Diseases and Pests Noxious to Pleurotus Spp.

+ModelRAM-242; No. of Pages 11 ARTICLE IN PRESS Rev Argent Microbiol. 2017;xxx(xx):xxx---xxx REVISTA ARGENTINA DE MICROBIOLOGÍA www.elsevier.es/ram SPECIAL ARTICLE Diseases and pests noxious to Pleurotus spp. mushroom crops Marcelo B. Bellettini a,∗ , Sebastião Bellettini b , Fernanda A. Fiorda c , Alessandra C. Pedro a , Fabiane Bach a , Miriam F. Fabela-Morón d , Rosemary Hoffmann-Ribani a a Department of Chemical Engineering, Graduate Program in Food Engineering, Federal University of Paraná, Curitiba, Brazil b Institute for Technical Assistance and Rural Extension of Paraná, Curitiba, Brazil c Department of Food Science and Technology, Federal University of Pampa, Itaqui, Brazil d Food Technology Department, CONACYT, Center for Research and Assistance in Technology and Design of the Jalisco State, Mérida, Mexico Received 24 April 2017; accepted 29 August 2017 KEYWORDS Abstract The Pleurotus genus is one of most extensively studied white-rot fungi due to its Oyster mushroom; exceptional ligninolytic properties. It is an edible mushroom that possesses biological effects, Bacteriosis; as it contains important bioactive molecules. It is a rich source of nutrients, particularly pro- Fungal diseases; teins, minerals as well as vitamins B, C and D. In basidiomycete fungi, intensive cultivations Mycovirus; of edible mushrooms can often be affected by some bacterial, mold and virus diseases that Nematodes; rather frequently cause dramatic production loss. These infections are facilitated by the par- Flies ticular conditions under which mushroom cultivation is commonly carried out such as warm temperatures, humidity, carbon dioxide (CO2 ) levels and presence of pests. There is not much bibliographic information related to pests of mushrooms and their substrates. The updated review presents a practical checklist of diseases and pests of the Pleurotus genus, providing useful information that may help different users. © 2017 Asociación Argentina de Microbiologı́a. Published by Elsevier España, S.L.U. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). PALABRAS CLAVE Enfermedades y plagas nocivas en el cultivo del hongo Pleurotus Hongo ostra; Bacteriosis; Resumen El Pleurotus es uno de los hongos de la podredumbre blanca más extensamente Micosis; estudiados debido a sus excepcionales propiedades lignocelulolíticas. Es un hongo comestible y Micovirus; también tiene varios efectos biológicos, ya que contiene importantes moléculas bioactivas. Es una fuente rica de nutrientes, particularmente de proteínas y minerales, así como de vitaminas ∗ Corresponding author. E-mail address: [email protected] (M.B. Bellettini). https://doi.org/10.1016/j.ram.2017.08.007 0325-7541/© 2017 Asociación Argentina de Microbiologı́a. Published by Elsevier España, S.L.U. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Bellettini MB, et al. Diseases and pests noxious to Pleurotus spp. mushroom crops. Rev Argent Microbiol. 2017. https://doi.org/10.1016/j.ram.2017.08.007 Diseases and pests noxious to Pleurotus spp. ity.U. The are still allowed have failed to adequately control major disease is characterized by a yellow discoloration of the mushroom diseases as resistance is easily induced25 .0/). which involve significant costs.) P. ticular conditions under which the mushroom cultivation is P. associated with brown-reddish blotches on P. which may act individually or have occurrence of morphological variants or aggressive patho- interactive effects among them4. and ventilation to prevent eases are very difficult to control. reactans are mostly challenged by mushroom disease of bacterial and fungal associated with superficial yellow lesions on P. are the excess of water in the casing layer and a low aeration Mushroom survival and multiplication are associated to rate in the growing-house. as well as cleaning including plant pathogenic fungi and mushrooms. namely Environmental controls. cultivation rooms play important roles in diminishing the tion has been known to cause few significant phenotypic spread of the disease3 . Kumm33 .org/licenses/by- nc-nd/4. Most chemicals that yellowing that can cause the most severe damage19 . mushroom growers are frequently pseudo-tissues. humid. tal conditions occurring at high relative humidity levels in This genus requires little growth time. Although careful farm management importance of keeping mushroom caps dry by regulating and extreme hygiene may prevent major attacks. ostreatus origin. temperature. P. ostreatus (Jacq. Pseudomonas agarici and P. plex composed by interactions between Pseudomonas spp. relative humidity. These infections are facilitated by the par. Estas infecciones son facilitadas por las condiciones par- ticulares bajo las cuales comúnmente se cultivan los hongos. tolaasii and P. There. the use of Among the diseases observable during the cultivation of chemicals in cultivation leaves undesired residues. S. 2017.2017. carbon dioxide level. on the entire stem. shelf life quality bacterial propagation. Destructive disease levels are induced by environmen- cultivated on non-composted lignocellulosic substrates15. C y D. particularly proteins. however individually these bacte- commonly carried out. mushroom crops.org/10. of basid. B. caused by various viral infections57 . Favorable to bacterial blotch outbreaks mushrooms1 . such as phenolic compounds. Bacteriosis is an unpredictable disease that can occur dur- iomycetes class belongs to a group known as ‘‘white rot ing the first or second sporophore flush. such as warm temperatures.1016/j. These conditions can induce the a number of factors.ram. temperature. growers have faced serious challenges low discoloration of the sporocarps. Publicado por Elsevier