Content area
Bacterial canker is a serious disease of sweet cherries (Prunus avium (L.) L.), affecting young and adult orchards worldwide. In Chile, the disease is mainly caused by the bacterial pathogen Pseudomonas syringae pv. syringae (Pss), which enters cherry tissues through abscission zones of leaves, lenticels, and flowers, wounds from pruning or frost injuries. The infection produces necrotic spots and perforation of the leaves, flower blights, spots and deformation in fruits, canker formation with abundant gummy exudation, as well as necrosis of buds, shoots and twigs. Canker disease management involves preventive strategies, including the application of chemical products like Cu and antibiotics, the use of biological control agents with antagonistic activity or ability to induce resistance genes, the selection of tolerant cultivar and rootstock combinations, as well as the use of pest control practices to reduce damage. The objective of this review was to compile and discuss existing information regarding different strategies for the control of bacterial canker of sweet cherry caused by Pss. This work provides an analysis of the advantages and disadvantages of the different disease management strategies available worldwide, with special attention to the current scenario of the disease in Chile, where cherry production has notoriously increased in the last decade.
ABSTRACT
Bacterial canker is a serious disease of sweet cherries (Prunus avium (L.) L.), affecting young and adult orchards worldwide. In Chile, the disease is mainly caused by the bacterial pathogen Pseudomonas syringae pv. syringae (Pss), which enters cherry tissues through abscission zones of leaves, lenticels, and flowers, wounds from pruning or frost injuries. The infection produces necrotic spots and perforation of the leaves, flower blights, spots and deformation in fruits, canker formation with abundant gummy exudation, as well as necrosis of buds, shoots and twigs. Canker disease management involves preventive strategies, including the application of chemical products like Cu and antibiotics, the use of biological control agents with antagonistic activity or ability to induce resistance genes, the selection of tolerant cultivar and rootstock combinations, as well as the use of pest control practices to reduce damage. The objective of this review was to compile and discuss existing information regarding different strategies for the control of bacterial canker of sweet cherry caused by Pss. This work provides an analysis of the advantages and disadvantages of the different disease management strategies available worldwide, with special attention to the current scenario of the disease in Chile, where cherry production has notoriously increased in the last decade.
Key words: Biological control, chemical control, Pseudomonas syringae pv. syringae.
INTRODUCTION
Sweet cherry (Prunus avium (L.) L.) is currently the most important fruit crop in Chile, with an average annual production of 373 000 t and an average cultivated area of about 54 000 ha between the years 2019 and 2023. During the same period, 87% of the production was exported, positioning Chile among the world's leading exporters of cherries (FAO, 2025a; 2025b). In recent years, the planted area has steadily increased in the southcentral and southern zones of Chile, specifically between Maule and Los Lagos Regions, with a 350% increase from 2012 to 2022 (ODEPA, 2024).
Sweet cherry trees can be affected by various diseases, which can have a significant economic impact and whose incidence is favored by conditions of high relative humidity and moderate temperature, while also being associated with frost and heavy rainfall events, and cool weather conditions like those found in the southcentral and southern zones of Chile. Bacterial canker, also known as gummosis, blossom blast, spur and twig blight, sour sap, or dieback, is considered the main disease affecting cherry orchards in the country. At the global scale, canker is caused by pathovars within the Pseudomonas syringae species complex including mainly P. syringae pv. syringae (Pss) (Beltrán et al., 2021; Marroni et al., 2024; Maguvu et al., 2024), followed by P. syringae pv. morsprunorum (Psm) race 1 and Psm race 2 (Hulin et al., 2018; Marroni et al., 2024). Of these Psm pathogens, in Chile, only Psm race 1 has been identified as the causal agent of bacterial canker of sweet cherry in Los Lagos Region (García et al., 2021), where climatic conditions are more favorable for bacterial infection and sweet cherry production has increased in the last 10 yr. Upon Psm race 1 detection, the Chilean Agricultural and Livestock Service (Servicio Agrícola y Ganadero de Chile [SAG]) established quarantine protocols (Resol. No. 3080, SAG, Chile) and implemented a phytosanitary program (Resol. Exenta No. 8948/2019, SAG, Chile) to avoid the spread of Psm race 1 in the country. According to Marroni et al. (2024), these two Gram negative bacteria (Pss and Psm) enter plant tissues through natural openings, such as stomata, petioles and lenticels; injuries caused by autumn leaf fall or weather events like hail or frost; or wounds from pruning or other mechanical damage. Once the bacterium has entered the plant, it moves through intercellular spaces, progresses into the bark and colonizes the cambial tissue, causing cankers in woody organs, resulting in gummosis and emission of a characteristic fermentation odor (Hulin et al., 2018; Marroni et al., 2024). Additionally, part of the epiphytic population enters through the leaves during the growth phase, causing brown and black spots that evolve into perforations (Hulin et al., 2018), and reducing the leaf photosynthetic area. Many strains are capable of producing and secreting characteristic secondary metabolites, known as cyclic lipodepsipeptides (CLPs), which are considered plant virulence factors and antifungal agents. Among CLPs, syringomycin and syringopeptin can substantially increase disease severity (Scholz-Schroeder et al., 2001), which will depend on the bacterial strain, plant cultivar, plant age, invaded tissue, and environmental conditions, causing yield losses of 10% to 20% in young orchards and even plant death under favorable environmental conditions (Khezri and Mohammadi, 2018). In Chile, according to Moya-Elizondo (2020), Pss causes a 10% yield reduction between Maule and La Araucania Regions, which would account for losses of about 156 million dollars.
Bacterial canker of sweet is commonly controlled by the use of preventive bactericides based on Cu compounds (Husseini and Akköprü, 2020) and antibiotics (Sundin and Wang, 2018). The Cu ions affect bacteria by altering enzymatic functions, displacing essential metal cofactors and generating reactive oxygen species (Husseini and Akkoprú, 2020), while Cu ions can also control fungal pathogens (Mitre et al., 2011). There are several and deep reviews about use of Cu compounds to management bacterial disease in agriculture (Lamichhane et al., 2018; Yu et al., 2023); however, reports of the implications of its use in particular crops are less frequent. In Chile, Cu salt-based active ingredients authorized by SAG are diverse and include Cu molecules based on oxychloride, hydroxide, oxide, sulfate pentahydrate, and basic sulfate (SAG, 2023). These products are effective in controlling bacteria but can cause phytotoxicity; repeated applications can lead to accumulation of active ingredients to toxic levels, resulting in the emergence of bacterial resistant strains (Aprile et al., 2021; Beltrán et al., 2021) and the alteration of soil microbiota (Alengebawy et al., 2021). Additionally, the use of Cu salts has a high cost due to the number of applications required throughout the season, which has been estimated to reach about 14.6 million dollars in orchards between Maule and La Araucania Regions in Chile (Moya-Elizondo, 2020). In the case of antibiotics, active ingredients such as kasugamycin hydrochloride hydrate, streptomycin sesquisulfate, gentamicin sulfate, and oxytetracycline hydrochloride (alone or in combination) are authorized for use in Chile. However, inappropriate use of antibiotics favors the rapid development of resistance (Sundin and Bender, 1993; Vasebi et al., 2019). All the problems associated with the use of these conventional bactericides have led to the development of new pest management strategies based on prevention, varietal resistance, and biological control, as well as integrated disease management programs for bacterial canker of sweet cherry.
The objective of this review was to compile and discuss existing information regarding different strategies for controlling bacterial canker of sweet cherry caused by Pseudomonas syringae pv. syringae. A systematic review of the literature was undertaken to analyze the advantages and disadvantages of the different disease management strategies available worldwide, with special attention to the current scenario of the disease in Chile.
