J. Crop Prot. 2014, 3 (4): 563-571______

Research Article Shot hole disease, survival and pathogenicity of the causal agent on stone fruit trees in Northeast

Azam Yousefi* and Mohammad Hajian Shahri

Department of Plant Protection, Khorasan Razavi Agricultural and Natural Resources Research Center, Mashhad, Iran.

Abstract: Shot hole caused by Wilsonomyces carpophilus is one of the main constraints to prune fruit production in Iran particularly in Khorasan Razavi province. It causes foliage shot hole in spring and early summer; fruit-spotting and cankers on limbs and twigs during autumn rains. The fungus was isolated from the lesions of twigs and was purified on PDA. The pathogenicity and virulence on detached twigs of stone fruit tree species was examined in vitro. Virulence of the pathogen as measured by lesion length was significantly different among the different host species, showing the nectarine as the most susceptible species. In contrast to other hosts, sour cherry did not show any canker on shoots or twigs and disease progress was just as tissue colonization by the fungus hyphae. However, other species such as prune, cherry, apricot and did not show significant differences. The results of bud and shoot evaluations indicated that the fungus overwinters as hyphae and conidia in buds, and in the form of hyphae as well as thick-walled globular chlamydospores in twigs. Additionally, viability of recovered conidia ranged from 33 to 90% throughout the dormant season. A better understanding of disease cycle and survival mode of the fungus will help to manage and prevent the disease.

Keywords: Shot-hole disease, overwintering, virulence, stone fruit shoots

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 Introduction12 hosts. The most limiting factor to their production is shot-hole disease. On , Shot hole disease is one of the major foliar nectarine and apricot perennial infections of diseases of Prunus species worldwide which is current-season twigs are more common than in caused by several pathogens and particularly by other Prunus hosts (Ogawa and English, 1991). Wilsonomyces carpophilus (Adaskaveg et al., A number of peach diseases such as peach 1990). The fungus was first observed on peach canker, constriction disease, constriction canker trees in France in 1843, later in Africa, Asia, in the Midwest and Mid-Atlantic States, shoot Europe, North, Central and South Americas, blight in Georgia and dieback in Europe have Australia and Oceania (Väcäroju et al., been reported to have symptoms similar to shot 2008).The fungus causes local lesions on stone hole (Cayley, 1923; Cohoon and Daines, 1956; fruit trees that are economically important Guba 1953; Selby, 1898) that may cause confusion in apparent identification of shot hole Handling Editor: Dr. Ziaeddin Banihashemi disease. Twig infections are catastrophic in shot ______hole because of devastation of buds. The * Corresponding author, e-mail: [email protected] disease causes blackish spots on twigs in close Received: 24 March 2013, Accepted: 17 June 2014 vicinity of buds. Spots gradually enlarge and Published online: 2 August 2014

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become brown in color with purple margin. The light condition according to Shaw et al. (1990) spots occur beneath flowering buds in spring. procedure. Plant’s sap suddenly stops in infected plants resulting in drying of twigs and blooms Overwintering assay of W. carpophilus in (Ashkan and Asadi, 1971). The disease is most buds harmful in very cool and wet conditions of Overwintering of W. carpophilus inside buds spring, although it can occur and cause damage of some stone fruit trees was examined based at any time during prolonged wet weather on Highberg and Ogawa (1986) procedure (Evans et al., 2008). W. carpophilus with a little modification. One hundred and overwinters as hyphae and conidia in the fifty flower and leaf buds were collected cankers on twigs and inside of scales in infected individually from infected twigs of peach, buds. In early spring, under suitable nectarine, apricot, almond and prune during environmental conditions conidia germinate winter 2007. The buds were removed from (Highberg and Ogawa, 1986). Then, the shoots, and all inner and outer bud scales sporodochia and spores are formed, inoculum were removed. The remaining scales of 150 builds up and conidia spread on leaves, twigs buds were chopped and placed in a glass and buds. Infection of these organs is critical centrifuge tube containing 3 ml of sterile for overwintering of the fungus in stone fruit distilled water. The tube contents were trees. It is important to conduct exact studies subsequently vortexed for 30-40 min, about overwintering of the fungus. The centrifuged at 3000 rpm for 5 min and objectives of the present study were to show the remixed for 2-3 min to suspend. Conidial importance of the causal agent, pathogen suspension obtained from the bud scales was survival in buds and twigs, inoculum buildup removed with a Pasteur pipette and and disease severity on shoots for determination transferred to a clean centrifuge tube. The of fungicides application times. entire washing procedure was repeated three times for each sample, and then suspensions Materials and Methods containing conidia and mycelial pieces were mixed and centrifuged for 3 min at 5000 rpm. Symptomatology and isolation of fungus Pelleted materials were resuspended in 0.5 ml from infected tissues of sterile distilled water and spread onto 1%

