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New insights from an old mutant: SPADIX4 governs fruiting body development but not hyphal fusion in Sordaria macrospora

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Abstract

During the sexual life cycle of filamentous fungi, multicellular fruiting bodies are generated for the dispersal of spores. The filamentous ascomycete Sordaria macrospora has a long history as a model system for studying fruiting body formation, and two collections of sterile mutants have been generated. However, for most of these mutants, the underlying genetic defect remains unknown. Here, we investigated the mutant spadix (spd) that was generated by X-ray mutagenesis in the 1950s and terminates sexual development after the formation of pre-fruiting bodies (protoperithecia). We sequenced the spd genome and found a 22 kb deletion affecting four genes, which we termed spd1-4. Generation of deletion strains revealed that only spd4 is required for fruiting body formation. Although sterility in S. macrospora is often coupled with a vegetative hyphal fusion defect, Δspd4 was still capable of fusion. This feature distinguishes SPD4 from many other regulators of sexual development. Remarkably, GFP-tagged SPD4 accumulated in the nuclei of vegetative hyphae and fruiting body initials, the ascogonial coils, but not in sterile tissue from the developing protoperithecium. Our results point to SPD4 as a specific determinant of fruiting body formation. Research on SPD4 will, therefore, contribute to understanding cellular reprogramming during initiation of sexual development in fungi.

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References

  • Aanen DK, Debets AJM, de Visser JAGM, Hoekstra RF (2008) The social evolution of somatic fusion. Bioessays 30:1193–1203

    Article  CAS  PubMed  Google Scholar 

  • Arnaise S, Leblon G, Lares L (1984) A system for the detection of chromosomal rearrangements using Sordaria macrospora. Mutat Res 125:33–42

    Article  CAS  PubMed  Google Scholar 

  • 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 Epichloe festucae in symbiosis with Lolium perenne. Mol Plant Microbe Interact 28:69–85

    Article  PubMed  Google Scholar 

  • Bistis GN, Perkins DD, Read ND (2003) Different cell types in Neurospora crassa. Fungal Genet Newsl 50:17–19

    Google Scholar 

  • Bloemendal S, Lord KM, Rech C, Hoff B, Engh I, Read ND, Kück U (2010) A mutant defective in sexual development produces aseptate ascogonia. Eukaryot Cell 9:1856–1866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bloemendal S, Bernhards Y, Bartho K, Dettmann A, Voigt O, Teichert I, Seiler S, Wolters DA, Pöggeler S, Kück U (2012) A homolog of the human STRIPAK complex controls sexual development in fungi. Mol Microbiol 84:310–323

    Article  CAS  PubMed  Google Scholar 

  • Bloemendal S, Löper D, Terfehr D, Kopke K, Kluge J, Teichert I, Kück U (2014) Tools for advanced and targeted genetic manipulation of the beta-lactam antibiotic producer Acremonium chrysogenum. J Biotechnol 169:51–62

    Article  CAS  PubMed  Google Scholar 

  • Cai ZD, Chai YF, Zhang CY, Qiao WR, Sang H, Lu L (2015) The Gβ-like protein CpcB is required for hyphal growth, conidiophore morphology and pathogenicity in Aspergillus fumigatus. Fungal Genet Biol 81:120–131

    Article  CAS  PubMed  Google Scholar 

  • Charlton ND, Shoji JY, Ghimire SR, Nakashima J, Craven KD (2012) Deletion of the fungal gene soft disrupts mutualistic symbiosis between the grass endophyte Epichloe festucae and the host plant. Eukaryot Cell 11:1463–1471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chi MH, Craven KD (2016) RacA-mediated ROS signaling is required for polarized cell differentiation in conidiogenesis of Aspergillus fumigatus. PLoS One 11:e0149548

    Article  PubMed  PubMed Central  Google Scholar 

  • Christianson TW, Sikorski RS, Dante M, Shero JH, Hieter P (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene 110:119–122

