You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Management of Bacterial Diseases of Hazelnut: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Peter Tang and Version 1 by Rosario Nicoletti.

The cultivation of hazelnut (Corylus avellana) has expanded in several areas of Europe, Asia, Africa, and North and South America following the increased demand for raw materials by the food industry. Bacterial diseases caused by Xanthomonas arboricola pv. corylina and Pseudomonas avellanae are threats of major concern for hazelnut farmers. These pathogens have been controlled with copper-based products, which are being phased out in the European Union. Following the need for alternative practices to manage these diseases, some progress has been achieved through the exploitation of the plant’s systemic acquired resistance mechanisms, nanoparticle technology, as well as preventive measures based on hot water treatment of the propagation material.

  • nut crops
  • bacterial diseases
  • endophytic microorganisms
  • plant growth promoting bacteria
  • sustainable disease management

1. Introduction

Hazelnut (Corylus avellana L.), belonging to the Betulaceae family, is a deciduous tree native to Europe and Asia, where it is widespread as an understorey species in mixed forests. Hazelnut is the fifth most important tree nut in the world, with a total cultivated area of about 1,027,000 ha and a global production of 1.1 million metric tons [1]. It is mostly cultivated in Mediterranean countries, with Turkey (665,000 tons) and Italy (140,560 tons) providing about 80% of the world production; however, following a steady increase in demand from the food industry, in recent years, hazelnut cultivation has spread to new growth areas, including the southern hemisphere, characterized by a humid temperate climate [2]. In the Mediterranean area, these conditions basically occur in the highlands at altitudes between 500 and 1500 m, where the plant is mostly cropped in semi-extensive production systems.
The crop product is represented by the nutrient-rich kernels, protected by a dark brown fibrous perisperm and a woody shell, which are widely used in confectionery, bakery, dairy, chocolate and candy products. Their intrinsic nutritional quality has gained attention for their beneficial effects on human health. In fact, hazelnut kernels are an energy-rich food that can play an important dietary role based on their high-value lipids, proteins, carbohydrates, dietary fiber, vitamins, minerals and antioxidant phenolics [2,3][2][3]. Several studies addressed the phenolic composition in the seed tegument of different hazelnut cultivars, highlighting differences in quantitative content [4,5,6,7][4][5][6][7]. Lipids are considered the main chemical components that contribute to the quality and storability of nuts and derived products [8,9][8][9].
In addition to food use, the hazelnut has recently disclosed medicinal properties. In fact, leaves and shells have been reported to contain taxol, a blockbuster antitumor product originally found as a secondary metabolite in yew trees (Taxus spp.) [12][10]. The availability of massive quantities of these byproducts has introduced perspectives for exploiting an alternative economic source of this drug, which could represent an integration of incomes for hazelnut farms [13,14][11][12] (Figure 1).
Figure 1.
The multifaceted interaction between hazelnut and bacteria.

2. Bacterial Diseases of Hazelnut

2.1. Bacterial Blight

Bacterial blight symptoms were first described in Oregon (USA) on Corylus maxima [15][13], and the related pathogen was named Xanthomonas corylina [16][14]. Afterward, this disease was recorded in Yugoslavia [17][15], Italy [18][16], Turkey [19][17], France [20][18], Russia [21][19], United Kingdom [22][20], Australia [23][21], Chile [24][22], Iran [25][23] and Poland [26][24]. Nowadays, Xanthomonas arboricola pv. corylina (syn. X. campestris pv. corylina) presents a worldwide distribution, with some genetic variation demonstrated by the existence of several clades and strain clusters [27,28,29][25][26][27]; therefore, it maintains an A2 quarantine microorganism status for the European Plant Protection Organization (EPPO), and its possible presence in plant propagation material is monitored in the territory of the European Union [30][28].
The pathogen enters trees via pruning cuts, wounds, fresh leaf scars and frost-injured tissues. Generally, its spread is higher in wet periods with temperatures above 20 °C. Symptoms include brown shriveled buds, brown leaf spots and reddish-brown slightly sunken cankers on the bark (Figure 2). The main mode of spread is on infected planting material; in fact, the potential for natural spread is relatively low, although seeds from fruits picked on infected trees can produce infected seedlings [27,31][25][29]. Recently, bacterial blight has been reported as a re-emerging disease in young hazelnut orchards in Oregon, following a rapid increase in acreage derived from a renewed development of the hazelnut industry in the United States [28][26].
Figure 2.
Typical symptoms induced by
Xanthomonas arboricola
pv.
corylina
on husks (
A
) and leaves (
B
).
At the molecular level, the population structure of X. a. pv. corylina shows some variation that is not necessarily related to the geographic origin of the strains [26,32,33][24][30][31]. Some differences also exist concerning the effector repertoire of the type III secretion system. The type-strain, isolated from C. maxima, and another strain obtained from an ornamental Corylus species, indeed, do not possess the xopH effector [34][32]. Moreover, the complete genome of three strains, respectively isolated in France, Poland and the United States, has been recently sequenced, and a single 24-k plasmid was found in two strains. In all strains, the copper resistance gene (i.e., copL) and operon (i.e., copAB), as well as other genes involved in resistance to the high concentration of copper (i.e., cutC and pCuAC), were also found [35][33].

