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Molecular Mechanisms Regulating Cell Fusion and Heterokaryon Formation in Filamentous Fungi

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  • Authors: Asen Daskalov1, Jens Heller2, Stephanie Herzog3, André Fleißner4, N. Louise Glass5
  • Editors: Joseph Heitman6, Neil A. R. Gow7
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Plant and Microbial Biology, The University of California, Berkeley, CA 94720; 2: Department of Plant and Microbial Biology, The University of California, Berkeley, CA 94720; 3: Institut für Genetik, Technische Universität Braunschweig, 38106 Braunschweig, Germany; 4: Institut für Genetik, Technische Universität Braunschweig, 38106 Braunschweig, Germany; 5: Department of Plant and Microbial Biology, The University of California, Berkeley, CA 94720; 6: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; 7: School of Medical Sciences, University of Aberdeen, Fosterhill, Aberdeen, AB25 2ZD, United Kingdom
  • Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
  • Received 11 June 2016 Accepted 22 November 2016 Published 03 March 2017
  • N. Louise Glass, Lglass@berkeley.edu
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  • Abstract:

    For the majority of fungal species, the somatic body of an individual is a network of interconnected cells sharing a common cytoplasm and organelles. This syncytial organization contributes to an efficient distribution of resources, energy, and biochemical signals. Cell fusion is a fundamental process for fungal development, colony establishment, and habitat exploitation and can occur between hyphal cells of an individual colony or between colonies of genetically distinct individuals. One outcome of cell fusion is the establishment of a stable heterokaryon, culminating in benefits for each individual via shared resources or being of critical importance for the sexual or parasexual cycle of many fungal species. However, a second outcome of cell fusion between genetically distinct strains is formation of unstable heterokaryons and the induction of a programmed cell death reaction in the heterokaryotic cells. This reaction of nonself rejection, which is termed heterokaryon (or vegetative) incompatibility, is widespread in the fungal kingdom and acts as a defense mechanism against genome exploitation and mycoparasitism. Here, we review the currently identified molecular players involved in the process of somatic cell fusion and its regulation in filamentous fungi. Thereafter, we summarize the knowledge of the molecular determinants and mechanism of heterokaryon incompatibility and place this phenomenon in the broader context of biotropic interactions and immunity.

  • Citation: Daskalov A, Heller J, Herzog S, Fleißner A, Glass N. 2017. Molecular Mechanisms Regulating Cell Fusion and Heterokaryon Formation in Filamentous Fungi. Microbiol Spectrum 5(2):FUNK-0015-2016. doi:10.1128/microbiolspec.FUNK-0015-2016.

Key Concept Ranking

Fungal Proteins
0.51328826
Cell Wall Proteins
0.42924044
Major Histocompatibility Complex
0.41202784
0.51328826