    Article  CAS  PubMed  Google Scholar 

  • Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci USA 103:10352–10357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coppin E, Berteaux-Lecellier V, Bidard F, Brun S, Ruprich-Robert G, Espagne E, Ait-Benkhali J, Goarin A, Nesseir A, Planamente S, Debuchy R, Silar P (2012) Systematic deletion of homeobox genes in Podospora anserina uncovers their roles in shaping the fruiting body. PLoS One 7:e37488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Debuchy R, Berteaux-Lecellier V, Silar P (2010) Mating systems and sexual morphogenesis in ascomycetes. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM Press, Washington, D.C., pp 501–535

    Chapter  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Dinkel H, Van Roey K, Michael S, Kumar M, Uyar B, Altenberg B, Milchevskaya V, Schneider M, Kühn H, Behrendt A, Dahl SL, Damerell V, Diebel S, Kalman S, Klein S, Knudsen AC, Mäder C, Merrill S, Staudt A, Thiel V, Welti L, Davey NE, Diella F, Gibson TJ (2016) ELM 2016-data update and new functionality of the eukaryotic linear motif resource. Nucleic Acids Res 44:D294–D300

    Article  PubMed  Google Scholar 

  • Dirschnabel DE, Nowrousian M, Cano-Dominguez 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dreyer J, Eichhorn H, Friedlin E, Kürnsteiner H, Kück U (2007) A homologue of the Aspergillus velvet gene regulates both cephalosporin C biosynthesis and hyphal fragmentation in Acremonium chrysogenum. Appl Environ Microbiol 73:3412–3422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan Y, Ge C, Liu S, Wang J, Zhou M (2013) A two-component histidine kinase Shk1 controls stress response, sclerotial formation and fungicide resistance in Sclerotinia sclerotiorum. Mol Plant Pathol 14:708–718

    Article  CAS  PubMed  Google Scholar 

  • Engh I, Würtz C, Witzel-Schlömp K, Zhang HY, Hoff B, Nowrousian M, Rottensteiner H, Kück U (2007) The WW domain protein PRO40 is required for fungal fertility and associates with Woronin bodies. Eukaryot Cell 6:831–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esser K (1982) Cryptogams—cyanobacteria, algae, fungi, lichens. Cambridge University Press, London

    Google Scholar 

  • Esser K, Straub J (1956) Fertility in the heterokaryon from two sterile mutants of Sordaria macrospora Auersw. Z Indukt Abstamm Vererb 87:625–626

    CAS  Google Scholar 

  • Esser K, Straub J (1958) Genetische Untersuchungen an Sordaria macrospora Auersw., Kompensation und Induktion bei genbedingten Entwicklungsdefekten. Z Vererb 89:729–746

    CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu C, Iyer P, Herkal A, Abdullah J, Stout A, Free SJ (2011) Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10:1100–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gull K (1978) Form and function of septa in filamentous fungi. In: Smith JE, Berry DR (eds) The filamentous fungi III. Developmental mycology. Wiley, New York, pp 78–93

    Google Scholar 

  • Harris K, Lamson RE, Nelson B, Hughes TR, Marton MJ, Roberts CJ, Boone C, Pryciak PM (2001) Role of scaffolds in MAP kinase pathway specificity revealed by custom design of pathway-dedicated signaling proteins. Curr Biol 11:1815–1824

    Article  CAS  PubMed  Google Scholar 

  • Harting R, Bayram O, Laubinger K, Valerius O, Braus GH (2013) Interplay of the fungal sumoylation network for control of multicellular development. Mol Microbiol 90:1125–1145