España. often elongated and coalescing areas fore. of Pages 11 ARTICLE IN PRESS 2 M.007 . reactans. steroids and polysaccharides39. and P. Bellettini et al. No. y proporciona información que puede ser de utilidad para los productores.69 . terpenes. pileus and hydropic. The use of disinfectants such as chlorine (household bleach) and the application of selected Bacterial yellowing fungicides is generally practiced in the cultivation of mush- rooms. fúngicas y virales. room cultivation (Table 1). it is of which have been banned from use.08. lo que con frecuencia produce Moscas pérdidas significativas en la producción.62 . ostreatus Due to these reasons. Los cultivos intensivos de hongos comestibles del tipo basidiomicetos a menudo son Nematodos. compared to other growing chambers. Moreover. Bacterial diseases stituents. but rapidly becomes offen- Diseases sive and nauseating8 .+Model RAM-242. Mushrooms are a rich source of nutrients. While an increasing number of commercial farms cul. Rev Argent Microbiol. which in pathogenicity assays have caused yel- tivate mushrooms.61. Symptomatic basidiomata then stop growing. good alternatives have to be found. Nair and Bradley51 emphasized the effects on mushrooms. afectados por enfermedades bacterianas. mineral vitamins as well as bioactive con.. P. carbon dioxide (CO2 ) levels and presence of pests3. Fungal viruses. several Pleurotus eryngii. including low relative humid- mycoviruses. tales como temperaturas cálidas y elevada humedad. Introduction are lost due to lower productivity. a high percentage of products eryngii and P. ria cause different symptoms. some dis. turn a reddish-brown color and are affected by rot- ting. of edible mushrooms can often be affected by some fungal According to Lo Cantore and Iacobellis45 . whatever the growing procedure is.36 . causing great yield fungi’’ as they produce a white mycelium and are generally loss. https://doi. © 2017 Asociación Argentina de Microbiologı́a. The infec. et al. is severely affected by diseases that are still asymptomatic at the time of harvest. the most likely causal agents of yellowing in both P. sporocarps. Este es un artı́culo Open Access bajo la licencia CC BY-NC-ND (http://creativecommons.4 . Pseudomonas spp. which is almost alcohol-like and pleasant at first. Esta revisión presenta una lista práctica y actualizada de enfermedades y plagas frecuentes durante el cultivo del hongo comestible Pleurotus. The Pleurotus spp. persistently infect fungal taxonomic groups. Diseased sporophores exhale an odor. tolaasii is consistently ity.B. Moreover. Intensive cultivations vars of Pseudomonas reactans and Pseudomonas tolaasii48 . reactans Please cite this article in press as: Bellettini MB. reactans are reported as Bacterial and fungal diseases are a major problem in mush.L. decrease in quality and shortened shelf life. the etiology of and bacterial diseases that rather frequently cause dramatic lesions on cultivated Pleurotus ostreatus involves a com- production loss7 . Zhang et al. albeit with disappointing results.58 France’’ Virus (OMIV) --. Munsch and Alatossova49 P. hazianum Kredics et al. such as lowering relative air humidity.25 .. factor48 . Several other disinfectants and antibiotics. tolaasii. https://doi. . such as chlo- room hyphosphere49 .71 .44 . from primordia nus edodes31. blotch disease26.2017. No. The bacterial brown blotch disease.10 . Kim et al.30 . and farm76 . crops 3 Table 1 Diseases and pathogens noxious to Pleurotus spp. Iacobellis and Lavermicocca33 Brown P. Rev Argent Microbiol. The stipes tended to recurve Bacterial brown blotch near the base and the sporocarp was upright. chlorine has symptom.50 .49 . Pleurotus ostreatus-Infecting Lim et al. watering with low concentration of chlorine solution (cal. Bessette et al.75. Differences in susceptibility/resistance exhibited by var. mushroom crops. Diseases and pests noxious to Pleurotus spp. 7.41 T. before all of the substrate bags were removed from the ease. tolaasii is a bacterium.70 . The adding sodium hypochlorite or chemicals containing iodine disease incidence has been different each year.58 --. 2017. it continues to rot due to a volatile toxin. Marlowe and Romaine46 Green mold Trichoderma atroviride Kredics et al. P. caused appearance to commercial maturation. and kasugamycin. ostreatus caused by P.+Model RAM-242. P. serious bacterial diseases for the oyster mushroom. which causes bacterial blotches ious commercial strains of P.42 T. P.08. When mushrooms remain wet. When P. little effect since the bacterial population reproduces at a tovsin. Much research has been done to figure ease occurred on a farm. Controls. tolaasii only when in contact with Please cite this article in press as: Bellettini MB. however. pulmonarius virus (Ppv) Molin and Lapierre47 belong to the V group of fluorescent Pseudomonas and is rate that neutralizes the effect of the oxidizing agent27 . González et al. role in disease incidence. eryngii can in oyster mushroom Pleurotus spp. longibrachiatum Kredics et al. According to Bruno et al. has been one of the most generally try. Once the dis- to irrigation water19 . Liu et al. Munsch and Alatossova49 . Mushroom producers by the bacterium P. and then deformed with an increase in severity.6 . and in Shitake Lenti- occur in all basidioma development phases.54 . eryngii. has proven to be the major virulence most commonly utilized chemicals for blotch disease con. say that acetic acid at 87. et al. et al. Yellowing of P..org/10.4 and 69. pleurotum Park et al. of Pages 11 ARTICLE IN PRESS Diseases and pests noxious to Pleurotus spp.31 . Tsukamoto et al. ostreatus develops the brown blotch trol. an extracellular lipodepsipeptide toxin pro- cium chloride and chlorinated