CONTROL STRATEGIES
Control strategies for bacterial canker of sweet cherry (Prunus avium (L.) L.) include the application of different products and the use of several cultural practices that provide secondary control with the aim to restrain bacterial populations under the damage threshold throughout the sweet cherry growth season. Determining the most appropriate integrated disease management procedure to be implemented is essential for prompt disease reduction.
Efficacy of chemical control
Chemical control is defined as the eradication, reduction, or halting of the replication of a pathogenic population using chemical substances. Common bactericides are Cu ions and antibiotics. Market formulations contain Cu salts, namely Cu hydroxide, Cu oxide, Cu sulfate pentahydrate, or Cu oxychloride (SAG, 2023). These salts require the solubilization of Cu ion (Cu·) into the environment, and once Cu is released and upon contact with target microorganisms, this exerts its action through various pathways. These include altering protein structure and function, competing with metallic protein cofactors, and accumulating reactive oxygen species, which damage the proper metabolism and permeability of the cell membrane, eventually leading to bacterial death (Ladomersky and Petris, 2015; Husseini and Akköprü, 2020). The Cu ions released into the environment are variable and depend on environmental conditions such as rainfall or application of other products (Vanneste, 2020), which will affect control efficacy. The use of Cu allows bacterial control by reducing the incidence and severity of bacterial canker, but this has disadvantages that include emergence of resistance due to frequent applications during the season, restrictions on applications in certain susceptible stages of plant development, potential phytotoxic reactions associated with misuse, and environmental damage. The main mechanisms of bacterial tolerance to Cu include the sequestration of the element by cysteine-rich metallothioneins, oxidation of Cu· to the less toxic Cu·? by multicopper oxidases, and export from the cytoplasm to other destinations, which occurs towards the periplasmic space, crossing the inner membrane in Gram negative bacteria (Ladomersky and Petris, 2015). The Cu resistance in Pss can have various determinants, such as siderophore production, and the presence and expression of genes belonging to the copABCD operon, specifically the copA gene, the copABCD-cusCBA-copG gene cluster, and/or transposons (Husseini and Akköprü, 2020; Aprile et al., 2021). The copA gene encodes the CopA protein, which is a P1B-type ATPase that can bind Cu in the periplasm through ATP hydrolysis, preventing its cytoplasmic accumulation (Husseini and Akköprü, 2020). The origin of this gene was initially reported as plasmidial in P. syringae, which is consistent with the findings of Husseini and Akköprü (2020) regarding Pss. However, Li et al. (2015) indicated that this can have a plasmidial or chromosomal origin depending on the species, possibly due to high polymorphism of the gene. In the case of transposons, Aprile et al. (2021) have referred to isolates of Pss from mango that carry the COARS Tn7-like transposon as hyper-resistant, reporting bacterial growth in vitro at concentrations up to 2.4 mM Cu sulfate. According to Cazorla et al. (2002), an isolate is considered resistant if it grows in a medium with a concentration of at least 0.8 mM Cu sulfate. In Chile, Beltrán et al. (2021) first reported the presence of Pss isolates with varying degrees of Cu resistance, as well as bacteria not characterized as Pss associated with the disease. This evidence shows the broad-spectrum action of this compound, which can cause phytotoxicity in native and agronomic species due to its environmental accumulation from use, resulting in decreases in chlorophyll biosynthesis, plant height, shoot length and, consequently, lower yields (Lamb et al., 2012; Alengebawy et al., 2021). Additionally, Cu accumulation in soils can significantly inhibit microbial activity by reducing the oxidative potential of rhizospheric bacteria, affecting extracellular enzymatic activity, reflected as restrictions on urease activity (Frenk et al., 2013; Caetano et al., 2016). In Chile, Cu-resistant soil-dwelling bacteria have been recorded as an adaptation to Cu exposure, some possessing the copA gene (Altimira et al., 2012), increasing the chances of gene transfer. Additionally, it has been observed that Cu exposure in Pss triggers the production of alginate (Kidambi et al., 1995), an exopolysaccharide that acts as a virulence factor, capable of increasing tolerance to environmental stress and Cu in other bacteria of the genus (Keith and Bender, 1999; Svenningsen et al., 2018). Thus, the use of Cu-based bactericides is considered to have generated a multifactorial bacterial adaptation that is transferable (Fan et al., 2022).
Regarding antibiotics, the number of products and active ingredients allowed for use in fruit production is limited in Chile, and include streptomycin sesquisulfate, gentamicin sulfate, kasugamycin hydrochloride, and oxytetracycline hydrochloride (SAG, 2023), which act at ribosomal level by inhibiting protein synthesis, leading to bacterial death. Streptomycin sesquisulfate, gentamicin sulfate, and kasugamycin hydrochloride belong to the aminoglycoside group and interact with the 30s ribosomal subunit, while oxytetracycline hydrochloride prevents aminoacyl-tRNA binding to ribosomal A site (Okuyama et al., 1971; Hancock, 1981; Sundin and Wang, 2018). Despite their effectiveness, their use must be strictly limited to situations of high susceptibility or high disease prevalence due to the rapid development of resistance (Vasebi et al., 2019) and metabolism alterations in the agroecosystem. For streptomycin, the main global determinant for resistance is the acquisition of the strA and strB gene pair, which encodes for enzymes capable of streptomycin inactivation through phosphorylation or adenylation. Their transfer depends on plasmids or the Tn5393 transposon (Sundin and Bender, 1993; Sundin and Wang, 2018). Regarding gentamicin, resistance in Pseudomonas spp. has been reported through various mechanisms, such as outer membrane stabilization through lipopolysaccharide modification via OprH porin overexpression, inactivation by acetylation through aminoglycoside acetyltransferase, inactivation by adenylation via aminoglycoside nucleotidyltransferase, or by acquiring a resistance gene cassette via plasmid (Pang et al., 2019). In kasugamycin, genes like aac(2')-lla encode an acetyltransferase and allow resistance acquisition in Acidovorax avenae subsp. avenae and Burkholderia glumae, which are both pathogens of rice (Oryza sativa); similarly, the chromosomal gene ksgA confers antibiotic resistance in Pseudomonas syringae pv. actinidiae, a kiwifruit pathogen (Sundin and Wang, 2018; Pan et al., 2020). There are currently no reports of resistance to the latter two antibiotics in Pss due to selection pressure caused by the use of antibiotics to control bacterial canker. Regarding oxytetracycline, resistance is due to the acquisition and expression of otr genes and, in the case of tetracycline, tet genes. Both groups are generally associated with plasmids and/or transposons. These genes enable resistance through various mechanisms, such as the synthesis of ribosomal protection proteins, tetracycline-inactivating enzymes, or energy-dependent efflux proteins (Connell et al., 2003; Roberts, 2005). There are reports of antibiotic resistance tests in Pss isolates, showing resistance to streptomycin or oxytetracycline; and combined resistance to tetracycline and kanamycin; Cu and streptomycin; and Cu, streptomycin, and oxytetracycline (Spotts and Cervantes, 1995; Hwang et al., 2005). Pseudomonas syringae pv. syringae isolates resistant to ampicillin, chloramphenicol, and/or rifampicin have been detected exclusively in laboratory studies (Hwang et al., 2005), raising an early warning for potential use in field applications. Nevertheless, although there are no reports of antibiotic resistance in Pss isolated from sweet cherries in Chile, given that horizontal and/or vertical transfer of these genes is possible, antibiotic resistance is likely to emerge if inappropriate and intensive use of these compounds occurs in some productive areas of the country.
