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1 식물병연구 Research Article Open Access Res. Plant Dis. 23(4): (2017) Monilinia fructicola Characteristics of Brown Rot Caused by Monilinia fructicola on Stone Fruit in Korea 1,2 1 * , 2, 3, 4 *Corresponding author Tel: Fax: choiiy21@korea.kr Hun-Tak Oh 1,2, In-Young Choi 1 *, Ju Kim 1, Young-Eun Na 1, Wang-Hyu Lee 2, Kui-Jae Lee 3, and Hyeon-Dong Shin 4 1 Jeollabuk-do Agricultural Research and Extension Services, Iksan 54591, Korea 2 Department of Agricultural Biology, Chonbuk National University, Jeonju 54896, Korea 3 Division of Biotechnology, College of Environmental and Bioresource Sciences, Chonbuk National University, Iksan 54596, Korea 4 Division of Environmental Science and Ecological Engineering, Korea University, Seoul 02841, Korea Received August 7, 2017 Revised September 10, 2017 Accepted September 10, 2017 In June and July 2015 and 2017, typical signs and symptoms of brown rot were observed on the fruit of Japanese apricot, peach, apricot, Japanese plum, and sweet cherry with incidence levels of 2-5% in Jeonju and Imsil, Korea. Early symptoms were small, circular, light brown spots that eventually destroyed entire fruit. Small sporodochia later appeared on the surface. Conidia isolated from each host were one-celled, hyaline, lemon-shaped and borne in branched monilioid chains. The optimal temperature range for hyphal growth of all the isolates was o C. The growth of hyphae was faster on potato dextrose agar and oatmeal agar than others. Multiple alignments using the ITS sequences from different host showed that they matched each other (100%). The ITS sequences showed 100% identity to those of M. fructicola. Based on the morphological characteristics and phylogenetic analysis via internal transcribed spacer (ITS), all the isolate was identified as M. fructicola. Pathogenicity of representative isolates was proved by artificial inoculation, fulfilling Koch s postulates. This is the first confirmed report on brown rot caused by M. fructicola on stone fruit in Korea. Keywords: Brown rot, Monilinia fructicola, Stone fruit ( ), ( ), [Prunus mume Siebold & Zucc.], [P. persica (L.) Batsch], Research in Plant Disease pissn , eissn [P. ameniaca var. ansu Maxim.], [P. salicina Lindl.], [P. avium (L.) L.].,,,. 5-6, 6-7, 7, (Rural Development Administration, 2007)., The Korean Society of Plant Pathology This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

2 Research in Plant Disease Vol. 23 No , ,114 ha ,082 ha 10 (Ministry of Agriculture, Food and Rural Affairs, 2017)., ton, ,383 ton (Ministry of Agriculture, Food and Rural Affairs, 2010).,. Alternaria sp., Botrytis cinerea (gray mold), Cercospora circumscissa (leaf spot), Cladosporium carpophilum (scab), Colletotrichum spp. (anthracnose), Monilinia fructicola (brown rot), Phomopsis vexans (brown rot), Phyllosticta circumscissa (leaf spot), Podosphaera tridactyla (powdery mildew), Septoria cerasina (leaf spot), Taphrina mume (leaf curl) (The Korean Society of Plant Pathology, 2009)., Monilinia, (Rural Development Administration, 2008)., Monilinia,,,,,,, M. fructicola (G. Winter) Honey, M. fructigena (Aderhold & Ruhland) Honey, M. laxa (Aderhold & Ruhland) Honey (Choi, 2016). M. fructicola,,, M. fructigena, M. laxa,,, (Fulton Brown, 1997; Hu, 2011; Shim, 2007)., M. fructicola M. laxa (blossom blight), brown rot. M. fructigena (Rungjindamai, 2014)., M. fructicola,,,,,, M. fructigena (The Korean Society of Plant Pathology, 2009). M. fructicola, (Shim, 2007), (Choi, 2014), (Choi, 2016).,.,,,,, ,,,. 3, ml eppendorf, 30. (Difco, MD, USA). 3, 25 o C 7. (Korea University Herbarium, KUS), (Korean Agricultural Culture Collection, KACC),,, (Table 1).. PDA 4 o C, 10 o C, 15 o C, 20 o C, 25 o C, 30 o C 7. PDA (Potato dextrose agar), OA (Oatmeal agar), CMA (Corn meal agar), WA (Water agar), RBA (Rose Bengal agar) 25 o C 7. 4, 1 mm, 35 mm.., 7 (scalpel) conidia/ml. 5,. 100%,