compounds) are currently the duced by P. pleuroticola Komoń-Zelazowska et al.37 . P.40 Virus (OMSV) ‘‘La Oyster Mushroom Isometric Ro et al. Ferri et al.76 Soft rot Pantoea spp.42 T. Sphingomonas spp. Murata blotch et al.42 T. Pantoea spp. The dis- vent yellowing or halt its development and spread by ease often occurs over a large geographical area. Enterobacter amnigenus. Bellettini and Fiorda2 T. to pre. mushroom crops. virens Kredics et al. in Flamulina spp. eryngii Spherical Virus (PeSV) Ro et al. produced by P.27 .56 Mold Dry bubble Lecanicillium fungicola Gea et al. essential oils. considered to be saprophytic bacteria inhabiting the mush. other bacterial species have been isolated from have also been tried for their ability to control bacterial symptomatic basidiomata (Pseudomonas costantinii. tolaasii Han et al.72 T.. citrinoviride Woo et al.37 .6 reported that the yellow blotch in yellowing of P. eryngii could play an important in the button mushroom Agaricus spp. agarici formed a clean yellow fluid on the surface of the cluster at first.9.38 Brown spot Gliocladium roseum Chen and Huang12 Virus Die-back Oyster Mushroom Spherical Kim et al. Source Diseases Patho-vars References Bacterium Bacterial Pseudomonas reactans Bruno et al. Reyes necrosis et al. agarici Bessette et al.ram. Geels et al. Tolaasin. tolaasii.43 Spherical (PoV1) --. According to Bruno et al. and Moraxella an interesting antibacterial tool to prevent and/or halt the osloensis). Rodriguez-Estrada and Royse59 Stipe Ewingella americana Fletcher and Gaze21 .42 Cobweb Cladobotryum mycophilum Carrasco et al.8 yellowing Iacobellis and Lavermicocca33 . Bacil.8 . it became very difficult to control out an adequate method to prevent or control this dis.9 mM may be considered Staphylococcus epidermidis. it is safe to lus cereus.007 .19 .8 and Kim ramine T and bronopol.1016/j. Kim et al.. Disease incidence of pri. the stipe and cap of mushrooms within 8 days after the duction. strain 9045. On inoculation of healthy P. et al. P. These lesions consist of slightly Compounds containing active chlorine are. The typical symptoms of soft rot disease include these isolates caused disease and could be reisolated25 .2017. but frequently. important to maintain good evaporation from the bed sur- isms and/or specific phages have also been investigated. at harvest. on symptomatic samples collected from mushroom farms. which can be round or spreading31 . https://doi. eryngii37 . Liu et al. Ewingella americana was identified as an opportunistic Bacteria may reach and colonize on the surface of the pathogen55 . either as epiphytes or as causes dry bubble disease in commercially cultivated mush- pathogens73 . ostreatus63 . strain and increases during storage. ostreatus. stalks at an early development stage. However. mucus- enable them to interact specifically with P. at present.56 reported that the pres- fluorescens. It is important to control variable browning reaction in the center of the mushroom the transfer of pathogen from the spawned substrate to the stipe34 . tolaasii. eryngii without affecting mushroom yield44 .ram. of Pages 11 ARTICLE IN PRESS 4 M. the disease affects Stipe necrosis only the top external layers of the pileus tissues and is restricted to 2---3 mm below the pileus surface76 . Diseases and pests noxious to Pleurotus spp. mushroom crops. Examined in longitudinal section. and it is therefore Biological control methods with antagonistic microorgan.56 demonstrated the predominance of E. In all cases. Concerning Enterobacteriaceae. detoxifies tolaasins produced by P. It supports the hypothesis that P. ameri- from the substrate. finally leading to a mushy soft rot accompanied The pathogen causes blotch symptoms on the pileus. In P. the most commonly utilized chemicals for bacterial disease cally.org/10. ostreatus. tolaasii and According to González et al. concave spots. tolaasii66 . which could be pathogenic to cultivated mush.007 . cana in biota of retail fresh P.44 isolated ing membrane pores and disrupting the cellular membrane strains belonging to Pantoea beijingensis (growth occurs at structure. but rarely order to manage this disease75 . although its presence was not dom- tus. This mold erally associated with plants. ostrea. 2017. discoloration of the stipes. the brown tissue pileus during the early fruiting body development stages in extends from the base of the stalk to the cap. little is known pileus during the early fruiting body development stage about their prevalence and their contribution to the total while the young pileus is still in contact with the substrate.+Model RAM-242. a dark brown water drop in the early stages of infection. eryngii. the commercial production of Pleurotus spp. ter. it has rarely been cultivated by growers. spotting occurs at or near the edge of mushroom caps. However. it has been isolated from numerous other symptoms of water-soaked lesions on the stipes and pileus of basidiomycetes. E. Bellettini et al. Rev Argent Microbiol. symptoms are visible only at harvest. eryngii The disease is characterized by the formation of brown exhibiting symptoms of water-soaked lesions and soft rot lesions on mushroom caps and by bacterial growth in and in the stipes and pilei. ostreatus50 . L. 10---37 ◦ C) from lesions on the fruiting body of P. like fluid. has room. the brown spots and blotches enlarge of P. leaving a hollow cen- tive biological or chemical control measures are scarce. ostreatus fruiting body components activate tolaasin pro. is dry and has completely collapsed. americana is significantly suppresses the onset of the disease in P. ostreatus and have mechanisms that lesions expand gradually and constitute a viscous. Disease severity in the pileus is consis.30 . the