2.2. Bacterial Canker

The first circumstantial description of the bacterial canker of hazelnut was carried out in Greece. The causal agent, a Gram-negative rod with one to four polar flagella, was identified as Pseudomonas sp., producing a blue-green diffusible fluorescent pigment, exhibiting oxidative metabolism of glucose, and inducing hypersensitive reaction on tobacco leaves [36][34]. It was proposed to represent a new pathovar of P. syringae, namely pv. avellanae [37][35]. This pathovar was subsequently isolated also in central Italy [38][36].
Before these reports, there were only two previous records concerning pseudomonads associated with hazelnut. The first one concerned a bacterium named Pseudomonas coryli, which was isolated from cankers and tumors from an old hazelnut tree in Poland; however, no adequate description and pathogenicity tests were reported [39][37]. Afterwards, a bacterial leaf spot of Corylus colurna caused by Pseudomonas colurnae was described in Illinois (USA) [40][38].
Characterization of strains that caused canker of hazelnut in Greece and Italy based on fatty acid and protein profiles, as well as 16S rRNA sequence analysis and percentage of DNA-DNA hybridization with other Pseudomonas strains, indicated that they are very distantly related to all pathovars of P. syringae examined, including pv. syringae. In addition, all other Pseudomonas species tested were closer to P. syringae than the bacterium-causing canker of hazelnut. Hence, P. s. pv. avellanae was proposed to represent a new species, namely P. avellanae [41][39]. From a taxonomic standpoint, the P. avellanae genomospecies also include pathogenic strains that infect Actinidia chinensis and Prunus avium [42][40]. The strains of this genomospecies show a restricted pathogenic aptitude, being capable of infecting solely the host plants from where they are isolated.
The extent of genetic variation found even within homogeneous groups of strains made it problematic to get to a reliable taxonomic placement [43][41]. Hence, a comprehensive study including 118 fluorescent pseudomonads associated with hazelnut decline was carried out, which differentiated two groups. The first group belonging to P. avellanae included strains isolated in northern Greece and central Italy, which do not have the syrB gene encoding for syringomycin production and are very virulent but pathogenically restricted to C. avellana. The second group, which proved to be mildly virulent for hazelnut, included other strains obtained from Piedmont, Campania, Latium, Sicily, and Sardinia, representing a distinct taxon closely related to P. s. pv. syringae [44][42]. A distinct pathovar inciting twig dieback only to hazelnut was later characterized from isolates collected in Piedmont and Sardinia. Both fatty acids and repetitive sequence-based PCR clearly discriminated these strains from other Pseudomonas species. Besides some nutritional tests differentiating them from related P. syringae pathovars, DNA sequencing indicated that they did not possess the syrB gene, unlike P. avellanae and P. s. pv. syringae [45][43]. As these strains represented a homogeneous group and a discrete phenom, the creation of a new pathovar named P. syringae pv. coryli was proposed [46][44].
The separate identity of several species and pathovars associated with hazelnuts [42,47][40][45] was also confirmed in a comprehensive revision of P. syringae [48][46], and the circumstantial finding that additional Italian strains responsible for the same symptoms were related to P. syringae induced to update the name P. syringae pv. avellanae with an emended description [49][47].