    Article  CAS  PubMed  Google Scholar 

  • Hoff B, Kamerewerd J, Sigl C, Mitterbauer R, Zadra I, Kürnsteiner H, Kück U (2010) Two components of a velvet-like complex control hyphal morphogenesis, conidiophore development, and penicillin biosynthesis in Penicillium chrysogenum. Eukaryot Cell 9:1236–1250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • James P, Halladay J, Craig EA (1996) Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425–1436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jamet-Vierny C, Debuchy R, Prigent M, Silar P (2007) IDC1, a pezizomycotina-specific gene that belongs to the PaMpk1 MAP kinase transduction cascade of the filamentous fungus Podospora anserina. Fungal Genet Biol 44:1219–1230

    Article  CAS  PubMed  Google Scholar 

  • Jerpseth B, Greener A, Short JM, Viola J, Kretz PL (1992) XL1-Blue MRF` E. coli cells: mcrA-, mcrCB-, mcrF-, mmr-, hsdR- derivative of XL1-Blue cells. Strateg Mol Biol 5:81–83

    Google Scholar 

  • Johnson TE (1976) Analysis of pattern formation in Neurospora perithecial development using genetic mosaics. Dev Biol 54:23–36

    Article  CAS  PubMed  Google Scholar 

  • Jonkers W, Leeder AC, Ansong C, Wang Y, Yang F, Starr TL, Camp DG 2nd, Smith RD, Glass NL (2014) HAM-5 functions as a MAP kinase scaffold during cell fusion in Neurospora crassa. PLoS Genet 10:e1004783

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamerewerd J, Jansson M, Nowrousian M, Pöggeler S, Kück U (2008) Three alpha-subunits of heterotrimeric G proteins and an adenylyl cyclase have distinct roles in fruiting body development in the homothallic fungus Sordaria macrospora. Genetics 180:191–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayano Y, Tanaka A, Akano F, Scott B, Takemoto D (2013) Differential roles of NADPH oxidases and associated regulators in polarized growth, conidiation and hyphal fusion in the symbiotic fungus Epichloe festucae. Fungal Genet Biol 56:87–97

    Article  CAS  PubMed  Google Scholar 

  • Khan IA, Lu JP, Liu XH, Rehman A, Lin FC (2012) Multifunction of autophagy-related genes in filamentous fungi. Microbiol Res 167:339–345

    Article  CAS  PubMed  Google Scholar 

  • Kicka S, Bonnet C, Sobering AK, Ganesan LP, Silar P (2006) A mitotically inheritable unit containing a MAP kinase module. Proc Natl Acad Sci USA 103:13445–13450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HR, Chae KS, Han KH, Han DM (2009) The nsdC gene encoding a putative C2H2-type transcription factor is a key activator of sexual development in Aspergillus nidulans. Genetics 182:771–783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim H, Wright SJ, Park G, Ouyang S, Krystofova S, Borkovich KA (2012) Roles for receptors, pheromones, G proteins, and mating type genes during sexual reproduction in Neurospora crassa. Genetics 190:1389–1404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kück U, Pöggeler S, Nowrousian M, Nolting N, Engh I (2009) Sordaria macrospora, a model system for fungal development. In: Anke T, Weber D (eds) The Mycota XV. Springer, Heidelberg, pp 17–39

    Google Scholar 

  • Kück U, Beier AM, Teichert I (2016) The composition and function of the striatin-interacting phosphatases and kinases (STRIPAK) complex in fungi. Fungal Genet Biol 90:31–38

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lehr NA, Wang Z, Li N, Hewitt DA, Lopez-Giraldez F, Trail F, Townsend JP (2014) Gene expression differences among three Neurospora species reveal genes required for sexual reproduction in Neurospora crassa. PLoS One 9:e110398

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Lichius A (2010) Cell fusion in Neurospora crassa. PhD thesis, The University of Edinburgh, UK

  • Lichius A, Lord KM (2014) Chemoattractive Mechanisms in Filamentous Fungi. Open Mycol J 8:28–57