Antibiotics can accumulate in the agroecosystem and cause enzymatic and microbial metabolic alterations in the soil. In fact, soil particles can adsorb a significant amount of incoming antibiotics into the soil system through application drift or excreta from treated animals, while residual amounts of these substances can be absorbed by plant species intended for human consumption. Rashtbari and Sinegani (2020) reported a 68.9% decrease in alkaline phosphatase activity in soils exposed to a concentration of 200 mg kg? gentamicin when compared to the control without the use of antibiotic, as well as negative impacts of soil applications of oxytetracycline on urease activity. Wei et al. (2009) conducted a pot experiment using Lolium perenne L. planted in clay soil and observed inhibitions of urease and dehydrogenase activity after soil applications of tetracycline at concentrations of 1, 10, and 100 mg kg? soil, resulting in a consequent decrease in soil organic matter decomposition rate. The authors also observed decreases in microbial populations up to 10 d after tetracycline application, along with declines in plant biomass, with greater reductions in dry weight at higher doses of the antibiotic. Furthermore, there are several reports on the persistence of gentamicin and oxytetracycline in leaves and roots of vegetables such as Lactuca sativa L., Daucus carota L., Capsicum annuum L., and Raphanus sativus L. after direct soil applications of the antibiotics or manure from treated animals (Xu and Zhang, 2014; Youssef and Bashour, 2017; Tasho et al., 2020). This constitutes a potential risk to human health, because frequent consumption of such foods can increase the risk of antibiotic resistance development by the human digestive microbiome (Rodriguez et al., 2006). Nevertheless, active ingredients such as kasugamycin and streptomycin leave low levels of residues in the environment and are easily degradable (Lu et al., 2012; Shade et al., 2013; Chen et al., 2020), making them an adequate alternative when an antibiotic is required to control Pss.
Genetic control
Genetic control aims to prevent and limit the development of a disease by selecting expressible traits that give the plant a range of disease tolerance, ideally avoiding economic damage. This selection is possible through compatible crossing between individuals of the same or different species through phenotype selection via conventional breeding, or by transgenesis. Currently, the cultivation and import of genetically modified plants or the use of genetically modified organisms are prohibited in Chile, except for research purposes (Resol. Exenta No.1523, SAG, Chile). Therefore, only rootstocks and cultivars obtained through conventional breeding are used for sweet cherry production.
Choice of rootstock has been suggested as a preventive measure to avoid bacterial canker in both sweet cherry and plum trees (Sayler et al., 2002). In an experiment with sweet cherry in Oregon (USA), there was по difference in susceptibility to bacterial canker in any combination of cultivar and rootstock (Spotts et al., 2010). However, the 'F12.1' is one of the most widely used cherry rootstocks, with reported disease tolerance to Pss (Long and Kaiser, 2010; Vignati et al., 2022). This rootstock is an improved clone developed from the 'Mazzard' rootstock through vegetative propagation, which has moderate tolerance to bacterial canker and high compatibility with current commercial cultivar patterns due to its genetic origin from P. avium. The 'F12.1' rootstock is cold-resistant and suitable for temperate cold climates, low-yielding, highly vigorous, and highly susceptible to crown gall caused by Agrobacterium tumefaciens (Long and Kaiser, 2010; Vignati et al., 2022). Colt, a rootstock derived from a cross between P. avium and P. pseudocerasus, is another widely distributed and used rootstock that can control the vigor of 'Mazzard', showing resistance to Phytophthora root rot and Pfeffefinger viral disease, which causes leaf deformation and dwarfism, and shows good compatibility with commercial cultivars (Askari et al., 2021; Vignati et al., 2022). Field studies have shown that 'Colt' has higher bacterial canker tolerance compared to 'F12.1' and 'Gisela 6' rootstocks when grafted with cultivars such as 'Napoleon' and 'Roundel' (Garrett, 1986), and 'Bing' (Spotts et al., 2010), respectively. Cirvilleri et al. (2008) reported increased tolerance to bacterial canker in transgenic lines of "Colt" compared to the non-transgenic rootstock, through the addition of the phyA gene from rice. This gene encodes phytochrome A, a photoreceptor involved in hormonal control of shoot growth in plants in response to variations in red and far-red light spectrum. According to the authors, this increase in tolerance could be explained by the stimulation of the salicylic acid pathway dependent on the light regime. 'Mahaleb', a seedling rootstock from Prunus mahaleb L., has also shown tolerance to bacterial canker as well as high drought tolerance due to its ability to produce deep roots, suitability for high-yield cultivars in traditional trellis systems, and tolerance to crown gall and nematodes. However, 'Mahaleb' rootstock is vigorous, highly sensitive to waterlogging, and incompatible with some commercial cultivars (Long and Kaiser, 2010; Vignati et al., 2022).
There is a need for sweet cherry commercial cultivars with tolerance to bacterial canker disease, particularly considering that unpredictable weather patterns are more frequent due to climate change and that changes in production systems, like the use of high or super-high-density orchards with intensive production practices such as the use of orthophytia, trellis systems, and mechanical or manual pruning, may leave many more wounds that can become infected by Pseudomonas bacteria. A study of Farhadfar et al. (2016) conducted in Iran, identified cherry cultivars that seem to be more tolerant to bacterial canker disease by measuring canker lesion length on trunks and/or shoots after 8 mo from the inoculation with Pss under field conditions (Table 1). However, the study did not include commercially relevant cultivars and failed to perform molecular identifications of re-isolated bacteria obtained from the lesions, which was only conducted using biochemical methods like LOPAT and GATTa. Nonetheless, the information obtained by the authors can be useful for future studies that include these genotypes for the development and introduction of new varieties into the market. Mgbechi-Ezeri et al. (2017) analyzed the disease response in commercial cultivars and seven advanced selections, evaluating canker length on shoots after 8 wk from the inoculation with Pss (Figure 1) and reported that: i) The most tolerant commercial cultivar was 'Regina', with an average lesion length of 3 cm, while all the advanced selections showed lower values, with a minimum of 1.8 cm; ii) the most susceptible cultivars were 'Sweetheart' and 'Rainier', with values close to 6 cm; and iii) there was a moderately high correlation between Pss population density and lesion length, with nonspecific population counts due to the lack of biochemical and molecular tests for an adequate identification of bacteria isolated from symptomatic tissue, indicating that registered bacterial population density is not attributable to Pss density. Likewise, other studies on woody tissues have reported that 'Merton Glory' and 'Colney' are resistant when exposed to Psm race 1 and Psm race 2 (Hulin et al., 2018; 2022). Moreover, llicié et al. (2018) assessed the susceptibility of different sweet (19) and sour cherry (3) cultivars to Pss and Psm1, determining that sweet cherry cvs. 'Carmen' and 'Margit' and sour cherry "Erdi botermd' exhibited a certain level of resistance.
Regarding cultivar-rootstock combination resistance, Spotts et al. (2010) evaluated the length of cankers developed after different horticultural and natural wound injuries, inoculated or non-inoculated with Pss, in different infection sites in young sweet cherry plants over a 3 yr period in 'Bing', 'Sweetheart', 'Sylvia', 'Regina', and 'Rainier' on rootstocks including 'Gisela 6', 'Mazzard', 'Maxma 14', 'Colt', and 'Krymsk 5'. The results showed that no combinations expressed high resistance to bacterial canker disease, with the combination of 'Bing' on 'Gisela 6' reaching a 90% mortality rate, while 'Bing' on "Colt" had a 0% mortality rate, highlighting the importance of the rootstock as a control option in this cultivar, and suggesting that the combination 'Bing"Gisela 6' should be avoided under favorable conditions for the disease. In recent research conducted by Bgrve et al. (2025), in Norway, determined that all sweet cherry cultivars ('Giorgia', 'Lapins', and 'Sweetheart') and rootstocks "Colt" and "Gisela 6 become infected and develop severe symptoms, it is important to avoid stress factors that may promote disease development.
