Occurrence of powdery mildew caused by Erysiphe corylacearum on Hazelnuts in Israel.

Hazelnut (Corylus avellana L) is an emerging crop in Israel, primarily cultivated as a host plant to establish truffle plantations through symbiosis with ectomycorrhizal fungi. A significant damage and yield reduction is caused by the prevalent occurrence of powdery mildew in hazelnut trees (Sezer et al., 2017). Until recently, Phyllactinia guttata was considered the primary pathogen in Western Asia, the Caucasus region, and Europe (Abasova et al. 2018; Arzanlou et al. 2018; Mezzalama et al. 2021). However, in the last years, a new destructive species Erysiphe corylacearum has been identified as the pathogen of powdery mildew on hazelnuts in these regions (Meparishvili et al. 2019; Mezzalama et al. 2021; Kalmár et al. 2022; Zajc et al. 2023). In May 2022, powdery mildew symptoms were observed on hazelnut plants in the Ein-Zivan truffle plantation, gardens of Merom-Golan, and the adjacent garden of the packing house Pri-Beresheet in the northern Golan region of Israel. Symptoms were observed on the abaxial and adaxial leaf surfaces, fruits, and husks. Disease incidence and severity ranged between 30-70% and 5-90%, respectively. Disease severity was significantly greater on the leaves of the offshoots compared to those on the tree canopy. Morphological characterization of leaf samples from ten different trees showed the following characteristics: hyphal appressoria were lobed, solitary, 1-4 µm in diameter; mycelium was amphigenous, hyaline, and septate; conidiophores vertically elevated from the mycelium 50- 80 µm long. Conidia (n= 30) on conidiophores were hyaline, ellipsoid to ovoid, 24 - 34 µm long and 15.5 - 23 µm wide. Chasmothecia in several maturation degrees appeared in October on both sides of the leaves. They were spherical (n= 30) 86 - 125 µm in diameter, with 7 - 14 aseptate straight appendages, 67 - 96 µm long, 4.9 - 7.1 µm wide, dichotomous branched at the end 42 - 56 µm wide. In each chasmothecia, there were 3-5 asci (n=30) with a width of 38 - 43 µm and a length of 48-64 µm of oval-ellipsoid shape. Asci contained 4-8 ascospores (n=30), 18 - 26 µm long and 11 - 15.5 µm wide. A pathogenicity test was conducted to fulfill Koсh's postulates. Both detached leaves and plants of C. avellana were artificially infected by brushing conidia from infected leaves. Inoculated leaves in Petri dishes on 2% water agar (n= 5), and plants (n= 5) were incubated under 25°C and 12-h photoperiod/day. Untreated leaves and plants served as control. Typical symptoms appeared on the upper surface of the leaves within 7-10 days after inoculation. No symptoms were found on untreated control plants or detached leaves. The fungus isolated from the inoculated leaves was morphologically identical to the original isolates from natural diseased plants. DNA was extracted and the rDNA internal transcribed spacer region of five isolates originated from leaves of the tree canopy and offshoots was amplified using primers ITS1 and ITS4, and sequenced. BLAST analysis of 595 bp fragments (all identical and represented by isolate Cora1, GenBank Accession No. OR752437) showed 99% identity to ITS rDNA sequences of E. corylacearum from Georgia (MK157199) and 100% identity to isolates from Azerbaijan, Turkey and Italy (LC270863, KY082910 and MW045425, respectively) and only 83% similarity to P. guttata (accession number AB080558). To the best of my knowledge this is the first report on E. corylacearum causing powdery mildew in Israel. Future control measures to manage the disease on hazelnuts in truffle plantations in Israel should be considered.

Mixtures of Macro and Micronutrients Control Grape Powdery Mildew and Alter Berry Metabolites.