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 Infected shoots of peach, apricot, nectarine, water agar plates. Plates were incubated at 25 prune and almond trees were collected from °C for a week in dark condition. The number different orchards in Khorasan Razavi of germinated conidia after 24h in each province, Iran, during 2007-2008. The sample was recorded using an Olympus symptoms were tan spots with purple to microscope at 10X. brownish margins that resulted in long canker on twigs (Fig. 1). Infected buds were darker Identification than healthy buds. Shoots with canker were To identify species of W. carpophilus based thoroughly washed under tap water, cut into on Adaskaveg et al. (1990), one week old segments (3-4 mm) from margin of healthy culture of the fungus grown on PDA in dark and infected tissues and surface-disinfested by at 25 °C was used. Based on morphological immersing in NaOCl 1% for 5 min. Tissue and physiological characters and optimal pieces were transferred onto potato dextrose temperatures for growth of the culture, all the agar (PDA) plates and kept in an incubator at isolates were identified as W. carpophilus and 22 °C for a week in dark, and then a week in used in pathogenicity test.

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Figure 1 Symptoms of shot hole disease on peach shoots in current season (left) and last season (right).

Pathogenicity chamber kept at 15 °C for two days and then at 25 °C for 30 days in growth chamber. The inoculated An isolate of W. carpophilus (Astan Qods Peach shoots were arranged in a completely randomized Fruit; APF1) was selected to pathogenicity test of design with 15 replicates for each species (5 twigs. Before each trial, percentage of spore treatments of stone fruit species). Ten days after germination was determined on water agar medium inoculation, cheese cloths were removed. The 1%. The test was carried out on detached shoots disease severity was evaluated by measuring the from young trees of Torouque Research Station length of each spot at 10, 20, and 30 days after according to Uddin et al. (1997) procedure with a inoculation. Data were subjected to analysis of little modification. Shoots of current season were variance using SAS (version 9.1) and means were collected from healthy young trees of nectarine, compared by LSD test (α = 0.05). Prunus persica cv. Sunking, apricot, Prunus armeniaca cv. Shahrudi, sour cherry, Prunus Results cerasus cv. Erdi, prune, Prunus domestica cv. Golden Drop and almond, Prunus amygdalus cv. Isolation and description of the pathogen domestic grown in Torouque Research Station. Wilsonomyces carpophilus was isolated from Shoots were cut to fragments of 10-30 cm in overwintering inoculum of different varieties of length. Shoots were thoroughly washed under tap stone fruit trees as hyphae, conidia and globular Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 water for 15 min, blotted dry and surface- chlamydospores. Colonies grown on PDA medium disinfested by ethanol 70% for 15 sec and then at the beginning were colorless and greenish brown immersed in NaOCl 1% for 20 min. After blotter to olive, conidiophores macronematous, usually drying the shoots were again surface disinfested short and packed closely together forming pulvinate with ethanol 70% for 5 sec. From sites of inter two sporodochia, subhyaline to olivaceous brown, 4-10 buds shoots were dissected horizontally using a × 10-37.5 µ, smooth or verrucose. Chlamydospores sterile blade. A 10-20 mm superficial V-shaped were pale brown to dark in color, and formed incisures was made at a 45 ° angle at the dissected terminally or intercalary as solitary or in chains of area to expose the tissue under the bark. An agar three to four and rarely more. Conidia cylindrical, plug culture of the fungus the size of incisures was clavate, ellipsoidal or fusiform, truncate at base, with placed under the bark. The inoculation site was 1-6 (mostly 3-5) transverse septa and occasionally 1- sealed with sterile moist cheesecloth according to 2 oblique septa, 7.5-17.5 × 22.5-67.5 µ long. the procedure described by Dhingra and Sinclair In addition, a number of other fungi including (1985). Control shoots were treated similarly but Alternaria sp., Penicillium and Cladosporium with sterile blocks of PDA. Six shoots were spp. were isolated from spots on twigs. selected from each species. Each shoot was usually The results of spore counts in buds of inoculated in three points. Control shoots for each different stone fruit trees and their viability are cv. were separately placed in a sterile moist shown in Table 1.