Therefore, developing new germplasm is necessary to promote the creation of resistant and commercially successful varieties. Hulin et al. (2022) identified new sources of resistance, such as the wild P. avium accession Groton B and the ornamental species P. incisa Thunb., after observing a positive correlation between reduced bacterial multiplication and decreased symptoms in wounded leaves separated from the tree, 10 d after inoculation of 2х10° cfu mL·. However, nonsignificant foliar symptom expressions were detected in P. incisa x Napoleon hybrid after performing the same inoculation method. Although parental material has resistance potential, the study should be complemented with woody tissue infections, where the greatest differentiation of resistance has been demonstrated, and with crosses with other commercial cultivars to ensure efficacy.
Few studies have focused on the mechanism by which bacterial canker resistance occurs. In this sense, Cui et al. (2023) conducted a comparative transcriptome analysis in Chile and identified some differentially expressed genes (DEGs) related to plant defense in canker infection with three strains of Pss in 'Lapins'. By Pss infection on growing twigs, DEGs vary according to the Pss strain and sampled tissue (next to canker lesion and 15-20 cm below Pss inoculation point). Despite this variation, under a Gene Ontology (GO) enrichment analysis, Pss strain 11116_b1 showed the highest level of virulence among 33 DEGs related to defense response, including genes that encoded for RPM1-like protein and TAO1-like protein. Both genes are involved in plant resistance to P. syringae by recognizing the type Ill effector protein encoded by the avirulence gene В, which triggers a hypersensitive response (Eitas et al., 2008). In addition, Pss strain 11116 _b1 increased the expression of the Rps6-like protein, which is involved in resistance related to P. syringae НорА1 effector (Kim et al., 2009), and for nematode resistance protein-like (HSPRO2). For this strain, robust resistance responses were induced on 15-20 cm below the inoculation point compared to tissue immediately surrounding a canker lesion. Therefore, these findings provide valuable information for future breeding with genetic control approaches, which could be based on identification and heredity of defense response genes. The use of this genetic assisted control strategy is highly desirable because it allows reducing pesticide applications, lowering the associated costs and risks since the development of a resistant variety is a long-term process that could take up to 20 yr (Quero-García et al., 2019).
Biological control
Biological control aims to reduce population density or disease-producing activities of a pathogen by creating an environment favorable to antagonists; stimulating resident beneficial microbiota or host resistance; or mass introduction of antagonists, non-pathogenic isolates, or other beneficial microorganisms (Cook and Baker, 1983; Lewis and Papavizas, 1991). Reported antagonistic microflora includes viruses, bacteria, and fungi. However, there is scarce information about the use of these biological control agents (BCAs) in the control of Pss in sweet cherry. In this regard, biocontrol capacity of phages (bacterial viruses) against Pss has been demonstrated under in vitro and/or in vivo conditions, reducing bacterial canker incidence or development in in vivo conditions (Pinheiro et al., 2019; Rabiey et al., 2020; Akbaba and Ozaktan, 2021). The isolates phages used in these studies were obtained from soils from orchards affected by the disease, leaves or woody tissue of cherry trees, or by using commercial products such as Phage D6, and they were applied separately or combined. The bacterial viruses used in these studies reduced disease incidence by over 50% compared to the absolute control and bacterial population by 80%; exhibited lytic capacity against other pathogenic species such as Psa or P. syringae pv. tomato; and had no impact on different beneficial strains of Pseudomonas fluorescens. The studied phages had an action capacity up to 5 wk after applications. However, the use of phages as BCAs can be complicated by the potential entry into the lysogenic cycle (viral reproductive stage where viral DNA gets integrated with a host cell's DNA and replicated along with it) or being restricted to nighttime applications because viruses are highly susceptible to high temperatures as well as exposure to sunlight and UV radiation (Jones et al., 2012).
The BCA-based products constitute another alternative for the control of bacterial canker. In fact, they can reduce Cu salt applications per season by covering periods of disease susceptibility when other products cannot be used, and result in a lower risk of bacterial bactericide to Cu and antibiotics. However, there is still a lack of extensive scientific evidence regarding the effectiveness of BCAs, mode of action, effects on plant physiology, and modification of the plant or environmental microbiota, while they have high costs, and a lower shelf life compared to chemical control products under similar storage conditions. In Chile, the use of products formulated with BCAs is scarce, with a limited number of bactericides authorized by SAG (2023), including Nacillus (Bacillus subtilis, Brevibacillus brevis, and Bacillus licheniformis strains), and Baciforte (8. subtilis strain C55); and bactericide-fungicides such as Amylo-X (Bacillus amyloliquefaciens strain D747), Coraza (Bionectria ochroleuca, Hypocrea virens, and Bacillus licheniformis), and Triwork Ibeta (Trichoderma viride, T. harzianum, and T. longibrachiatum). The use of BCAs requires adequate knowledge of the identity, ecology, and pathogenicity of the involved organisms.
Nacillus is a bacterial consortium composed of strains of Bacillus subtilis, B. licheniformis, and Brevibacillus brevis; Serenade is a formulated from B. subtilis strain QST 713; and Coraza, a microbial consortium based on the bacterium B. licheniformis and the fungi Bionectria ochroleuca and Hypocrea virens (SAG, 2023). Nacillus and Serenade present a systemic action, and their effectiveness has been studied through trials reported in technical bulletins, forming part of a mixed seasonal management plan, which included foliar applications and some applications of Cu salts, such as Cu oxychloride and Cu hydroxide, whereas Coraza has a local action and has been evaluated in curative treatments of cankers (Osorio et al., 2020). In the study conducted by Osorio et al. (2020), after three seasons of foliar applications, treatments that included Nacillus and Serenade showed lower bacterial counts attributed to fluorescent Pseudomonas compared to the absolute control, but only in some assessment dates, whereas bacterial counts were equal to the absolute control at some points in the case of Serenade. However, bacterial counts were non-specific because they did not include biochemical or molecular identifications, and bacterial identification was only based on the colony fluorescence under UV light. In the same study, Osorio et al. (2020) conducted a trial for healing cankers caused by Pss, which included a single application of various products after canker was removed, and following the healing process, Coraza achieved the best sealing values and reduction of gummosis.
Other potential alternatives for biocontrol include suppression of quorum sensing (QS) through applications of endophytic bacteria and induction of systemic acquired resistance in sweet cherry plants. Akbari et al. (2020) reported reductions in 3-oxo-hexanoyl-homoserine lactone levels, biofilm production, and swarming motility in Pss through a possible enzymatic degradation of the signaling molecule in in vitro trials, using endophytic strains of Bacillus cereus Si-Ps1 and Pseudomonas azotoformans La-Pot3-3, and these QS suppressive-bacteria decreased Pss virulence when they were co-inoculated on citrus plants in greenhouse trials. Although the use of QS-inhibiting bacteria obtained from sweet cherry trees can be implemented, it should be considered that inoculations of Pss combined with epiphytic bacteria capable of interfering with the QS system and with the capacity to limit Fe availability have shown increases in disease incidence in experiments with bean plants (Dulla et al., 2010). Therefore, QS interferences and their effect on virulence are not entirely clear and may depend significantly on the origin of the interference process. Regarding induction of systemic acquired resistance (SAR), which is a mechanism that increases the physical or chemical barriers of the host plant after being preconditioned with elicitors, Lillrose et al. (2017) conducted a prophylactic application of a plant defense inducer (Actigard, acibenzolar-S-methyl) against flower infections, observing that the plant defense inducer was less effective and more variable than the antibiotic, ranging from little or no apparent control effect. However, Rubilar-Hernandez et al. (2024) have recently reported reductions of necrotic lesions in detached leaves and branches inoculated with Pss in juvenile sweet cherry plants by previously spraying sodium nitroprusside (SNP), a precursor for nitric oxide (NO) synthesis. Leaves of 'Lapins' treated with 0.5 mM SNP showed a reduction in necrotic area around 36 percentual points after 10 d of Pss inoculation (dpi) compared to no SNP treatment under in vitro conditions. Meanwhile, under in planta conditions, 0.5 mM SNP sprayed to fully expanded leaves attached to lignified seasonal branches, which were subsequently inoculated with Pss, reduced inner canker lesions by 50% after 60 dpi. This decrease in susceptibility to Pss caused by SNP could be explained because NO is involved in stomatal closure, which also enhances the activity of antioxidant enzymes as ascorbate peroxidase and catalase, thereby reducing reactive oxygen species (ROS) content and plant susceptibility to biotic and abiotic stresses (Rubilar-Hernández et al., 2024).
