Nuclear and genome dynamics in multinucleate ascomycete fungi

Current Biology

Volumn 21, Issue 18, 2011, Pages

  Roper, Marcus ^a,b   Ellison, Chris ^c   Taylor, John W ^c   Glass, N Louise ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ASCOMYCETES; CYTOLOGY; EVOLUTION; FUNGAL GENE; FUNGAL GENOME; GENETIC VARIABILITY; GENETICS; PHYSIOLOGY; REPRODUCTION; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ASCOMYCOTA; BIOLOGICAL EVOLUTION; GENES, FUNGAL; GENETIC VARIATION; GENOME, FUNGAL; REPRODUCTION;

FUNGI; NEUROSPORA CRASSA; SCLEROTINIA SCLEROTIORUM;

EID: 80053307852     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2011.06.042     Document Type: Review

References (85)

1. N.D. Read, A. Fleißner, M.G. Roca, and N.L. Glass Hyphal fusion K.A. Borkovich, D.J. Ebbole, Cellular and Molecular Biology of Filamentous Fungi 2010 ASM Press Washington, D.C. 260 273
2. R. Maheshwari Nuclear behavior in fungal hyphae FEMS Microbiol. Lett. 249 2005 7 14 (Pubitemid 40981875)
3. G.S. Sidhu Genetics of Gibberella fujikuroi. III. Significance of heterokaryosis in naturally occurring corn isolates Can. J. Bot. 61 1983 3320 3325
4. C.E. Caten, and J.L. Jinks Heterokaryosis: its significance in wild homothallic ascomycetes and fungi imperfecti Trans. Br. Mycol. Soc. 49 1966 81 93
5. J.L. Jinks Heterokaryosis: A system of adaptation in wild fungi Proc. R. Soc. Lond. B Biol. Sci. 140 1952 83 99
6. C.E. Caten The mutable and treacherous tribe revisited Plant Pathol. 45 1966 1 12
7. M. Rep, and H.C. Kistler The genomic organization of plant pathogenicity in Fusarium species Curr. Opin. Plant Biol. 13 2010 420 426
8. L.J. Ma, H.C. van der Does, K.A. Borkovich, J.J. Coleman, M.J. Daboussi, A. Di Pietro, M. Dufresne, M. Freitag, M. Grabherr, and B. Henrissat Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium Nature 464 2010 367 373
9. A. Rayner The challenge of the individualistic mycelium Mycologia 83 1991 48 71
10. G. Pontecorvo Genetic systems based on heterokaryosis. Cold Spring Harb Symp. Quant. Biol. 11 1946 193 201
11. A. Debets, and J.F. Griffiths Polymorphism of het-genes prevents resource plundering in Neurospora crassa Mycol. Res. 102 1998 1343 1349 (Pubitemid 28548043)
12. B. Turner, and D.D. Perkins Meiotic drive in Neurospora and other fungi Am. Nat. 137 1991 416 429
13. D.E. Neafsey, B.M. Barker, T.J. Sharpton, J.E. Stajich, D.J. Park, E. Whiston, C.Y. Hung, C. McMahan, J. White, and S. Sykes Population genomic sequencing of Coccidioides fungi reveals recent hybridization and transposon control Genome Res. 20 2010 938 946
14. C.E. Ellison, C. Hall, D. Kowbel, J. Welch, R.B. Brem, N.L. Glass, and J.W. Taylor Population genomics and local adaptation in wild isolates of a model microbial eukaryote Proc. Natl. Acad. Sci. USA 108 2011 2831 2836
15. T.L. Friesen, E.H. Stukenbrock, Z. Liu, S. Meinhardt, H. Ling, J.D. Faris, J.B. Rasmussen, P.S. Solomon, B.A. McDonald, and R.P. Oliver Emergence of a new disease as a result of interspecific virulence gene transfer Nat. Genet. 38 2006 953 956 (Pubitemid 44141666)
16. V.P. Miao, S.F. Covert, and H.D. VanEtten A fungal gene for antibiotic resistance on a dispensable ("B") chromosome Science 254 1991 1773 1776 (Pubitemid 21917522)
17. A.H. Buller Researches on Fungi Vol IV 1931 Longmans, Green and Co. London
18. T.Y. James, J. Stenlid, A. Olson, and H. Johannesson Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the basidiomycete fungus Heterobasidion parviporum Evolution 62 2008 2279 2296
19. I.R. Sanders, and D. Croll Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner Annu. Rev. Genet. 44 2010 271 292
20. C. Angelard, A. Colard, H. Niculita-Hirzel, D. Croll, and I.R. Sanders Segregation in a mycorrhizal fungus alters rice growth and symbiosis-specific gene transcription Curr. Biol. 20 2010 1216 1221