3 324 Research in Plant Disease Vol. 23 No. 4 Table 1. Summary of Monilinia fructicola isolates investigated in this study Host plant/isolation source Japanese apricot [Prunus mume] Peach [P. persica] Apricot [P. ameniaca var. ansu] Japanese plum [P. salicina] Sweet cherry [P. avium] Geographic origin Date Incidence of brown rot (%) Herbarium voucher ITS GenBank Acc. No. Imsil, Korea Jun KACC47998 KU <2.0 Imsil, Korea Jul JBARES-F33 MF Imsil, Korea Jul KACC47999 KU <3.0 Jeoju, Korea Jul JBARES-F35 MF Jeonju, Korea Jun KACC48000 KU <5.0 Jeonju, Korea Jun JBARES-F37 MF Imsil, Korea Jun JBARES-F41 MF <2.0 Jeonju, Korea Jul JBARES-F40 MF Jeonju, Korea Jun KACC48001 MF <4.0 Jeonju, Korea Jun JBARES-F39 MF o C.. 7 Stereo (SteREO Discovery. V8, Zeiss, Munich, Germany) DIC (differential interference contrast) (AXIO, Zeiss) 200-1,000. (n=30) AxioVision LE Module Interactive Measurement (Zeiss).. 7 ribosomal DNA (rdna) internal transcribed spacer (ITS). Genomic DNA DNeasy Plant Mini kit (QIAGEN, Valencia, Canada), ITS1/ITS4 pirmer PCR (White, 1990). PCR. autosequencer (ABI 3030), GenBank database (National Centre for Biotechnology Information [NCBI] US National Institute of Health Bethesda, ncbi.nlm.nih.gov/blast.cgi). GenBank ITS, MEGA 6.0 neighbor-joining. Sequence distance Tajima-Nei parameter model (Saitou Nei, 1987; Tamura, 2013)., Botrytis cinerea (GenBank accession No. KX229751) outgroup. [ ] (2009) Monilinia fructicola (G. Winter) Honey. M. fructicola (Japan), M. kusanoi (Japan), M. laxa (China, Japan), M. mume (Japan) (Farr Rossman, 2017) (35 o 38'10"N; 127 o 19'02"E), <2.0% (Table 1)., (Fig. 1A).,, (Fig. 1B).,,., o C, o C. 4 o C 30 o C. OA PDA, WA, RBA, CMA. -, (flat)/ (effuse), (lobate) (Table 2, Fig. 1E).. 4

Research in Plant Disease Vol. 23 No. 4 325 Fig. 1. Brown rot caused by Monilinia fructicola on Japanese apricot.

4 Research in Plant Disease Vol. 23 No Fig. 1. Brown rot caused by Monilinia fructicola on Japanese apricot. (A) Occurrence of brown rot in a farm in June 2015, (B) A brown rotted fruit covered with the grayish spore mass, sporodochia, (C, D) Monilioid chains and lemon shaped conidia, (E) Five-day-old colony of M. fructicola on PDA., 6,... (monilioid chains) (Fig. 1C),,, m (Table 2, Fig. 1D).. KACC47998 JBARES-F33 ITS sequence 499 bp NCBI GenBank KU513384, MF NCBI Blast search M. fructicola GenBank accession number KC544809, JN176564, FJ515894, KM %., M. fructicola (Table 1, Fig. 6)..,, Monilinia fructicola (G. Winter) Honey (Pellegrino, 2009). M. fructicola. M. kusanoi, M. laxa, M. mume (Farr Rossman, 2017). (2009). [ ] (2009) Monilinia fructicola (G. Winter) Honey. M. fructicola (Australia, Brazil, Canada, China, Croatia, Czech Republic, Ecuador, Greece, Hungary, Japan, Mexico, New Zealand, Norway, Slovenia, South Africa, Spain, Tasmania, United States, Venezuela), M. fructigena (Bulgaria, China, Cuba, Croatia, France, Hungary, Italy, Sicily, Netherlands, Spain), M. laxa (Australia, Brazil, Bulgaria, Chile, China, Croatia, Greece, Hungary, Iraq, Italy, Sicily, New Zealand, Norway, Serbia, Slovenia, South Africa, Spain, United States), M.