Future studies and applications are needed to enable a robust response to a potential Pss infection in sweet cherry, since elicitor applications have been carried out in other species to increase tolerance against other pathovars of P. syringae (Schnake et al., 2020), making SAR a viable alternative for bacterial control.
Cultural control
Cultural control refers to practices that minimize conditions for pathogen development, such as host weed control, proper fertilization, pruning, among others. The pathogenic potential of weeds and plant residues as inoculum sources was early studied by Latorre and Jones (1979), who found presence of Pss, pathogenic to cherry fruit in Taraxacum officinale, Trifolium spp., Stellaria media, Bromus inermis, and in semi-decomposed leaves and plant residues. There is a lack of recent information that could clarify these inoculum sources, considering that the isolated bacteria in the work of Latorre and Jones (1979) were characterized only biochemically and morphologically and that their pathogenic potential in lignified tissues was not studied.
Weed control includes the use of mulches, hand-weeding, herbicide applications, flame weeding, cover crops, subsurface drip irrigation or the use of animals to graze weeds (e.g., geese) because weeds compete with trees for water and nutrients, and they can harbor insect pests and promote crown diseases in sweet cherries. On the other hand, nutritional and pH imbalances in cherries can be predisposing factors for the disease, considering that low pH decreases nutrient availability of P, K, Mg, and Ca in the soil (Melakeberhan et al., 2000), which will negatively affect the physical barrier against the pathogen and immune response of the plant. In 1-yr-old seedlings of 'Mazzard' rootstock, the imbalance caused by low pH resulted in higher seedling mortality, more severe lesions, and reduced growth, while Pss was able to infect seedlings between 3.9 and 7.0 soil pH levels, with increases in shoot lesion length at pH below 5.5 (Melakeberhan et al., 2000). Considering that low soil pH predisposes the seedlings to Pss, amendments to increase pH should be considered to reduce the risk of bacterial canker in the south-central and southern zones of Chile since Andisol soils, which are characterized by low pH, are mainly found here. However, in other Prunus species, no positive correlation has been observed between reduction of susceptibility to Pss infection and foliar and soil fertilization of Ca and N, even though increases in foliar and bark concentrations of these elements were observed (Cao et al., 2013). This suggests that supplementation would not be a protective factor against the disease, but adequate nutritional levels must be maintained to avoid increasing susceptibility.
Pruning plays a significant role in bacterial canker control. In susceptible cultivars, fall and spring pruning can increase the risk of infection due to a potential concurrence with cooler, rainy, and moist weather. If winter pruning is needed to promote growth or renew branches, this should be done during dry conditions (Spotts et al., 2010). Cherry trees should not be pruned in spring, since there is a peak in bacterial population growth that increases the risk of infection by Pss. Instead, pruning should take place during summer (after fruit harvest), when there is a decline in bacterial epiphytic populations, which is associated with drier environmental conditions. Additionally, flush cuts of branches in sweet cherry trees should be avoided to separate the main axis trunk from possible inoculum infection, whereas leaving a stub when pruning out a branch may protect against Pss-incited cankers by 'distancing' the main trunk from invasion (Carroll et al., 2010). Given that all injuries are susceptible to infection by P. syringae, special attention should be given to injury prevention. In this sense, the use of steel wires in trellis systems in high-density sweet cherry orchards should be avoided and replaced with plastic-coated steel wires or high-tension plastic wires, considering that both reduce Pss infection by 50% to 75% compared to traditional high tensile steel wire (Lillrose et al., 2017).
Plastic rain covers to protect against fruit cracking have become a standard practice in rainy areas. The potential use of similar covers in early spring may be a strategy for reducing the infection pressure of diseases caused by fungi and bacteria (Hggetveit and Jakobsen, 2005). In sweet cherries, use of plastic rain shield or production under plastic cover has been reported to reduce fungal disease (Bgrve and Stensvand, 2003; Bgrve et al., 2007; Thomidis and Exadaktylou, 2013). However, to our knowledge, there is not an adequate report of the use of this crop protection system to reduce Pss in sweet cherries.
In summary, an integrated approach is necessary for the successful management of bacterial canker of sweet cherry. In this sense, this work provides valuable insights that can help farmers make informed decisions regarding the most appropriate integrated disease management procedure to be implemented.
CONCLUSIONS
Pseudomonas syringae pv. syringae (Pss) is a highly virulent bacterial pathogen, causing canker disease and affecting both woody and non-woody tissues of sweet cherry. Current control measures are preventive and unable to eradicate the disease. Chemical compounds such as Cu and antibiotics have shown negative effects on the environment, while their applications pose risks of chemical resistance by Pss. The development of resistant cultivar and rootstock combinations is an economically viable alternative, but it has not proved highly effective. There have been advances in the understanding of the physiological mechanisms and genes involved in the defense mechanism against bacterial pathogens in sweet cherries, but further research is still needed. The use of biological control agents (BCAs) represents an environmentally friendly strategy as they do not have the negative effects associated with chemical compounds. Nevertheless, there is limited scientific literature on this subject, and thus more in-depth study is required to evaluate the efficacy of BCA-based products. In addition, cultural practices like adequate weed control, pruning, fertilization, and pH management are useful tools to be considered for integrated disease management of bacterial canker of sweet cherry.
Author contributions Conceptualization, Y.L., E.M-E., J.H., M.G., R.B. Writing-original draft, Y.L. Writing-review & editing, E.M-E., Y.L., J.H., M.G., R.B. Supervision, E.M-E. All co-authors reviewed the final version and approved the manuscript before submission.
References
Akbaba, M., Ozaktan, H. 2021. Evaluation of bacteriophages in the biocontrol of Pseudomonas syringae pv. syringae isolated from cankers on sweet cherry (Prunus avium L.) in Turkey. Egypt Journal of Biological Pest Control 31(1):1-11. doi:10.1186/s41938-021-00385-7.
Akbari, S.L., Rahnama, K., Golmohammadi, M., Nasrollanejad, S. 2020. Quorum-quenching endophytic bacteria inhibit disease caused by Pseudomonas syringae pv. syringae in Citrus cultivars. Journal of Basic Microbiology 60(9):746-757. doi:10.1002/jobm.202000038.
Alengebawy, A., Abdelkhalek, S.T., Qureshi, S.R., Wang, M.Q. 2021. Heavy metals and pesticides toxicity in agricultural soil and plants: Ecological risks and human health implications. Toxics 9(3):42-74. doi:10.3390/toxics9030042.
Altimira, F., Yáñez, C., Bravo, G., González, M., Rojas, L.A., Seeger, М. 2012. Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiology 12(1):193. doi:10.1186/1471-2180-12-193.
Aprile, F., Heredia-Ponce, Z., Cazorla, F.M., de Vicente, A., Gutiérrez-Barranquero, J.A. 2021. A large Tn7-like transposon confers hyperresistance to copper in Pseudomonas syringae pv. syringae. Applied and Environmental Microbiology 87(5):е02528-20. doi:10.1128/AEM.02528-20.
