Exobasidium Leaf and Fruit Spot of Blueberry in the Southeastern United States W.O. Cline , M.T. Brewer , P.M. Brannen , H. Sche
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Exobasidium leaf and fruit spot of blueberry in the southeastern United States W.O. Cline1, M.T. Brewer2, P.M. Brannen2, H. Scherm2 1Department of Plant Pathology, North Carolina State University, Raleigh 27695 2Department of Plant Pathology, University of Georgia, Athens 30602 Subject category: Fungal Pests of Blueberry Abstract First identified in 1997, Exobasidium leaf and fruit spot has emerged as an important disease of both rabbiteye and highbush blueberry in the southeastern US. Yield losses up to 60% have been recorded on ‘Premier’ rabbiteye blueberry. The pathogen, recently described as Exobasidium maculosum M. T. Brewer, is a species unique to the region. The life cycle of the pathogen is currently not known. Infection of leaves and fruit appear to occur simultaneously or in close sequence in early spring, with leaf symptoms appearing in spring and berry symptoms most obvious when fruit ripens. Berry infections appear as green unripe spots on otherwise ripe, blue fruit. Leaf infection produces round, pale-green spots averaging 7-8 mm in diameter that are white when viewed from below. Symptoms do not occur on later leaves, suggesting a springtime, mono- or oligocyclic disease cycle. Disease intensity appears to be highest in wet fields with dense growth and poor air circulation. Fungicides applied beginning at bud break are effective in reducing disease intensity, but there is evidence of resistance to some fungicides. Single, delayed-dormant applications of lime-sulfur have provided significant control in initial trials in Georgia. Index words: plant disease, fungus, plant pathology, small fruit, Ericaceae Introduction Exobasidium leaf and fruit spot caused by Exobasidium maculosum is a once-rare problem that is now common in the southeastern US. Initially thought to be stinkbug injury, the cause was first identified as a plant-parasitic fungus in North Carolina (Cline, 1998) and at that time was identified as E. vaccinii sensu lato. More recent work using phylogenetic analysis led to identification as E. maculosum, a new species (Brewer et al., 2014). The life cycle of the pathogen is currently not known. It produces both sexual basidiospores and asexual conidia, the latter of which are yeast-like and possibly serve as the oversummering and overwintering stages of the pathogen. Infection of leaves and fruit appear to occur simultaneously or in close sequence in early spring, with leaf symptoms appearing in the spring (Fig. 1) and berry symptoms becoming most obvious when fruit ripens (Fig. 2). Berry infections appear as green unripe spots on otherwise ripe, blue fruit. Leaf infection produces round, pale-green spots averaging 7-8 mm in diameter that are slightly raised and white when viewed from below (Fig 3). During mid- summer, leaf spots become necrotic and develop a shothole-like appearance (Fig. 4). Symptoms do not occur on later leaves, suggesting a springtime, mono- or oligocyclic disease cycle, and a pathogen that is epiphytic rather than systemic in the host. Disease incidence appears to be highest in wet fields with dense growth and poor air circulation. Leaf infection is most severe in the lower part of the plant, whereas fruit infection is most severe in the interior of the bush, compared with fruit on more exposed shoots. The disease is increasing in frequency and severity, but fungicides show promise for control (Ingram and Braswell, 2008; Brannen et al., 2014; Scherm et al., 2014; Cline and Bloodworth, 2014). Figure 1. Exobasidium symptoms on blueberry leaves (upper surface) May 24th in North Carolina. Figure 2. Infected ripe berries with highly visible green spots, cultivar Legacy. Figure 3. White fungal growth visible on the underside of leaf lesions. Figure 4. Old lesions become necrotic and may fall out, leaving holes in leaves Other Exobasidium species Many Exobasidium species are reported as parasites of the Ericaceae and related families. They are usually specialized to single or closely related species, with common signs including the production of a white hymenium over the infected area. This thin layer of fungal growth produces characteristic basidia and basidiospores that can be used to identify the genus. Symptoms on various hosts include leaf and stem galls, red shoots, and spots. Infections may be either local or systemic. A frequent symptom of Exobasidium infection is swelling, distortion and enlargement of the infected plant part (hypertrophy and hyperplasia) and this too is often diagnostic. The taxonomy of this species is largely unexplored. There are at least 11 species reported in the US, but host ranges may overlap and descriptions are often antiquated. Exobasidium vaccinii alone is reported on 21 host species (source: Index Fungorum). Previous reports on blueberry Previously described Exobasidium diseases of blueberry include red leaf, a systemic disease of lowbush and northern highbush blueberries (Caruso and Ramsdell, 1995) often referred to as being caused by