A comparison of the draft genomes of nine Pseudomonas strains isolated from symptomatic C. avellana trees was performed to identify common and distinctive genomic traits, which revealed two clearly distinct clusters corresponding to P. avellanae and P. syringae, with the latter including the pathovars avellanae, coryli and syringae. No indication of recombination between these two clusters was found. All nine strains presented a genomic island of approximately 20 kb, containing the hrp/hrc type III secretion system gene cluster. The type III secretion system effector repertoires were remarkably different in the two groups, with a higher number of effectors in P. avellanae. Homologue genes of the antimetabolite mangotoxin and ice nucleation activity clusters were only detected in all P. syringae pvs., whereas the siderophore yersiniabactin was only present in P. avellanae. Moreover, all nine strains have genes related to sucrose metabolism and pectic enzymes, while they do not have genes coding for indoleacetic acid (IAA) and anti-insect toxin [50][48]. The complete genome sequence of two P. avellanae isolates revealed that strains infecting hazelnut have a peculiar set of three type III secretion effectors, while P. avellanae strains infecting Prunus and Actinidia possess the genomic WHOP island that is relevant for the infection of woody hosts. Comparatively, the genome of P. syringae contains more sequences encoding for phytotoxin synthesis, the ice nucleation cluster, but fewer effectors. Coupled with previous observations, these findings support the conjecture that the convergence into the same host by the several Pseudomonas species and pathovars is possible due to different unrelated mechanisms of infection and virulence tools that could suppress the host defense mechanisms. The integration into their genomes of a horizontally acquired genomic island could drive their evolution, possibly enabling them to exploit new ecological niches [51][49].
During 2018 and 2019, a putative new pathovar was isolated in Iran. Based on phylogenetic analysis and phenotypic and pathogenicity characteristics, it is supposed to belong to Pseudomonas amygdali, hence provisionally named P. amygdali pv. corylicola. Symptoms observed in Iranian hazelnut orchards consisted of irregular reddish-brown necrotic spots surrounded by a yellow halo on the leaves and bracts, leading to wilting of leaves, defoliation and decay of branches [52][50].
Besides the known ways of transmission, such as penetration of leaf scars during autumn through rain and wind [44][42], Pseudomonas spp. have been found to be associated with adults of the lignicolous beetle Anisandrus dispar (Coleoptera, Scolytinae), both internally and as an external contaminant [53][51], calling for further assessments concerning the possible role of insect pests of hazelnut as vectors.
As mentioned above, for X. a. pv. corylina, P. avellanae is prescribed to be monitored at the introduction in the EU territory of plant material from some countries [30][28]. At a first glance, there are some similarities between the symptoms of bacterial blight and bacterial canker, with reference to shoots, twigs and stems. However, P. avellanae does not cause symptoms in leaves and husks [36][34] (Figure 3).
Figure 3. Disease symptoms incited by Pseudomonas spp.: sudden wilting in summer caused by P. avellanae (A); bark discoloration and swelling induced by P. avellanae on branch (B); longitudinal necrosis of wood caused by P. avellanae (C); twig dieback incited by P. syringae pv. coryli (D).

