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Dynamics of infection-related morphogenesis and pathogenesis in Colletotrichum orbiculare

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Abstract

Colletotrichum orbiculare (syn. C. lagenarium) is the causal agent of anthracnose disease on cucurbit plants. This fungus forms dome-shaped, melanized appressoria as a host invasion structure. Strain 104-T (MAFF240422) of C. orbiculare, which was originally isolated from a cucumber plant in 1951 by Dr. Yasumori, Kyoto University, has proven to be an excellent experimental model for the study of fungal pathogenesis and morphogenesis because of its stable pathogenicity and synchronous infection-related morphogenesis. This review considers the discoveries made during 60 years of study on C. orbiculare. In particular, we focus on advances made in the last two decades, which have provided a basis for the molecular analysis not only of fungal morphogenesis, but also of plant–microbe interactions, including plant immunity to adapted and nonadapted Colletotrichum fungi. This substantial body of innovative research was originated by the Phytopathological Society of Japan and represents a major contribution to the international research communities working on plant pathology, plant–microbe interactions, and fungal molecular genetics. This review deals with the past achievements and future prospects in the study of Colletotrichum biology, focusing on the molecular genetics of C. orbiculare with regard to four aspects: (1) metabolic and functional development of infection structures, (2) signaling pathways required for fungal pathogenesis, (3) pathogen-associated molecular patterns (PAMPs) and host basal resistance, and (4) establishment of host specificity.

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References

  • Adams J, Kelso R, Cooley L (2000) The kelch repeat superfamily of proteins: propellers of cell function. Trends Cell Biol 10:17–24

    Article  PubMed  CAS  Google Scholar 

  • Akai S, Ishida N (1968) An electron microscopic observation on the germination of conidia of Colletotrichum lagenarium. Mycopath Mycol Appl 34:337–345

    Article  Google Scholar 

  • Asakura M, Okuno T, Takano Y (2006) Multiple contributions of peroxisomal metabolic function to fungal pathogenicity in Colletotrichum lagenarium. Appl Environ Microbiol 72:6345–6354

    Article  PubMed  CAS  Google Scholar 

  • Asakura M, Ninomiya S, Sugimoto M, Oku M, Yamashita S, Okuno T, Sakai Y, Takano Y (2009) Atg26-mediated pexophagy is required for host invasion by the plant pathogenic fungus Colletotrichum orbiculare. Plant Cell 21:1291–1304

    Article  PubMed  CAS  Google Scholar 

  • Asakura M, Yoshino K, Hill AM, Kubo Y, Sakai Y, Takano Y (2012) Primary and secondary metabolism regulates lipolysis in appressoria of Colletotrichum orbiculare. Fung Genet Biol 49:967–975

    Article  CAS  Google Scholar 

  • Bednarek P, Pislewska-Bednarek M, Svatoš A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, Molina A, Schulze-Lefert P (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106

    Article  PubMed  CAS  Google Scholar 

  • Behrens R, Nurse P (2002) Roles of fission yeast tea1p in the localization of polarity factors and in organizing the microtubular cytoskeleton. J Cell Biol 157:783–793

    Article  PubMed  CAS  Google Scholar 

  • Bhambra GK, Wang ZY, Soanes DM, Wakley GE, Talbot NJ (2006) Peroxisomal carnitine acetyl transferase is required for elaboration of penetration hyphae during plant infection by Magnaporthe grisea. Mol Microbiol 61:46–60

    Article  PubMed  CAS  Google Scholar 

  • Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum—current status and future directions. Stud Mycol 73:181–213

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  CAS  Google Scholar 

  • Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci USA 98:373–378

    Article  PubMed  CAS  Google Scholar 

  • Fujihara N, Sakaguchi A, Tanaka S, Fujii S, Tsuji G, Shiraishi T, O’Connell R, Kubo Y (2010) Peroxisome biogenesis factor PEX13 is required for appressorium-mediated plant infection by the anthracnose fungus Colletotrichum orbiculare. Mol Plant-Microbe Interact 23:436–445

    Article  PubMed  CAS  Google Scholar 

  • Furusawa I, Nishiguchi M, Tani M, Ishida N (1977) Evidence of early protein synthesis essential to the spore germination of Colletotrichum lagenarium. J Gen Microbiol 101:307–310

    Article  CAS  Google Scholar 

  • Gan P, Ikeda K, Irieda H, Narusaka M, O’Connell RJ, Narusaka Y, Takano Y, Kubo Y, Shirasu K (2013) Comparative genomic and transcriptomic analyses reveal the hemibiotrophic stage shift of Colletotrichum fungi. New Phytol 197:1236–1249