565 Survival and pathogenicity of agent ______J. Crop Prot.

Table 1 Numberand viability of overwintering conidia in buds of Wilsonomyces carpophilus in washings from buds of different stone fruit trees.

Number Spore germination Host Collection Date and site Other isolated fungi spores (%)

Almond cv. Domestic Dec 2006 Torouque 0 0 Alternaria sp.

Apricot (cv. unknown) Feb 2007 Zarkesh Kal 10 90 Alternaria sp.

Peach cv. Missouri Feb 2007 Torouque 6 0 Stemphylium sp., Alternaria sp.

Almond cv. Domestic Feb 2007 Torouque 0 0 Alternaria sp.

Apricot cv. Shahrudi Feb 2007 Torouque 3 66.66 -

Ghods Astan Nectarine cv. Quota Feb 2007 0 0 Cladosporium sp., etc. orchards (1)

Ghods Astan Peach cv. Amestan Feb 2007 0 0 Unknown spores orchards (2)

Ghods Astan Alternaria sp., Stemphylium sp., Apricot cv. Lasgerdi Feb 2007 8 50 orchards (2) Cladosporium sp., etc. Stemphylium sp., Alternaria sp., Peach (cv. unknown) Mar 2007 Zarkesh Kale 739 91.47 Ulocladium sp., Cladosporium sp., etc. Ghods Astan Peach cv. Platycarpa Mar 2007 6 33.33 - orchards (2)

Ghods Astan Prune cv. Compote Mar 2007 0 0 Cladosporium sp. orchards (2)

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 Pathogenicity test was more frequent around buds (Fig. 2-C, D). The hyphae were compressed in some areas Germination percentage of conidia was 80% as a flat layer, and seemed white to in on 1%water agar medium. Six to seven days color (Fig. 2-B, I). As the size of spots post inoculation the disease symptoms increased the active growth of inoculated appeared as tan to brown and purple brownish shoot stopped while the control shoots spots on inoculation sites of detached shoots. showed active growth and produced young Small cavities were formed around leaves. Thirty days after inoculation of the inoculation sites of detached shoots of fungus, the longest spots (20 mm) appeared Nectarine and Shahrudi apricot. The cavity on cherry shoots. Appearance of infection in size progressed on the entire bark around the some replications was just as hyphae instead inoculated sites, and finally the infested bark of lesions. The results of analysis of variance wrinkled. Buds in those sites were hindered revealed a significant difference in lesion in growth (Fig. 2-A). In all inoculated shoots length among the five species (Table 2). except almond cv. Domestic, surfaces of buds and shoots in close vicinity of inoculation sites were covered by fungal white hyphae (Fig. 2-H). The appearance of white hyphae

566 Yousefi and Hajian Shahri ______J. Crop Prot. (2014) Vol. 3 (4)

(A) (B)

(C) (D)

(E) (F)

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 (G) (H)

Figure 2 Symptoms of Wilsonomyces carpophilus on shoots of different stone fruit trees. A: Apricot shoot bark showing wrinkle at inoculated sites, B and H: Tissue colonization by the fungus, C, D: The appearance of white hyphae around buds, E, F: conidia formation at colonized sites, G: The appearance of white hyphae on shoots on two-sides of inoculated sites.

Of course, sour cherry cv. Erdi was exception. Microscopic identification of white hyphae and It produced small restricted spots covered by fungal colonies of the bark surface of inoculated detached hyphae. Nectarine was placed in one group (A) and shoots confirmed that W. carpophilus was the the other species in another group (B) (Table 3). disease causal agent (Fig. 2-E, F).