References

1. Huppertz B, Bartz C, Kokozidou M. 2006. Trophoblast fusion: fusogenic proteins, syncytins and ADAMs, and other prerequisites for syncytial fusion. Micron 37:509–517. http://dx.doi.org/10.1016/j.micron.2005.12.011
2. Read ND, Goryachev AB, Lichius A. 2012. The mechanistic basis of self-fusion between conidial anastomosis tubes during fungal colony initiation. Fungal Biol Rev 26:1–11. http://dx.doi.org/10.1016/j.fbr.2012.02.003
3. Richardson BE, Nowak SJ, Baylies MK. 2008. Myoblast fusion in fly and vertebrates: new genes, new processes and new perspectives. Traffic 9:1050–1059. http://dx.doi.org/10.1111/j.1600-0854.2008.00756.x
4. Vignery A. 2008. Macrophage fusion: molecular mechanisms. Methods Mol Biol 475:149–161. http://dx.doi.org/10.1007/978-1-59745-250-2_9 [PubMed]
5. Cadavid LF, Powell AE, Nicotra ML, Moreno M, Buss LW. 2004. An invertebrate histocompatibility complex. Genetics 167:357–365. http://dx.doi.org/10.1534/genetics.167.1.357
6. Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. 2013. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. MBio 4:e00374-13. doi:10.1128/mBio.00374-13. [PubMed]
7. Gibbs KA, Urbanowski ML, Greenberg EP. 2008. Genetic determinants of self identity and social recognition in bacteria. Science 321:256–259. http://dx.doi.org/10.1126/science.1160033 [PubMed]
8. Strassmann JE, Zhu Y, Queller DC. 2000. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature 408:965–967. http://dx.doi.org/10.1038/35050087
9. Li SI, Purugganan MD. 2011. The cooperative amoeba: Dictyostelium as a model for social evolution. Trends Genet 27:48–54. http://dx.doi.org/10.1016/j.tig.2010.11.003 [PubMed]
10. Sanabria N, Goring D, Nürnberger T, Dubery I. 2008. Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity. New Phytol 178:503–514. http://dx.doi.org/10.1111/j.1469-8137.2008.02403.x [CrossRef]
11. Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11:539–548. http://dx.doi.org/10.1038/nrg2812
12. Gabriela Roca M, Read ND, Wheals AE. 2005. Conidial anastomosis tubes in filamentous fungi. FEMS Microbiol Lett 249:191–198. http://dx.doi.org/10.1016/j.femsle.2005.06.048 [PubMed]
13. Hickey PC, Jacobson D, Read ND, Glass NL. 2002. Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet Biol 37:109–119. http://dx.doi.org/10.1016/S1087-1845(02)00035-X [PubMed]
14. Pieuchot L, Lai J, Loh RA, Leong FY, Chiam KH, Stajich J, Jedd G. 2015. Cellular subcompartments through cytoplasmic streaming. Dev Cell 34:410–420. http://dx.doi.org/10.1016/j.devcel.2015.07.017
15. Simonin A, Palma-Guerrero J, Fricker M, Glass NL. 2012. Physiological significance of network organization in fungi. Eukaryot Cell 11:1345–1352. http://dx.doi.org/10.1128/EC.00213-12
16. Roper M, Simonin A, Hickey PC, Leeder A, Glass NL. 2013. Nuclear dynamics in a fungal chimera. Proc Natl Acad Sci USA 110:12875–12880. http://dx.doi.org/10.1073/pnas.1220842110 [PubMed]
17. Heaton L, Obara B, Grau V, Jones N, Nakagaki T, Boddy L, Fricker M. 2012. Analysis of fungal networks. Fungal Biol Rev 26:12–29. http://dx.doi.org/10.1016/j.fbr.2012.02.001
18. Charlton ND, Shoji JY, Ghimire SR, Nakashima J, Craven KD. 2012. Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte Epichloë festucae and the host plant. Eukaryot Cell 11:1463–1471. http://dx.doi.org/10.1128/EC.00191-12
19. Craven KD, Vélëz H, Cho Y, Lawrence CB, Mitchell TK. 2008. Anastomosis is required for virulence of the fungal necrotroph Alternaria brassicicola. Eukaryot Cell 7:675–683. http://dx.doi.org/10.1128/EC.00423-07 [PubMed][CrossRef]
20. Gruber S, Zeilinger S. 2014. The transcription factor Ste12 mediates the regulatory role of the Tmk1 MAP kinase in mycoparasitism and vegetative hyphal fusion in the filamentous fungus Trichoderma atroviride. PLoS One 9:e111636. http://dx.doi.org/10.1371/journal.pone.0111636
21. Pontecorvo G. 1956. The parasexual cycle in fungi. Annu Rev Microbiol 10:393–400. http://dx.doi.org/10.1146/annurev.mi.10.100156.002141 [PubMed]
22. Schoustra SE, Debets AJ, Slakhorst M, Hoekstra RF. 2007. Mitotic recombination accelerates adaptation in the fungus Aspergillus nidulans. PLoS Genet 3:e68. http://dx.doi.org/10.1371/journal.pgen.0030068
23. Debets AJM, Griffiths AJF. 1998. Polymorphism of het-genes prevents resource plundering in Neurospora crassa. Mycol Res 102:1343–1349. http://dx.doi.org/10.1017/S095375629800639X
24. Debets AJ, Dalstra HJ, Slakhorst M, Koopmanschap B, Hoekstra RF, Saupe SJ. 2012. High natural prevalence of a fungal prion. Proc Natl Acad Sci USA 109:10432–10437. http://dx.doi.org/10.1073/pnas.1205333109 [PubMed]
25. Son M, Yu J, Kim KH. 2015. Five questions about mycoviruses. PLoS Pathog 11:e1005172. http://dx.doi.org/10.1371/journal.ppat.1005172 [PubMed]
26. Pearson MN, Beever RE, Boine B, Arthur K. 2009. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol Plant Pathol 10:115–128. http://dx.doi.org/10.1111/j.1364-3703.2008.00503.x [CrossRef]
27. Saupe SJ. 2000. Molecular genetics of heterokaryon incompatibility in filamentous ascomycetes. Microbiol Mol Biol Rev 64:489–502. http://dx.doi.org/10.1128/MMBR.64.3.489-502.2000
