Abstract
Hyphal interactions of 10 Rosellinia necatrix isolates were analyzed. Most incompatible pairings produced broad melanized barrage lines, with a few exceptions. The variation in barrage lines revealed using light microscopy might result from distinct frequencies of different hyphal interaction types. In incompatible pairings, hyphal anastomosis was rarely observed. Activated-charcoal treatment of oatmeal agar media prevented both incompatible and compatible reactions. FUN-1 staining showed vacuole dysfunction at hyphal interaction sites, and the localization of a Lifeact-GFP mutant revealed that actin dynamics was prominent in compatible pairings. These results suggested that self/nonself recognition commonly proceeded to vacuole dysfunction and that actin dynamics played a critical role in the restoration of vacuole integrity.
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References
Ainsworth AM, Rayner ADM (1986) Responses of living hyphae associated with self and non-self fusions in the basidiomycete Phanerochaete velutina. J Gen Microbiol 132:191–201
Araki T (1967) Soil conditions and the violet and white root rot diseases of fruit trees. Bull Natl Inst Agric Sci C 21:1–109
Armengol J, Vicent A, León M, Berbegal M, Abad-Campos P, García-Jiménez J (2010) Analysis of population structure of Rosellinia necatrix on Cyperus esculentus by mycelial compatibility and inter-simple sequence repeats (ISSR). Plant Pathol 59:179–185
Berepiki A, Lichius A, Shoji J, Tilsner J, Read ND (2010) F-actin dynamics in Neurospora crassa. Eukaryot Cell 9:547–557
Caten CE (1972) Vegetative incompatibility and cytoplasmic infection in fungi. J Gen Microbiol 72:221–229
Essary BD, Marshall PA (2009) Assessment of FUN-1 vital dye staining: yeast with a block in the vacuolar sorting pathway have impaired ability to form CIVS when stained with FUN-1 fluorescent dye. J Microbiol Methods 78:208–212
Esser K (2006) Heterogenic incompatibility in fungi. In: Kües U, Fischer R (eds) The Mycota I. Growth, differentiation and sexuality. Springer, Berlin, pp 141–165
Fleissner A, Leeder AC, Roca MG, Read ND, Glass NL (2009) Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion. Proc Natl Acad Sci USA 106:19387–19392
Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245
Ghabrial SA, Suzuki N (2009) Viruses of plant pathogenic fungi. Annu Rev Phytopathol 47:353–384
Giovannetti M, Sbrana C, Strani P, Agnolucci M, Rinaudo V, Avio L (2003) Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Appl Environ Microbiol 69:616–624
Glass NL, Dementhon K (2006) Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9:553–558
Glass NL, Jacobson DJ, Shiu PKT (2000) The genetics of hyphal fusion and vegetative incompatibility in filamentous ascomycete fungi. Annu Rev Genet 34:165–186
Hatsugai N, Kuroyanagi M, Nishimura M, Hara-Nishimura I (2006) A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11:905–911
Hutchison E, Brown S, Tian C, Glass NL (2009) Transcriptional profiling and functional analysis of heterokaryon incompatibility in Neurospora crassa reveals that reactive oxygen species, but not metacaspases, are associated with programmed cell death. Microbiology 155:3957–3970
Hyakumachi M, Ui T (1987) Non-self-anastomosing isolates of Rhizoctonia solani obtained from fields of sugarbeet monoculture. Trans Br Mycol Soc 89:155–159
Ikeda K, Nakamura H, Arakawa M, Matsumoto N (2004) Diversity and vertical transmission of double-stranded RNA elements in root rot pathogens of trees, Helicobasidium mompa and Rosellinia necatrix. Mycol Res 108:626–634
Ikeda K, Inoue K, Nakamura H, Hamanaka T, Ohta T, Kitazawa H, Kida C, Kanematsu S, Park P (2011) Genetic analysis of barrage line formation during mycelial incompatibility in Rosellinia necatrix. Fungal Biol 115:80–86
