BOTRYTIS DISEASES OF RASPBERRIES AND BLUEBERRIES

Dalphy O.C. Harteveld and Tobin L. Peever

Department of Plant Pathology, Washington State University

Figure 1. Botrytis blossom blight symptoms on blueberry. Photo Jay Pscheidt, OSU

Botrytis diseases cause large annual losses (up to 30%) to the raspberry and blueberry industries in the Pacific Northwest (PNW). Levels of disease are highly variable from year to year and control is costly and inconsistent. The disease affects many different hosts, different tissues of each host, and control is dependent upon frequent, calendar-based applications of fungicides. The pathogen is notorious worldwide for its ability to develop resistance to fungicides making Botrytis diseases a persistent threat to berry production in the PNW.

 

Significance

The causal agent of Botrytis diseases, Botrytis cinerea, has a wide host range and causes economically significant losses to more than 200 crops worldwide 16 including protein, oil, fibre and horticultural crops in both temperate and subtropical regions. Small fruit crops and vegetables are the most severely affected by this pathogen 16. In small fruit crops, the disease is referred to as “gray mold”. Gray mold or Botrytis bunch rot of wine grapes is the most studied Botrytis disease among the small fruit crops. Other small fruit crops that are affected by B. cinerea include blueberries, blackberries, raspberries and strawberries. In highbush blueberry (Vaccinium corymbosum) the pathogen is known to cause three diseases: tip blight, blossom blight and fruit rot. In red raspberry (Rubus ideaus) the pathogen causes three diseases: blossom blight, fruit rot and cane Botrytis. In this article, we will focus on the biology and management of Botrytis diseases of berries.

 

Disease symptoms

Tip blight of blueberry

Infected twigs become brown to black and turn tan or grey at a later stage. The twig blight progresses from the tip toward the base. Black sclerotia (overwintering structure of the fungus) can be found near the tip of the blighted twigs 10. Blossom blight of blueberry Blossoms appear as brown and water-soaked (Fig. 1). The blossoms are often covered in dense, gray, powdery growth of the pathogen 10.

 

Fruit rot of blueberry

There are two types of fruit rot, green berry fruit rot starts as a brown discoloration near the calyx end of the fruit 10. The brown area expands until the entire berry rots and shrivels. The berry either drops from the cluster or adheres to the plant and often displays the gray, powdery growth of the pathogen (Fig. 2 and 3). Ripe berry fruit rot occurs post-harvest, where rot symptoms appear and the fungus shows growth on the surface of the fruits.

 

Raspberry cane Botrytis

The fungus infects mature, senescent leaves causing a wedge-shaped brown lesion with yellow margin that spreads to the nodes of primocanes 16. Lesions appear as tan to brown, often incorporating more than one node. The lesions show concentric ring patterns (Fig. 4). These infections

 

Blossom blight of raspberry

Infected flowers turn brown and shrivel. Green, gray, powdery mass of fungal growth is visible on the surface of the flowers at a later stage.

 

Fruit rot of raspberry

Fruit rotting appears as soft spots on the fruit, which enlarge over time. The fruit shows dense, gray, powdery growth of the pathogen (Fig. 5 and 6).

 

Identity of the pathogen

The Botrytis pathogen of raspberries and blueberries is commonly known as Botrytis cinerea. However, recent studies have demonstrated that B. cinerea infecting grapes is actually a complex of species that look the same and are called “cryptic” species 6. Genetic markers are required to differentiate them. Similarly, multiple cryptic Botrytis species may infect raspberry ands strawberry 1and a recent study of blueberries in California has similarly demonstrated infection by two species: B. pseudocinerea and B. cinerea 12 that are similar in appearance. These species may respond differently to fungicides which makes identification important for disease control. It is currently not known if B. cinerea populations infecting raspberry and blueberry in the PNW are different or if they might be specialized on particular plant parts (e.g. raspberry fruit versus canes).

 

The disease cycle

The disease cycle of B. cinerea has been studied for many years, particularly on grapes, yet many questions remain. The great flexibility of the pathogen to adapt to different environments and the possible involvement of multiple cryptic species demonstrate that disease cycles may be specific to each region and host. Particular disease control strategies may be effective in some areas and not in others. More specific, in depth studies of the disease cycle of B. cinerea in berries is urgently needed in the PNW.

 

Overwintering and sources of inoculum

In raspberry, the fungus overwinters as black, oblong sclerotia (black compact mass of hardened fungal mycelium) in infected canes and as mycelium in infected leaves in the plant canopy and leaves and canes on the ground. Under conducive environmental conditions, fungal mycelium develops from the sclerotia (Fig. 7). This mycelium produces specialized structures for producing spores (conidia) called conidiophores. These conidiophores develop further to produce conidia (Fig. 8 and 9). The main sources of primary inoculum for Botrytis diseases are conidia produced from overwintering sclerotia, dead leaves, and mummified berries 3. In blueberries, the fungus overwinters as dormant mycelium and sclerotia in plant debris, including dead twigs and pruned branches 4, 10.