    Article  Google Scholar 

  • Lichius A, Lord KM, Jeffree CE, Oborny R, Boonyarungsrit P, Read ND (2012) Importance of MAP kinases during protoperithecial morphogenesis in Neurospora crassa. PLoS One 7:e42565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lord KM, Read ND (2011) Perithecium morphogenesis in Sordaria macrospora. Fungal Genet Biol 48:388–399

    Article  PubMed  Google Scholar 

  • Malagnac F, Lalucque H, Lepere G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:982–997

    Article  CAS  PubMed  Google Scholar 

  • Malagnac F, Klapholz B, Silar P (2007) PaTrx1 and PaTrx3, two cytosolic thioredoxins of the filamentous ascomycete Podospora anserina involved in sexual development and cell degeneration. Eukaryot Cell 6:2323–2331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayrhofer S, Weber JM, Pöggeler S (2006) Pheromones and pheromone receptors are required for proper sexual development in the homothallic ascomycete Sordaria macrospora. Genetics 172:1521–1533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowrousian M, Cebula P (2005) The gene for a lectin-like protein is transcriptionally activated during sexual development, but is not essential for fruiting body formation in the filamentous fungus Sordaria macrospora. BMC Microbiol 5:64

    Article  PubMed  PubMed Central  Google Scholar 

  • Nowrousian M, Frank S, Koers S, Strauch P, Weitner T, Ringelberg C, Dunlap JC, Loros JJ, Kück U (2007) The novel ER membrane protein PRO41 is essential for sexual development in the filamentous fungus Sordaria macrospora. Mol Microbiol 64:923–937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowrousian M, Stajich JE, Chu M, Engh I, Espagne E, Halliday K, Kamerewerd J, Kempken F, Knab B, Kuo HC, Osiewacz HD, Pöggeler S, Read ND, Seiler S, Smith KM, Zickler D, Kück U, Freitag M (2010) De novo assembly of a 40 Mb eukaryotic genome from short sequence reads: Sordaria macrospora, a model organism for fungal morphogenesis. PLoS Genet 6:e1000891

    Article  PubMed  PubMed Central  Google Scholar 

  • Nowrousian M, Teichert I, Masloff S, Kück U (2012) Whole-genome sequencing of Sordaria macrospora mutants identifies developmental genes. G3 (Bethesda) 2:261–270

    Article  CAS  Google Scholar 

  • Peraza-Reyes L, Berteaux-Lecellier V (2013) Peroxisomes and sexual development in fungi. Front Physiol 4:244

    Article  PubMed  PubMed Central  Google Scholar 

  • Pöggeler S, Kück U (2006) Highly efficient generation of signal transduction knockout mutants using a fungal strain deficient in the mammalian ku70 ortholog. Gene 378:1–10

    Article  PubMed  Google Scholar 

  • Pöggeler S, Nowrousian M, Kück U (2006) Fruiting-body development in ascomycetes. In: Kües U, Fischer R (eds) The Mycota I. Springer, Berlin, pp 325–355

    Google Scholar 

  • Prados Rosales RC, Di Pietro A (2008) Vegetative hyphal fusion is not essential for plant infection by Fusarium oxysporum. Eukaryot Cell 7:162–171

    Article  CAS  PubMed  Google Scholar 

  • Read ND, Lichius A, Shoji JY, Goryachev AB (2009) Self-signalling and self-fusion in filamentous fungi. Curr Opin Microbiol 12:608–615

    Article  PubMed  Google Scholar 

  • Rech C, Engh I, Kück U (2007) Detection of hyphal fusion in filamentous fungi using differently fluorescence-labeled histones. Curr Genet 52:259–266

    Article  CAS  PubMed  Google Scholar 

  • Saito H (2010) Regulation of cross-talk in yeast MAPK signaling pathways. Curr Opin Microbiol 13:677–683

    Article  CAS  PubMed  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Sarikaya-Bayram O, Bayram O, Feussner K, Kim JH, Kim HS, Kaever A, Feussner I, Chae KS, Han DM, Han KH, Braus GH (2014) Membrane-bound methyltransferase complex VapA-VipC-VapB guides epigenetic control of fungal development. Dev Cell 29:406–420