28. Glass NL, Dementhon K. 2006. Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9:553–558. http://dx.doi.org/10.1016/j.mib.2006.09.001 [PubMed]
29. Bastiaans E, Debets AJ, Aanen DK. 2016. Experimental evolution reveals that high relatedness protects multicellular cooperation from cheaters. Nat Commun 7:11435. http://dx.doi.org/10.1038/ncomms11435
30. van Diepeningen AD, Debets AJ, Hoekstra RF. 1997. Heterokaryon incompatibility blocks virus transfer among natural isolates of black Aspergilli. Curr Genet 32:209–217. http://dx.doi.org/10.1007/s002940050268
31. Zhang DX, Spiering MJ, Dawe AL, Nuss DL. 2014. Vegetative incompatibility loci with dedicated roles in allorecognition restrict mycovirus transmission in chestnut blight fungus. Genetics 197:701–714. http://dx.doi.org/10.1534/genetics.114.164574
32. Debets F, Yang X, Griffiths AJF. 1994. Vegetative incompatibility in Neurospora: its effect on horizontal transfer of mitochondrial plasmids and senescence in natural populations. Curr Genet 26:113–119. http://dx.doi.org/10.1007/BF00313797 [PubMed]
33. Bastiaans E, Debets AJ, Aanen DK. 2015. Experimental demonstration of the benefits of somatic fusion and the consequences for allorecognition. Evolution 69:1091–1099. http://dx.doi.org/10.1111/evo.12626
34. Glass NL, Grotelueschen J, Metzenberg RL. 1990. Neurospora crassa A mating-type region. Proc Natl Acad Sci USA 87:4912–4916. http://dx.doi.org/10.1073/pnas.87.13.4912 [PubMed]
35. Glass NL, Kuldau GA. 1992. Mating type and vegetative incompatibility in filamentous ascomycetes. Annu Rev Phytopathol 30:201–224. http://dx.doi.org/10.1146/annurev.py.30.090192.001221 [PubMed]
36. Roca MG, Arlt J, Jeffree CE, Read ND. 2005. Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryot Cell 4:911–919. http://dx.doi.org/10.1128/EC.4.5.911-919.2005 [PubMed]
37. Glass NL, Rasmussen C, Roca MG, Read ND. 2004. Hyphal homing, fusion and mycelial interconnectedness. Trends Microbiol 12:135–141. http://dx.doi.org/10.1016/j.tim.2004.01.007 [PubMed]
38. Herzog S, Schumann MR, Fleißner A. 2015. Cell fusion in Neurospora crassa. Curr Opin Microbiol 28:53–59. http://dx.doi.org/10.1016/j.mib.2015.08.002 [PubMed][CrossRef]
39. Leeder AC, Jonkers W, Li J, Glass NL. 2013. Early colony establishment in Neurospora crassa requires a MAP kinase regulatory network. Genetics 195:883–898. http://dx.doi.org/10.1534/genetics.113.156984
40. Ishikawa FH, Souza EA, Shoji JY, 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. http://dx.doi.org/10.1371/journal.pone.0031175
41. Lichius A, Lord KM. 2014. Chemoattractive mechanisms in filamentous fungi. Open Mycol J 8:28–57.
42. Weichert M, Fleissner A. 2015. Anastomosis and heterokaryon formation, p 3–21. In van den Berg M, Maruthachalam K (ed), Genetic Transformation Systems in Fungi, vol 2. Springer International Publishing, Cham, Switzerland.
43. Maerz S, Ziv C, Vogt N, Helmstaedt K, Cohen N, Gorovits R, Yarden O, Seiler S. 2008. The nuclear Dbf2-related kinase COT1 and the mitogen-activated protein kinases MAK1 and MAK2 genetically interact to regulate filamentous growth, hyphal fusion and sexual development in Neurospora crassa. Genetics 179:1313–1325. http://dx.doi.org/10.1534/genetics.108.089425
44. Pandey A, Roca MG, Read ND, Glass NL. 2004. Role of a mitogen-activated protein kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryot Cell 3:348–358. http://dx.doi.org/10.1128/EC.3.2.348-358.2004 [PubMed]
45. 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. http://dx.doi.org/10.1073/pnas.0907039106
46. Read ND, Lichius A, Shoji JY, Goryachev AB. 2009. Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12:608–615. http://dx.doi.org/10.1016/j.mib.2009.09.008 [PubMed]
47. Dettmann A, Heilig Y, Valerius O, Ludwig S, Seiler S. 2014. Fungal communication requires the MAK-2 pathway elements STE-20 and RAS-2, the NRC-1 adapter STE-50 and the MAP kinase scaffold HAM-5. PLoS Genet 10:e1004762. http://dx.doi.org/10.1371/journal.pgen.1004762
48. Jonkers W, Leeder AC, Ansong C, Wang Y, Yang F, Starr TL, Camp DG, Smith RD, Glass NL. 2014. HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa. PLoS Genet 10:e1004783. http://dx.doi.org/10.1371/journal.pgen.1004783
49. Fleissner A, Sarkar S, Jacobson DJ, Roca MG, Read ND, Glass NL. 2005. The so locus is required for vegetative cell fusion and postfertilization events in Neurospora crassa. Eukaryot Cell 4:920–930. http://dx.doi.org/10.1128/EC.4.5.920-930.2005 [PubMed]
50. Goryachev AB, Lichius A, Wright GD, Read ND. 2012. Excitable behavior can explain the “ping-pong” mode of communication between cells using the same chemoattractant. BioEssays 34:259–266. http://dx.doi.org/10.1002/bies.201100135 [PubMed]
51. Teichert I, Steffens EK, Schnaß N, Fränzel B, Krisp C, Wolters DA, Kück U. 2014. PRO40 is a scaffold protein of the cell wall integrity pathway, linking the MAP kinase module to the upstream activator protein kinase C. PLoS Genet 10:e1004582. http://dx.doi.org/10.1371/journal.pgen.1004582
