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Mating-Type Genes from the Homothallic Fungus Sordaria Macrospora Are Functionally Expressed in a Heterothallic Ascomycete

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Mating-Type Genes from the Homothallic Fungus Sordaria Macrospora Are Functionally Expressed in a Heterothallic Ascomycete Copyright 0 1997 by the Genetics Society of America Mating-Type Genes From the Homothallic Fungus Sordaria macrospora Are Functionally Expressed in a Heterothallic Ascomycete Stefanie Poggeler," Siegfried Risch,* Ulrich Kiick* andHeinz D. Osiewaczt *Lehrstuhl fur Allgemeine Botanik, Ruhr-Universitat, 44780 Bochum, Germany and tMolekulare Entwicklungsbiologie und Biotechnologie, J. W. Goethe-Universitat, 60439 Frankfurt, Germany Manuscript received May 12, 1997 Accepted for publication June 16, 1997 ABSTRACT Homokaryons from the homothallic ascomycteSordaria macrospora are able to enter the sexual pathway and to form fertile fruiting bodies. To analyze the molecular basisof homothallism and to elucidate the role of mating-products during fruiting body development, we cloned and sequenced the entire S. macrospora mating-type locus. Comparison of the Sordaria mating-type locus with mating-type idiomorphs from the heterothallic ascomycetesNeurospora crassa and Podospora ansa'na revealed that sequences from both idiomorphs (A/a and mat-/mat+, respectively) are contiguous in S. macrospora. DNA sequencing of the S. macrospora mating-type region allowed the identification offour open reading frames (ORFs), which were termed Smt-al, SmtA-I, SmtA-2 and SmtA-3. While Smt-al, SmtA-1, and SmtA-2 show strong sequence similarities with the correspondingN. crassa mating-type ORFs, SmtA-3 has a chimeric character. It comprises sequences that are similar to the A and a mating-type idiomorph from N. crassa. To determine functionalityof the S. macrospora mating-type genes,we show that allORFs are transcriptionally expressed. Furthermore,we transformed the S. macrospma mating-type genesinto mat- and mat+ strains of the closely related heterothallic fungusP. ansa'na. The transformation experiments show that mating- type genes from S. macrospora induce fruiting body formation in P. anserina. HE regulation of sexual reproduction is one of the crassa and Podospora anserina, a homokaryotic ascospore T central processes in the life cycle of most eukary- is not capable of completing the sexual cycle. N. crmsa otes. The recent cloning and characterization ofse- and P. anserina are composed of two mating-type popu- quences specifylng mating types from mycelial fungi lations, designated A and a or mat- and mat+, respec- has allowed insights into the regulatory processes con- tively. Mating occurs only between sexual structures of trolling sexual reproduction in ascomycetes (reviewed opposite matingtype. The sequences conferring mating in GLASSand NELSON1994; METZENBERGand RANDALL behavior in N. crassa and P. anserha consist of dissimilar 1995; NELSON1996). Mating behavior in ascomycetes DNA sequences (idiomorphs), which are present at a can be either homothallic or heterothallic. In contrast homologous locus in the mating partners (GLASSet al. to the well-studied mating types in heterothallic fila- 1988; PICARDet aL 1991). Database searches revealed mentous ascomycetes, the genetic basis of homothal- that conserved DNA binding motifs, such asHMG lism remains largely uncharacterized. No instance of boxes, a domains, or amphipathic alpha helical do- mating-type switching or interconversion that occurs in mains, are found in allof the mating-type products homothallic yeasts have been reported for Neurospora (GLASSet al. 1990a; STABENand YANOFSKY1990; DEBU- (PERKINS1987). CHY et al. 1993; FERREIRAet al. 1996). For this reason, The homothallic ascomycete Sordaria macrospora (Py- the mating-type genes are believed to encode master renomycetidae,Sordariaceae) has beenan excellent transcriptional regulators that control sexual develop- model system for studying not only meiotic pairing and ment in filamentous ascomycetes (NELSON1996). recombination (ZICKLER 1977) but also fruiting body In an effort to elucidate the phenomenon of homo- development (ESSERand STRAUB1958; HESLOT1958). thallism in mycelial ascomycetes,homothallic members In contrast to heterothallicspecies of the Sordariaceae, of Sordariaceae were probed with the A and a mating- in S. macrospora, a homokaryotic ascospore gwes rise to type sequences from N. crassa. The analysis revealed hyphae