2.3. Other Bacterial Pathogens

In Chile, besides bacterial blight by X. a. pv. corylina and bacterial canker (reported as incited by P. s. pv. syringae), Agrobacterium tumefaciens has been mentioned as a bacterial pathogen of hazelnut [54][52]. In Poland, Pseudomonas fluorescens, Bacillus spp. and Erwinia spp. were recovered from diseased kernels and found to be able to infect young fruits [55][53].
This brief overview of hazel bacterial pathogens cannot overlook phytoplasmas. A few articles report on their finding and noxious impact on this crop [56,57,58,59,60,61][54][55][56][57][58][59]; however, this subject requires to be more specifically treated in a dedicated review, considering that it is basically connected with the insect vectors in terms of both spread and management [62,63][60][61].

3. Management of Bacterial Diseases of Hazelnut

Traditionally, bacterial and other cryptogamic diseases of hazelnut are supposed to be controlled through spray treatments based on copper compounds [64][62]. Either Bordeaux mixture, copper hydroxide, copper oxychloride or new formulations that contain micronized copper particles are sprayed at certain key periods to reduce the possibility of penetration in some points of entry explored by the pathogens, such as the leaf scars in autumn (P. avellanae) or leaf, bud and husk surface during spring (X. a. pv. corylina). In addition, copper compounds are also frequently used before or after some adverse climatic events, such as hail, frost and heavy rain, to protect the wounds caused by such events along the twigs or branches. Likewise, their use is suggested for disinfecting and protecting pruning wounds. The success of controlling these diseases through copper compounds mainly depends on the precise timing of distribution to prevent the colonization of the tree by the bacteria. In case of delay in the treatments and in the presence of the pathogen inoculum in the orchard, indeed, it becomes impossible to reach the internal tissues of the plant organ already colonized by the bacterial cells. A new approach to control P. avellanae was developed a couple of decades ago through the spray on the tree canopy of an activator of the plant defense mechanisms based on pathogenesis-related proteins, namely acibenzolar-S-methyl [65][63]. Through this approach, the disease is reduced by means of the systemic acquired resistance (SAR) mechanisms; in fact, the compound has no direct bactericidal activity but enhances the synthesis of proteins related to the defense against microbial pathogens. The compound is to be sprayed onto the tree canopy three times, once a month, starting from the leaf sprouting. Concerning bacterial blight, an innovative technology based on the utilization of cellulose nanocrystals obtained from pruning and shelling wastes has been shown to reduce severity without inciting any phytotoxic effect [66][64]. In nurseries, the occurrence of X. a. pv. corylina onto the buds of suckers can be limited through the application of hot water treatments [67][65], consisting in soaking the suckers in water for 30 min at a temperature ranging between 42 and 45 °C. This treatment can be applied prior to the sucker shipment.
The intensive use of copper products for more than one century has produced a negative impact on both human health and biodiversity. Throughout this long period, copper has massively contaminated the cultivated soils; in fact, Cu residues typically accumulate in the upper 15 cm of soil, leading to plant stress, reducing fertility, and decreasing microbiota diversity. By affecting organisms in the soil food web, copper negatively interferes with crop residue decomposition, nutrient storage and release, soil structure and stability, plant resistance against pathogens, and degradation or immobilization of pesticides and other pollutants. Besides the environmental risk, there is some concern for the repeated utilization of copper as the sole way to control hazelnut bacterial diseases, which could induce the development of tolerance or resistance, as already observed for X. a. pv. corylina [68][66].
For all these deleterious side effects, the maximum copper quantity allowed in plant protection has been successively restricted in Europe over the last decades; currently, it is limited by the European plant protection legislation to a maximum of 28 kg ha−1 over a period of 7 years (regulation EU 2018/1981). The final objective would be to phase copper fungicides out, as included in the list of candidates for substitution in the territory of the European Union (Part E of the Annex to Regulation 540/2011) [69][67].

