Diseases of blueberry, in particular V. corymbosum, caused by P. cinnamomi have long been reported from all over the world. First reports from the U.S. date back to the 1970s (Sterne 1982), and the disease has since been reported from South America, Asia and Europe (Tamietti 2003; Larach et al. 2009; Orlikowski et al. 2015; Lan et al. 2016; Huarhua et al. 2018). While in 2010 P. × cambivora was isolated from a young plantation of V. ovata in Germany (Jung et al. 2016), so far no incidence of Phytophthora spp. in general and P. cinnamomi in particular on V. corymbosum has been reported from Germany.
In the present study, P. cinnamomi and P. cactorum were isolated from the rhizosphere of declining plants of V. corymbosum in a “pick-your-own” berry farm in Southern Germany suffering from symptoms like wilting and yellowing of foliage, dieback of twigs and a severe reduction of the root system. Phytophthora cinnamomi was also recovered from V. corymbosum plants purchased from a commercial nursery in Northern Germany. Both P. cinnamomi and P. cactorum proved to be aggressive to V. corymbosum in an underbark inoculation assay.
Phytophthora cinnamomi is undoubtedly the most notorious globalised plant pathogen with a confirmed host range of almost 5,000 plant species (Erwin and Ribeiro 1996; Hardham and Blackman 2018). The origin of P. cinnamomi lies in Southeast Asia where both mating types A1 and A2 co-occur in a balanced ratio (Ko et al. 1978; Jung et al. 2020). The global epidemic is driven by two clonally spreading genotypes of the A2 mating type (Engelbrecht et al. 2017; Socorro-Serrano et al. 2019). Based on old reports of typical ink disease symptoms of Castanea sativa in Portugal, P. cinnamomi is suspected to have been introduced to Southern Europe in the early 1800s (Crandall et al. 1945). Mating type A2, in particular, is generally considered to be more adapted to warmer regions, suffering from, or unable to survive, severe winter frost (Erwin and Ribeiro 1996; Jung et al. 2020). Accordingly, only few records of this pathogen to occur in Germany exist, mostly from nurseries (Jung et al. 2016). Zinkernagel and Kröber (1978) already suggested that P. cinnamomi can tolerate winter temperatures in Germany in climatically favoured areas. However, with a changing climate and rising temperatures on a global scale, a range expansion of the pathogen to regions previously too cold for its survival can be expected (Brasier and Scott 1994; Bergot et al. 2004; Burgess et al. 2017). Indeed, there are a number of recent reports indicating that P. cinnamomi will increasingly be able to thrive in Central Europe under outdoor conditions. Recently, P. cinnamomi was detected in C. sativa stands in SW Germany, a region known for its mild climate and comparably high mean winter temperatures, constituting its first detection in a forest stand in Germany. Remarkably, the affected trees originated from natural regeneration and had no direct connection to a nursery (Peters et al. 2019). In 2015 and 2017, P. cinnamomi was isolated from bleeding stem cankers of mature Juglans regia in Austria and Araucaria araucana in Germany, respectively (T. Jung, T. Cech and T. Corcobado, unpublished results). In Poland, P. cinnamomi was found causing a decline of a Quercus robur stand (Oszako and Orlikowski 2005). The present report provides additional evidence that this pathogen is increasingly able to survive Central European winter, in particular when severe frost events are lacking, causing severe disease symptoms in the field. The affected blueberry stand in Lower Bavaria was established two years before the pathogen’s detection. Assuming that P. cinnamomi was already present in the nursery plants at the time of planting, the pathogen had already survived two winter periods in a region not known for having mild winters. Mean winter minimum temperatures in the region in 2018–2020 have been considerably higher than the long-term average (1971–2000) (www.wetter-by.de).
Phytophthora cactorum is another species frequently detected in nurseries all over Europe. It is well established in Central Europe and has been found associated with many different woody hosts, both in nurseries and in forest stands (Jung et al. 2016). An association with highbush blueberry has not been reported from anywhere in the world yet. However, according to the results of the twig inoculation test and the disease incidence in the stand, P. cactorum appears to be similarly aggressive as P. cinnamomi. However, while the virulence of P. cinnamomi to highbush blueberry is undoubted and disease aetiology well understood, for P. cactorum a soil infestation test is needed to finally confirm its aggressiveness and pathological importance.
Together with the well-documented susceptibility of V. corymbosum to P. cinnamomi and its frequent association with several other Phytophthora spp. in European nurseries (Jung et al. 2016), the results of the present study suggest that V. corymbosum (just like Vaccinium spp. in general and other members of the Ericaceae) is susceptible to a range of Phytophthora species, while at the same time Vaccinium nursery stock might be heavily infested with Phytophthora spp. The latter was impressively demonstrated by the isolation of P. cinnamomi from young V. corymbosum plants purchased during the present study from a commercial nursery. In accordance with results from a Europe-wide study on ubiquitous Phytophthora infestations of nursery stock, a widespread contamination of V. corymbosum nursery plants and beds with Phytophthora spp. can be assumed. Therefore, newly established blueberry farms are in danger of experiencing severe disease problems when using these plants. Interestingly, in that study, over all nursery stands high proportions of the > 1,800 Phytophthora isolates belonged to either P. cinnamomi or P. cactorum (Jung et al. 2016).
Although infestation of the affected “pick-your-own” berry stand via re-circulated irrigation water originating from a natural spring, substrates or other sources, such as strawberry plants growing nearby, cannot be excluded, it seems likely that the pathway of both Phytophthora pathogens into the stand was via infested nursery stock. Being soilborne primary pathogens, P. cactorum and P. cinnamomi do not thrive in aquatic ecosystems. In numerous surveys in various countries, P. cinnamomi could not be isolated from streams and waterbodies even when it was commonly found in the soils surrounding the waterbodies (Hüberli et al. 2013; Shrestha et al. 2013; Jung et al. 2020). With a changing climate and, in particular, increasingly milder winter temperatures, the risk of nursery-transmitted, invasive, exotic Phytophthora species to become established in outdoor agricultural, horticultural or silvicultural stands in temperate zones is significantly increasing (Brasier and Scott 1994; Bergot et al. 2004; Jung et al. 2016). Perhaps the most notorious candidate species is the (sub) tropical and Mediterranean pathogen P. cinnamomi which currently appears to be on its way to become a serious threat to Central European fields, gardens and forests.