21. J.L. Jany, and T.E. Pawlowski Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota Am. Nat. 175 2010 424 435
22. M. Hijri, and I.R. Sanders Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei Nature 433 2005 160 163
23. O. Hallatschek, and D.R. Nelson Gene surfing in expanding populations Theor. Popul. Biol. 73 2008 158 170
24. M.C. Ruiz-Roldan, M. Kohli, M.I. Roncero, P. Philippsen, A. Di Pietro, and E.A. Espeso Nuclear dynamics during germination, conidiation, and hyphal fusion of Fusarium oxysporum Eukaryot. Cell 9 2010 1216 1224
25. R. Koenig, and F.L. Howard Nuclear division and septum formation in hyphal tips of Fusarium oxysporum Am. J. Bot. 49 1962 666
26. S.B. King, and L.J. Alexander Nuclear behavior, septation and hyphal growth of Alternaria solani Am. J. Bot. 56 1969 249 253
27. A.J. Clutterbuck Synchronous nuclear division and septation in Aspergillus nidulans J. Gen. Microbiol. 60 1970 133 135
28. A.S. Gladfelter Nuclear anarchy: asynchronous mitosis in multinucleated fungal hyphae Curr. Opin. Microbiol. 9 2006 547 552 (Pubitemid 44791982)
29. A.S. Gladfelter, A.K. Hungerbuehler, and P. Philippsen Asynchronous nuclear division cycles in multinucleated cells J. Cell Biol. 172 2006 347 362 (Pubitemid 43187932)
30. D.R. Nair, C.A. D'Ausilio, P. Occhipinti, M.E. Borsuk, and A.S. Gladfelter A conserved G regulatory circuit promotes asynchronous behavior of nuclei sharing a common cytoplasm Cell Cycle 9 2010 3771 3779
31. C. Lang, S. Grava, T. van den Hoorn, R. Trimble, P. Philippsen, and S.L. Jaspersen Mobility, microtubule nucleation and structure of microtubule- organizing centers in multinucleated hyphae of Ashbya gossypii Mol. Biol. Cell 21 2010 18 28
32. T. Kasuga, and N.L. Glass Dissecting colony development of Neurospora crassa using mRNA profiling and comparative genomics approaches Eukaryot. Cell 7 2008 1549 1564
33. A.M. Levin, R.P. de Vries, A. Conesa, C. de Bekker, M. Talon, H.H. Menke, N.N. van Peij, and H.A. Wosten Spatial differentiation in the vegetative mycelium of Aspergillus niger Eukaryot. Cell 6 2007 2311 2322
34. A. Vinck, C. de Bekker, A. Ossin, R.A. Ohm, R.P. de Vries, and H.A. Wosten Heterogenic expression of genes encoding secreted proteins at the periphery of Aspergillus niger colonies Environ. Microbiol. 13 2011 216 225
35. L. Araujo-Bazan, S. Dhingra, J. Chu, J. Fernandez-Martinez, A.M. Calvo, and E.A. Espeso Importin alpha is an essential nuclear import carrier adaptor required for proper sexual and asexual development and secondary metabolism in Aspergillus nidulans Fungal Genet. Biol. 46 2009 506 515
36. T.A. Schuurs, H.J. Dalstra, J.M. Scheer, and J.G. Wessels Positioning of nuclei in the secondary mycelium of Schizophyllum commune in relation to differential gene expression Fungal Genet. Biol. 23 1998 150 161 (Pubitemid 28403161)
37. N. Paquin, M. Menade, G. Poirier, D. Donato, E. Drouet, and P. Chartrand Local activation of yeast ASH1 mRNA translation through phosphorylation of Khd1 p by the casein kinase Yck1 p Mol. Cell 26 2007 795 809 (Pubitemid 46921005)
38. P.A. Takizawa, A. Sil, J.R. Swedlow, I. Herskowitz, and R.D. Vale Actin-dependent localization of an RNA encoding a cell-fate determinant in yeast Nature 389 1997 90 93 (Pubitemid 27387697)
39. K. Zarnack, and M. Feldbrugge Microtubule-dependent mRNA transport in fungi Eukaryot. Cell 9 2010 982 990
40. A.C. Leeder, J. Palma-Guerrero, and N.L. Glass The social network: deciphering fungal language Nat. Microbiol. 9 2011 440 451
41. A. Fleissner, A.C. Leeder, M.G. Roca, N.D. Read, and N.L. Glass Oscillatory recruitment of signaling proteins to cell tips promotes coordinated behavior during cell fusion Proc. Natl. Acad. Sci. USA 106 2009 19387 19392