References

  1. FAO. World Food and Agriculture-Statistical Yearbook; FAO: Rome, Italy, 2020; p. 366.
  2. Silvestri, C.; Bacchetta, L.; Bellincontro, A.; Cristofori, V. Advances in cultivar choice, hazelnut orchard management, and nut storage to enhance product quality and safety: An overview. J. Sci. Food Agric. 2021, 101, 27–43.
  3. Alasalvar, C.; Shahidi, F.; Liyanapathirana, C.M.; Ohshima, T. Turkish tombul hazelnut (Corylus avellana L.). 1. Compositional characteristics. J. Agric. Food Chem. 2003, 51, 3790–3796.
  4. Köksal, A.İ.; Artik, N.; Şimşek, A.; Güneş, N. Nutrient composition of hazelnut (Corylus avellana L.) varieties cultivated in Turkey. Food Chem. 2006, 99, 509–515.
  5. Jakopic, J.; Petkovsek, M.M.; Likozar, A.; Solar, A.; Stampar, F.; Veberic, R. HPLC–MS identification of phenols in hazelnut (Corylus avellana L.) kernels. Food Chem. 2011, 124, 1100–1106.
  6. Shahidi, F.; Alasalvar, C.; Liyana-Pathirana, C.M. Antioxidant phytochemicals in hazelnut kernel (Corylus avellana L.) and hazelnut byproducts. J. Agric. Food Chem. 2007, 55, 1212–1220.
  7. Pelvan, E.; Alasalvar, C.; Uzman, S. Effects of roasting on the antioxidant status and phenolic profiles of commercial Turkish hazelnut varieties (Corylus avellana L.). J. Agric. Food Chem. 2012, 60, 1218–1223.
  8. Cristofori, V.; Ferramondo, S.; Bertazza, G.; Bignami, C. Nut and kernel traits and chemical composition of hazelnut (Corylus avellana L.) cultivars. J. Sci. Food Agric. 2008, 88, 1091–1098.
  9. Bacchetta, L.; Aramini, M.; Zini, A.; Di Giammatteo, V.; Spera, D.; Drogoudi, P.; Rovira, M.; Silva, A.P.; Solar, A.; Botta, R. Fatty acids and alpha-tocopherol composition in hazelnut (Corylus avellana L.): A chemometric approach to emphasize the quality of European germplasm. Euphytica 2013, 191, 57–73.
  10. Shao, F.; Wilson, I.W.; Qiu, D. The research progress of taxol in Taxus. Curr Pharm Biotechnol 2021, 22, 360–366.
  11. Gallego, A.; Malik, S.; Yousefzadi, M.; Makhzoum, A.; Tremouillaux-Guiller, J.; Bonfill, M. Taxol from Corylus avellana: Paving the way for a new source of this anti-cancer drug. Plant Cell Tissue Organ Cult. 2017, 129, 1–16.
  12. Bottone, A.; Cerulli, A.; D’Urso, G.; Masullo, M.; Montoro, P.; Napolitano, A.; Piacente, S. Plant specialized metabolites in hazelnut (Corylus avellana) kernel and byproducts: An update on chemistry, biological activity, and analytical aspects. Planta Med. 2019, 85, 840–855.
  13. Barss, H.P. A new filbert disease in Oregon. Oregon Agric. Coll. Exp. Sta. Biennial Crop Pest Hort. Rep. 1913, 14, 213–223.
  14. Miller, P.W.; Bollen, W.B.; Simmons, J.E.; Gross, H.N.; Barss, H.P. The pathogen of filbert bacteriosis compared with Phytomonas juglandis, the cause of walnut blight. Phytopathology 1940, 30, 713–733.
  15. Sutic, D. Bacterial spots on leaves of filbert. Zast Biija 1956, 37, 47–53.
  16. Noviello, C. Osservazioni sulle malattie parassitarie del nocciolo, con particolare riferimento alla Campania. Ann. Fac. Sci. Agrar. Univ. Studi Napoli Portici 1968, 3, 11–39.
  17. Alay, K.; Altinyay, N.; Hancioglu, O.; Dundar, F.; Unal, A. Studies on desiccation of hazel nut branches in the Black Sea region. Bitki Koruma Bul. 1973, 13, 202–213.
  18. Luisetti, J.; Jailloux, F.; Germain, E.; Prunier, J.P.; Gardan, L. Caracterisation de Xanthomonas corylina (Miller et al.) Starr et Burkholder responsable de la bacteriose du noisetier recemment observee en France. Compte Rendu Acad. Agric. Fr. 1975, 61, 845–849.
  19. Koval, G.K. Diseases of hazel. Zashchita Rastenii 1978, 8, 44–45.