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Table 2 Analysis of variance of lesion length in during the inoculation influence the different stone fruit species inoculated by development of shot-hole disease on leaves of Wilsonomyces carpophilus in vitro. the Prunus species caused by W. carpophilus (Väcäroiu et al., 2009). Results of study on the Source df MS Pr > F presence of spores inside buds (Table 1) showed that conidia associated with dormant Host 4 116.54 0.0242 buds on higher twigs of the trees were being Error 70 38.87 washed down by rain onto dormant buds on lower branches of the tree. For this reason, Corrected Total 74 samplings that mainly were conducted from available lower buds in the tree can’t be indicative of actual population of overwintering Table 3 Means comparison of lesion length of conidia. Also, in areas and at periods of high Wilsonomyces carpophilus (APF1) inoculated on shoots of five stone fruit species and recorded 30 rainfall, greater conidial populations are days after inoculation. observed in buds. The insignificant increase in number of conidia detected in bud samples Host N Lesion length (mm)1 collected in the Zarkesh Kal orchard over time can be explained in terms of both climatic and Nectarine 15 12.467a disease conditions that existed within the orchard during the dormant period. Also, some Prune 15 7.400b decrease in number of conidia was detected in Apricot 15 7.267b bud samples collected in other areas where overwintering form is as hyphae in buds. Almond 15 7.000b However, studies on inoculation of almond buds with this fungus by Highberg and Ogawa Cherry 15 4.933b (1986) indicated that the greatest increase in

1 Means followed by the same letters in a column are numbers of detected conidia occurred during not significantly different (LSD test, P < 0.05) the period between bud swell and early pink bud stage of bloom. Our evaluation of infected Discussion trees revealed that when healthy buds were in Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 pink stage, both hyphae and conidia were Results showed that viable conidia of W. observed in the blighted buds, but where W. carpophilus were associated with apparently carpophilus overwintered only as hyphae in healthy dormant blossom buds throughout the infected twigs and blighted buds on almond, 2007-2008 dormant seasons in orchards. This any infection of leaves and fruit was not observation together with results obtained from observed in spring. Also, in comparison with pathogenicity test on shoots support the other hosts, sour cherry did not show any hypothesis that W. carpophilus conidia cankers on shoots or twigs although its buds contribute to the overwintering of the fungus were infected and blighted as was confirmed by and disease development on stone fruit trees laboratory tests of shoots. This suggests that the (Shaw et al., 1990). The infection is spread by buildup of inoculum levels that occur during conidia. In dry conditions conidia remain viable Rain fall is an important component in the for several months but cannot be detached or shot hole disease cycle. The conidia formed on spread by the wind. Rain is necessary for their infected leaves during rainy periods in fall dispersal. In humid conditions, they can contribute not only to the overwintering germinate at highly varying temperatures above population of the fungus but also provide a 2 °C, which accounts for the winter infection of ready source of primary inoculum for spring buds. Temperature and duration of wet periods infections. Unlike the situation observed for

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other multiple–cycle diseases, the amount of because winter spraying of fungicides is not primary inoculum present for initial infections effective on hyphae inside of host tissue appears to be an important factor in (Ashkan and Asadi, 1971). This indicated the development of shot hole disease. Infection survival ability of the pathogen for several periods are determined by duration of moisture years inside twig cankers and infected buds conditions and the temperature. At cooler under unfavorable environmental conditions. temperatures, longer periods of moisture are The pathogenicity test on different species of required (Shaw et al., 1990). Yousefi et al. stone fruits by W. carpophilus showed a little (2010) observed that conidium germination constriction associated with wrinkle in started at a temperature of 1 °C (1-2%), the inoculated sites in Peach and Nectarine species optimal temperature was recorded between 12 which caused wilting and death of the shoot. and 24 °C (25-80%) and it decreased to 5% at This was in conformity with the observed 30 °C. Germination of spore was recorded results of Uddin et al. (1997) for infection by starting from 1 °C, the highest colony growth Phomopsis sp. on peach. Uddin et al. (1997) rate was reached at 20 °C and decreased again also, indicated that rapid development of at 35 °C. The conidia generated by inoculum disease from wounded dormant buds may be source are transported by rain and infect due to easy penetration and colonization of the flowers and young leaves. After penetration of wood, a conclusion that was confirmed by our the infection hypha, the fungus produces examination of pathogenicity on inoculated intercellular mycelium. From this mycelium, shoots. Ahmadpour et al. (2009) isolated from loosely packed cushions of hyphal cells emerge infected leaves, fruits and twigs of different to the surface, and give rise to conidia Prunus species (apricot, almond, peach, (Väcäroiu et al., 2008). Results of this study nectarine, plum, sweet cherry and sour cherry) indicated that the fungus overwinters as hyphae hyphae of the fungus W. carpophilus but its and conidia in buds and as hyphae in twig spots. importance in disease cycle was not mentioned. These results are in conformity with those of According to Evans et al. (2008), the disease is Highberg and Ogawa (1986). Also, most harmful in extended cool and moist overwintering as chlamydospore in spots of periods in spring, while it can occur and cause twigs was in conformity with the results of damage at any time and any season during long Koul and Naarain (1983). Chlamydospores lasting wet weather. This is the first