Askari, T.H., Gani, M., Wani, A.R. 2021. Nematodes associated with stone fruits and their management strategies. p. 423436. In Mir, M.M., Igbal, U., Mir, S.A. (eds.) Production technology of stone fruits. Springer, Singapore, Singapore. doi:10.1007/978-981-15-8920-1_16.
Beltrán, M.F., Osorio, V., Lemus, G., Millas, P., France, A., Correa, F., et al. 2021. Bacterial community associated with canker disease from sweet cherry orchards of central valley of Chile presents high resistance to copper. Chilean Journal of Agricultural Research 81:378-389. doi:10.4067/50718-58392021000300378.
Børve, J., Meland, M., Stensvand, A. 2007. The effect of combining rain protective covering and fungicide sprays against fruit decay in sweet cherry. Crop Protection 26(8):1226-1233. doi:10.1016/j.cropro.2006.10.020.
Børve, J., Stensvand, A. 2003. Use of a plastic rain shield reduces fruit decay and need for fungicides in sweet cherry. Plant Disease 87(5):523-528. doi:10.1094/PDIS.2003.87.5.523.
Børve, J., Wenneker, M., Spies, J.I., Brurberg, M.B., Pham, K., Stensvand, A. 2025. Impact of Pseudomonas syringae on sweet cherry and plum trees in nurseries and in early-stage sweet cherry orchards. European Journal of Plant Pathology 2025:03042. doi:10.1007/s10658-025-03042-7.
Caetano, A.L., Marques, C.R., Gongalves, F., Da Silva, E.F., Pereira, R. 2016. Copper toxicity in a natural reference soil: ecotoxicological data for the derivation of preliminary soil screening values. Ecotoxicology 25(1):163-177. doi:10.1007/s10646-015-1577-7.
Cao, T., Duncan, R.A., Kirkpatrick, B.C., Shackel, K.A., DeJong, Т.М. 2013. Effect of calcium and nitrogen fertilization on bacterial canker susceptibility in stone fruits. Fruits 68(3):245-254. doi:10.1051/fruits/2013071.
Carroll, J., Robinson, T., Burr, T., Hoying, S., Cox, K. 2010. Evaluation of pruning techniques and bactericides to manage bacterial canker of sweet cherry. New York Fruit Quarterly 18(1):9-15.
Cazorla, F.M., Arrebola, E., Sesma, A., Pérez-García, A., Codina, J.C., Murillo, J., et al. 2002. Copper resistance in Pseudomonas syringae strains isolated from mango is encoded mainly by plasmids. Phytopathology 92(8):909-916. doi:10.1094/PHYTO.2002.92.8.909.
Chen, G., Qiao, Y., Liu, F., Zhang, X., Liao, H., Zhang, R., et al. 2020. Dissipation and dietary risk assessment of kasugamycin and saisentong in Chinese cabbage. Environmental Science and Pollution Research 27:35228-35238. doi:10.1007/s11356-020-09827-5.
Cirvilleri, G., Spina, S., lacona, C., Catara, A., Muleo, R. 2008. Study of rhizosphere and phyllosphere bacterial community and resistance to bacterial canker in genetically engineered phytochrome A cherry plants. Journal of Plant Physiology 165(10):1107-1119. doi:10.1016/j.jplph.2008.01.009.
Connell, S.R., Tracz, D.M., Nierhaus, K.H., Taylor, D.E. 2003. Ribosomal protection proteins and their mechanism of tetracycline resistance. Antimicrobial Agents and Chemotherapy 47(12):3675-3681. doi:10.1128/aac.47.12.36753681.2003.
Cook, R.J., Baker, K.F. 1983. The nature and practice of biological control of plant pathogens. American Phytopathological Society, Saint Paul, Minnesota, USA.
Cui, W., Fiore, N., Figueroa, F., Rubilar, C., Pizarro, L., Pinto, M., et al. 2023. Transcriptome analysis of sweet cherry (Prunus avium |.) cultivar 'Lapins' upon infection of Pseudomonas syringae pv. syringae. Plants 12(21):3718. doi:10.3390/plants12213718.
Dulla, G.F., Krasileva, K.V., Lindow, S.E. 2010. Interference of quorum sensing in Pseudomonas syringae by bacterial epiphytes that limit iron availability. Environmental Microbiology 12(6):1762-1774. doi:10.1111/j.14622920.2010.02261.x.
Eitas, T.K., Nimchuk, Z.L., Dangl, J.L. 2008. Arabidopsis TAO1 is a TIR-NB-LRR protein that contributes to disease resistance induced by the Pseudomonas syringae effector AvrB. Proceedings of the National Academy of Sciences of the United States of America 105(17):6475-6480. doi:10.1073/pnas.0802157105.
Fan, X., Saleem, T., Zou, H. 2022. Copper resistance mechanisms in plant pathogenic bacteria. Phytopathologia Mediterranea 61(1):29-138. doi:10.36253/phyto-13282.
FAO. 2025a. Production: Crops and livestock products. FAO, Rome, Italy. Available at https://www.fao.org/faostat/en/#data/QCL (accessed 30 January 2025).
FAO. 2025b. Trade: Crops and livestock products. FAO, Rome, Italy. Available at http://www.fao.org/faostat/en/#rankings/countries_by commodity exports (accessed 30 January 2025).
Farhadfar, S., Keshavarzi, M., Bouzari, N., Moghadam, L., Soleimani, A. 2016. Susceptibility of cherries to bacterial canker (Pseudomonas syringae pv. syringae) in field and laboratory. International Journal of Agriculture and Forestry 6(1):2027. d0i:10.5923/j.ijaf.20160601.04.
Frenk, S., Ben-Moshe, T., Dror, |., Berkowitz, B., Minz, D. 2013. Effect of metal oxide nanoparticles on microbial community structure and function in two different soil types. PLOS ONE 8(12):е84441. doi:10.1371/journal.pone.0084441.
García, H., Miranda, E., López, M.A., Parra, S., Rubilar, C., Silva, E., et al. 2021. First report of bacterial canker caused by Pseudomonas syringae pv. morsprunorum race 1 on cherry in Chile. Plant Disease 105(10):3287. doi:10.1094/PDIS-1120-2524-PDN.
Garrett, C.M. 1986. Influence of rootstock on the susceptibility of sweet cherry scions to bacterial canker, caused by Pseudomonas syringae pvs morsprunorum and syringae. Plant Pathology 35(1):114-119. doi:10.1111/j.13653059.1986.tb01989.x.
Hancock, R.E. 1981. Aminoglycoside uptake and mode of action-with special reference to streptomycin and gentamicin: I. Antagonists and mutants. Journal of Antimicrobial Chemotherapy 8(4):249-276.
Hogetveit, W.R., Jakobsen, H. 2005. Cause of damage to sweet cherry flower buds in southern Norway. Acta Horticulturae 667:467-470. doi:10.17660/ActaHortic.2005.667.67.
Hulin, M.T., Mansfield, J.W., Brain, P., Xu, X., Jackson, R.W, Harrison, R.J. 2018. Characterization of the pathogenicity of strains of Pseudomonas syringae towards cherry and plum. Plant Pathology 67(5):1177-1193. doi:10.1111/ppa.12834.
Hulin, M.T., Vadillo Dieguez, A., Cossu, F., Lynn, S., Russell, K., Neale, H.C., et al. 2022. Identifying resistance in wild and ornamental cherry towards bacterial canker caused by Pseudomonas syringae. Plant Pathology 71(4):949-965. doi:10.1111/ppa.13513.