 

Dispersal

In early spring, the fungal mycelium becomes active and produces large numbers of conidia on the surface of leaf debris. Conidia are spread by wind and rain throughout the field where they are deposited on blossoms and fruit 3. Fluctuations in temperature and humidity control the production and dissemination of the conidia 7.

 

Infection

Germination of conidia that land on plant surfaces occurs within a few hours when free water is present and when temperatures are between 70 and 80 degrees F (20 to 27 degrees C)3. This water can come in the form of rain, dew, or fog, or from water from irrigation (Fig. 10). Temperature and periods of moisture are the main factors controlling infection of blueberry and raspberry 10, 11. Infection can occur at lower temperatures if the tissue remains wet for longer periods. Under appropriate conditions, the germinated spores (Fig. 11) produce a germ tube which then penetrates and invades the host tissue. Infected cells collapse and disintegrate and the tissue rots. On the surface of the infected tissue the pathogen produces new conidiophores and conidia which are then dispersed to new plants and the cycle of infection is repeated. Infection can also occur through wounds in plant tissue created by equipment, mechanical harvesting or by insects such as the raspberry beetle Byturus tomentosus 17.

 

Flowers of raspberry are highly susceptible to B. cinerea in¬fection. Flower buds are generally not infected, but open flowers are rapidly colonized and leads to subsequent fruit infection 2. Flower infection occurs when conidia are dispersed to stigmas which provide a nutrient source for the germinating conidia 9. In raspberry and other small fruit, infections appear to occur during bloom, but symptoms only appear as the fruit ripens 9. These types of infections are referred to as “latent” or “quies¬cent” because the fungus colonizes floral parts but remains latent and emerges as the fruit starts to mature 3. Despite the available evidence that B. cinerea infects raspberry floral parts and these infections lead to fruit rot, many questions about the infection process remained unanswered. A better understanding of this infection process is key to improved control of Botrytis fruit rot. Studies using highbush blueberry cultivars Duke and Brigitta showed that the most susceptible infection stages for flowers are late pink bud and full bloom and over-mature fruit showed to be the most susceptible fruit stage 11.

 

Disease control

Fungicide applications have been the main disease control strategy in berry crops. However, an increasing number of reports from around the world have demonstrated that B. cinerea has developed resistance to most of the fungicides that are currently used. In Germany, Botrytis isolates affecting small fruit have demonstrated resistance to multiple fungicides 13, and these resistant populations pose a major threat to small fruit production. Alternative measures to control these diseases are urgently needed.

 

Cultivar selection also plays a major role in the control of plant diseases. Although no raspberry or blueberry cultivars with high levels of resistance have been reported, some cultivars may develop less disease than others. The raspberry cultivars “Meeker”, “Munger”, “Chilliwack”, “Comox”, “Fairview” and “Meeker” appear less susceptible than other cultivars that are grown in the Pacific Northwest 10. The cultivar “Meeker” has shown to be less susceptible than other cultivars in British Columbia 5. The cultivar “Latham” appeared to have resistance to cane Botrytis in Hungary 8. Specific traits of cultivars may help in the selection of more resistant cultivars e.g. some cultivars may have a stigmatic fluid that is inhibitory to B. cinerea,, thereby avoiding the latent fruit infections 14, 15 and cultivars that flower over a longer period of time may be more susceptible 10.

 

Cultural practices such as pruning to promote air movement and reduced periods of leaf and flower wetness has been shown to reduce disease development 4. In addition, the consistent removal of as many sources of inoculum as possible, including leaf debris, mummified berries and pruned canes also helps to reduce Botrytis infection 4.

 

Botrytis Research in the Pacific Northwest

Researchers from Washington State University and Oregon State University are currently studying the timing and environmental conditions required for infection of raspberry canes, flowers and fruit by the pathogen as well as the status of fungicide resistance of B. cinerea infecting blueberry, raspberry and strawberry. We are also attempting to determine if different populations or species of Botrytis infect berry crops in the PNW and if so, how this might affect disease management strategies. These studies are designed to improve our understanding of the local Botrytis populations infecting berries and provide a foundation for improved disease management.

 

Contact information: Dr. Dalphy Harteveld, email: doc.harteveld@wsu.edu, phone: 360-421-1598, address: WSU Mount Vernon Research and Extension Center, 16650 State Route 536, Mount Vernon, WA 98273 and Dr. Tobin Peever, email: tpeever@wsu.edu, phone: 509-335-3754, address: Department of Plant Pathology, WSU, Pullman, WA 99164-6430.