5 326 Research in Plant Disease Vol. 23 No. 4 Table 2. Comparison of morphological and cultural characteristics between the present isolates obtained from infected stone fruit and Monilinia fructicola species described previously Characters Present isolates a KACC47998 KACC47999 KACC48000 JBARES-F41 KACC48001 M. fructicola b Conidia size (mm ) Conidia type Monilioid chains Monilioid chains Monilioid chains Monilioid chains Monilioid chains Monilioid chains Sporulation Abundant Abundant Abundant Abundant Abundant Abundant Colony morphology Flat/Effuse Lobate Flat/Effuse Lobate Flat/Effuse Lobate Raised Lobate Flat/Effuse Lobate Flat/Effuse Lobate a All structures were investigated on PDA plates incubated at 25 o C for 7 days. b Monilinia fructicola species described by EPPO/CABI (2010). Fig. 2. Brown rot caused by Monilinia fructicola on peach. (A) Occurrence of brown rot in a farm in July 2015, (B) A brown rotted fruit covered with the grayish spore mass, sporodochia, (C, D) Monilioid chains and lemon shaped conidia, (E) Five-day-old colony of M. fructicola on PDA. polystroma (Italy, Japan, Slovenia), M. seaveri (United States), Monilinia sp. (Brazil) (Farr Rossman, 2017) (35 o 38'10"N; 127 o 19'02"E) (35 o 51'51"N; 127 o 02'49"E), <3.0% (Table 1)., (Fig. 2A). (Fig. 2B).,, o C,

Research in Plant Disease Vol. 23 No. 4 327 10-25 o C. 4 o C 30 o C. OA PDA, WA, RBA, CMA. -, (flat)/ (effuse), (lobate) (Table 2, Fig. 2E).. 4, 5,... (monilioid chains) (Fig. 2C),,, - 15.0-18.7 9.

6 Research in Plant Disease Vol. 23 No o C. 4 o C 30 o C. OA PDA, WA, RBA, CMA. -, (flat)/ (effuse), (lobate) (Table 2, Fig. 2E).. 4, 5,... (monilioid chains) (Fig. 2C),,, m (Table 2, Fig. 2D).. KACC47999 JBARES-F35 ITS sequence 499 bp NCBI GenBank KU513385, MF NCBI Blast search M. fructicola GenBank accession number KC544809, JN176564, FJ515894, KM %., M. fructicola (Table 1, Fig. 6)..,, Monilinia fructicola (G. Winter) Honey (Pellegrino, 2009). M. fructicola. M. fructigena, M. laxa, M. polystroma, M. seaveri (Farr Rossman, 2017). (2009). Fig. 3. Brown rot caused by Monilinia fructicola on Apricot, (A) Occurrence of brown rot in a farm in June The fruit was infected, dark black mummified the whole fruit, (B) A brown rotted fruit covered with the grayish spore mass, sporodochia, (C, D) Monilioid chains and lemon shaped conidia, (E) Five-day-old colony of M. fructicola on PDA.

328 Research in Plant Disease Vol. 23 No. 4 [ ] Research in Plant Disease (Choi, 2016) Monilinia fructicola (G. Winter) Honey. (Farr Rossman, 2017).. 2015 6 (35 o 52'18"N; 127 o 06'49"E), <5.

7 328 Research in Plant Disease Vol. 23 No. 4 [ ] Research in Plant Disease (Choi, 2016) Monilinia fructicola (G. Winter) Honey. (Farr Rossman, 2017) (35 o 52'18"N; 127 o 06'49"E), <5.0% (Table 1).., (Fig. 3A).,, (Fig. 3A). (Fig. 3B). CMA. -, (flat)/ (effuse), (lobate) (Table 2, Fig. 3E).. 3,, 5,... (monilioid chains) (Fig. 3C),,, m (Table 2, Fig. 3D).. 25 o C, o C. 4 o C 30 o C. OA PDA, WA, RBA,. KACC48000 JBARES-F37 ITS sequence 499 bp NCBI GenBank KU513386, MF NCBI Blast search M. fructicola Fig. 4. Brown rot caused by Monilinia fructicola on Japanese plum. (A) Occurrence of brown rot in a farm in July 2017, (B) A brown rotted fruit covered with the grayish spore mass, sporodochia, (C, D) Monilioid chains and lemon shaped conidia, (E) Five-day-old colony of M. fructicola on PDA.