    Article  PubMed  CAS  Google Scholar 

  • Heath MC (2000) Nonhost resistance and nonspecific plant defenses. Curr Opin Plant Biol 3:315–319

    Article  PubMed  CAS  Google Scholar 

  • Heiland I, Erdmann R (2005) Biogenesis of peroxisomes: topogenesis of the peroxisomeal membrane and matrix proteins. FEBS J 272:2362–2372

    Article  PubMed  CAS  Google Scholar 

  • Hiruma K, Onozawa-Komori M, Takahashi F, Asakura M, Bednarek P, Okuno T, Schulze-Lefert P, Takano Y (2010) Entry mode-dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22:2429–2443

    Article  PubMed  CAS  Google Scholar 

  • Hiruma K, Nishiuchi T, Kato T, Bednarek P, Okuno T, Schulze-Lefert P, Takano Y (2011) Arabidopsis ENHANCED DISEASE RESISTANCE 1 is required for pathogen-induced expression of plant defensins in nonhost resistance, and acts through interference of MYC2-mediated repressor function. Plant J 67:980–992

    Article  PubMed  CAS  Google Scholar 

  • Hughes HB, Carzaniga R, Rawlings SL, Green JR, O’Connell RJ (1999) Spore surface glycoproteins of Colletotrichum lindemuthianum are recognized by a monoclonal antibody which inhibits adhesion to polystyrene. Microbiology 145:1927–1936

    Article  PubMed  CAS  Google Scholar 

  • Ishida N, Akai S (1968) Electron microscopic observation of cell wall structure during appressorium formation in Colletotrichum lagenarium. Mycopath Mycol Appl 35:68–74

    Article  CAS  Google Scholar 

  • Ishida N, Akai S (1969) Relation of temperature to germination of conidia and appressorium formation in Colletotrichum lagenarium. Mycologia 61:382–386

    Article  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Kaeberlein M, Guarente L (2002) Saccharomyces cerevisiae MPT5 and SSD1 function in parallel pathways to promote cell wall integrity. Genetics 160:83–95

    PubMed  CAS  Google Scholar 

  • Katoh M, Hirose I, Kubo Y, Hikichi Y, Kunoh H, Furusawa I, Shishiyama J (1988) Use of mutants to indicate factors prerequisite for penetration of Colletotrichum lagenarium by appressoria. Physiol Mol Plant Pathol 32:177–184

    Article  Google Scholar 

  • Kimura A, Takano Y, Furusawa I, Okuno T (2001) Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell 13:1945–1957

    PubMed  CAS  Google Scholar 

  • Kojima K, Kikuchi T, Takano Y, Oshiro E, Okuno T (2002) The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. Mol Plant Microbe Interact 15:1268–1276

    Article  PubMed  CAS  Google Scholar 

  • Kojima K, Takano Y, Yoshimi A, Tanaka C, Kikuchi T, Okuno T (2004) Fungicide activity through activation of a fungal signalling pathway. Mol Microbiol 53:1785–1796

    Article  PubMed  CAS  Google Scholar 

  • Kubo Y, Furusawa I (1986) Localization of melanin in appressoria of Colletotrichum lagenarium. Can J Microbiol 32:280–282

    Article  CAS  Google Scholar 

  • Kubo Y, Furusawa I (1991) Melanin biosynthesis: prerequisite for successful invasion of the plant host by appressoria of Colletotrichum and Pyricularia. In: Cole GT, Hoch HC (eds) The fungal spore and disease initiation in plants and animals. Plenum, New York, pp 205–217

    Google Scholar 

  • Kubo Y, Tanaka S (2010) Pathogenesis and plant basal resistance in Colletotrichum orbiculare and Magnaporthe oryzae infection. In: Wolpert T, Shiraishi T, Allen C, Akimitsu K, Glazebrook J (eds) Genome-enabled analysis of plant-pathogen interactions. APS Press, pp 101–110

  • Kubo Y, Suzuki K, Furusawa I, Ishida N, Yamamoto M (1982a) Relation of appressorium pigmentation and penetration of nitrocellulose membranes by Colletotrichum lagenarium. Phytopathology 72:498–501

    Article  CAS  Google Scholar 

  • Kubo Y, Suzuki K, Furusawa I, Yamamoto M (1982b) Effect of tricyclazole on appressorial pigmentation and penetration from appressoria of Colletotrichum lagenarium. Phytopathology 72:1198–1200