Inoue K, Kanematsu S, Park P, Ikeda K (2011) Cytological analysis of mycelial incompatibility in Rosellinia necatrix. Fungal Biol 115:87–95
Ishikawa FH, Souza EA, Shoji J, Connolly L, Freitag M, Read ND, Roca MG (2012) Heterokaryon incompatibility is suppressed following conidial anastomosis tube fusion in a fungal plant pathogen. PLoS One 7:e31175
Kanematsu S, Arakawa M, Oikawa Y, Onoue M, Osaki H, Nakamura H, Ikeda K, Kuga-Uetake Y, Nitta H, Sasaki A, Suzaki K, Yoshida K, Matsumoto N (2004) A reovirus causes hypovirulence of Rosellinia necatrix. Phytopathology 94:561–568
Kimura N, Tsuge T (1993) Gene cluster involved in melanin biosynthesis of the filamentous fungus Alternaria alternata. J Bacteriol 175:4427–4435
López M, Ruano-Rosa D, López-Herrera CJ, Monte E, Hermosa R (2008) Intraspecific diversity within avocado field isolates of Rosellinia necatrix from south-east Spain. Eur J Plant Pathol 121:201–205
Marek SM, Wu J, Glass NL, Gilchrist DG, Bostock RM (2003) Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 40:126–137
Millard PJ, Roth BL, Thi HP, Yue ST, Haugland RP (1997) Development of the FUN-1 family of fluorescent probes for vacuole labeling and viability testing of yeasts. Appl Environ Microbiol 63:2897–2905
Pérez-Jiménez RM (2006) A review of the biology and pathogenicity of Rosellinia necatrix—the cause of white root rot disease of fruit trees and other plants. J Phytopathol 154:257–266
Pérez-Jiménez RM, Jiménez-Díaz RM, López-Herrera CJ (2002) Somatic incompatibility of Rosellinia necatrix on avocado plants in southern Spain. Mycol Res 106:239–244
Pinan-Lucarré B, Paoletti M, Dementhon K, Coulary-Salin B, Clavé C (2003) Autophagy is induced during cell death by incompatibility and is essential for differentiation in the filamentous fungus Podospora anserina. Mol Microbiol 47:321–333
Prasad I (1970) Genetic analysis of the coloured mutants of Aspergillus niger. Genetica 41:388–398
Ramsdale M (2008) Programmed cell death in pathogenic fungi. Biochim Biophys Acta 1783:1369–1380
Ranganath RM, Nagashree NR (2001) Role of programmed cell death in development. Int Rev Cytol 202:159–242
Read ND, Lichius A, Shoji J, Goryachev AB (2009) Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12:608–615
Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R (2008) Lifeact: a versatile marker to visualize F-actin. Nat Methods 5:605–607
Roberson RW (1992) The actin cytoskeleton in hyphal cells of Sclerotium rolfsii. Mycologia 84:41–51
Saupe SJ (2000) Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64:489–502
Sbrana C, Nuti MP, Giovannetti M (2007) Self-anastomosing ability and vegetative incompatibility of Tuber borchii isolates. Mycorrhiza 17:667–675
Van Zandycke SM, Simal O, Smart KA (2003) Vitality assessment using the fluorescent stain FUN1. In: Smart K (ed) Brewing yeast fermentation performance. Blackwell Science, Oxford, pp 162–168
Zakeri Z, Bursch W, Tenniswood M, Lockshin RA (1995) Cell death: programmed, apoptosis, necrosis, or other? Cell Death Differ 2:87–96
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This research was supported by the program for Science and Technology Research Promotion Program for Agriculture, Forestry, Fisheries and Food Industry.
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Uwamori, T., Inoue, K., Kida, C. et al. Self- and nonself recognition during hyphal interactions in Rosellinia necatrix . J Gen Plant Pathol 81, 420–428 (2015). https://doi.org/10.1007/s10327-015-0622-y
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DOI: https://doi.org/10.1007/s10327-015-0622-y