42. M.G. Roca, H.C. Kuo, A. Lichius, M. Freitag, and N.D. Read Nuclear dynamics, mitosis, and the cytoskeleton during the early stages of colony initiation in Neurospora crassa Eukaryot. Cell 9 2010 1171 1183
43. S. Biella, M.L. Smith, J.R. Aist, P. Cortesi, and M.G. Milgroom Programmed cell death correlates with virus transmission in a filamentous fungus Proc. R. Soc. Lond. B Biol. Sci. 269 2002 2269 2276 (Pubitemid 35341913)
44. M.R. Goddard, and A. Burt Recurrent invasion and extinction of a selfish gene Proc. Natl. Acad. Sci. USA 96 1999 13880 13885
45. D.K. Aanen, A.J.M. Debets, N.L. Glass, and S.J. Saupe Biology and genetics of vegetative incompatibility in fungi K.A. Borkovich, D.J. Ebbole, Cellular and Molecular Biology of Filamentous Fungi 2009 ASM Press Washington, D.C. 274 288
46. C. Hall, J. Welch, D.J. Kowbel, and N.L. Glass Evolution and diversity of a fungal self/nonself recognition locus PLoS One 5 2010 e14055
47. N.L. Glass, and I. Kaneko Fatal attraction: Nonself recognition and heterokaryon incompatibility in filamentous fungi Eukaryot. Cell 2 2003 1 8 (Pubitemid 36770370)
48. C. He, A.G. Rusu, A.M. Poplawski, J.A. Irwin, and J.M. Manners Transfer of a supernumerary chromosome between vegetatively incompatible biotypes of the fungus Colletotrichum gloeosporioides Genetics 150 1998 1459 1466 (Pubitemid 28555549)
49. N.L. Glass, and G.A. Kuldau Mating type and vegetative incompatibility in filamentous ascomycetes Annu. Rev. Phytopathol 30 1992 201 224 (Pubitemid 24410624)
50. M.P. Backus The mechanics of conidial fertilization in Neurospora sitophila Bull. Torrey Bot. Club 1939 63 76
51. E.R. Sansome The use of heterokaryons to determine the origin of the ascogeneous nuclei in Neurospora crassa Genetica 24 1949 59 64
52. K. Nakamura, and T. Egashira Genetically mixed perithecia in Neurospora Nature 190 1961 1129 1130
53. F. Trail Fungal cannons: explosive spore discharge in the Ascomycota FEMS Microbiol. Lett. 276 2007 12 18 (Pubitemid 47620454)
54. J.K. Brown, and M.S. Hovmoller Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease Science 297 2002 537 541 (Pubitemid 34815327)
55. M. Roper, R.E. Pepper, M.P. Brenner, and A. Pringle Explosively launched spores of ascomycete fungi have drag-minimizing shapes Proc. Natl. Acad. Sci. USA 105 2008 20583 20588
56. M. Roper, A. Seminara, M.M. Bandi, A. Cobb, H.R. Dillard, and A. Pringle Dispersal of fungal spores on a cooperatively generated wind Proc. Natl. Acad. Sci. USA 107 2010 17474 17479
57. J.E. Strassmann, Y. Zhu, and D.C. Queller Altruism and social cheating in the social amoeba Dictyostelium discoideum Nature 408 2000 965 967 (Pubitemid 32101640)
58. J.W. Taylor, D.J. Jacobson, and M.C. Fisher The evolution of asexual fungi: Reproduction, speciation and classification Annu. Rev. Phytopathol 37 1999 197 246 (Pubitemid 29523934)
59. J.E. Galagan, and E.U. Selker RIP: the evolutionary cost of genome defense Trends Genet. 20 2004 417 423 (Pubitemid 39094570)
60. E. Turner, D.J. Jacobson, and J.W. Taylor Reinforced postmating reproductive isolation barriers in Neurospora, an Ascomycete microfungus J. Evol. Biol. 23 2010 1642 1656
61. M. Paoletti, K.W. Buck, and C.M. Brasier Selective acquisition of novel mating type and vegetative incompatibility genes via interspecies gene transfer in the globally invading eukaryote Ophiostoma novo-ulmi Mol. Ecol. 15 2006 249 262
62. S.K. Dutcher Internuclear transfer of genetic information in kar1-1/KAR1 heterokaryons in Saccharomyces cerevisiae Mol. Cell. Biol. 1 1981 245 253 (Pubitemid 11108200)