    Article  CAS  Google Scholar 

  • Kubo Y, Suzuki K, Furusawa I, Yamamoto M (1983) Scytalone as a natural intermediate of melanin biosynthesis in appressoria of Colletotrichum lagenarium. Exp Mycol 7:208–215

    Article  CAS  Google Scholar 

  • Kubo Y, Furusawa I, Yamamoto M (1984) Regulation of melanin biosynthesis during appressorium formation in Colletotrichum lagenarium. Exp Mycol 8:364–369

    Article  CAS  Google Scholar 

  • Kubo Y, Suzuki K, Furusawa I, Yamamoto M (1985) Melanin biosynthesis as a prerequisite for penetration by appressoria of Colletotrichum lagenarium: site of inhibition by melanin-inhibiting fungicides and their action in appressoria. Pestic Biochem Physiol 23:47–55

    Article  CAS  Google Scholar 

  • Kubo Y, Katoh M, Furusawa I, Shishiyama J (1986) Inhibition of melanin biosynthesis by cerulenin in appressoria of Colletotrichum lagenarium. Exp Mycol 10:301–306

    Article  CAS  Google Scholar 

  • Kubo Y, Furusawa I, Shishiyama J (1987) Relation between pigment intensity and penetration ability in appressoria of Colletotrichum lagenarium. Can J Microbiol 33:870–873

    Article  CAS  Google Scholar 

  • Kubo Y, Takano Y, Endo N, Yasuda N, Tajima S, Furusawa I (1996) Cloning and structural analysis of the melanin biosynthesis gene SCD1 encoding scytalone dehydratase in Colletotrichum lagenarium. Appl Environ Microbiol 62:4340–4344

    PubMed  CAS  Google Scholar 

  • Lin SY, Okuda S, Ikeda K, Okuno T, Takano Y (2012) LAC2 encoding a secreted laccase is involved in appressorial melanization and conidial pigmentation in Colletotrichum orbiculare. Mol Plant Microbe Interact 25:1552–1561

    Article  PubMed  CAS  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piate L (2004) Innate immunity in plants and animals: striking similarity and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • O’Connell RJ, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171:699–718

    Article  PubMed  Google Scholar 

  • O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J et al (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44:1060–1065

    Article  PubMed  Google Scholar 

  • Perfect SE, Hughes HB, O’Connell RJ, Green JR (1999) Colletotrichum: a model genus for studies on pathology and fungal–plant interactions. Fungal Genet Biol 27:186–198

    Article  PubMed  CAS  Google Scholar 

  • Perpetua NS, Kubo Y, Yasuda N, Takano Y, Furusawa I (1996) Cloning and characterization of a melanin biosynthetic THR1 reductase gene essential for appressorial penetration of Colletotrichum lagenarium. Mol Plant-Microbe Interact 9:323–329

    Article  PubMed  CAS  Google Scholar 

  • Prusky D, Freeman S, Dickman M (eds) (2000) Colletotrichum: host specificity, pathogenicity and host pathogen interaction. APS Press, St. Paul

  • Ramos-Pamplona M, Naqvi NI (2006) Host invasion during rice-blast disease requires carnitine-dependent transport of peroxisomal acetyl-CoA. Mol Microbiol 61:61–75

    Article  PubMed  CAS  Google Scholar 

  • Saitoh H, Fujisawa S, Mitsuoka C, Ito A, Hirabuchi A, Ikeda K, Irieda H, Yoshino K, Yoshida K, Matsumura H, Tosa Y, Win J, Kamoun S, Takano Y, Terauchi R (2012) Large-scale gene disruption in Magnaporthe oryzae identifies MC69, a secreted protein required for infection by monocot and dicot fungal pathogens. PLoS Pathog 8:e1002711

    Article  PubMed  CAS  Google Scholar 

  • Sakaguchi A, Miyaji T, Tsuji G, Kubo Y (2008) Kelch repeat protein Clakel2p and calcium signaling control appressorium development in Colletotrichum lagenarium. Eukaryot Cell 7:102–111

    Article  PubMed  CAS  Google Scholar 

  • Sakaguchi A, Miyaji T, Tsuji G, Kubo Y (2010a) A Kelch repeat protein, Cokel1p, associates with microtubules and is involved in appressorium development in Colletotrichum orbiculare. Mol Plant Microbe Interact 23:103–111

    Article  PubMed  CAS  Google Scholar 

  • Sakaguchi A, Tsuji G, Kubo Y (2010b) A yeast STE11 homologue CoMEKK1 is essential for pathogenesis-related morphogenesis in Colletotrichum orbiculare. Mol Plant Microbe Interact 23:1563–1572

