Systematic deletion of homeobox genes in Podospora anserina uncovers their roles in shaping the fruiting body

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Coppin, Evelyne ^a,b   Berteaux Lecellier, Véronique ^a,b,d   Bidard, Frédérique ^a   Brun, Sylvain ^a,b,c   Ruprich Robert, Gwenaël ^a,b,c   Espagne, Eric ^a   Aït Benkhali, Jinane ^a   Goarin, Anne ^a,b,c   Nesseir, Audrey ^a   Planamente, Sara ^a   Debuchy, Robert ^a,b   Silar, Philippe ^a,b,c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CNRS   (France)

^c UNIVERSITÉ PARIS DESCARTES   (France)

^d Université de Perpignan   (French Polynesia)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HOMEODOMAIN TRANSCRIPTION FACTOR; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 1; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 2; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 3; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 4; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 5; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 6; PODOSPORA ANSERINA HOMEODOMAIN TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BASIDIOMYCETES; CLAMP FORMATION; CONTROLLED STUDY; CROZIER FORMATION; FRUITING BODY; FUNGAL DEVELOPMENT; FUNGAL GENE; FUNGAL STRAIN; FUNGUS HYPHAE; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE INTERACTION; HOMEOBOX; MATURATION; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; PAH1 GENE; PAH2 GENE; PAH3 GENE; PAH4 GENE; PAH5 GENE; PAH6 GENE; PAH7 GENE; PODOSPORA ANSERINA; STRAIN DIFFERENCE;

AMINO ACID SEQUENCE; EVOLUTION, MOLECULAR; FERTILITY; FRUITING BODIES, FUNGAL; GENE DELETION; GENES, HOMEOBOX; GENOTYPE; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; PODOSPORA; SEQUENCE ALIGNMENT; TRANSCRIPTION FACTORS;

ANIMALIA; ASCOMYCOTA; BASIDIOMYCOTA; FUNGI; PODOSPORA ANSERINA;

EID: 84861468929     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037488     Document Type: Article

References (51)