  20. Locke, T.; Barnes, D. Xanthomonas corylina on cob-nuts and filberts. Plant Pathol. 1979, 28, 53.
  21. Wimalajeewa, D.L.S.; Washington, W.S. Bacterial blight of hazelnut. Australas. Plant Pathol. 1980, 9, 113–114.
  22. Guerrero, C.J.; Lobos, A.W. Xanthomonas campestris pv. corylina, causal agent of bacterial blight of hazel in Region IX, Chile. Agric. Técnica 1987, 47, 422–426.
  23. Kazempour, M.N.; Ali, B.; Elahinia, S.A. First report of bacterial blight of hazelnut caused by Xanthomonas arboricola pv. corylina in Iran. J. Plant Pathol. 2006, 88, 341.
  24. Pulawska, J.; Kaluzna, M.; Kolodziejska, A.; Sobiczewski, P. Identification and characterization of Xanthomonas arboricola pv. corylina causing bacterial blight of hazelnut: A new disease in Poland. J. Plant Pathol. 2010, 92, 803–806.
  25. Kałużna, M.; Fischer-Le Saux, M.; Pothier, J.F.; Jacques, M.A.; Obradović, A.; Tavares, F.; Stefani, E. Xanthomonas arboricola pv. juglandis and pv. corylina: Brothers or distant relatives? Genetic clues, epidemiology, and insights for disease management. Mol. Plant Pathol. 2021, 22, 1481–1499.
  26. Webber, J.B.; Putnam, M.; Serdani, M.; Pscheidt, J.W.; Wiman, N.G.; Stockwell, V.O. Characterization of isolates of Xanthomonas arboricola pv. corylina, the causal agent of bacterial blight, from Oregon hazelnut orchards. J. Plant Pathol. 2020, 102, 799–812.
  27. Webber, J.B.; Wada, S.; Stockwell, V.O.; Wiman, N.G. Susceptibility of some Corylus avellana L. cultivars to Xanthomonas arboricola pv. corylina. Front. Plant Sci. 2021, 12, 800339.
  28. EFSA Panel on Plant Health (PLH); Bragard, C.; Dehnen-Schmutz, K.; Di Serio, F.; Jacques, M.A.; Miret, J.A.J.; Justesen, A.F.; MacLeod, A.; Magnusson, C.S.; Milonas, P.; et al. Commodity risk assessment of Corylus avellana and Corylus colurna plants from Serbia. EFSA J. 2021, 19, e06571.
  29. Lamichhane, J.R.; Varvaro, L. Xanthomonas arboricola disease of hazelnut: Current status and future perspectives for its management. Plant Pathol. 2014, 63, 243–254.
  30. Scortichini, M.; Rossi, M.P.; Marchesi, U. Genetic, phenotypic and pathogenic diversity of Xanthomonas arboricola pv. corylina strains question the representative nature of the type strain. Plant Pathol. 2002, 51, 374–381.
  31. Fischer-Le Saux, M.; Bonneau, S.; Essakhi, S.; Manceau, C.; Jacques, M.A. Aggressive emerging pathovars of Xanthomonas arboricola represent widespread epidemic clones distinct from poorly pathogenic strains, as revealed by multilocus sequence typing. Appl. Environ. Microbiol. 2015, 81, 4651–4668.
  32. Caballero, J.I.; Zerillo, M.M.; Snelling, J.; Boucher, C.; Tisserat, N. Genome sequence of Xanthomonas arboricola pv. corylina, isolated from Turkish filbert in Colorado. Genome Announ. 2013, 1, e00246-13.
  33. Pothier, J.F.; Kałużna, M.; Prokić, A.; Obradović, A.; Rezzonico, F. Complete genome and plasmid sequence data of three strains of Xanthomonas arboricola pv. corylina, the bacterium responsible for bacterial blight of hazelnut. Phytopathology 2022, 112, 956–960.
  34. Psallidas, P.G.; Panagopoulos, C.G. A bacterial canker of Corylus avellana in Greece. J. Phytopathol. 1979, 94, 103–111.
  35. Psallidas, P.G. Pseudomonas syringae pv. avellanae pathovar nov., the bacterium causing canker disease on Corylus avellana. Plant Pathol. 1993, 42, 358–363.
  36. Scortichini, M.; Tropiano, F.G. Severe outbreak of Pseudomonas syringae pv. avellanae on hazelnut in Italy. J. Phytopathol. 1994, 140, 65–70.
  37. Brzezinski, M.G. Le chancre des arbres, ses causes et ses symptoms. Bull. Intern. Acad. Sci. Cracovie 1903, 7, 139–140.