    Article  PubMed  CAS  Google Scholar 

  • Shen S, Goodwin PH, Hsiang T (2001) Infection of Nicotiana species by the anthracnose fungus, Colletotrichum orbiculare. Eur J Plant Pathol 107:767–773

    Article  Google Scholar 

  • Shimada C, Lipka V, O’Connell R, Okuno T, Schulze-Lefert P, Takano Y (2006) Nonhost resistance in ArabidopsisColletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant Microbe Interact 19:270–279

    Article  PubMed  CAS  Google Scholar 

  • Stephenson SA, Hatfield J, Rusu AG, Maclean DJ, Manners JM (2000) CgDN3: an essential pathogenicity gene of Colletotrichum gloeosporioides necessary to avert a hypersensitive-like response in the host Stylosanthes guianensis. Mol Plant Microbe Interact 13:929–941

    Article  PubMed  CAS  Google Scholar 

  • Suzuki K, Furusawa I, Ishida N, Yamamoto M (1981) Protein synthesis during germination and appressorium formation of Colletotrichum lagenarium spores. J Gen Microbiol 124:61–69

    CAS  Google Scholar 

  • Suzuki K, Furusawa I, Ishida N, Yamamoto M (1982a) Chemical dissolution of cellulose membranes as a prerequisite for penetration from appressoria of Colletotrichum lagenarium. J Gen Microbiol 128:1035–1039

    CAS  Google Scholar 

  • Suzuki K, Kubo Y, Furusawa I, Ishida N, Yamamoto M (1982b) Behavior of colorless appressoria in an albino mutant of Colletotrichum lagenarium. Can J Microbiol 28:1210–1213

    Article  Google Scholar 

  • Suzuki K, Furusawa I, Yamamoto M (1983) Role of chemical dissolution of cellulose membranes in the appressorial penetration by Colletotrichum lagenarium. Ann Phytopathol Soc Japan 49:481–487

    Article  CAS  Google Scholar 

  • Takano Y, Kubo Y, Shimizu K, Mise K, Okuno T, Furusawa I (1995) Structural analysis of PKS1, a polyketide synthase gene involved in melanin biosynthesis in Colletotrichum lagenarium. Mol Gen Genet 249:162–167

    Article  PubMed  CAS  Google Scholar 

  • Takano Y, Kubo Y, Kuroda I, Furusawa I (1997) Temporal transcriptional pattern of three melanin biosynthesis genes, PKS1, SCD1, and THR1, in appressorium-differentiating and nondifferentiating conidia of Colletotrichum lagenarium. Appl Environ Microbiol 63:351–354

    PubMed  CAS  Google Scholar 

  • Takano Y, Kikuchi T, Kubo Y, Hamer JE, Mise K, Furusawa I (2000) The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol Plant Microbe Interact 13:374–383

    Article  PubMed  CAS  Google Scholar 

  • Takano Y, Komeda K, Kojima K, Okuno T (2001) Proper regulation of cyclic AMP-dependent protein kinase is required for growth, conidiation, and appressorium function in the anthracnose fungus Colletotrichum lagenarium. Mol Plant Microbe Interact 14:1149–1157

    Article  PubMed  CAS  Google Scholar 

  • Takano Y, Takayanagi N, Hori H, Ikeuchi Y, Suzuki T, Kimura A, Okuno T (2006) A gene involved in modifying transfer RNA is required for fungal pathogenicity and stress tolerance of Colletotrichum lagenarium. Mol Microbiol 60:81–92

    Article  PubMed  CAS  Google Scholar 

  • Takano Y, Asakura M, Sakai Y (2009) Atg26-mediated pexophagy and fungal phytopathogenicity. Autophagy 5:1041–1042

    Article  PubMed  Google Scholar 

  • Tanaka S, Yamada K, Yabumoto K, Fujii S, Huser A, Tsuji G, Koga H, Dohi K, Mori M, Shiraishi T, O’Connell R, Kubo Y (2007) Saccharomyces cerevisiae SSD1 orthologues are essential for host infection by the ascomycete plant pathogens Colletotrichum lagenarium and Magnaporthe grisea. Mol Microbiol 64:1332–1349

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Ishihama N, Yoshioka H, Huser A, O’Connell R, Tsuji G, Tsuge S, Kubo Y (2009) The Colletotrichum orbiculare ssd1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway. Plant Cell 21:2517–2526