8 Research in Plant Disease Vol. 23 No GenBank accession number KC544809, JN176564, FJ515894, KM %., M. fructicola (Table 1, Fig. 6)..,, Monilinia fructicola (G. Winter) Honey (Pellegrino, 2009). Choi (2016),. [ ] (2009) Monilinia fructicola (G. Winter) Honey. M. fructicola (Australia, Brazil, Chile, China, Japan, New Zealand, Spain, United States), M. fructigena (China), M. laxa (China, Japan, South Africa, United States) (Farr Rossman, 2017) (35 o 35'18"N; 127 o 18'43"E) (35 o 52'42"N; 127 o 06'39"E), <2.0% (Table 1)., (Fig. 4A, 4B).,,. Fig. 4D).. JBARES-F40 JBARES-F41 ITS sequence 499 bp NCBI GenBank MF597786, MF NCBI Blast search M. fructicola GenBank accession number KC544809, JN176564, FJ515894, KM %., M. fructicola (Table 1, Fig. 6)..,, Monilinia fructicola (G. Winter) Honey (Pellegrino, 2009). M. fructicola. M. fructigena, M. laxa (Farr Rossman, 2017). (2009). [ ] (Choi, 2014) Monilinia fructicola (G. Winter) Honey. M. fructicola (Australia, Canada, China, Greece, Japan, Maryland, United States), M. fructigena (Bulgaria, Serbia), M. kusanoi (Japan), M. laxa (Australia, Bulgaria, Canada, Greece, Japan, Norway, Serbia, Slovenia, United States), Monilinia sp. (Japan) (Farr Rossman, 2017) o C, o C. 4 o C 30 o C. OA PDA, WA, RBA, CMA. -, (raised), (lobate) (Table 2, Fig. 4E).. 3, 4,... (monilioid chains) (Fig. 4C),,, m (Table 2, (35 o 52'42"N; 127 o 06'39"E), <4.0% (Table 1)..,, (Fig. 5A). (Fig. 5B) o C, o C. 4 o C 30 o C. OA PDA, WA, RBA, CMA. -, (flat)/ (effuse), (lobate) (Table 2, Fig. 5E).

9 330 Research in Plant Disease Vol. 23 No. 4 Fig. 5. Brown rot caused by Monilinia fructicola on sweet cherry. (A) Occurrence of brown rot in a farm in June 2017, (B) A brown rotted fruit covered with the grayish spore mass, sporodochia, (C, D) Monilioid chains and lemon shaped conidia, (E) Five-day-old colony of M. fructicola on PDA.. 5, 7,... (monilioid chains) (Fig. 5C),,, m (Table 2, Fig. 5D).. KACC48001 JBARES-F39 ITS sequence 499 bp NCBI GenBank MF597791, MF NCBI Blast search M. fructicola GenBank accession number KC544809, JN176564, FJ515894, KM %., M. fructicola (Table 1, Fig. 6)..,, Monilinia fructicola (G. Winter) Honey (Pellegrino, 2009). M. fructicola. M. fructigena, M. kusanoi, M. laxa (Farr Rossman, 2017). Choi (2014).,,, (Rural Development Administration, 2008) ,,,,

10 Research in Plant Disease Vol. 23 No Fig. 6. Phylogenetic analysis by means of the neighbor-joining method comparing the internal transcribed spacer ribosomal DNA (rdna) region of Monilinia fructicola with that of other Monilinia spp. retrieved from GenBank. The numbers above the nodes are the bootstrap values obtained from 1,000 replicates. The isolates obtained in this study are shown in boldface.,.,,..,., 1-2. M. fructicola, (Gell, 2008). 1., (Sinclair Lyon, 2005)., 50-75% (Rural Development Administration, 2008)., M. fructicola (Pellegrino, 2009)., M. fructicola M. laxa,