brown tissue the bacterial pathogen in P. soft rot and mild browning of the tissues. ACCC50618 was resistant to brown blotch disease.08. Affected mushrooms may be wet Huge economic damage is due to a rapid spread of in appearance. some Pseudomonas isolates were screened for occurrence of internal stipe necrosis disease has occasion- their antagonistic ability toward P. E. The gram-negative bacterium Pantoea spp. The cause disease in P.1016/j. P. The affected areas are sunken and covered with sticky material.70 reported that a gram-positive bacterium. Typi. Dry bubble Soft rot Lecanicillium fungicola is a devastating pathogen in the mushroom industry. tent with primordia disease incidence for tested strains with The symptoms of internal stipe necrosis appear as a inoculation on spawned substrates. which causes significant losses in The genus Pantoea includes several species that are gen. and coalesce with others. rooms by producing various antifungal agents14 and is closely These results indicate that the pathogen is found in crops related to P. Another advantage of using strain 9405 is that it is inant in the analyzed samples. Watering with concentrations at 175 ppm active Blotches occur when mushrooms remain wet for a period of chlorine were effective for the reduction of soft rot disease 4---6 h after watering. control. being isolated in only 10% saprophytic to P. form. eryngii cultivations and effec.75 . ostreatus. however their ally been associated with water-logging of the mushroom in vivo suppressive effect was not satisfactorily proven20 . fungicola has also been mentioned as a pathogen of Please cite this article in press as: Bellettini MB. symptoms consisted of Tsukamoto et al. ostreatus. The In fact. Preliminary data also indicates that followed by the development of water-soaked lesions on P.B. ence of this bacterium was high in commercial products. No. Reyes et al. pathogenic in P. penetrates the cap tissue. by an offensive odor during growth59 . americana was Greater bacterial population from spawned substrates may identified as the causal agent of internal stipe necrosis result in more severe infection. However. tolaasii strains mushrooms are transferred to the cultivation room. in contrast to Pseudomonas of them. mordia may result directly from the bacterial colonization Reyes et al. microbial load of cultivated mushrooms. Although its pathogenicity for other species has not been reported as a causal agent of soft rot disease with been established. According to Zhang et al. because the fruit- ing bodies are very fragile and can easily be broken during Fungal diseases harvest and transport. face at all times21 . tion suggests that adjusting the pH of the substrate to 8---9 tion. C.72 . pleu.. Woo One of the main symptoms is a cobweb-like growth et al. This informa- development stage of the sporophores at the time of infec. The again in the substrate after inoculation with Pleurotus spp. mushroom crops. Trichoderma pleuroticola has disturbances such as watering. Green mold Cobweb The commercial production of oyster mushroom has been Several species of Cladobotryum. The colonies on the surface rapidly overwhelm the mush- appear with pasteurization.72 have observed that Trichoderma species are present of fungal mycelium over the surface of the mushrooms. fungicola increase pH to 7. brown. Diseases and pests noxious to Pleurotus spp. eryn- are asexual. pleuroticola. fungicola relies on strict hygiene.ram. The mycelial growth of green mold occurred depressed. The optimal pH for Trichoderma spp. fungicola is not often temperature is increased up to 30 ◦ C due to the generation found on wild mushroom. asperellum. accompanied by Please cite this article in press as: Bellettini MB. stalks. and the pathogen outbreaks. disease’’ in the cultivated mushroom Agaricus bisporus and T.08. fungicola. is observed at 15 ◦ C. some commercially grown P. T. gii began to show similar symptoms to the fungal disease morphs belonging to the genus Hypocrea (Ascomycota. and been found both on wild and cultivated P.5 is widely practiced. This is the main nated substrates54 .41 suggested the application of surface of infected sporophores46 . including C. Prochloraz was shown to (active ingredient: prochloraz-manganese). eryngii. where the addition of lime to cides. crops 5 Pleurotus pulmonarius46 .16 . citrinoviride. eventually result- the harvesting cycles. to inhibit spore germination of benomyl-susceptible iso- ol on infected hosts of L. Conidia were able to germinate and grow in 4 h. it has for benomyl-resistant strains. Pyrenomycetes. However. T. could rapidly spread from farm to farm. The causal C. et al.25 mg ml. While more research lates in a proper way. mycelium can quickly cover the king oyster mushroom (spawning). amor. ver- agents of green mold disease of cultivated oyster mush. 2017. mature choderma spp. at the initial phase of substrate preparation. The factor of cobweb disease in P. dendroides. The control dry bubble disease5 . green mold is not reported to be a severe dry bubble because the host is also sensitive to fungi. growth in green molds.1016/j. is completely inhibited by pasteurization at sporophores showed cracking and curling of the tissues and 60 ◦ C for 10 h. no mushrooms are produced from the contami. The hypothesis The control of L. ostreatus easily dislodged from the sporulating colony by external and its substrate. mode of transmission by which the pathogen is distributed Green mold infection of P. during spawn run (incubation phase) and in debris. atroviride. In severe substrates. rotum. thy- been shown that 1-octen-3-ol inhibits the germination of L. Trichoderma The spores are relatively large and multicellular. Rev Argent Microbiol. However. longibrachiatum.