Powdery mildew caused by the fungus Erysiphe necator is a major grape disease worldwide. It attacks foliage and berries and reduces yield and wine quality. Fungicides are mainly used for combating the disease. Fungicide resistance and the global requisite to reduce pesticide deployment encourage the use of environment-friendly alternatives for disease management. Our field experiments showed that the foliar application of the potassium phosphate fertilizer Top-KP+ (1-50-33 NPK) reduced disease incidence on leaves and clusters by 15-65% and severity by 75-90%, compared to untreated vines. Top-KP+ mixed with Nanovatz (containing the micronutrients boron (B) and zinc (Zn)) or with TruPhos Platinum (a mixture containing N, P2O5, K2O, Zn, B, Mg, Fe, Mn, Cu, Mo, and CO) further reduced disease incidence by 30-90% and disease severity by 85-95%. These fertilizers were as effective as the fungicide tebuconazole. Tank mixtures of fertilizers and tebuconazole further enhanced control efficacy in the vineyards. The modes of action of fertilizers in disease control were elucidated via tests with grape seedlings, microscopy, and berry metabolomics. Fertilizers applied preventively to the foliage of grape seedlings inhibited powdery mildew development. Application onto existing mildew colonies plasmolyzed mycelia and conidia and arrested the development of the disease. Berries treated with fertilizers or with a fungicide showed a significant increase in anti-fungal and antioxidant metabolites. Twenty-two metabolites, including non-protein amino acids and carbohydrates, known for their anti-fungal and bioactive effects, were significantly upregulated in grapes treated with fertilizers as compared to grapes treated with a fungicide, suggesting possible indirect activity against the pathogen. Esters and organic acids that contribute to wine quality were also upregulated. We conclude that integrating macro and micronutrients in spray programs in commercial vineyards shall control powdery mildew, reduce fungicide deployment, delay the buildup of fungicide resistance, and may improve wine quality.

ß-Aminobutyric Acid Induced Resistance against Alternaria Fruit Rot in Apple Fruits.

Fruit body rot and calyx rot caused by Alternaria alternata f. sp. mali is an important disease of apple worldwide. The disease has recently become severe in cv. Pink Lady apple in Israel to an extent that has never been reported elsewhere in the world. No alternative control measures of the disease except fungicides are known. Here, we show for the first time that dl-ß-aminobutyric acid (BABA) induces resistance against Alternaria fruit rot (AFR) in apple fruits in the laboratory and in the orchard. AFR was inhibited in fruits treated with BABA of 1000 µg/mL. BABA did not inhibit spore germination or mycelial growth of the pathogen in vitro (up to 2000 µg/mL). It was most inhibitory when applied 4 days prior to inoculation of detached fruits. BABA inhibited AFR also curatively when applied at 24 h post inoculation. Five other isomers of aminobutyric acid failed to protect the fruits from rot formation. Three field trials in commercial apple orchards proved that BABA was as protective against AFR as the commercial standard fungicidal mixture of azoxystrobin and difenoconazole. This research suggests that BABA may serve as a resistance inducer in apple against AFR. It can be used as an adequate alternative to the currently used fungicides or integrated in disease management programs to reduce fungicide load and buildup of fungicide resistance.

Population structure of Erysiphe necator on domesticated and wild vines in the Middle East raises questions on the origin of the grapevine powdery mildew pathogen.

Plant pathogens usually originate and diversify in geographical regions where hosts and pathogens co-evolve. Erysiphe necator, the causal agent of grape powdery mildew, is a destructive pathogen of grapevines worldwide. Although Eastern US is considered the centre of origin and diversity of E. necator, previous reports on resistant native wild and domesticated Asian grapevines suggest Asia as another possible origin of the pathogen. By using multi-locus sequencing, microsatellites and a novel application of amplicon sequencing (AmpSeq), we show that the population of E. necator in Israel is composed of three genetic groups: Groups A and B that are common worldwide, and a new group IL, which is genetically differentiated from any known group in Europe and Eastern US. Group IL showed distinguished ecological characteristics: it was dominant on wild and traditional vines (95%); its abundance increased along the season; and was more aggressive than A and B isolates on both wild and domesticated vines. The low genetic diversity within group IL suggests that it has invaded Israel from another origin. Therefore, we suggest that the Israeli E. necator population was founded by at least two invasions, of which one could be from a non-East American source, possibly from Asian origin.

Phenology-Based Management of Alternaria Fruit Rot in Pink Lady Apples.

Fruit body rot and calyx rot caused by Alternaria alternata f. sp. mali has recently become a severe disease of Pink Lady apple in Israel. Severe fruit rot caused by A. alternata f. sp. mali has not been reported elsewhere in the world, and control measures are not currently known. Our objective was to determine the peak periods of susceptibility and develop methods to manage the disease by timing fungicide applications according to fruit phenological stage. We determined the relationship between fruit phenological stage and rot susceptibility by (i) monitoring the appearance of first fruit symptoms in the orchard; (ii) inoculating detached and attached fruit in the laboratory and orchard, respectively, at various time intervals after petal fall; and (iii) starting fungicide applications at various time intervals after petal fall. Fruit of Pink Lady acquired susceptibility to the disease at about 115 days after petal fall (DAPF) when reaching a diameter of ≥55 mm. Based on these findings, a new spray strategy was adopted involving a limited number of 4 to 6 foliar sprays of azoxystrobin + difenoconazole or tebuconazole + captan, or their alternation, starting at 115 DAPF. This strategy provided excellent control of both body rot and calyx rot in Pink Lady apple fruit in Israel.