52. Becker Y, Eaton CJ, Brasell E, May KJ, Becker M, Hassing B, Cartwright GM, Reinhold L, Scott B. 2015. The fungal cell-wall integrity MAPK cascade is crucial for hyphal network formation and maintenance of restrictive growth of Epichloë festucae in symbiosis with Lolium perenne. Mol Plant Microbe Interact 28:69–85. http://dx.doi.org/10.1094/MPMI-06-14-0183-R
53. Hou Z, Xue C, Peng Y, Katan T, Kistler HC, Xu JR. 2002. A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15:1119–1127. http://dx.doi.org/10.1094/MPMI.2002.15.11.1119
54. Dettmann A, Heilig Y, Ludwig S, Schmitt K, Illgen J, Fleißner A, Valerius O, Seiler S. 2013. HAM-2 and HAM-3 are central for the assembly of the Neurospora STRIPAK complex at the nuclear envelope and regulate nuclear accumulation of the MAP kinase MAK-1 in a MAK-2-dependent manner. Mol Microbiol 90:796–812. http://dx.doi.org/10.1111/mmi.12399
55. Bloemendal S, Bernhards Y, Bartho K, Dettmann A, Voigt O, Teichert I, Seiler S, Wolters DA, Pöggeler S, Kück U. 2012. A homologue of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol 84:310–323. http://dx.doi.org/10.1111/j.1365-2958.2012.08024.x
56. Nordzieke S, Zobel T, Fränzel B, Wolters DA, Kück U, Teichert I. 2015. A fungal sarcolemmal membrane-associated protein (SLMAP) homolog plays a fundamental role in development and localizes to the nuclear envelope, endoplasmic reticulum, and mitochondria. Eukaryot Cell 14:345–358. http://dx.doi.org/10.1128/EC.00241-14
57. Simonin AR, Rasmussen CG, Yang M, Glass NL. 2010. Genes encoding a striatin-like protein (ham-3) and a forkhead associated protein (ham-4) are required for hyphal fusion in Neurospora crassa. Fungal Genet Biol 47:855–868. http://dx.doi.org/10.1016/j.fgb.2010.06.010
58. Wang CL, Shim WB, Shaw BD. 2015. The Colletotrichum graminicola striatin ortholog Str1 is necessary for anastomosis and is a virulence factor. Mol Plant Pathol 10.111/mpp.12339. [PubMed]
59. Pöggeler S, Kück U. 2004. A WD40 repeat protein regulates fungal cell differentiation and can be replaced functionally by the mammalian homologue striatin. Eukaryot Cell 3:232–240. http://dx.doi.org/10.1128/EC.3.1.232-240.2004
60. Dirschnabel DE, Nowrousian M, Cano-Domínguez N, Aguirre J, Teichert I, Kück U. 2014. New insights into the roles of NADPH oxidases in sexual development and ascospore germination in Sordaria macrospora. Genetics 196:729–744. http://dx.doi.org/10.1534/genetics.113.159368
61. Takemoto D, Kamakura S, Saikia S, Becker Y, Wrenn R, Tanaka A, Sumimoto H, Scott B. 2011. Polarity proteins Bem1 and Cdc24 are components of the filamentous fungal NADPH oxidase complex. Proc Natl Acad Sci USA 108:2861–2866. http://dx.doi.org/10.1073/pnas.1017309108
62. Roca MG, Weichert M, Siegmund U, Tudzynski P, Fleissner A. 2012. Germling fusion via conidial anastomosis tubes in the grey mould Botrytis cinerea requires NADPH oxidase activity. Fungal Biol 116:379–387. http://dx.doi.org/10.1016/j.funbio.2011.12.007 [PubMed]
63. Sbrana C, Nuti MP, Giovannetti M. 2007. Self-anastomosing ability and vegetative incompatibility of Tuber borchii isolates. Mycorrhiza 17:667–675. http://dx.doi.org/10.1007/s00572-007-0144-3 [PubMed]
64. 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. http://dx.doi.org/10.1128/AEM.69.1.616-624.2003
65. Heller J, Zhao J, Rosenfield G, Kowbel DJ, Gladieux P, Glass NL. 2016. Characterization of greenbeard genes involved in long-distance kind discrimination in a microbial eukaryote. PLoS Biol 14:e1002431. http://dx.doi.org/10.1371/journal.pbio.1002431 [PubMed]
66. Cayley DM. 1923. The phenomenon of mutual aversion between mono-spore mycelia of the same fungus (Diaporthe perniciosa, Marchal). With a discussion of sex-heterothallism in fungi. J Genet 13:353–370. http://dx.doi.org/10.1007/BF02983069
67. Todd NK, Rayner ADM. Fungal individualism. Sci Progr (1933-). 66:331–354. http://www.jstor.org/stable/43420507.
68. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, Porcel BM, Couloux A, Aury JM, Ségurens B, Poulain J, Anthouard V, Grossetete S, Khalili H, Coppin E, Déquard-Chablat M, Picard M, Contamine V, Arnaise S, Bourdais A, Berteaux-Lecellier V, Gautheret D, de Vries RP, Battaglia E, Coutinho PM, Danchin EG, Henrissat B, Khoury RE, Sainsard-Chanet A, Boivin A, Pinan-Lucarré B, Sellem CH, Debuchy R, Wincker P, Weissenbach J, Silar P. 2008. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9:R77. http://dx.doi.org/10.1186/gb-2008-9-5-r77
69. Jacobson DJ, Beurkens K, Klomparens KL. 1998. Microscopic and ultrastructural examination of vegetative incompatibility in partial diploids heterozygous at het loci in Neurospora crassa. Fungal Genet Biol 23:45–56. http://dx.doi.org/10.1006/fgbi.1997.1020
70. Pinan-Lucarré B, Paoletti M, Clavé C. 2007. Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17:101–111. http://dx.doi.org/10.1016/j.semcancer.2006.11.009 [PubMed]
71. Jedd G, Chua NH. 2000. A new self-assembled peroxisomal vesicle required for efficient resealing of the plasma membrane. Nat Cell Biol 2:226–231. http://dx.doi.org/10.1038/35008652 [PubMed]
72. Jedd G, Pieuchot L. 2012. Multiple modes for gatekeeping at fungal cell-to-cell channels. Mol Microbiol 86:1291–1294. http://dx.doi.org/10.1111/mmi.12074 [PubMed]