  38. Thornberry, H.H.; Anderson, H.W. Some bacterial diseases of plants in Illinois. Phytopathology 1937, 27, 946–949.
  39. Janse, J.D.; Rossi, P.; Angelucci, L.; Scortichini, M.; Derks, J.H.J.; Akkermans, A.D.L.; De Vrijer, R.; Psallidas, P.G. Reclassification of Pseudomonas syringae pv. avellanae as Pseudomonas avellanae (spec. nov, the bacterium causing canker of hazelnut (Corylus avellana L.). Syst. Appl. Microbiol. 1996, 19, 589–595.
  40. Marcelletti, S.; Scortichini, M. Definition of plant-pathogenic Pseudomonas genomospecies of the P. syringae complex through multiple comparative approaches. Phytopathology 2014, 104, 1274–1282.
  41. Scortichini, M.; Marchesi, U.; Dettori, M.T.; Angelucci, L.; Rossi, M.P.; Morone, C. Genetic and pathogenic diversity of Pseudomonas avellanae strains isolated from Corylus avellana trees in north-west of Italy, and comparison with strains from other regions. Eur. J. Plant Pathol. 2000, 106, 147–154.
  42. Scortichini, M.; Marchesi, U.; Rossi, M.P.; Di Prospero, P. Bacteria associated with hazelnut (Corylus avellana L.) decline are of two groups: Pseudomonas avellanae and strains resembling P. syringae pv. syringae. Appl. Environ. Microbiol. 2002, 68, 476–484.
  43. Kaluzna, M.; Ferrante, P.; Sobiczewski, P.; Scortichini, M. Characterization and genetic diversity of Pseudomonas syringae from stone fruits and hazelnut using repetitive-PCR and MLST. J. Plant Pathol. 2010, 92, 781–787.
  44. Scortichini, M.; Rossi, M.P.; Loreti, S.; Bosco, A.; Fiori, M.; Jackson, R.W.; Stead, D.E.; Aspin, A.; Marchesi, U.; Zini, M.; et al. Pseudomonas syringae pv. coryli, the causal agent of bacterial twig dieback of Corylus avellana. Phytopathology 2005, 95, 1316–1324.
  45. Scortichini, M.; Marcelletti, S.; Ferrante, P.; Firrao, G. A genomic redefinition of Pseudomonas avellanae species. PLoS ONE 2013, 8, e75794.
  46. Berge, O.; Monteil, C.L.; Bartoli, C.; Chandeysson, C.; Guilbaud, C.; Sands, D.C.; Morris, C.E. A user’s guide to a data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLoS ONE 2014, 9, e105547.
  47. Scortichini, M.; Ferrante, P.; Cozzolino, L.; Zoina, A. Emended description of Pseudomonas syringae pv. avellanae, causal agent of European hazelnut (Corylus avellana L.) bacterial canker and decline. Eur. J. Plant Pathol. 2016, 144, 213–215.
  48. Marcelletti, S.; Scortichini, M. Comparative genomic analyses of multiple Pseudomonas strains infecting Corylus avellana trees reveal the occurrence of two genetic clusters with both common and distinctive virulence and fitness traits. PLoS ONE 2015, 10, e0131112.
  49. Turco, S.; Zuppante, L.; Drais, M.I.; Mazzaglia, A. Dressing like a pathogen: Comparative analysis of different Pseudomonas genomospecies wearing different features to infect Corylus avellana. J. Phytopathol. 2022, 170, 504–516.
  50. Maleki-Zadeh, H.R.; Falahi Charkhabi, N.; Khodaygan, P.; Rahimian, H. Bacterial leaf spot and die-back of hazelnut caused by a new pathovar of Pseudomonas amygdali. Eur. J. Plant Pathol. 2022, 163, 293–303.
  51. Bucini, D.; Balestra, G.M.; Pucci, C.; Paparatti, B.; Speranza, S.; Proietti Zolla, C.; Varvaro, L. Bio-ethology of Anisandrus dispar F. and its possible involvement in dieback (Moria) diseases of hazelnut (Corylus avellana L.) plants in central Italy. Acta Hort. 2004, 686, 435–444.
  52. Guerrero, J.C.; Pérez, S.F.; Ferrada, E.Q.; Cona, L.Q.; Bensch, E.T. Phytopathogens of hazelnut (Corylus avellana L.) in southern Chile. Acta Hort. 2014, 1052, 269–274.
  53. Krol, E.; Machowicz-Stefaniak, Z.; Zalewska, E. Bacteria damaging the fruit of hazel (Corylus avellana L.) cultivated in South-East Poland. Acta Sci. Pol. Hortorum Cultus 2004, 3, 75–84.