Husseini, A., Akköprü, А. 2020. The possible mechanisms of copper resistance in the pathogen Pseudomonas syringae pathovars in stone fruit trees. Phytoparasitica 48(5):705-718. doi:10.1007/s12600-020-00828-1.
Hwang, M.S., Morgan, R.L., Sarkar, S.F., Wang, P.W., Guttman, D.S. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Applied Environmental Microbiology 71(9):5182-5191. doi:10.1128/AEM.71.9.5182-5191.2005.
Iliéié, R., Balaz, J., Ognjanov, V., Josié, D., Vlajié, S., Ljubojevié, M., et al. 2018. Evaluation of cherry cultivar susceptibility to bacterial canker and leaf spot disease. Journal of Phytopathology 166:799-808. doi:10.1111/jph.12763.
Jones, J.B., Vallad, G.E., Iriarte, F.B., Obradovi, A., Wernsing, M.H., Jackson, L.E., et al. 2012. Considerations for using bacteriophages for plant disease control. Bacteriophage 2(4):208-214. doi:10.4161/bact.23857.
Keith, L.M., Bender, C.L. 1999. AlgT (с22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. Journal of Bacteriology 181(23):7176-7184. doi:10.1128/jb.181.23.7176-7184.1999.
Khezri, M., Mohammadi, M. 2018. Identification and characterization of Pseudomonas syringae pv. syringae strains from various plants and geographical regions. Journal of Plant Protection Research 58(4):354-361. doi:10.24425/jppr.2018.124647.
Kidambi, S.P., Sundin, G.W., Palmer, D.A., Chakrabarty, A.M., Bender, C.L. 1995. Copper as a signal for alginate synthesis in Pseudomonas syringae pv. syringae. Applied and Environmental Microbiology -61(6):2172-2179. doi:10.1128/aem.61.6.2172-2179.1995.
Kim, S.H., Kwon, S.1., Saha, D., Anyanwu, N.C., Gassmann, W. 2009. Resistance to the Pseudomonas syringae effector HopA1 is governed by the TIR-NBS-LRR protein RPS6 and is enhanced by mutations in SRFR1. Plant Physiology 150(4):17231732. doi:10.1104/pp.109.139238.
Ladomersky, E. Petris, M.J. 2015. Copper tolerance and virulence in bacteria. Metallomics 7(6):957-964. doi:10.1039/c4mt00327f.
Lamb, D.T., Naidu, R., Ming, H., Megharaj, М. 2012. Copper phytotoxicity in native and agronomical plant species. Ecotoxicology and Environmental Safety 85:23-25. doi:10.1016/j.ecoenv.2012.08.018.
Lamichhane, J.R., Osdaghi, E., Behlau, F., Köhl, J., Jones, J.B., Aubertot, J.N. 2018. Thirteen decades of antimicrobial copper compounds applied in agriculture. A review. Agronomy for Sustainable Development 38:28. doi:10.1007/s13593-0180503-9.
Latorre, B.A., Jones, A.L. 1979. Evaluation of weeds and plant refuse as potential sources of inoculum of Pseudomonas syringae in bacterial canker of cherry. Phytopathology 69(10):1122-1125.
Lewis, J.A., Papavizas, С.С. 1991. Biocontrol of plant diseases: the approach for tomorrow. Crop Protection 10(2):95-105. doi:10.1016/0261-2194(91)90055-V.
Li, X., Zhu, Y.G., Shaban, B., Bruxner, T.J., Bond, P.L., Huang, L. 2015. Assessing the genetic diversity of Cu resistance in mine tailings through high-throughput recovery of full-length copA genes. Scientific Reports 5(1):13258. doi:10.1038/srep13258.
Lillrose, T., Lang, G.A., Sundin, G.W. 2017. Strategies to minimize bacterial canker in high density sweet cherry orchards. Acta Horticulturae 1(1161):457-462. doi:10.17660/ActaHortic.2017.1161.73.
Long, L.E., Kaiser, С. 2010. Sweet cherry rootstocks for the Pacific Northwest. Pacific Northwest Extension Publishing 619:1-8.
Lu, L., Zhao, S., Deng, L., Chen, Y., Liu, X., Li, D. 2012. Residues and dynamics of kasugamycin in chilli and soil. Bulletin of Environmental Contamination and Toxicology 89:649-653. doi:10.1007/s00128-012-0746-0.
Maguvu, T.E., Frias, R.J., Hernandez-Rosas, A.l., Shipley, E., Dardani, G., Nouri, M.T., et al. 2024. Pathogenicity, phylogenomic, and comparative genomic study of Pseudomonas syringae sensu lato affecting sweet cherry in California. Microbiology Spectrum 12(10):e01324-24. doi:10.1128/spectrum.01324-24.
Marroni, M.V., Casonato, S., Pitman, A.R., Visnovsky, S.B., Beresford, R.M., Jones, E.E. 2024. Review of Pseudomonas species causing bacterial canker of Prunus species with emphasis on sweet cherry (Prunus avium) in New Zealand. European Journal of Plant Pathology 168(2):297-314. doi:10.1007/s10658-023-02755-3.
Melakeberhan, H., Jones, A.L., Bird, G.W. 2000. Effects of soil pH and Pratylenchus penetrans on the mortality of 'Mazzard' cherry seedlings and their susceptibility to Pseudomonas syringae pv. syringae. Canadian Journal of Plant Pathology 22(2):131-137. doi:10.1080/07060660009500486.
Mgbechi-Ezeri, J., Porter, L., Johnson, K.B., Oraguzie, № 2017. Assessment of sweet cherry (Prunus avium L.) genotypes for response to bacterial canker disease. Euphytica 213:145. doi:10.1007/s10681-017-1930-4.
Mitre, |, Mitre, V., Sestras, A., Sestras, В. 2011. A new fungicide based on copper with low concentration and high dispersion for plum, sweet cherry, and sour cherry. Bulletin of University of Agricultural Sciences and Veterinary Medicine ClujNapoca, Horticulture 68(1):97-102.
Moya-Elizondo, E. (ed.) 2020. Impact of phytopathogenic bacteria in Chilean fruit crop productions and advances in management and control. p. 37-51. In The plant health, a view from the plant bacteriology. Ediciones Facultad de Agronomía-Universidad de Concepción, Chillán, Chile.
ODEPA. 2024. Catastro frutícola principales resultados región de Atacama. ODEPA, Santiago, Chile. Available at https://www.odepa.gob.cl/estadisticas-del-sector/catastros-fruticolas/catastro-fruticola-ciren-odepa (accessed 30 January 2025).
Okuyama, A., Machiyama, N., Kinoshita, T., Tanaka., N. 1971. Inhibition by kasugamycin of initiation complex formation on 30S ribosomes. Biochemical and Biophysical Research Communications 43(1):196-199. doi:10.1016/S0006291X(71)80106-7.
Osorio, V., Millas, P., Lemus, G., Otárola, J., France, A. 2020. Detección en campo y alternativas de control. р. 47-61. In Lemus, S. (ed.) Cáncer bacterial del cerezo: Epidemiología de la enfermedad y estrategias de control. Boletín INIA. N·420. Instituto de Investigaciones Agropecuarias (INIA), Rengo, Chile.
Pan, X., Zhao, S., Wang, Y., Li, M., He, L., Zhuang, Q. 2020. Complete genome sequencing of Pseudomonas syringae pv. actinidiae Biovar 3, P155, kiwifruit pathogen originating from China. Bioscience Journal 36(6):2220-2228. doi:10.14393/BJ-v36n6a2020-47896.
Pang, Z., Raudonis, R., Glick, B.R., Lin, T.J., Cheng, Z. 2019. Antibiotic resistance in Pseudomonas aeruginosa: Mechanisms and alternative therapeutic strategies. Biotechnology Advances 37(1):177-192. doi:10.1016/j.biotechadv.2018.11.013.