73. Maruyama J, Juvvadi PR, Ishi K, Kitamoto K. 2005. Three-dimensional image analysis of plugging at the septal pore by Woronin body during hypotonic shock inducing hyphal tip bursting in the filamentous fungus Aspergillus oryzae. Biochem Biophys Res Commun 331:1081–1088. http://dx.doi.org/10.1016/j.bbrc.2005.03.233
74. Lai J, Koh CH, Tjota M, Pieuchot L, Raman V, Chandrababu KB, Yang D, Wong L, Jedd G. 2012. Intrinsically disordered proteins aggregate at fungal cell-to-cell channels and regulate intercellular connectivity. Proc Natl Acad Sci USA 109:15781–15786. http://dx.doi.org/10.1073/pnas.1207467109
75. Fleissner A, Glass NL. 2007. SO, a protein involved in hyphal fusion in Neurospora crassa, localizes to septal plugs. Eukaryot Cell 6:84–94. http://dx.doi.org/10.1128/EC.00268-06 [PubMed]
76. 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. http://dx.doi.org/10.1099/mic.0.032284-0
77. 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. http://dx.doi.org/10.1016/S1087-1845(03)00086-0
78. Pinan-Lucarré B, Balguerie A, Clavé C. 2005. Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell 4:1765–1774. http://dx.doi.org/10.1128/EC.4.11.1765-1774.2005 [PubMed]
79. 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. http://dx.doi.org/10.1046/j.1365-2958.2003.03208.x [PubMed][CrossRef]
80. Liu Y, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP. 2005. Autophagy regulates programmed cell death during the plant innate immune response. Cell 121:567–577. http://dx.doi.org/10.1016/j.cell.2005.03.007
81. Mylyk OM. 1975. Heterokaryon incompatibility genes in Neurospora crassa detected using duplication-producing chromosome rearrangements. Genetics 80:107–124. [PubMed]
82. Labarére J, Bègueret J, Bernet J. 1974. Incompatibility in Podospora anserina: comparative properties of the antagonistic cytoplasmic factors of a nonallelic system. J Bacteriol 120:854–860. [PubMed]
83. Zhao J, Gladieux P, Hutchison E, Bueche J, Hall C, Perraudeau F, Glass NL. 2015. Identification of allorecognition loci in Neurospora crassa by genomics and evolutionary approaches. Mol Biol Evol 32:2417–2432. http://dx.doi.org/10.1093/molbev/msv125 [PubMed]
84. Hall C, Welch J, Kowbel DJ, Glass NL. 2010. Evolution and diversity of a fungal self/nonself recognition locus. PLoS One 5:e14055. http://dx.doi.org/10.1371/journal.pone.0014055 [PubMed]
85. Richman A. 2000. Evolution of balanced genetic polymorphism. Mol Ecol 9:1953–1963. http://dx.doi.org/10.1046/j.1365-294X.2000.01125.x
86. Charlesworth D. 2006. Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:e64. http://dx.doi.org/10.1371/journal.pgen.0020064 [PubMed]
87. Roux C, Pauwels M, Ruggiero MV, Charlesworth D, Castric V, Vekemans X. 2013. Recent and ancient signature of balancing selection around the S-locus in Arabidopsis halleri and A. lyrata. Mol Biol Evol 30:435–447. http://dx.doi.org/10.1093/molbev/mss246 [PubMed]
88. Apanius V, Penn D, Slev PR, Ruff LR, Potts WK. 1997. The nature of selection on the major histocompatibility complex. Crit Rev Immunol 17:179–224. http://dx.doi.org/10.1615/CritRevImmunol.v17.i2.40 [PubMed]
89. Perkins DD. 1992. Neurospora: the organism behind the molecular revolution. Genetics 130:687–701. [PubMed]
90. Beadle GW, Tatum EL. 1941. Genetic control of biochemical reactions in Neurospora. Proc Natl Acad Sci USA 27:499–506. http://dx.doi.org/10.1073/pnas.27.11.499 [PubMed]
91. Beadle GW, Coonradt VL. 1944. Heterocaryosis in Neurospora crassa. Genetics 29:291–308. [PubMed]
92. Kown KJ, Raper KB. 1967. Heterokaryon formation and genetic analyses of color mutants in Aspergillus heterothallicus. Am J Bot 54:49–60. http://dx.doi.org/10.2307/2440886
93. Shiu PK, Glass NL. 1999. Molecular characterization of tol, a mediator of mating-type-associated vegetative incompatibility in Neurospora crassa. Genetics 151:545–555. [PubMed]
94. Metzenberg RL, Glass NL. 1990. Mating type and mating strategies in Neurospora. BioEssays 12:53–59. http://dx.doi.org/10.1002/bies.950120202 [PubMed]
95. Glass NL, Vollmer SJ, Staben C, Grotelueschen J, Metzenberg RL, Yanofsky C. 1988. DNAs of the two mating-type alleles of Neurospora crassa are highly dissimilar. Science 241:570–573. http://dx.doi.org/10.1126/science.2840740 [PubMed]
96. Griffiths AJ, Delange AM. 1978. Mutations of the a mating-type gene in Neurospora crassa. Genetics 88:239–254. [PubMed]
97. Philley ML, Staben C. 1994. Functional analyses of the Neurospora crassa mt a-1 mating type polypeptide. Genetics 137:715–722. [PubMed]
98. Newmeyer D. 1970. A suppressor of the heterokaryon-incompatibility associated with mating type in Neurospora crassa. Can J Genet Cytol 12:914–926. http://dx.doi.org/10.1139/g70-115 [PubMed]
99. Jacobson DJ. 1992. Control of mating type heterokaryon incompatibility by the tol gene in Neurospora crassa and N. tetrasperma. Genome 35:347–353. http://dx.doi.org/10.1139/g92-053 [PubMed]
100. Metzenberg RL, Ahlgren SK. 1973. Behaviour of Neurospora tetrasperma mating-type genes introgressed into N. crassa. Can J Genet Cytol 15:571–576. http://dx.doi.org/10.1139/g73-068 [PubMed]