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 which are formed in natural conditions may act documentation of the pathogenicity of W. as a source of inoculum for the pathogen. carpophilus on shoots of stone fruit species in According to Highberg and Ogawa (1986), if vitro. conidia were found to survive the dormant season in association with healthy dormant Acknowledgments buds, a control program aimed at preventing fall buildup of inoculum could reduce the amount This study was carried out in Iran, Mashhad, of primary inoculum for the following spring Torouque Agricultural and Natural Resources because conidia may be deposited on bud scales Research Center of Khorasan Razavi. Authors of healthy dormant buds during fall rains and acknowledge the support of officials in remain there viable until the next season. agricultural and natural resources research center Fungicidal tests conducted by Wilson (1937) of Khorasan. for destruction of W. carpophilus conidia in infected buds showed that 80-90 percent of References conidia on twigs were destroyed after a week. However orchard studies have shown that great Adaskaveg, J. E., Ogawa, J. M. and Buttler, E. numbers of conidia in spring were produced E. 1990. Morphology and ontogeny of from these sprayed buds with fungicides conidia in Wilsonomyces carpophilus gen.

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nov. and comb. nov., causal pathogen of shot Publication. 3345. University of California, hole disease of Prunus species. Mycotaxon, Division of Agriculture and Natural 31: 275-290. Resources, Oakland, CA. Ahmadpour, A., Ghosta, Y., Javan-Nikkhah, Selby, A. D. 1898. Preliminary reports upon M., Fatahi, R. and Ghazanfari, K. 2009. diseases of stem and branch. Ohio Isolation and pathogenicity tests of Iranian Agriculture Experimental Station Research cultures of the shot hole pathogen of Prunus Bulletin, 92: 233-234. species, Wilsonomyces carpophilus. Shaw, D. A., Adaskaveg, J. E. and Ogawa, J. Australian Plant Disease Note, 4: 133-134. M. 1990. Influence of wetness period and Ashkan, M. and Asadi, P. 1971. Shot hole temperature on infection and development of disease. Iranian Journal of Plant Pathology, shot hole disease of almond caused by 2: 39-62. Wilsonomyces carpophilus. Phytopathology, Cayley, D. M. 1923. Fungi associated with 80: 749-756. "dieback" in stone fruit trees. I. Annals of Uddin, W., Stvenson, K. L. and Pardo- Applied Biology, 10: 235-274. Schulthesis, R. A. 1997. Pathogenicity of a Cohoon, D. F. and Daines, R. H. 1956. Peach species of Phomopsis causing a shoot canker (Fusicoccum amygdali): Times and blight on peach in Georgia and evaluation sites of infections. Plant Disease Report, 40: of possible infection courts. Plant Disease, 304-308. 81: 983-989. Dhingra, O. D. and Sinclair, J. B. 1985. Basic Väcäroju, C., Zalä, C. R. and Cristea, S. plant pathology methods. Department of 2008. Research on the morphology and Plant Pathol. Univ. Illinois at Urbana- biology of the Stigmina carpophila Champaign, 355. fungus. In scientific conferences with Ellis, M. B. and Ellis, J. P. 1997. Microfungi on international participation durable Land Plants: An Identification Handbook. agriculture-Agriculture of future, 4th Slough: Richmond Publishing. edition. Craiova (Romania): Faculty of Evans, K., Frank, E., Gunnell, J. D. and Shao, Agriculture, University of Craiova, 110. M. 2008. Coryneum or Shot Hole Blight. Väcäroju, C., Zalä, C. R., Cristea, S. and Utah Pests Fact Sheet. Utah State University Oprea, M. 2009. Research regarding the Extension. [Utah]: Utah State University influence of temperature, atmospheric