    Article  CAS  PubMed  Google Scholar 

  • Schindler D, Nowrousian M (2014) The polyketide synthase gene pks4 is essential for sexual development and regulates fruiting body morphology in Sordaria macrospora. Fungal Genet Biol 68:48–59

    Article  CAS  PubMed  Google Scholar 

  • Siegmund U, Marschall R, Tudzynski P (2015) BcNoxD, a putative ER protein, is a new component of the NADPH oxidase complex in Botrytis cinerea. Mol Microbiol 95:988–1005

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Simonin A, Palma-Guerrero J, Fricker M, Glass NL (2012) Physiological significance of network organization in fungi. Eukaryot Cell 11:1345–1352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Teichert I, Wolff G, Kück U, Nowrousian M (2012) Combining laser microdissection and RNA-seq to chart the transcriptional landscape of fungal development. BMC Genom 13:511

    Article  CAS  Google Scholar 

  • Teichert I, Nowrousian M, Pöggeler S, Kück U (2014a) The filamentous fungus Sordaria macrospora as a genetic model to study fruiting body development. Adv Genet 87:199–244

    CAS  PubMed  Google Scholar 

  • Teichert I, Steffens EK, Schnass N, Fränzel B, Krisp C, Wolters DA, Kück U (2014b) 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Tong LC, Silar P, Lalucque H (2014) Genetic control of anastomosis in Podospora anserina. Fungal Genet Biol 70:94–103

    Article  PubMed  Google Scholar 

  • Tsui S, Dai T, Roettger S, Schempp W, Salido EC, Yen PH (2000) Identification of two novel proteins that interact with germ-cell-specific RNA-binding proteins DAZ and DAZL1. Genomics 65:266–273

    Article  CAS  PubMed  Google Scholar 

  • Turra D, El Ghalid M, Rossi F, Di Pietro A (2015) Fungal pathogen uses sex pheromone receptor for chemotropic sensing of host plant signals. Nature 527:521–524

    Article  CAS  PubMed  Google Scholar 

  • Voigt O, Pöggeler S (2013) Autophagy genes Smatg8 and Smatg4 are required for fruiting-body development, vegetative growth and ascospore germination in the filamentous ascomycete Sordaria macrospora. Autophagy 9:33–49

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voigt O, Herzog B, Jakobshagen A, Pöggeler S (2013) bZIP transcription factor SmJLB1 regulates autophagy-related genes Smatg8 and Smatg4 and is required for fruiting-body development and vegetative growth in Sordaria macrospora. Fungal Genet Biol 61:50–60

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This paper is dedicated to Karl Esser, who generated the spd mutant, on the occasion of his 92nd birthday. We thank Ingeborg Godehardt, Kerstin Kalkreuter, Regina Krampe, and Susanne Schlewinski for excellent technical assistance. We thank Gabriele Frenßen-Schenkel for graphical work. This work was funded by the Deutsche Forschungsgemeinschaft (KU517/12-2, KU 517/11-2, NO407/5-1).

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  1. Miriam Lutomski

    Present address: Abteilung Molekulare Genetik I, Universität Duisburg-Essen, 45141, Essen, Germany

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  1. Lehrstuhl für Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, ND6/166, Universitätsstrasse 150, 44780, Bochum, Germany

    Ines Teichert, Miriam Lutomski, Ramona Märker, Minou Nowrousian & Ulrich Kück

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This study was funded by the Deutsche Forschungsgemeinschaft (KU517/12-2, KU 517/11-2, NO407/5-1).

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Teichert, I., Lutomski, M., Märker, R. et al. New insights from an old mutant: SPADIX4 governs fruiting body development but not hyphal fusion in Sordaria macrospora . Mol Genet Genomics 292, 93–104 (2017). https://doi.org/10.1007/s00438-016-1258-0

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