101. Garnjobst L, Wilson JF. 1956. Heterocaryosis and protoplasmic incompatibility in Neurospora crassa. Proc Natl Acad Sci USA 42:613–618. http://dx.doi.org/10.1073/pnas.42.9.613 [PubMed]
102. Perkins DD. 1975. The use of duplication-generating rearrangements for studying heterokaryon incompatibility genes in Neurospora. Genetics 80:87–105. [PubMed]
103. Kaneko I, Dementhon K, Xiang Q, Glass NL. 2006. Nonallelic interactions between het-c and a polymorphic locus, pin-c, are essential for nonself recognition and programmed cell death in Neurospora crassa. Genetics 172:1545–1555. http://dx.doi.org/10.1534/genetics.105.051490
104. Smith ML, Micali OC, Hubbard SP, Mir-Rashed N, Jacobson DJ, Glass NL. 2000. Vegetative incompatibility in the het-6 region of Neurospora crassa is mediated by two linked genes. Genetics 155:1095–1104. [PubMed]
105. Sarkar S, Iyer G, Wu J, Glass NL. 2002. Nonself recognition is mediated by HET-C heterocomplex formation during vegetative incompatibility. EMBO J 21:4841–4850. http://dx.doi.org/10.1093/emboj/cdf479
106. Lafontaine DL, Smith ML. 2012. Diverse interactions mediate asymmetric incompatibility by the het-6 supergene complex in Neurospora crassa. Fungal Genet Biol 49:65–73. http://dx.doi.org/10.1016/j.fgb.2011.11.001
107. Mir-Rashed N, Jacobson DJ, Dehghany MR, Micali OC, Smith ML. 2000. Molecular and functional analyses of incompatibility genes at het-6 in a population of Neurospora crassa. Fungal Genet Biol 30:197–205. http://dx.doi.org/10.1006/fgbi.2000.1218
108. Saupe SJ, Kuldau GA, Smith ML, Glass NL. 1996. The product of the het-C heterokaryon incompatibility gene of Neurospora crassa has characteristics of a glycine-rich cell wall protein. Genetics 143:1589–1600. [PubMed]
109. Saupe SJ, Glass NL. 1997. Allelic specificity at the het-c heterokaryon incompatibility locus of Neurospora crassa is determined by a highly variable domain. Genetics 146:1299–1309. [PubMed]
110. Xiang Q, Glass NL. 2002. Identification of vib-1, a locus involved in vegetative incompatibility mediated by het-c in Neurospora crassa. Genetics 162:89–101. [PubMed]
111. Xiang Q, Glass NL. 2004. The control of mating type heterokaryon incompatibility by vib-1, a locus involved in het-c heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 41:1063–1076. http://dx.doi.org/10.1016/j.fgb.2004.07.006
112. Dementhon K, Iyer G, Glass NL. 2006. VIB-1 is required for expression of genes necessary for programmed cell death in Neurospora crassa. Eukaryot Cell 5:2161–2173. http://dx.doi.org/10.1128/EC.00253-06 [PubMed][CrossRef]
113. Espagne E, Balhadère P, Penin ML, Barreau C, Turcq B. 2002. HET-E and HET-D belong to a new subfamily of WD40 proteins involved in vegetative incompatibility specificity in the fungus Podospora anserina. Genetics 161:71–81. [PubMed]
114. Chevanne D, Bastiaans E, Debets A, Saupe SJ, Clavé C, Paoletti M. 2009. Identification of the het-r vegetative incompatibility gene of Podospora anserina as a member of the fast evolving HNWD gene family. Curr Genet 55:93–102. http://dx.doi.org/10.1007/s00294-008-0227-5
115. Paoletti M, Clavé C. 2007. The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryot Cell 6:2001–2008. http://dx.doi.org/10.1128/EC.00129-07 [PubMed]
116. Saupe S, Turcq B, Bégueret J. 1995. A gene responsible for vegetative incompatibility in the fungus Podospora anserina encodes a protein with a GTP-binding motif and G beta homologous domain. Gene 162:135–139. http://dx.doi.org/10.1016/0378-1119(95)00272-8
117. Koonin EV, Aravind L. 2000. The NACHT family: - a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem Sci 25:223–224. http://dx.doi.org/10.1016/S0968-0004(00)01577-2
118. Yuan S, Akey CW. 2013. Apoptosome structure, assembly, and procaspase activation. Structure 21:501–515. http://dx.doi.org/10.1016/j.str.2013.02.024 [PubMed]
119. Stirnimann CU, Petsalaki E, Russell RB, Müller CW. 2010. WD40 proteins propel cellular networks. Trends Biochem Sci 35:565–574. http://dx.doi.org/10.1016/j.tibs.2010.04.003 [PubMed]
120. Zhou M, Li Y, Hu Q, Bai XC, Huang W, Yan C, Scheres SH, Shi Y. 2015. Atomic structure of the apoptosome: mechanism of cytochrome c- and dATP-mediated activation of Apaf-1. Genes Dev 29:2349–2361. http://dx.doi.org/10.1101/gad.272278.115 [PubMed]
121. Espagne E, Balhadère P, Bégueret J, Turcq B. 1997. Reactivity in vegetative incompatibility of the HET-E protein of the fungus Podospora anserina is dependent on GTP-binding activity and a WD40 repeated domain. Mol Gen Genet 256:620–627. http://dx.doi.org/10.1007/s004380050610
122. Saupe S, Descamps C, Turcq B, Bégueret J. 1994. Inactivation of the Podospora anserina vegetative incompatibility locus het-c, whose product resembles a glycolipid transfer protein, drastically impairs ascospore production. Proc Natl Acad Sci USA 91:5927–5931. http://dx.doi.org/10.1073/pnas.91.13.5927 [PubMed]
123. Kenoth R, Kamlekar RK, Simanshu DK, Gao Y, Malinina L, Prendergast FG, Molotkovsky JG, Patel DJ, Venyaminov SY, Brown RE. 2011. Conformational folding and stability of the HET-C2 glycolipid transfer protein fold: does a molten globule-like state regulate activity? Biochemistry 50:5163–5171. http://dx.doi.org/10.1021/bi200382c