+Model RAM-242. mycophilum. while chlorothalonil was effective is needed to contribute its effects on management. fungicola to Sporgon has decreased. Hypocreaceae).007 . Hypocreales. In contrast. T. caused by Cladobotryum mycophilum in A. virens). benomyl and propineb were found been recently researched is the use of volatile 1-octen-3. pileus and gills. ostreatus is supposed to be to mushroom farms38 . Two distinct symptom syndromes are observed on the growth is acidic-neutral conditions (pH 5---7). substrates are they typical green mold symptoms. in a decrease of infection spread. are found in mushroom-growing countries worldwide9. of a possible reduction of T. https://doi. However. and (−)-menthol inhibited fungicola and that enhanced levels can effectively control green mold growth at concentrations as low as 0. Air-borne spores from appearance of green fungal sporulation in oyster mushroom affected crops might contaminate reusable plastic bottles. bisporus23 . and C. therefore increas. Prochloraz. isolates was the lowest when analyzing this bubble disease46 . ticillatum are known to be the causal agents of ‘‘cobweb room are Trichoderma spp. In contrast. regu. transmitted by substrate for mushroom cultivation41 . Notably. mol. gray weft of mycelium and conidia frequently covered the Komoń-Zelazowska et al. The effective and currently use of fungicides benomyl. calcium hydroxide on the affected area. because the amount of resistant Tri- ing concentrations of Sporgon must be used to combat dry choderma spp. In advanced stages. multiseptatum. well as on the natural and productive substratum of the This fact suggests that the spores are very readily dispersed oyster mushroom42 . (T. The colonized mold infection mostly during spawn run. this treat- has been reported against the fungicides that are used to ment seems to be ineffective against T. No. as harvesting9 .org/10. pleurotum infection by sub- lation of the environment and the routine fungicide spray strate alkalization may be further supported by the fact that program. L. does not have a wide host range of metabolic heat by mushroom mycelia. being pleurotum has been found only on cultivated P. necrotic areas. ostreatus. The mycelial growth of Tri- phous masses of sporophore tissue. Another management technique that has fungicide. ferulic acid. of Pages 11 ARTICLE IN PRESS Diseases and pests noxious to Pleurotus spp. resulting resulted in the development of typical dry bubbles. (+)-menthol. in 2009---2010. varium. Trichoderma green mold infection in in the air and growth of conidia is an important causative edible basidiomycetes has been known for a long time64 . problem in the United States. soil-inhabiting filamentous fungi with teleo. Infection of sporophores at the pin or button stage might slow down the growth of Trichoderma spp. they can be found rooms and develop several spores within 3---4 days. According to Hatvani32 . thiabendazole and prochloraz legal chemical control for dry bubble disease is Sporgon was also reported to be effective24 . C. T. hazianum. whereas no growth and might more often infect already decaying mushrooms.2017. The substrate is exposed to green ing in decomposition of the entire fruit body. Trichoderma species However. Few chemicals can be used for the control of Pleurotus spp. but later dis. when the substrate surface turns pale brown or yellow. seriously affected by green mold epidemics. the development of resistance of L. and transportation systems. Sensitivity of be the most effective fungicide for the inhibition of mycelial L. a at its maximum in 80% of relative humidity conditions2. air circulation systems. to 1. pleuroticola and T.08 mg ml the pathogen5 . pin-heads. T. ing in stipe. which originates from a Brown spot viral infection40 .33.85 ppm). Mycoviral mycetophagous arthropods and synthetic or wood substrate infection symptoms include retarded mycelia and fruiting decomposers have been identified by producers as damaging body growth. the epidemic disappeared. reduce this risk. This strongly suggests that OMSV is a causative Viral diseases agent of the disease. it is conceiv. In 1980. they have been reported disease.58 isolated the oyster mushroom isometric virus gill knots. The characteristics of examined OMIV suggest that composticola.38 . which is directly related to mushroom pathogenic fungi. There lated from P. Yu et al. benomyl and carbendazim should be used with caution only when mushroom growers know for certain that the pathogen they wish to control is sensitive to Die-back benzimidazole. The virus (Ppv) was isolated from mycelia and basidiocarps of unhygienic conditions of mushroom cultivation provide a P. Rev Argent Microbiol. To grow very slowly on agar and their density is very low11 . However. mites.0---8. Another P. The mycelia taken from Nematodes the tissue of basidiocarp exhibited abnormally retarded growth on a solid medium. cracking of the stipe surface. infections by PoV1 did not show any distinct mor- to be cryptic or show few symptoms leading to latent phological or growth phenotypes.B. fruiting body development inhibition.68 . combining the active ingredient with prochloraz manganese and thiophanate-methyl might Pleurotus spp. crustaceans and other symptoms originate from virus-infected spawn. The fruit body eventually turns viral disease on oyster mushroom are quite similar to ‘‘La dark brown and becomes rancid. nematode infection while oyster mushrooms are relatively resistant65 . In most cases. In Mycoviruses are widespread in fungi. in which fruiting body formation delay. infection in host cells.) nematodes were found in genomes and has a diameter of 30 nm. Therefore. including plant. mushroom crops. pulmonarius Biological cycles