Pinheiro, L.A., Pereira, C., Frazäo, C., Balcäo, V.M., Almeida, A. 2019. Efficiency of phage фб for biocontrol of Pseudomonas syringae pv. syringae: an in vitro preliminary study. Microorganisms 7(9):286-309. doi:10.3390/microorganisms7090286.
Quero-García, J., Campoy, J.A., Barreneche, T., Le Dantec, L., Wenden, B., Fouché, M., et al. 2019. Present and future of marker-assisted breeding in sweet and sour cherry. Acta Horticulturae 1(1235):1-14. doi:10.17660/ActaHortic.2019.1235.1.
Rabiey, M., Roy, S.R., Holtappels, D., Franceschetti, L., Quilty, B.J., Creeth, R., et al. 2020. Phage biocontrol to combat Pseudomonas syringae pathogens causing disease in cherry. Microbial Biotechnology 13(5):1428-1445. doi:10.1111/1751-7915.13585.
Rashtbari, M., Sinegani, A.A. 2020. Efficiency of soil extracellular enzymes in soils treated by organic and mineral conditioners against mostly applied veterinary antibiotics (gentamicin, oxytetracycline and penicillin). Journal of Soil Management and Sustainable Production 10(3):1-26. doi:10.22069/ejsms.2021.17664.1931.
Roberts, M.C. 2005. Update on acquired tetracycline resistance genes. FEMS Microbiology Letters 245(2):195-203. doi:10.1016/j.femsle.2005.02.034.
Rodriguez, C., Lang, L., Wang, A., Altendorf, K., Garcia, F., Lipski, A. 2006. Lettuce for human consumption collected in Costa Rica contains complex communities of culturable oxytetracycline-and gentamicin-resistant bacteria. Applied and Environmental Microbiology 72(9):5870-5876. doi:10.1128/AEM.00963-06.
Rubilar-Hernandez, C., Alvarez-Maldini, C., Pizarro, L., Figueroa, F., Villalobos-González, L., Pimentel, P., et al. 2024. Nitric oxide mitigates the deleterious effects caused by infection of Pseudomonas syringae pv. syringae and modulates the carbon assimilation process in sweet cherry under water stress. Plants 13(10):1361. doi:10.3390/plants13101361.
SAG. 2023. Lista de plaguicidas con autorización. Servicio Agrícola y Ganadero (SAG), Santiago, Chile. Available at https://www.sag.gob.cl/content/lista-de-plaguicidas-autorizados-0 (accessed 25 June 2024).
Sayler, R., Southwick, S., Yeager, J., Glozer, K., Little, E., Kirkpatrick, В. 2002. Effects of rootstock and budding height on bacterial canker in French prune. Plant Disease 86(5):543-546. doi:10.1094/PDIS.2002.86.5.543.
Schnake, A., Hartmann, M., Schreiber, S., Malik, J., Brahmann, L., Yildiz, |, et al. 2020. Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants. Journal of Experimental Botany 71(20):6444-6459. doi:10.1093/jxb/eraa317.
Scholz-Schroeder, B.K., Hutchison, M.L., Grgurina, |., Gross, D.C. 2001. The contribution of syringopeptin and syringomycin to virulence of Pseudomonas syringae pv. syringae strain B301D on the basis of sypA and syrB1 biosynthesis mutant analysis. Molecular Plant Microbe Interactions 14(3):336-348. doi:10.1094/MPMI.2001.14.3.336.
Shade, A., Klimowicz, A.K., Spear, R.N., Linske, M., Donato, J.J., Hogan, C.S., et al. 2013. Streptomycin application has no detectable effect on bacterial community structure in apple orchard soil. Applied and Environmental Microbiology 79(21):6617-6625. doi:10.1128/AEM.02017-13.
Spotts, R.A., Cervantes, L.A. 1995. Copper, oxytetracycline, and streptomycin resistance of Pseudomonas syringae pv. syringae strains from pear orchards in Oregon and Washington. Plant Disease 79(11):1132-1135. doi:10.1094/PD-79-1132.
Spotts, R.A., Wallis, K.M., Serdani, M., Azarenko, А.М. 2010. Bacterial canker of sweet cherry in Oregon-Infection of horticultural and natural wounds, and resistance of cultivar and rootstock combinations. Plant Disease 94(3):345-350. doi:10.1094/PDIS-94-3-0345.
Sundin, G.W., Bender, C.L. 1993. Ecological and genetic analysis of copper and streptomycin resistance in Pseudomonas syringae pv. syringae. Applied and Environmental Microbiology 59(4):1018-1024. doi:10.1128/aem.59.4.1018-1024.1993.
Sundin, G., Wang, N. 2018. Antibiotic resistance in plant pathogenic bacteria. Annual Review of Phytopathology 56(1):161180. doi:10.1146/annurev-phyto-080417-045946.
Svenningsen, N.B., Martínez-García, E., Nicolaisen, M.H., de Lorenzo, V., Nybroe. O. 2018. The biofilm matrix polysaccharides cellulose and alginate both protect Pseudomonas putida mt-2 against reactive oxygen species generated under matric stress and copper exposure. Microbiology 164(6):383-888. doi:10.1099/mic.0.000667.
Tasho, R.P., Ryu, S.H., Cho, J.Y. 2020. Effect of sulfadimethoxine, oxytetracycline, and streptomycin antibiotics in three types of crop plants-root, leafy, and fruit. Applied Sciences 10(3):1111. doi:10.3390/app10031111.
Thomidis, T., Exadaktylou, E. 2013. Effect of a plastic rain shield on fruit cracking and cherry diseases in Greek orchards. Crop Protection 52:125-129. doi:10.1016/j.cropro.2013.05.022.
Vanneste, J., 2020. Copper resistance in Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit, in New Zealand: a review. p. 67-78. In Moya-Elizondo, E. (ed.) The plant health, a view from the plant bacteriology. Ediciones Facultad de Agronomía-Universidad de Concepción, Chillán, Chile.
Vasebi, Y., Khakvar, R., Faghihi, M.M., Vinatzer, B.A. 2019. Genomic and pathogenic properties of Pseudomonas syringae pv. syringae strains isolated from apricot in East Azerbaijan province, Iran. Biocatalysis and Agricultural Biotechnology 19(1):101167-101176. doi:10.1016/j.bcab.2019.101167.
Vignati, E., Lipska, M., Dunwell, J.M., Caccamo, M., Simkin, A.J. 2022. Fruit development in sweet cherry. Plants 11(12):15311554. doi:10.3390/plants11121531.
Wei, X., Wu, S.C., Nie, X.P., Yediler, A., Wong, М.Н. 2009. The effects of residual tetracycline on soil enzymatic activities and plant growth. Journal of Environmental Science and Health, Part B 44(5):461-471. doi:10.1080/03601230902935139.
Xu, Q., Zhang, M. 2014. Oxytetracycline uptake and growth of radish plants (Raphanus sativus L.) in animal manureamended soils. Agricultural Science and Technology 15(7):1229. doi:10.1371/journal.pone.0148015.
Youssef, S.A., Bashour, 1.1. 2017. Uptake of antibiotics by plants. р. 221-237. In Hashmi, M., Strezov, V., Varma, A. (eds.) Antibiotics and antibiotics resistance genes in soils. Springer, Cham, Germany.
Yu, Y., Liu, H., Xia, H., Chu, Z. 2023. Double- or triple-tiered protection: Prospects for the sustainable application of copperbased antimicrobial compounds for another fourteen decades. International Journal of Molecular Sciences 24:10893. doi:10.3390/ijms241310893.
© 2025. This work is published under https://creativecommons.org/licenses/by/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.