Downloaded from jcp.modares.ac.ir at 0:48 IRST on Tuesday October 5th 2021 Extension, Utah Plant Pest Diagnostic humidity and light upon the biology of Laboratory, 3. the Stigmina carpophila fungus. Guba, E. F. 1953. Large leaf spot and canker of Scientific Papers. Series A. Agronomy, peach caused by the fungus Fusicoccum Bucharest, 52: 398-403. amygdali Delark. Plant Disease Report, 37: Wilson, E. E. 1937. The shot hole disease of 560-564. stone fruit trees. California University Highberg, L. M. and Ogawa, J. M. 1986. Agriculture Experimental Station Research Survival of shot hole inocolum in an Bulletin, 608: 3-40. association with dormant almond buds. Plant Yousefi A., Panjehkeh, N., Hagian Shahri, Disease, 70: 828-831. M., Salari M. and Fallahati Rastegar, M. Koul, A. K. and Naarain, U. 1983. Existence 2010. Evaluation of shot hole disease of chlamydospores in the culture of incidence and severity on stone fruit trees Stigmina carpophila. Indian in Razavi Khorasan province. Journal of Phytopathology, 36: 769-770. Plant Protection 24: 218-221. Ogawa, J. M. and English, H. 1991. Disease of Temperate Zone Tree Fruit and Crops.

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ﺑﻴﻤﺎري ﻏﺮﺑﺎﻟﻲ، ﺑﻘﺎ و ﺑﻴﻤﺎرﻳﺰاﻳﻲ ﻋﺎﻣﻞ ﺑﻴﻤﺎري روي درﺧﺘﺎن ﻣﻴﻮه ﻫﺴﺘﻪدار ﺷﻤﺎل ﺷﺮق اﻳﺮان

اﻋﻈﻢ ﻳﻮﺳﻔﻲ و ﻣﺤﻤﺪ ﺣﺎﺟﻴﺎن ﺷﻬﺮي

ﺑﺨﺶ آﻓﺎت و ﺑﻴﻤﺎرﻳﻬﺎي ﮔﻴﺎﻫﻲ، ﻣﺮﻛﺰ ﺗﺤﻘﻴﻘﺎت ﻛﺸﺎورزي ﺧﺮاﺳﺎن رﺿﻮي. * ﭘﺴﺖ اﻟﻜﺘﺮوﻧﻴﻜﻲ ﻧﻮﻳﺴﻨﺪه ﻣﺴﺌﻮل ﻣﻜﺎﺗﺒﻪ: [email protected] درﻳﺎﻓﺖ: 4 ﻓﺮوردﻳﻦ 1392؛ ﭘﺬﻳﺮش: 27 ﺧﺮداد 1393