    Article  PubMed  CAS  Google Scholar 

  • Tanaka S, Ichikawa A, Yamada K, Tsuji G, Nishiuchi T, Mori M, Koga H, Nishizawa Y, O’Connell R, Kubo Y (2010) HvCEBiP, a gene homologous to rice chitin receptor CEBiP, contributes to basal resistance of barley to Magnaporthe oryzae. BMC Plant Biol 10:288

    Article  PubMed  CAS  Google Scholar 

  • Tani M, Ishida N, Furusawa I (1977) Effect of temperature and antibiotics on appressorium formation in spores of Colletotrichum lagenarium. Can J Microbiol 23:626–629

    Article  PubMed  CAS  Google Scholar 

  • Titorenko VI, Rachubinski RA (2004) The peroxisome: orchestrating important developmental decisions from inside the cell. J Cell Biol 164:641–645

    Article  PubMed  CAS  Google Scholar 

  • Tsuji G, Kenmochi Y, Takano Y, Sweigard J, Farrall L, Furusawa I, Horino O, Kubo Y (2000) Novel fungal transcriptional activators, Cmr1p of Colletotrichum lagenarium and Pig1p of Magnaporthe grisea, contain Cys2His2 zinc finger and Zn(II)2Cys6 binuclear cluster DNA-binding motifs and regulate transcription of melanin biosynthesis genes in a developmentally specific manner. Mol Microbiol 38:940–954

    Article  PubMed  CAS  Google Scholar 

  • Tsuji G, Fujii S, Fujihara N, Hirose C, Tsuge S, Shiraishi T, Kubo Y (2003a) Agrobacterium tumefaciens-mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium. J Gen Plant Pathol 69:230–239

    Article  CAS  Google Scholar 

  • Tsuji G, Fujii S, Tsuge S, Shiraishi T, Kubo Y (2003b) The Colletotrichum lagenarium Ste12-like gene CST1 is essential for appressorium penetration. Mol Plant Microbe Interact 16:315–325

    Article  PubMed  CAS  Google Scholar 

  • Tsuji G, Sugawara T, Fujii I, Mori Y, Ebizuka Y, Shiraishi T, Kubo Y (2003c) Evidence for involvement of two naphthol reductases in the first reduction step of melanin biosynthesis pathway of Colletotrichum lagenarium. Mycol Res 107:854–860

    Article  PubMed  CAS  Google Scholar 

  • Tsuji G, Tsuge S, Shiraishi T, Kubo Y (2003d) Expression pattern of melanin biosynthesis enzymes during infectious morphogenesis of Colletotrichum lagenarium. J Gen Plant Pathol 69:169–175

    Article  CAS  Google Scholar 

  • Wanders RJA, Waterham HR (2004) Peroxisomal disorders I: biochemistry and genetics of peroxisome biogenesis disorder. Clin Genet 67:107–133

    Article  Google Scholar 

  • Xu JR, Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. Genes Dev 10:2696–2706

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi J, Takayanagi N, Komeda K, Takano Y, Okuno T (2004) cAMP-pKA signaling regulates multiple steps of fungal infection cooperatively with Cmk1 MAP kinase in Colletotrichum lagenarium. Mol Plant Microbe Interact 17:1355–1365

    Article  PubMed  CAS  Google Scholar 

  • Yoshino K, Irieda H, Sugimoto F, Yoshioka H, Okuno T, Takano Y (2012) Cell death of Nicotiana benthamiana is induced by secreted protein NIS1 of Colletotrichum orbiculare and is suppressed by a homologue of CgDN3. Mol Plant Microbe Interact 25:625–636

    Article  PubMed  CAS  Google Scholar 

  • Zhao X, Mehrabi R, Xu JR (2007) Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6:1701–1714

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We express sincere thanks to Dr. Yasumori who originally isolated C. orbiculare strain 104-T and started studies on C. orbiculare 60 years ago. Thanks are also extended to Drs. Ishida and Furusawa, who initiated studies on appressorial morphogenesis in the 1970s and provided a firm basis for later Colletotrichum research. We are also thankful to all the scientists, including many graduate students and postdoctorates, for their enthusiastic activity on Colletotrichum research, which has allowed this tremendous progress to be realized. We thank Dr. Richard O’Connell for his critical reading of the manuscript and valuable comments.

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Kubo, Y., Takano, Y. Dynamics of infection-related morphogenesis and pathogenesis in Colletotrichum orbiculare . J Gen Plant Pathol 79, 233–242 (2013). https://doi.org/10.1007/s10327-013-0451-9

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