  54. Marcone, C.; Ragozzino, A.; Seemüller, E. Association of phytoplasmas with the decline of European hazel in southern Italy. Plant Pathol. 1996, 45, 857–863.
  55. Postman, J.D.; Johnson, K.B.; Jomantiene, R.; Maas, J.L.; Davis, R.E. The Oregon hazelnut stunt syndrome and phytoplasma associations. Acta Hort. 2001, 556, 407–409.
  56. Cieślińska, M.; Kowalik, B. Detection and molecular characterization of ‘Candidatus Phytoplasma asteris’ in European hazel (Corylus avellana) in Poland. J. Phytopathol. 2011, 159, 585–588.
  57. Hodgetts, J.; Flint, L.J.; Davey, C.; Forde, S.; Jackson, L.; Harju, V.; Skelton, A.; Fox, A. Identification of’ Candidatus Phytoplasma fragariae’(16Sr XII-E) infecting Corylus avellana (hazel) in the United Kingdom. New Dis. Rep. 2015, 32, 3.
  58. Mehle, N.; Jakoš, N.; Mešl, M.; Miklavc, J.; Matko, B.; Rot, M.; Ferlež Rus, A.; Brus, R.; Dermastia, M. Phytoplasmas associated with declining of hazelnut (Corylus avellana) in Slovenia. Eur. J. Plant Pathol. 2019, 155, 1117–1132.
  59. Gentili, A.; Donati, L.; Bertin, S.; Manglli, A.; Ferretti, L. First report of ‘Candidatus Phytoplasma fragariae’ infecting hazelnut in Italy. Plant Dis. 2022, 106, 2254.
  60. Lessio, F.; Picciau, L.; Gonella, E.; Tota, F.; Mandrioli, M.; Alma, A. The mosaic leafhopper Orientus ishidae: Host plants, spatial distribution, infectivity, and transmission of 16SrV phytoplasmas to vines. Bull. Insectol. 2016, 69, 277–289.
  61. Mehle, N.; Dermastia, M. Towards the evaluation of potential insect vectors of phytoplasmas infecting hazelnut plants in Slovenia. Phytopath. Mollicutes 2019, 9, 49–50.
  62. Vuono, G.; Balestra, G.M.; Varvaro, L. Control of dieback (“Moria”) of Corylus avellana in central Italy using copper compounds. J. Plant Pathol. 2006, 88, 215–218.
  63. Scortichini, M.; Liguori, R. Integrated management of bacterial decline of hazelnut, by using Bion as an activator of systemic acquired resistance (SAR). In Pseudomonas Syringae and Related Pathogens; Springer: Dordrecht, The Netherlands, 2003; pp. 483–487.
  64. Schiavi, D.; Ronchetti, R.; Di Lorenzo, V.; Salustri, M.; Petrucci, C.; Vivani, R.; Giovagnoli, S.; Camaioni, E.; Balestra, G.M. Circular hazelnut protection by lignocellulosic waste valorization for nanopesticides development. Appl. Sci. 2022, 12, 2604.
  65. Pisetta, M.; Albertin, I.; Petriccione, M.; Scortichini, M. Effects of hot water treatment to control Xanthomonas arboricola pv. corylina on hazelnut (Corylus avellana L.) propagative material. Sci. Hort. 2016, 211, 187–193.
  66. Prokić, A.; Ivanović, M.; Gasic, K.; Kuzmanovic, N.; Zlatković, N.; Obradovic, A. Studying Xanthomonas arboricola pv. corylina strains from Serbia for streptomycin and kasugamycin resistance and copper sulfate sensitivity in vitro. In Proceedings of the 12th International Congress of Plant Pathology: Plant Health in a Global Economy, Boston, MA, USA, 29 July–3 August 2018; Available online: https://apsnet.confex.com/apsnet/ICPP2018/meetingapp.cgi/Paper/11264 (accessed on 15 October 2022).
  67. European Food Safety Authority (EFSA); Arena, M.; Auteri, D.; Barmaz, S.; Bellisai, G.; Brancato, A.; Brocca, D.; Bura, L.; Byers, H.; Chiusolo, A.; et al. Peer review of the pesticide risk assessment of the active substance copper compounds copper(I), copper(II) variants namely copper hydroxide, copper oxychloride, tribasic copper sulfate, copper(I) oxide, Bordeaux mixture. EFSA J. 2018, 16, e05152.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Academic Video Service
Feedback