E. vaccinii, but likely a different species. Red leaf is not known to occur in the Southeast, and is not closely related to the E. maculosum species reported herein as causing spots in Georgia, Mississippi and North Carolina. There is also a report of Exobasidium leaf spot of lowbush blueberry, and in this case the symptoms are very similar to those of E. maculosum in the Southeast. It was first described in Nova Scotia in 1997 (Nickerson and Vander Kloet). The species causing the leaf spot on lowbush blueberry is closely related, but not identical, to E. maculosum (Brewer et al. 2014). Defining Exobasidium maculosum The unique characteristics shown in the images above suggested a previously undescribed species. Other evidence supporting species status comes from the study by Brewer et al. (2014), whereby isolates were collected from symptomatic plant tissue in several states and from highbush, rabbiteye and hybrid blueberry cultivars, for comparison with each other and with known isolates of Exobasidium species from other blueberry, cranberry and related hosts in other parts of the US. The isolates from the southeastern US sites were unique, different from those collected in other regions and from those on other Vaccinium host species. A full description of the fungus including consensus tree phylogenetic analysis, and images including scanning electron micrographs of basidia and basidiospores, was published earlier this year (Brewer et al., 2014). Fungicide trials in 2012-2013 Fungicides were evaluated for control of Exobasidium leaf and fruit spot control both in Georgia and North Carolina. For a complete description of materials and methods, see Brannen et al., 2014; Scherm et al., 2014; Cline and Bloodworth, 2014. All trials were conducted on rabbiteye (Vaccinium virgatum) cultivars. Georgia -- Fungicide trials were conducted in Bacon County on two grower sites with different cultivars (Premier and Tifblue). Treatment factors included application timing and fungicide. Application timing included early-, mid-, and full-season blocks, factored across the fungicides Captan, Indar, Pristine, and an untreated check. The early-season block corresponded to pre- bloom and bloom applications, whereas the mid-season block included petal fall and cover sprays. A commercial airblast sprayer was used at 40 gallons per acre. There was also a lime sulfur application at delayed dormant, and this was applied once in 50 gallons per acre of water, as a stand-alone treatment in early February. North Carolina – A grower site in Bladen County, cultivar Premier, was selected due to a history of severe Exobasidium symptoms and little or no previous fungicide use. The trial compared the fungicides Indar, Pristine, Captan and Elevate with an untreated check. Five sprays of each fungicide treatment were applied, at bud swell (28 Feb), bud break (13 Mar), pink tip (27 Mar), early bloom (3 Apr) and late bloom (10 Apr). A backpack sprayer was used at 25 gallons per acre. Leaf spots were evaluated on 14 May, and fruit infection at harvest on 20 Jun. Results Georgia – The full Captan schedule performed best (8 applications), although lime sulfur (1 application) and Captan (5 early applications) gave statistically equivalent control of both leaf and fruit spots (Figs. 5 and 6). Indar was also effective in the full schedule, giving acceptable control under this regimen. Pristine was not effective in the ‘Tifblue’ trial (data not shown) and was also less effective than other fungicides in the ‘Premier’ trial. North Carolina -- All standard fungicides were significantly better than the untreated control (Tables 1 and 2) and were not different from each other statistically. Pristine performed well in NC in this previously untreated field. Early sprays beginning in late February were targeted based on earlier data from GA, and again the early sprays appear to be critical for successful control. Based on lime-sulfur data from GA, a single delayed-dormant application of lime-sulfur was tested in NC in the spring of 2014, and has performed quite well (data not shown). 0.6 0.5 a a 0.4 0.3 b b b 0.2 bc cd 0.1 cd cd cd d Incidenceof symptomatic leaves 0.0 IndarL IndarF IndarE CaptanL CaptanF CaptanE PristineL PristineF PristineE Untreated Lime sulfur Early Mid-season Full Figure 5. Incidence of symptomatic leaves on ‘Premier’, Bacon Co. GA, 2013. 0.4 a a 0.3 0.2 b b bc bcd bc 0.1 cde cde de e Incidence ofsymptomatic fruit 0.0 IndarL IndarF IndarE CaptanL CaptanF CaptanE PristineL PristineF PristineE Untreated Lime sulfur Early Mid-season Full Figure 6. Incidence of symptomatic fruit on ‘Premier’, Bacon Co. GA, 2013. Table 1. Efficacy of fungicides in reducing incidence and severity of Exobasidium on blueberry leaves of rabbiteye blueberry cultivar Premier in NC (Bladen County) in 2013. Leaf Symptoms Treatment and Rate/A % leaves with one Average no. of spots or more spots per leaf Untreated check 89.8 a* 7.81 a Indar 2F 6 fl oz 3.8 b 0.03 b Pristine 38 WG 23 oz 5.2 b 0.06 b Captan 80WDG 3.12 lb 1.8 b 0.01 b Elevate 50WDG 1.5 lb 4.0 b 0.04 b *Means within a column followed by the same letter are not significantly different, LSD, (α=0.05).