1. Leeder AC, Palma-Guerrero J, Glass NL, (2011) The social network: deciphering fungal language. Nat Rev Micro 9: 440-451.
2. Mueller G, Schmit J, (2007) Fungal biodiversity: what do we know? What can we predict? Biodiversity and Conservation 16: 1-5.
3. James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, et al. (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443: 818-822.
4. Giovannetti M, Azzolini D, Citernesi AS, (1999) Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl Environ Microbiol 65: 5571-5575.
5. Hansen PV, Bianchinotti MV, Rajchenberg M, (2007) Anatomy and cytology of Taphrina entomospora during infection of Nothofagus. Mycol Res 111: 592-598.
6. Kramer CL, (1960) Morphological development and nuclear behavior in the genus Taphrina. Mycologia 52: 295-320.
7. Brown AJ, Casselton LA, (2001) Mating in mushrooms: increasing the chances but prolonging the affair. Trends Genet 17: 393-400.
8. Casselton LA, Feldbrügge M, (2010) Mating and sexual morphogenesis in basidiomycete fungi. In: Borkovich KA, Ebbole DJ, editors. Cellular and Molecular Biology of Filamentous Fungi Washington, DC ASM Press pp. 536-555.
9. Bürglin TR, (2005) Homeodomain proteins. In: Meyers RA, editors. Encyclopedia of Molecular Cell Biology and Molecular Medicine Weinheim Wiley and Co pp. 179-222.
10. Derelle R, Lopez P, Le Guyader H, Manuel M, (2007) Homeodomain proteins belong to the ancestral molecular toolkit of eukaryotes. Evol Dev 9: 212-219.
11. Lewis EB, (1978) A gene complex controlling segmentation in Drosophila. Nature 276: 565-570.
12. Mallo M, Wellik DM, Deschamps J, (2010) Hox genes and regional patterning of the vertebrate body plan. Dev Biol 344: 7-15.
13. Mukherjee K, Brocchieri L, Burglin TR, (2009) A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol 26: 2775-2794.
14. Hay A, Tsiantis M, (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137: 3153-3165.
15. Arnaise S, Zickler D, Poisier C, Debuchy R, (2001) pah1: a homeobox gene involved in hyphal morphology and microconidiogenesis in the filamentous ascomycete Podospora anserina. Mol Microbiol 39: 54-64.
16. Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, et al. (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103: 10352-10357.
17. Kim S, Park SY, Kim KS, Rho HS, Chi MH, et al. (2009) Homeobox transcription factors are required for conidiation and appressorium development in the rice blast fungus Magnaporthe oryzae. PLoS Genet 5: e1000757.
18. El-Khoury R, Sellem CH, Coppin E, Boivin A, Maas MF, et al. (2008) Gene deletion and allelic replacement in the filamentous fungus Podospora anserina. Curr Genet 53: 249-258.
19. Marcou D, (1961) Notion de longévité et nature cytoplasmique du déterminant de la sénescence chez quelques champignons. Ann Sci Natur Bot Paris Sér 12, 2: 653-764.
20. Brun S, Malagnac F, Bidard F, Lalucque H, Silar P, (2009) Functions and regulation of the Nox family in the filamentous fungus Podospora anserina: a new role in cellulose degradation. Mol Microbiol 74: 480-496.
21. Silar P, (2005) Peroxide accumulation and cell death in filamentous fungi induced by contact with a contestant. Mycol Res 109: 137-149.
22. Silar P, (2011) Grafting as a method for studying development in the filamentous fungus Podospora anserina. Fungal Biol 115: 793-802.
23. Coppin E, Arnaise S, Contamine V, Picard M, (1993) Deletion of the mating-type sequences in Podospora anserina abolishes mating without affecting vegetative functions and sexual differentiation. Mol Gen Genet 241: 409-414.
24. Lambou K, Malagnac F, Barbisan C, Tharreau D, Lebrun MH, et al. (2008) The crucial role during ascospore germination of the Pls1 tetraspanin in Podospora anserina provides an example of the convergent evolution of morphogenetic processes in fungal plant pathogens and saprobes. Eukaryot Cell 7.
25. van der Graaff E, Laux T, Rensing SA, (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10: 248.
26. Buller AHR, (1958) The formation of hyphal fusions in the fusions in the mycelium of the higher fungi. Researches on Fungi, vol. 5 New York Hafner Publishing Co pp. 1-74.
27. Shaffer RL, (1975) The major groups of Basidiomycetes. Mycologia 67: 1-18.
28. Martens P, (1932) L'origine du crochet et de l'anse d'anastomose chez les Champignons supérieurs. Bull Soc Mycol France 48: 259-282.
29. Webster J, Weber RWS, (2007) Introduction to Fungi, 3rd edition Cambridge Cambridge University Press.
30. Scherer M, Heimel K, Starke V, Kämper J, (2006) The Clp1 Protein Is Required for Clamp Formation and Pathogenic Development of Ustilago maydis. The Plant Cell Online 18: 2388-2401.
31. Landvik S, Schumacher TK, Eriksson OE, Moss ST, (2003) Morphology and ultrastructure of Neolecta species. Mycol Res 107: 1021-1031.
32. Syrop M, Beckett A, (1976) Leaf curl disease of almond caused by Taphrina deformans. III. Ultrastructural cytology of the pathogen. Can J Bot 54: 293-305.
33. Bauer R, Begerow D, Sampaio J, Weiβ M, Oberwinkler F, (2006) The simple-septate basidiomycetes: a synopsis. Mycological Progress 5: 41-66.
34. Oberwinkler F, Bauer R, (1990) Cryptococolax: a new mycoparasitic heterobasidiomycete. Mycologia 82: 671-692.
35. Kirschner R, Bauer R, Oberwinkler F, (2001) Colacosiphon: a new genus described for a mycoparasitic fungus. Mycologia 93: 634-644.
36. Bauer R, Metzler B, Begerow D, Oberwinkler F, (2009) Cystobasidiopsis nirenbergiae, a new agaricostilbomycete (Pucciniomycotina). Mycol Res 113: 960-966.
37. Inada K, Morimoto Y, Arima T, Murata Y, Kamada T, (2001) The clp1 gene of the mushroom Coprinus cinereus is essential for A-regulated sexual development. Genetics 157: 133-140.
38. Ekena JL, Stanton BC, Schiebe-Owens JA, Hull CM, (2008) Sexual development in Cryptococcus neoformans requires CLP1, a target of the homeodomain transcription factors Sxi1alpha and Sxi2a. Eukaryot Cell 7: 49-57.
39. Heimel K, Scherer M, Schuler D, Kamper J, (2010) The Ustilago maydis Clp1 protein orchestrates pheromone and b-dependent signaling pathways to coordinate the cell cycle and pathogenic development. Plant Cell 22: 2908-2922.
40. Lord M, Sladewski TE, Pollard TD, (2008) Yeast UCS proteins promote actomyosin interactions and limit myosin turnover in cells. Proc Natl Acad Sci U S A 105: 8014-8019.
41. Berteaux-Lecellier V, Zickler D, Debuchy R, Panvier-Adoutte A, Thompson-Coffe C, et al. (1998) A homologue of the yeast SHE4 gene is essential for the transition between the syncytial and cellular stages during sexual reproduction of the fungus Podospora anserina. Embo J 17: 1248-1258.
42. Fleissner A, Diamond S, Glass NL, (2009) The Saccharomyces cerevisiae PRM1 homolog in Neurospora crassa is involved in vegetative and sexual cell fusion events but also has postfertilization functions. Genetics 181: 497-510.
43. Coppin E, de Renty C, Debuchy R, (2005) The function of the coding sequences for the putative pheromone precursors in Podospora anserina is restricted to fertilization. Eukaryot Cell 4: 407-420.
44. Espagne E, Lespinet O, Malagnac F, Da Silva C, Jaillon O, et al. (2008) The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol 9: R77.
45. Rizet G, (1952) Les phénomènes de barrage chez Podospora anserina. I. Analyse génétique des barrages entre souches S and s. Rev Cytol Biol Veg 13: 51-92.
46. Bidard F, Ait Benkhali J, Coppin E, Imbeaud S, Grognet P, et al. (2011) Genome-wide gene expression profiling of fertilization competent mycelium in opposite mating types in the heterothallic fungus Podospora anserina. PLoS One 6: e21476.
47. Coppin E, Debuchy R, (2000) Co-expression of the mating-type genes involved in internuclear recognition is lethal in Podospora anserina. Genetics 155: 657-669.
48. Thompson-Coffe C, Zickler D, (1994) How the cytoskeleton recognizes and sorts nuclei of opposite mating type during the sexual cycle in filamentous ascomycetes. Dev Biol 165: 257-271.
49. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
50. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ, (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
51. Bidard F, Imbeaud S, Reymond N, Lespinet O, Silar P, et al. (2010) A general framework for optimization of probes for gene expression microarray and its application to the fungus Podospora anserina. BMC Res Notes 3: 171.