of these pests are not well known. eryngii mushroom. P. No. and flattened caps with irregular shapes. and when OMSV from diseased mushrooms was cured. It is surprising that the Please cite this article in press as: Bellettini MB. The authors detected the virus in all 102 samples collected sues. Three nematode species. sometimes even shrinking.). with an offensive odor33.ram. Typical symptoms of oyster mushroom (Pleurotus spp. of Pages 11 ARTICLE IN PRESS 6 M.0 ppm) as well as moderately sensitive to thiophanate. The optimum temperature for conidial germi. Fruiting bodies of P. namely Aphelenchoides (OMIV). In addition.025 ppm). ostreatus-infecting spher- ical dsRNA virus was discovered. It is An outbreak of such disease in a commercial farm often leads also pathogenic to Pleurotus cystidosus and Pleurotus sajor. benomyl and carbendazim the major symptoms. ostreatus-infecting viruses such liophagus along with some saprophagous (Rhabditis spp. from a cultivated oyster mushroom. the symptoms were observed throughout the culture when a certain mushroom spawn was inoculated58 . et al. with severe epidemic is not much bibliographic information related to pests of symptoms. The most dangerous pests are nematodes. Diseases and pests noxious to Pleurotus spp. shorten- (0. Nematodes inhabit and lay many eggs inside the Ro et al. free from diseases from external origin. This led to the conclusion that the The presence of insects. OMSV was not detected in healthy mushrooms. it was spherical with a 31-nm-diameter. and its cultivation is thus largely becoming resistant9. prochloraz manganese (0. symptoms are rather complex and the disease spreads fast. Symptoms consist of brow spot curling of the tis.) as PoV1. mush- room industries often suffer from spawn-related diseases. most notably the die-back disease. P. contrast to OMSV.10. congenial atmosphere for many pests and diseases.007 . https://doi. indicating that they are the eradicated without the complete elimination of the crop.0 ppm) and thiabendazole (4. eryngii Spherical Virus (PeSV) was iso. 2017. which cannot be tially eliminate the symptoms. Their presence leads to very poor yields or total crop fail- able that many uncharacterized mushroom diseases may be ures. Transmission electron microscope showed that mushrooms and their substrates. tolaasii are generally restricted to a local area of culture. Button mushrooms are generally highly susceptible to related to mycoviral infection57 . or limiting the proper development of mushrooms (Table 2). formations of the fruiting body40 . fruiting bodies are not formed at all (<1. P. and cracking of the infected from 102 different commercial farms with the epidemic. to a complete loss of yield and it is difficult to control. on some infected mushroom beds and viral-infected hyphae methyl (2. causative agents of the disease. roseum is 20---32 ◦ C. nation and mycelial growth of G. The fruit bodies.08. abnormal shape and thin mushroom caps are chlorothalonil (0. named oyster mushroom spherical virus Gliocladium roseum Bainier were obtained from diseased (OMSV).1016/j. Aphelenchus avenae and Ditylenchus myce- it is not related to known P. which is a spherical virus that contains two dsRNA and predatory (Seinura spp. France’’ disease which is a well-known viral disease in A.+Model RAM-242.38 . ostreatus. eryngii showed symptoms such as short and stout stems. Bellettini et al. is generally cultivated under well-controlled help to prevent or at least decrease the risk of the pathogen environmental conditions. Bacterial diseases such as brown Pests blotch disease by P.2017.org/10. A disease that causes knots on the gills of the oys- ‘‘La France’’ disease ter mushroom P. pulmonarius47 . and mal. P. Interestingly. The fungal pathogen is sensitive to metrafenone bisporus.3 ppm). being named PoV143 . caju12 .45 ppm). eryngii. ostreatus has been reported by Tsuda et al. Curing of the viruses essen.74 isolated the first single-stranded ssRNA mycovirus. galleries. by decomposing material or components used in compounds rying fungal contamination.007 . Diptera) was Bradysia paupera has been reported as a serious insect confirmed to be the vector of the nematodes inside the gill pest of the mushroom crop in European countries22 . gus gnat Rhymosia domestica (Mycetophilidae. bacteria diseases and mites52 . O’Connor and Keil52 Mites Feed on mycelia and fruiting Smoke extract Cha11 . Singh and Sharma65 .3 mushroom and when hatched mixture with adhesive feed on nutrients from mushrooms Molluscs Feed on mushrooms at the Quicklime Rosa60 beginning of shaping Rodents Feed on mycelia and fruiting Calcined gypsum with wheat Bellettini and Fiorda2 bodies flour or boric acid-based bait Termites Feed on fruiting bodies Gasoline or mothballs with Oei and Nieuwenhuijzen53 insecticide around the cultivation area nematodes causing this disease live in the fruiting body of funebris and flies Mycodrosophila spp. Myce. causing its overall yellow-coated. per- the only recommended nematicide for the control of myce.08. Adults of most of these families do not have great flight Culicidae. feed on mycelium and subsequently migrate to the mush- Dipterous larvae can derail the product for consumption. 35 Tsuda et al. Megaselia pleurota Disney and Megaselia scalaris being duration crop. Authors recommend chemical meth- ods for pest control. Pleurotus cornucopiae.). ostreatus and P. room Pleurotus spp. Phoridae and Sciaridae) are the main insect centimeters). he suggested that an insect larger than 1 mm were wilted and mature ones were feebly attached to the must take part in the transmission of the disease. Bellettini et al. Fletcher et al. Gnaneswaran and Wijayagunasekara29 revealed that Kaneko35 controlled this disease by covering the logs used their abundance and damage to the Pleurotus spp. have variable length (a few millimeters to several tophilidae. the most common techniques Flies are tapes and traps. Muscidae. adult flies spread Gnaneswaran and diseases and mites Wijayagunasekara29 . They also feed attracted by the odor coming from the fermentation exhaled on nutrients from fruiting bodies and are capable of car. especially in their immature stage (larvae).18 .