124. Saupe S, Turcq B, Bégueret J. 1995. Sequence diversity and unusual variability at the het-c locus involved in vegetative incompatibility in the fungus Podospora anserina. Curr Genet 27:466–471. http://dx.doi.org/10.1007/BF00311217 [PubMed]
125. Bastiaans E, Debets AJ, Aanen DK, van Diepeningen AD, Saupe SJ, Paoletti M. 2014. Natural variation of heterokaryon incompatibility gene het-c in Podospora anserina reveals diversifying selection. Mol Biol Evol 31:962–974. http://dx.doi.org/10.1093/molbev/msu047
126. Chevanne D, Saupe SJ, Clavé C, Paoletti M. 2010. WD-repeat instability and diversification of the Podospora anserina hnwd non-self recognition gene family. BMC Evol Biol 10:134. http://dx.doi.org/10.1186/1471-2148-10-134 [PubMed]
127. Paoletti M, Saupe SJ, Clavé C. 2007. Genesis of a fungal non-self recognition repertoire. PLoS One 2:e283. http://dx.doi.org/10.1371/journal.pone.0000283 [PubMed]
128. Daskalov A, Habenstein B, Martinez D, Debets AJ, Sabaté R, Loquet A, Saupe SJ. 2015. Signal transduction by a fungal NOD-like receptor based on propagation of a prion amyloid fold. PLoS Biol 13:e1002059. http://dx.doi.org/10.1371/journal.pbio.1002059 [PubMed]
129. Saupe SJ. 2011. The [Het-s] prion of Podospora anserina and its role in heterokaryon incompatibility. Semin Cell Dev Biol 22:460–468. http://dx.doi.org/10.1016/j.semcdb.2011.02.019 [PubMed]
130. Maddelein ML, Dos Reis S, Duvezin-Caubet S, Coulary-Salin B, Saupe SJ. 2002. Amyloid aggregates of the HET-s prion protein are infectious. Proc Natl Acad Sci USA 99:7402–7407. http://dx.doi.org/10.1073/pnas.072199199 [PubMed]
131. Beisson-Schecroun J. 1962. Cellular incompatibility and nucleo-cytoplasmic interactions in the “barrage” phenomena in Podospora anserina. Ann Genet 4:4–50. [PubMed]
132. Wickner RB. 1997. A new prion controls fungal cell fusion incompatibility. Proc Natl Acad Sci USA 94:10012–10014. http://dx.doi.org/10.1073/pnas.94.19.10012 [PubMed]
133. Seuring C, Greenwald J, Wasmer C, Wepf R, Saupe SJ, Meier BH, Riek R. 2012. The mechanism of toxicity in HET-S/HET-s prion incompatibility. PLoS Biol 10:e1001451. http://dx.doi.org/10.1371/journal.pbio.1001451 [PubMed][CrossRef]
134. Mathur V, Seuring C, Riek R, Saupe SJ, Liebman SW. 2012. Localization of HET-S to the cell periphery, not to [Het-s] aggregates, is associated with [Het-s]-HET-S toxicity. Mol Cell Biol 32:139–153. http://dx.doi.org/10.1128/MCB.06125-11 [PubMed]
135. Cortesi P, McCulloch CE, Song H, Lin H, Milgroom MG. 2001. Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159:107–118. [PubMed]
136. Cortesi P, Milgroom MG. 1998. Genetics of vegetative incompatibility in Cryphonectria parasitica. Appl Environ Microbiol 64:2988–2994. [PubMed]
137. Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom MG, Nuss DL. 2012. Molecular characterization of vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus Cryphonectria parasitica. Genetics 190:113–127. http://dx.doi.org/10.1534/genetics.111.133983
138. Zhang DX, Nuss DL. 2016. Engineering super mycovirus donor strains of chestnut blight fungus by systematic disruption of multilocus vic genes. Proc Natl Acad Sci USA 113:2062–2067. http://dx.doi.org/10.1073/pnas.1522219113 [PubMed]
139. Paoletti M, Saupe SJ. 2009. Fungal incompatibility: evolutionary origin in pathogen defense? BioEssays 31:1201–1210. http://dx.doi.org/10.1002/bies.200900085
140. Rinkevich B. 2004. Allorecognition and xenorecognition in reef corals: a decade of interactions. Hydrobiologia 530-531:443–450. http://dx.doi.org/10.1007/s10750-004-2686-0
141. Proell M, Riedl SJ, Fritz JH, Rojas AM, Schwarzenbacher R. 2008. The Nod-like receptor (NLR) family: a tale of similarities and differences. PLoS One 3:e2119. http://dx.doi.org/10.1371/journal.pone.0002119 [PubMed]
142. Daskalov A, Paoletti M, Ness F, Saupe SJ. 2012. Genomic clustering and homology between HET-S and the NWD2 STAND protein in various fungal genomes. PLoS One 7:e34854. http://dx.doi.org/10.1371/journal.pone.0034854
143. Dyrka W, Lamacchia M, Durrens P, Kobe B, Daskalov A, Paoletti M, Sherman DJ, Saupe SJ. 2014. Diversity and variability of NOD-like receptors in fungi. Genome Biol Evol 6:3137–3158. http://dx.doi.org/10.1093/gbe/evu251 [PubMed]
144. Daskalov A, Habenstein B, Sabaté R, Berbon M, Martinez D, Chaignepain S, Coulary-Salin B, Hofmann K, Loquet A, Saupe SJ. 2016. Identification of a novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is related to necroptosis. Proc Natl Acad Sci USA 113:2720–2725. http://dx.doi.org/10.1073/pnas.1522361113
145. Chen D, Yu J, Zhang L. 2016. Necroptosis: an alternative cell death program defending against cancer. Biochim Biophys Acta 1865:228–236. [PubMed]
146. Glass NL, Kaneko I. 2003. Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2:1–8. http://dx.doi.org/10.1128/EC.2.1.1-8.2003
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/content/journal/microbiolspec/10.1128/microbiolspec.FUNK-0015-2016
2017-03-03
2017-09-21