 

References

1M. Asadollahi, E. Fekete, et al. ‘Comparison of Botrytis cinerea populations isolated from two open-field cultivated host plants’, Microbiological Research, 168 (2013), 379-88.

 

2E. P. Dashwood, and R. A. Fox, ‘Infection of flowers and fruits of red raspberry by Botrytis cinerea’, (Oxford, UK: 1988), pp. 423-30.

 

3M. A. Ellis, ‘Botrytis fruit rot “Gray Mold” of strawberry, raspberry and blackberry’, Fact Sheet: Agriculture and Natural Resources 2008.

 

4P. A. G. Elmer, and T. J. Michailides, ‘Chapter 14 Epidemiology of Botrytis cinerea in orchard and vine crops’, in Botrytis: Biology, Pathology and Control, ed. by Y. Elad (Boston, USA: Kluwer Academic Publishers, 2004).

 

5J. Elmhirst, Crop profile for raspberry in Canada (Ontario, Canada: Pest Management Centre, 2007), p. 63.

 

6E. Fournier, Y. Brygoo, T. Giraud, and C. Albertini, ‘Partition of the Botrytis cinerea complex in France using multiple gene genealogies’, Mycologia, 97 (2005), 1251-67.

 

7W. R. Jarvis, ‘The dispersal of spores of Botrytis cinerea Fr. in a raspberry plantation’, Transactions of the British Mycology Society, 45 (1962), 549-59.

 

8R. Kollanyi, ‘Responses of red raspberry cultivars and selections to Botrytis cinerea infection of canes’, Acta Horticulturae, 183 (1986), 143-50.

 

9R. J. McNicol, B. Williamson, and A. Dolan, ‘Infection of red raspberry styles and carpels by Botrytis cinerea and its possible role in post-harvest grey mould’, Annals of Applied Biology, 106 (1985), 49-53.

 

10J. W. Pscheidt, and C. M. Ocamb, senior editors. Pacific Northwest Plant Disease Management Handbook (Corvallis, Oregon: Oregon State University, 2014). http://pnwhandbooks.org/plantdisease/

 

11S. A. Rivera, J. P. Zoffoli, and B. A. Latorre, ‘Infection risk and critical period for the postharvest control of gray mold (Botrytis cinerea) on blueberry in Chile’, Plant Disease, 97 (2013), 1069-74.

 

12S. Saito, T. J. Michailides, and L. Xiao, ‘First report of Botrytis pseudocinerea causing gray mold on blueberry in North America’, Plant Disease, 98 (2014), 1793.

 

13R. W. S. Weber, ‘Resistance of Botrytis cinerea to multiple fungicides in northern German small-fruit production’, Plant Disease, 95 (2011), 1263-69.

 

14B. Williamson, and D. L. Jennings, ‘Resistance to cane and foliar diseases in red raspberry (Rubus idaeus) and related species’, Euphytica, 63 (1992), 59-70.

 

15B. Williamson, R. J. McNicol, and A. Dolan, ‘The effect of inoculating flowers and developing fruits with Botrytis cinerea on post-harvest grey mould of red raspberry’, Annals of Applied Biology, 111 (1987), 285-94.

 

16B. Williamson, B. Tudzynski, P. Tudzynski, and J. A. L. Van Kan, ‘Botrytis cinerea: The cause of grey mould disease’, Molecular Plant Pathology, 8 (2007), 561-80.

 

17J. A. T. Woodfor, B. Williamson, and S. C. Gordon, ‘Raspberry beetle damage decreases shelflife of raspberries also infected with Botrytis cinerea‘, Acta Horticulturae 585 (2002), 423-26.

 

 

Figure 2 and 3. Botrytis fruit rot symptoms on blueberry. Photos Dalphy Harteveld and Olga Kozhar, WSU

Figure 4. Raspberry cane Botrytis symptom. Photo Dalphy Harteveld, WSU

Figure 5 and 6. Botrytis fruit rot symptoms on raspberry. Photos Dalphy Harteveld, WSU

 

Figure 7. Botrytis sclerotia (black compact mass) and mycelium (white) on agar medium. Photo Dalphy Harteveld, WSU

 

Figure 8 and 9. Botrytis sporulation structures (conidiophores) and spores (conidia) produced on a blueberry leaf. Photos Dalphy Harteveld, WSU

Figure 10. A moist environment induces Botrytis infections. Photo Dalphy Harteveld, WSU

 

Figure 11. Germinated Botrytis cinerea spore in agar medium. Photo Dalphy Harteveld, WSU