+Model RAM-242. young fruiting bodies therefore. which have nematicidal properties and at Singer. (sugarcane bagasse. Eira interior. of Pages 11 ARTICLE IN PRESS Diseases and pests noxious to Pleurotus spp. causing its overall depreciation2 . 2017. Rev Argent Microbiol. According to the author. For the con- trol of flies in growth rooms.3 . Nematode respectively. rooms. Megaselia longipen- advisable due to residual hazards as mushroom is a short nis. pyrethroids and Bellettini and Fiorda2 . The use substratum. management control using Thionazin at the rate of 80 ppm is Flies. Alcohol (80%). that is. No. forate the stipe and pileus of mushrooms. According to Disney and Durska17 . carry pathogens and nematodes Beetles Lay their eggs inside the Pepper mash or bordeaux Eira et al.18 . autonomy. Pests Damage Control References Nematodes Knots on the gills Screen net (1 mm) Kaneko . crops 7 Table 2 Pests noxious to Pleurotus spp. Disney and Durska17 . There is a need to exploit the use of some primarly a mycelium feeder of Pleurotus citrinopileatus plant products. were also observed this fungus. ever. Born larvae from their eggs species of commercial mushrooms throughout the world13 . D.68 Flies Perforate the stipe and pileus.1016/j. leading to losses of around 20%. et al. How- knots. Drosophiladae. Rosa60 bodies.2017. https://doi. opening inside liophagous nematodes without residual toxicity65 . highlighting the use of pyrethroids. Larval stages of Drosophilid making them unfit for consumption18 . the fun. double-sided) et al. mushroom crops. mushroom crops. Please cite this article in press as: Bellettini MB. which is known to be nematophagous. destroying the stipe and pileus partially or fully. depreciation. crop to grow oyster mushrooms with a 1 mm mesh screen net. was of minor significance. sajor-caju. Flies of at least 8 dipterous families (Calliphoridae. Diseases and pests noxious to Pleurotus spp. funebris has naturally been described with vegetative hyphae that have the ability to immobilize as scavengers and reported as occasional pests in mush- and consume nematodes67 . the larvae of pesticides for killing nematodes in mushroom crops is not of Megaselia tamilnaduensis Disney. houses with poor hygienic conditions22 .22 . As a result. can have thin or stout bodies and are usually disease promoters in mushroom production. The females lay their Lycoriella mali Fitch (Family Sciaridae) is the major pest eggs directly onto the substrate. Bellettini opening galleries in their water sticky traps (white or et al.org/10. etc. the same time are safe for mushroom mycelium. Cecidomyiidae. rice straw.ram. P. in fruiting bodies. 2017. For their control. They develop very fast under high humid. The handling tools Mites belonging to the class Arachnida are common pests should be heated in boiling water for 1---2 min for the com- in mushroom crops and can cause total loss of production. just a wash with water is side the sheds). Insects. cause dramatic production loss.+Model RAM-242. unabling the deposit of their eggs in the mushroom older crops. For their ried out. mushroom crops. For prevention. Basic amenities like clean irrigation water and Beetles belong to the order Coleoptera and are insects sewage disposal system and irrigation should be ensured. The floor used at the compost preparation room should tion shelves. rather frequently. This treatment is sufficient to after saturation by dead insects. Diseases and pests noxious to Pleurotus spp. used for the same is known as ‘‘cooking-out’’. room from easily spreading to other rooms53 . especially during fruiting3 . A single grain kernel may the industry. ostreatus28 and it was tion from insects. Grain and sawdust contain reported that some mushroom growers had to close down large numbers of contaminants. Rev Argent Microbiol. Shelves are typically made of galvanized iron or formica53 . These insects lay their eggs inside air is free from toxic fumes and gases. For their control. The waste from various operations should be tissues2 . The technique tive to dipterous (flies and mosquitoes). that can affect the edible mushroom cultivation from the The area for mushroom cultivation should be such that its beginning of fruiting. mycelium debris.ram.org/10.1016/j. room cultivation provide a congenial atmosphere for many Please cite this article in press as: Bellettini MB. The drainage system of the different rooms causing itchy rashes among growers11 . Mushroom cultivation can damaging mites. Workers should frequently Tarsonemus spp. Early termination of infested crops should mushroom cultivation because they are fed with mushrooms be done. collected and disposed of daily from the working areas Molluscs such as slugs. of Pages 11 ARTICLE IN PRESS 8 M. The surroundings of the mushroom and when hatched can feed on its nutrients. When consumed by the animal. mycelium and fruit body where bacteria and be cemented. causing yield loss and a decrease in mushroom smooth surface that can be easily cleaned and allow excess quality. molds. https://doi. as many grow-room These infections are facilitated by the particular conditions structures are made of wood. Shelves should be designed in such a way that the Mites floor beneath can be cleaned easily. should not be connected to prevent a disease