Abstract:

For the majority of fungal species, the somatic body of an individual is a network of interconnected cells sharing a common cytoplasm and organelles. This syncytial organization contributes to an efficient distribution of resources, energy, and biochemical signals. Cell fusion is a fundamental process for fungal development, colony establishment, and habitat exploitation and can occur between hyphal cells of an individual colony or between colonies of genetically distinct individuals. One outcome of cell fusion is the establishment of a stable heterokaryon, culminating in benefits for each individual via shared resources or being of critical importance for the sexual or parasexual cycle of many fungal species. However, a second outcome of cell fusion between genetically distinct strains is formation of unstable heterokaryons and the induction of a programmed cell death reaction in the heterokaryotic cells. This reaction of nonself rejection, which is termed heterokaryon (or vegetative) incompatibility, is widespread in the fungal kingdom and acts as a defense mechanism against genome exploitation and mycoparasitism. Here, we review the currently identified molecular players involved in the process of somatic cell fusion and its regulation in filamentous fungi. Thereafter, we summarize the knowledge of the molecular determinants and mechanism of heterokaryon incompatibility and place this phenomenon in the broader context of biotropic interactions and immunity.

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Image of FIGURE 1
FIGURE 1

Germling and hyphal fusion in . Germinating spores undergo mutual attraction and fusion (A: 0 min; B: 40 min; C: 80 min). Consecutive fusion events result in network formation. Hyphal branches fuse and form cross connections. (E: DIC; F: cell walls stained with calcofluor white). Asterisks in all images indicate fusion points. Adapted from reference 38 .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 2
FIGURE 2

Working model of the molecular events governing germling and hyphal fusion. The signal-emitting cell releases the ligand in a pulse-like manner, probably by exocytosis. Binding of the signal molecules to their cognate receptors results in assembly and activation of the MAK-2 module at the plasma membrane. MAK-2 phosphorylates MOB-3 of the STRIPAK complex, thereby promoting nuclear entry of MAK-1. In the nucleus MAK-2 activates the transcription factor PP-1, which controls cell fusion factor-encoding genes. Activation of MAK-2 involves reactive oxygen species production by the NADPH oxidase (NOX) complex either upstream or downstream of the MAP kinase cascade. Adapted from reference 38 .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 3
FIGURE 3

Heterokaryosis and its possible outcomes. Genetically distinct individuals can undergo hyphal anastomosis. If there are no allelic specificity differences at loci, a viable heterokaryon is established and nuclei (blue and brown dots) are exchanged. If allelic specificity is different between the two strains for any of the loci, septal plugging isolates the heterokaryotic compartments and cell death occurs.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 4
FIGURE 4

Macroscopic visualization of vegetative incompatibility. The heterokaryon (vegetative) incompatibility reaction is visualized by the occurrence of a demarcation line called “barrage” that separates the incompatible strains. Evidence of barrage on wood (spalted wood) occurring in the wild. Barrage reaction (black arrows) between genetically incompatible strains. Identical individuals fuse without inducing allorecognition PCD and do not form the barrage (white arrows).

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 5
FIGURE 5

Microscopic visualization of programmed cell death during vegetative incompatibility. A time course of compatible and incompatible hyphal fusion in . The programmed cell death reaction is followed by the fluorescent vital dye (membrane staining) FM4-64. Fusion between two strains that have identical specificities at all loci. Arrow shows the fusion pore (p). Nuclei or large vacuoles (v) are transported through the pore with the cytoplasmic flow. Fusion between two strains that differ in specificity. Heterokaryotic cells are compartmentalized by septal plugs (solid arrow and insert). Permeabilization of the plasma membrane leads to increased cytoplasmic staining and vacuolization. Open arrows show large vacuoles within incompatible fusion cells, while the asterisk shows a nearby healthy cell. Bar = 10 μM. Adapted from reference 146 .

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 6
FIGURE 6

Incompatibility systems and genetically identified () loci in model filamentous ascomycete species. Round-headed arrows connecting the genes indicate nonallelic HI systems, and square-headed arrows indicate allelic HI systems. Blue arrows indicate that the incompatibility reaction influences the distribution of mycoviruses that result in hypovirulence in . Genes in red encode for proteins with a HET domain, and boxed genes (loci) are still not identified molecularly.

Source: microbiolspec March 2017 vol. 5 no. 2 doi:10.1128/microbiolspec.FUNK-0015-2016
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Image of FIGURE 7
FIGURE 7

Domain organization of fungal and metazoan NLRs (NOD-like receptors) and NLR-like proteins. The heterokaryon determinants HET-E (also HET-D and HET-R as paralogues of HET-E) and VIC4 present a typical NLR-like domain organization. NLRs have a tripartite domain organization with a central nucleotide-binding and oligomerization (NOD) domain, an N-terminal effector domain, and a C-terminal sensor domain. The sensor domain can be composed of various repeated motifs (LRR or WD40, in the examples presented here) that trigger the activation of the receptors upon recognition of defined molecular cues. The recognition of the signal activates the formation by the receptors of multimeric protein platforms. The oligomerization of the receptors is mediated by the NOD domain (NACHT or NB-ARC type) in characterized cases, such as APAF-1 (the human apoptosis-controlling factor) and NLRC4 (an innate immunity receptor). Abbreviations: CARD, caspase recruitment domain; LRR, leucine rich repeats.

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