ﭼﻜﻴﺪه: ﺑﻴﻤﺎري ﻏﺮﺑﺎﻟﻲ ﺑﺎ ﻋﺎﻣﻞ ﺑﻴﻤﺎري Wilsonomyces carpophilus ﻳﻜﻲ از ﻋﻮاﻣﻞ ﻣﺤﺪودﻛﻨﻨﺪه ﺗﻮﻟﻴﺪ ﻣﻴﻮه درﺧﺘﺎن ﻣﻴﻮه ﻫﺴﺘﻪدار در اﻳﺮان ﺑﻪ وﻳﮋه در ﺧﺮاﺳﺎن رﺿﻮي ﻣﻲﺑﺎﺷﺪ. اﻳﻦ ﺑﻴﻤﺎري ﺑﺎﻋﺚ رﻳﺰش ﺑﺮگﻫﺎ در ﺑﻬﺎر و اواﻳﻞ ﺗﺎﺑﺴﺘﺎن، ﻟﻜﻪدار ﺷﺪن ﻣﻴﻮه و اﻳﺠﺎد ﺷﺎﻧﻜﺮ در ﺳﺮﺷﺎﺧﻪﻫﺎ در ﻃﻲ ﺑﺎرﻧﺪﮔﻲﻫﺎي ﭘﺎﻳﻴﺰه ﻣﻲﺷﻮد. ﻗﺎرچ ﻋﺎﻣﻞ ﺑﻴﻤﺎري از ﻟﻜﻪﻫﺎي ﺳﺮﺷﺎﺧﻪﻫﺎ ﺟﺪا ﺷﺪ و روي ﻣﺤﻴﻂ ﻛﺸﺖ PDA ﺧﺎﻟﺺﺳﺎزي ﮔﺮدﻳﺪ. ﺑﻴﻤﺎرﻳﺰاﻳﻲ ﻗﺎرچ روي ﺷﺎﺧﻪ ﺑﺮﻳﺪه ﮔﻮﻧﻪﻫﺎي ﻣﺨﺘﻠﻒ درﺧﺘﺎن ﻣﻴﻮه ﻫﺴﺘﻪدار در ﺷﺮاﻳﻂ آزﻣﺎﻳﺸﮕﺎه ﻣﻮرد ﺑﺮرﺳﻲ ﻗﺮار ﮔﺮﻓﺖ. در ﻣﻘﺎﻳﺴﻪ ﺑﺎ ﺳﺎﻳﺮ ﻣﻴﺰﺑﺎنﻫﺎ، آﻟﺒﺎﻟﻮ ﻫﻴﭻ ﺷﺎﻧﻜﺮ ﻳﺎ ﻟﻜﻪاي ﺑﺮ روي ﺳﺮﺷﺎﺧﻪ ﻧﺸﺎن ﻧﺪاد و ﻋﻼﺋﻢ ﺑﻴﻤﺎري ﻣﻨﺤﺼﺮ ﺑﻪ ﻛﻠﻨﻴﺰه ﻛﺮدن ﺑﺎﻓﺖ ﻣﻴﺰﺑﺎن ﺑﻪ وﺳﻴﻠﻪ ﻫﻴﻒﻫﺎي ﺳﻔﻴﺪ رﻧﮓ ﻗﺎرچ ﻣﻲﺷﺪ. ﺷﺪت ﺑﻴﻤﺎري ﺑﻪ وﺳﻴﻠﻪ اﻧﺪازهﮔﻴﺮي ﻃﻮل ﻟﻜﻪﻫﺎ در ﻣﻴﺎن ارﻗﺎم ﺗﻔﺎوت ﻣﻌﻨﻲداري داﺷﺖ. ﺑﻪﻃﻮري ﻛﻪ ﺑﻴﺸﺘﺮﻳﻦ ﺣﺴﺎﺳﻴﺖ ﺑﻪ آﻟﻮدﮔﻲ را ﺳﺮﺷﺎﺧﻪﻫﺎي ﺷﻠﻴﻞ داﺷﺘﻨﺪ اﻣﺎ ﮔﻮﻧﻪﻫﺎي ﮔﻴﻼس، زردآﻟﻮ، آﻟﻮ و ﺑﺎدام اﺧﺘﻼف ﻣﻌﻨﻲداري ﺑﺎ ﻫﻢ ﻧﺪاﺷﺘﻨﺪ. ﻧﺘﺎﻳﺞ ارزﻳﺎﺑﻲ ﺟﻮاﻧﻪ و ﺳﺮﺷﺎﺧﻪ ﻣﺸﺨﺺ ﻛﺮد ﻛﻪ ﻗﺎرچ ﺑﻪ ﺻﻮرت ﻫﻴﻒ و ﻛﻨﻴﺪي در ﺟﻮاﻧﻪ و ﻫﻴﻒ و ﻫﻢﭼﻨﻴﻦ ﻛﻼﻣﻴﺪوﺳﭙﻮرﻫﺎﻳﻲ ﺑﺎ دﻳﻮاره ﺿﺨﻴﻢ در ﺳﺮﺷﺎﺧﻪﻫﺎ زﻣﺴﺘﺎنﮔﺬراﻧﻲ ﻣﻲﻛﻨﺪ. ﻫﻢﭼﻨﻴﻦ ﺟﻮاﻧﻪزﻧﻲ ﻛﻨﻴﺪيﻫﺎي ﻳﺎﻓﺖ ﺷﺪه در ﻓﺼﻞ ﺧﻮاب، 33 ﺗﺎ 90 درﺻﺪ ﺑﻮد. اﻃﻼﻋﺎت ﺑﻪدﺳﺖ آﻣﺪه از ﭼﺮﺧﻪ ﺑﻴﻤﺎري و ﻧﺤﻮه ﺑﻘﺎي ﻗﺎرچ ﻣﻲﺗﻮاﻧﺪ ﺑﻪ ﻣﺪﻳﺮﻳﺖ و ﭘﻴﺸﮕﻴﺮي اﻳﻦ ﺑﻴﻤﺎري ﻛﻤﻚ ﻣﺆﺛﺮي ﻧﻤﺎﻳﺪ.

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