11 332 Research in Plant Disease Vol. 23 No. 4 M. fructicola (Sinclair Lyon, 2005; Zhu, 2005). M. fructicola, Shim (2007) 30 o C. M. fructicola (Petroczy Palkovics, 2006; Pellegrino, 2009)., 10 o C 4 o C., OA PDA, WA, RBA, CMA. RBA WA, RBA, WA,. RBA, M. fructicola (Martin, 1950). OA, CMA (sporulation) PDA (Crous, 2009). M. fructicola, M. fructigena, M. laxa, M. yunnanensis ITS, ITS 100%, 4 (Hu, 2011). M. fructigena M. laxa M. fructicola small subunit (SSU) rdna 418 bp group-i intron M. fructigena M. laxa M. fructicola (Fulton Brown, 1997). M. fructicola M. fructicola, M. fructigena, M. laxa, M. polystroma, M. seaveri (Farr Rossman, 2017)., M. fructicola ,,,, 2-5%.,.,,,. (monilioid chains),,, o C, OA PDA.,, ribosomal DNA (rdna) ITS Monilinia fructicola.. M. fructicola. Conflicts of Interest No potential conflict of interest relevant to this article was reported. Acknowledgement This study was carried out with the support of Cooperative Research Program for Agricultural Science & Technology Development (Project No. PJ011690) Rural Development Administration, Republic of Korea. References Choi, I. Y., Kim, J., Seo, K. W., Oh, H. T., Cho, J. H., Kim, J. H. and Song, Y. J Occurrence of brown rot on apricot caused by Monilinia fructicola in Korea. Res. Plant Dis. 22: (In Korean) Choi, H. W., Hong, S. K., Lee, Y. K., Nam, Y. J., Lee, J. G. and Shim, H. S Characterization of Monilinia fructicola associated with brown rot of cherry fruit in Korea. Kor. J. Mycol. 42: (In Korean) Crous, P. W., Verkley, G. J. M., Groenewald, J. Z. and Samon, R. A Fungal Biodiversity, pp CBS-KNAW Fungal Biodiversity Centre Utrecht, The Netherlands. EPPO/CABI Data sheets on quarantine pests: Monilinia fructicola. Farr, D. F. and Rossman, A. Y. Fungal Databases, Systematic Mycology & Microbiology Laboratory, ARS, USDA [Internet]. United States Department of Agriculture, Washington, DC. Cited 24th July URL Fulton, C. E. and Brown, A. E Use of SSU rdna group-i intron to distinguish Monilinia fructicola from M. laxa and M. fructigena. FEMS Microbiol. Lett. 157:

12 Research in Plant Disease Vol. 23 No Gell, I., De Cal, A., Torres, R., Usall, J. and Melgarejo, P Relationship between the incidence of latent infections caused by Monilinia spp. and the incidence of brown rot of peach fruit: factors affecting latent infection. Eur. J. Plant Pathol. 121: Hu, M. J., Cox, K. D., Schnabel, G. and Luo, C. X Monilinia species causing brown rot of peach in China. PLoS One 6: e Martin, J. P Use of acid, rose bengal, and streptomycin in the plate method for estimating soil fungi. Soil Sci. 69: Ministry of Agriculture, Food and Rural Affairs Statistics of Cultivation and Production of Industrial Crops in Ministry of Agriculture, Food and Rural Affairs, Sejong, Korea. Ministry of Agriculture, Food and Rural Affairs Statistics of Cultivation and Production of Industrial Crops in Ministry of Agriculture, Food and Rural Affairs, Sejong, Korea. Pellegrino, C., Gullino, M. L., Garibaldi, A. and Spadaro, D First report of brown rot of stone fruit caused by Monilinia fructicola in Italy. Plant Dis. 93: 668. Petroczy, M. and Palkovics, L First report of brown rot caused by Monilinia fructicola on imported peach in Hungary. Plant Dis. 90: 375. Rungjindamai, N., Jeffries, P. and Xu, X. M Epidemiology and management of brown rot on stone fruit caused by Monilinia laxa. Eur. J. Plant Pathol. 140: Rural Development Administration Monography of Stone Fruit Cultivars. Suwon, Korea. 252 pp. (In Korean) Rural Development Administration New Illustrated Book on Diseases, Insect Pests in Fruit Trees. Suwon, Korea. 550 pp. (In Korean) Saitou, N. and Nei, M The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: Shim, M. Y., Jeon, Y. J. and Kim, S. H Characterization of a brown rot fungus isolated from dwarf flowering almond in Korea. Mycobiology 35: Sinclair, W. A. and Lyon, H. H Diseases of Trees and Shrubs. 2nd ed. pp Ithaca and London, Comstock Publication Associates, Cornell University Press. Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30: The Korean Society of Plant Pathology List of Plant Disease in Korea. 5th ed. The Korean Society of Plant Pathology, Suwon, Korea. 853 pp. White, T. J., Bruns, T., Lee, S. and Taylor, J Amplification anddirect sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods and Applications, eds. by M. A. Innis, D. H. Gelfand, J. J. Shinski and T. J. White, pp Academic Press, San Diego, CA, USA. Zhu, X. Q., Chen, X. Y., Luo, Y. and Guo, L. Y First report of Monilinia fructicola on peach and nectarine in China. Plant Pathol. 54: 575.

식물병연구 Note Open Access Res. Plant Dis. 22(2): (2016) Monilinia fructicola 에의한살구잿빛무늬병 Occurrence of

식물병연구 Note Open Access Res. Plant Dis. 22(2): 122-126 (2016) http://dx.doi.org/10.5423/rpd.2016.22.2.122 Monilinia fructicola 에의한살구잿빛무늬병 Occurrence of Brown Rot on Apricot Caused by Monilinia fructicola