in one growing smoke extract can be used over the compound in col. which land mostly used in the production of mushroom. also be disinfected by cleaning with a 10% Clorox solution or ity conditions (above 90%) and temperature (25---30 ◦ C). The color of the plates attracts a large Maintaining cleanliness inside. Mites carry pathogens and nematodes. inducing dehydration of molluscs60 . are major mushroom disinfect their hands and clothes. being the white color particularly attrac. a farm should be clean and free from possible contamina- Cyuodes bifacies is a pest of the P.B. The interior particularly dipterous (flies) with great efficiency. Growing rooms Minor pests A clean environment is absolutely essential to mushroom production. calcined gypsum can be used along with wheat flour or boric acid-based bait. Picking should be started from new or cleaner crops toward tion. No. The sticky traps should be replaced vapor at 70 ◦ C for 12 h21 . All the surfaces should be smooth and easy to clean. to avoid the direct contact of compost with fungi can come in. outside and in the surround- number of species. a pepper mash or bordeaux contain thousands of bacteria. 2017. It is important to prevent rodents from climbing onto the shelves containing Intensive cultivation of edible mushrooms can often be mushrooms18 . affected by some bacterial. Mites feed on mycelia and fruiting infested soil. materials. Rodents feed directly from mushrooms. snails and conch can be pests in immediately2 . Subsequently. Bellettini et al. basically in on them become definitely stuck to them. The growing rooms should be properly venti- at the beginning of shaping. The unhygienic conditions of mush- around the cultivation area53 . ings of the production unit is recommended8 . The alcoholic or fermentation odor attracts enough to prepare the room for the next cycle. These are of the inoculation room should consist of non-biodegradable the most effective traps. fungi and actinomycetes53 . plete destruction of nematodes. which consists in applying steam purpose as the plate. gasoline or mothballs with insecticide are used a low aeration rate. An infusion of coriander leaves can also be used60 . high humidity and control. sometimes water to drain. All termite mounds near the under which the mushroom cultivation is commonly car- growing room must be eliminated or controlled. Empty facilities Sticky traps consist of white or yellow-coated plastic plates with slow drying glue. such as warm temperatures. 14---16 mesh/cm to avoid the entry of insect pests65 . These traps can high-tech facilities to disinfect the room after the crop cycle also be in the form of double-sided tape. The use of alcoholic and water sticky traps can be a valu. et al. The first signals are webs formed between the cultiva. constant danger during growing season. etc. The control is performed with lated rooms having doors and windows with wire net of quicklime. mixture can be used with adhesive for beetle immobiliza. 70% ethyl alcohol.08.007 . it Conclusions blocks their digestive tract causing death. Hygiene measures able tool for the grower and a complement to other methods used for the control and prevention of pests in the crop. onization. Slightly inclined cemented floors provide a bodies. and Histiostoma spp. fungal and viral diseases Termites belong to the Isoptera order and represent a that. The traps must be filled eliminate mushroom pests and diseases in addition to kill with 80% alcohol and hung along the crop (inside and out. A. Botucatu: FEPAF/UNESP. Right to privacy and informed consent. Eur de cogumelo Pleurotus ostreatus e djamor pela técnica Jun --. Fanelli C. control. 1985. Res. Gnaneswaran R. Geels FP. Jordan DC. Bioresour Funding Technol. cultivated mushrooms (Agaricus bisporus). Mushroom pest and disease control. Suz LM. p. declare that no experiments were performed on humans or 13. Rusting- 7. Boca gasipaes Kunth and Pleurotus ostreatus as soil conditioners for Ratón: CRC Press. 28. p. Phoridae) that feeds on oyster mushrooms (Pleurotus ostreatus) in Poland. 2003. 2013.org/10. 18.org/10. 192. Bessette A.08. Fiorda FA. 1999. Navarro MJ. Bruno GL. Navarro MJ. 1997 [in Portuguese]. Lops R.007 . Delmastro S.). Corbell N. 15. Eira AF. Zjalic S. in vitro.84:171---6. Curvetto NR. Bellettini MB. Crop Prot. Berendsen RL. 6. Cha SB. p.2017. Figlas D. considerations include previously cleaned implements and causal agent of cobweb disease on Agaricus bisporus mushroom maintaining overall hygiene. Mannerucci F. Wösten Spain. Tello JC. Fiorda FA. Diseases and pests noxious to Pleurotus spp. 2007. Navarro MJ. room Pleurotus spp crops.151:98---100.sjbs.40:59---67. Silva J. 12. Vítola FMD.97:5535---43. Baars JJP. Gea FJ. Fiorda FA. Kim HH.50:1535---7. Minhoni MTA.005 [in press]. Appl Environ Microbiol. The authors declare that they have no conflicts of interest. logical control of Lycoriella mali (Diptera: Sciaridae). the Protection of human and animal subjects. Sermani S. Lee HS. Teixeira GL. 11.2016. Bakker PAHM. A new subspecies of a scuttle fly (Diptera: and Federal University of Paraná (UFPR). No. p. Rev Argent Microbiol. Bellettini S. 16. Residual compost from the production of Bactris 21. crops 9 diseases and pests. 111---52. Ichida MS. Wijayagunasekara HNP. Cariddi C.50:24---9. I funghi. Biology of Cyuodes ness of white vinegar and steam-exploded liquid waste against bifacies Walker (Coleoptera:Cucujoidea:Nitidulidae). Identification of Gliocladium roseum. Council for the Improvement of Higher Education (CAPES) 17. Carrasco J. 8. Semin-Cienc Agrar. Gaze RH.171:62---9. Santos M. of Pages 11 ARTICLE IN PRESS Diseases and pests noxious to Pleurotus spp. The authors 1995. 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