63. H.F. Tsai, J.S. Liu, C. Staben, M.J. Christensen, G.C. Latch, M.R. Siegel, and C.L. Schardl Evolutionary diversification of fungal endophytes of tall fescue grass by hybridization with Epichloe species Proc. Natl. Acad. Sci. USA 91 1994 2542 2546
64. A.E. Arnold, L.C. Mejia, D. Kyllo, E.I. Rojas, Z. Maynard, N. Robbins, and E.A. Herre Fungal endophytes limit pathogen damage in a tropical tree Proc. Natl. Acad. Sci. USA 100 2003 15649 15654 (Pubitemid 38021044)
65. S.M. Marek, J. Wu, N.L. Glass, D.G. Gilchrist, and R.M. Bostock Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa Fungal Genet. Biol. 40 2003 126 137 (Pubitemid 37152533)
66. K.C. Atwood, and F. Mukai Nuclear distribution in conidia of Neurospora heterokaryons Genetics 40 1955 438 443
67. A.N. Namboodiri, and R.J. Lowry Vegetative nuclear division in Neurospora Am. J. Bot. 54 1967 735 748
68. S.L. Ramos-Garcia, R.W. Roberson, M. Freitag, S. Bartnicki-Garcia, and R.R. Mourino-Perez Cytoplasmic bulk flow propels nuclei in mature hyphae of Neurospora crassa Eukaryot. Cell 8 2009 1880 1890
69. A. Kaufmann, and P. Philippsen Of bars and rings: Hof1-dependent cytokinesis in multiseptated hyphae of Ashbya gossypii Mol. Cell. Biol. 29 2009 771 783
70. A.J. Clutterbuck, and J.A. Roper A direct determination of nuclear distribution in heterokaryons of Aspergillus nidulans Genetic Res. 7 1966 185 194
71. R. Suelmann, N. Sievers, and R. Fischer Nuclear traffic in fungal hyphae: in vivo study of nuclear migration and positioning in Aspergillus nidulans Mol. Microbiol. 25 1997 757 769 (Pubitemid 27394572)
72. J.A.L. Wong, and H. Willetts Cytology of Sclerotinia sclerotiorum and related species J. Gen. Microbiol. 112 1979 29 34 (Pubitemid 9174629)
73. K.J. Czymmek, T.M. Bourett, Y. Shao, T.M. DeZwann, J.A. Sweigard, and R.J. Howard Live cell imaging of tubulin in the filamentous fungi Magnaporthe grisea treated with anti-microtubule and anti-microfilament agents Protoplasma 225 2005 23 32 (Pubitemid 40660362)
74. H. Yaegashi, and T.T. Hebert Perithecial development and nuclear behavior in Pyricularia Phytopathol 66 1976 122 126
75. R.W. Weber, G.E. Wakley, and D. Pitt Histochemical and ultrastructural characterization of vacuoles and spherosomes as components of the lytic system in hyphae of the fungus Botrytis cinerea Histochem. J. 31 1999 293 301 (Pubitemid 29332063)
76. G. Steinberg, M. Schliwa, C. Lehmler, M. Bolker, R. Kahmann, and J.R. McIntosh Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration J. Cell Sci. 111 1998 2235 2246 (Pubitemid 28403528)
77. P.J. Snider, and J.R. Raper Nuclear migration in the basidiomycete Schizophyllum commune Am. J. Bot. 45 1958 538 546
78. I.K. Ross Nuclear migration rates in Coprinus congregatus: a new record? Mycologia 68 1976 418 422
79. J. Stenlid, and A.D.M. Rayner Patterns of nuclear migration and heterokaryosis in pairings between sibling homokaryons of Heterobasidion annosum Mycol. Res. 95 1991 1275 1283
80. H.E. Ahrberg Untersuchungen zur Cytologie und zum Wachstum verschiedener Stamme von Fomes annosus (Fr.) Cooke Eur. J. Forest Pathol. 5 1975 287 303
81. M. Giovannetti, C. Sbrana, and C. Logi Microchambers and video-enhanced light microscopy for monitoring cellular events in living hyphae of arbuscular mycorrhizal fungi Plant Soil 226 2000 153 159 (Pubitemid 32100675)
82. J.E. Sass The cytological basis for homothallism and heterothallism in the Agaricaceae. Am. J. Bot. 16 1929 663 701
83. P.C. Hickey, D. Jacobson, N.D. Read, and N.L. Louise Glass Live-cell imaging of vegetative hyphal fusion in Neurospora crassa Fungal Genet. Biol. 37 2002 109 119
84. N.L. Glass, and K. Dementhon Non-self recognition and programmed cell death in filamentous fungi Curr. Opin. Microbiol. 9 2006 553 558 (Pubitemid 44791981)
85. L.S. Olive The structure and behavior of fungus nuclei Bot. Rev. 19 1953 439 486