the chemical and biological treatments significantly and/or consistently prevented infection. Hot water treatment of uprooted dormant nursery grapevines completely eradicated Cylindrocarpon and Campylocarpon infection in the plants.
Conclusion
The diversity of species associated with black foot disease has been confirmed by this study. The fact that Cylindrocarpon and Campylocarpon spp. have the ability to infect grafted grapevines in nursery soils has clearly placed the emphasis on the importance of suitable control measures to prevent or eradicate these infections. However, none of the chemical and biological treatments evaluated in this study prevented infection of nursery grapevines. The reduction of Cylindrocarpon and Campylocarpon infection in uprooted dormant nursery grapevines caused by the hot water treatment clearly demonstrated the potential of this control measure. This treatment was also recommended for the eradication of Phytophthora cinnamomi (Von Broembsen & Marais, 1978) and Meloidogyne javanica (Barbercheck, 1986) from dormant nursery grapevines and was also found to be effective against Phaeomoniella chlamydospora and Phaeoacremonium spp. that cause Petri disease of grapevine (Fourie & Halleen, 2004). Apart from these pro-active management strategies in grapevine nurseries, no cure is known for declining grapevines in vineyards. Producers are therefore urged to heed general recommendations to prevent and/or correct predisposing stress situations, such as soil compaction and poor drainage.
For further information contact Francois Halleen at Nietvoorbij on (021) 809-3040, e-mail halleenf@arc.agric.za.
Acknowledgements
The following people and organisations are thanked for their contribution towards this research. Winetech for financial support of projects WW06/20, WW06/25 and WW06/26. Carine Vermeulen, Linda Nel, Julia Marais and Zane Sedeman from the Plant Protection Division for technical assistance. Voor-Groenberg Nursery where field trials were conducted. KWV-Vititec (especially Dirk Visser) for assistance with hot water treatment.
Literature cited
Barbercheck, M., 1986. Control of Meloidogyne javanica in dormant grapevine nursery stock. Phytophylactica 18: 39-40.
Fourie, P.H. & Halleen, F., 2001. Diagnose van swamsiektes en hul betrokkenheid by terugsterwing van jong wingerd. Wynboer 149: 19-23.
Fourie, P.H. & Halleen, F., 2004. Proactive control of Petri disease of grapevine through treatment of propagation material. Plant Disease 88: 1241-1245.
Halleen, F., Crous, P.W. & Petrini, O., 2003. Fungi associated with healthy grapevine cuttings in nurseries, with special reference to pathogens involved in the decline of young vines. Australasian Plant Pathology 32: 47-52.
Halleen, F., Schroers, H-J., Groenewald, J.Z. & Crous, P.W., 2004. Novel species of Cylindrocarpon (Neonectria) and Campylocarpon gen. nov. associated with black foot disease of grapevines (Vitis spp. L.). Studies in Mycology 50: 431-455.
Von Broembsen, S. & Marais, P.G., 1978. Eradication of Phytophthora cinnamomi from grapevine by hot water treatment. Phytophylactica 10: 25-27.
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