First report of Golovinomyces cichoracearum sensu lato on Cannabis sativa in Israel

In recent years, the use of cannabis (Cannabis sativa) has gained popularity for medical and other purposes, and its cultivation worldwide has expanded rapidly (Ruchlemer et al., 2015; Jerushalmi et al., 2020).

During April 2020, symptoms of powdery mildew were observed on commercially cultivated medical cannabis in the greenhouses of several farms in Israel, causing serious concerns, since affected material was discarded, deemed unfit for medical consumption. Symptoms initially appeared as small, white circular patches of epiphytic mycelia with conidia on the upper sides of mature leaf surfaces, similar to those described by Pépin et al. (2018). As the disease progressed, colonies expanded in size, coalescing and covering entire leaf surfaces, succulent stems and inflorescences (Fig. 1). Conidia were produced in chains on conidiophores that were single and erect, unbranched and cylindrical, arising from the colonies (Fig. 2). The conidia were hyaline, cylindrical to ellipsoid in shape, measuring 38.8-45.4 µm in length and 15.9-21.1 µm in width (Fig. 3). No chasmothecia were observed.

The pathogen was identified by molecular analyses and sequencing of the internal transcribed spacer (ITS) region of rDNA following amplification by PCR using ITS1 and ITS4 primers. Sequences were deposited in GenBank (Accession Nos. MT791387- MT791389), and BLAST analyses revealed 100% identity to Golovinomyces cichoracearum sensu lato, as recently reported from cannabis plants in Canada (Pépin et al., 2018). Due to its complex taxonomy, G. cichoracearum is considered a species complex, composed of specialised as well as less specialised races, taxa or even cryptic species.

Pathogenicity of the Israeli isolate was confirmed following inoculation of eight-week-old healthy C. sativa cv. 'BB 734' from the Agricultural Research Organization (Jerushalmi et al., 2020), by brushing conidia and pressing naturally infected leaves onto healthy ones. Inoculated plants were maintained at 22 ±2°C in a growth chamber under  a photoperiod of 18 hr light (3000 lux) and 6 hr dark. Powdery mildew symptoms developed on mature leaves from two to five weeks post-inoculation, whereas non-inoculated plants remained healthy (Fig. 4).

Until the recent discovery of Golovinomyces cichoracearum sensu lato, on C. sativa from Canada, powdery mildew on cannabis was thought to be caused by Sphaerotheca macularis and Leveillula taurica (McPartland et al., 2017). The Golovinomyces sp. isolate that we obtained shared 100% identity with the strain from Canada and to the best of our knowledge, is the first report from Israel of this species on C. sativa. Golovinomyces cichoracearum has been reported from Israel on lettuce and other hosts, particularly belonging to the Asteraceae, however no molecular confirmation or pathogenicity tests were done (Chorin & Palti 1962; Voytyuk et al., 2006). The disease has already spread to three of the largest medical cannabis facilities over the past year and there is an imminent threat of further dissemination. The appearance of powdery mildew in these facilities is of concern and will require appropriate management strategies to ensure procurement of healthy and safe products for use by predominantly immunocompromised patients.