that can enter the sexual reproductive pathway that sequences hybridizing to the N. crassa mating-type and produce fruiting bodies (perithecia) enclosing the locus are conserved in both heterothallic and homo- ascospore progeny. thallic Sordariaceae species. Twogroups of homothallic species could be distinguished in this study: the first In heterothallicSordariaceae, such as Neurospora group contains only sequences similar to the N. crmsa A idiomorph (A type) and a second group contains Correspolzding authm: Ulrich Kiick, Lehrstuhl fiir Allgemeine Bo- tanik, Ruhr-UniversitAt Bochum, 44780 Bochum, Germany. sequences similar to both the A and the a idiomorphs E-mail: u1rich.kueckQrz.ruhr-uni-hochum.de (A/atype) (GLASSet al. 1988, 1990b). Genetics 147: 567-580 (October, 1997) 568 S. Poggeler et al. Recently the mating-type locus from N. afncana, mat- (700005) and mat+ (700004) were derived from homo- which is a representative of A-type homothallic Sordari- karyotic spores of P. ansa'na wild-type strain s (ESSER1974) containing only one of the two mating types and were used aceae, has been examined in some detail and the N. as hosts for transformation experiments. Standard media and crassa mt A-1 homologue has been sequenced and was conditions for thecultivation of P. ansm'na were as described shown to function as mating activator in N. crassa byESSER (1974) and OSIEWACZet al. (1991). Escha'chia coli (GLASSand SMITH1994). In addition, the mating-type strain XLl-Blue MR (Stratagene,Heidelberg, Germany) loci of selected members of the A/qpe Sordariaceae served as a recipient strain for recombinant cosmids, and have been compared with the mating-type idiomorphs strain XL-1 Blue (BULLOCKet al. 1987) was used for propaga- tion of recombinant plasmids. of N. crassa by means of Southern hybridization. How- Cloning of the S. mamspora mating-type locus: An indexed ever, a direct linkage of the A- and especific sequences genomic cosmid library from S. macrospma was screened by a could not be confirmed in thisstudy (BEATTYet al. rapid method (POGGELERet al. 1997) with heterologous 1994). probes carrying sequences from theN. crmsa A or aidiomorph To our knowledge, this paper provides the first mo- probes. For this purpose, a O.&kb NcoI/EcoRI fragment from lecular description of the entire mating-type locus from plasmid pmtAG2, which carries a 1.2-kb EcoRI/Bcll fragment from the A mating-type specific region (GLASSet al. 1990a), a homothallic mycelial fungus. The ascomycete S. mac- was used. Similarly, a 1.1-kb PstI/NcoI fragment from plasmid rospora is a memberof the A/etypehomothallic Sordar- pCSN4, which contains a 1.9-kb BamHI/EcoRV fragment from iaceae, and, due to the development of optimized mo- then a mating-type specific region (STABENand YANOWFSKY lecular tools, this fungus became more suitable for mo- 1990), served as a mating-type specific probe. Two out of 96 lecular genetic investigations (WALZ and KUCK 1995; cosmid pools of 48 wells each hybridized to the A-specific as well as to the aspecific probe from N. crassa. A colony filter POGGELERet al. 1997). We show that the four mating- hybridization between clones from the two pools was subse- type genes in S. macrospora are transcriptionally ex- quently hybridized with the A- and &specific probes giving pressed and demonstrate that the introduction of ho- rise to three labeled clones designated Dl, D9 and H2. Cos- mothallic mating-type genes from S. macrospora leads mid DNA from these three clones was prepared according to to the initiation of fruiting body development in the the protocol provided by Stratagene together with cosmid heterothallic fungus P. anserina. The result indicates SCOS. Standardmethods of molecular biology were used ac- that both A- and especific mating-type genes are func- cording to SAMBROOKet al. (1989). Subcloning of hybridizing tionally expressed in homothallic species. Our findings DNA fragments from cosmid clone Dl resulted in the con- provide new aspects to the understanding of the molec- struction of pBluescript (=+) (Stratagene) derivatives (Fig- ular basis of homothallism and the involvement of mat- ure 1 and Table 1). ing-type genes in fruiting body development in ascomy- Oligonucleotides: Oligonucleotides (Table 2) were synthe- cetes. sized for use as sequencing primers and/or primers for spe- cific reverse transcription PCR (RT-PCR) amplifications. DNA sequencing and sequence analysis: Double-stranded MATERIALSAND METHODS sequence reactions were performed with a sequenasekit (Am- ersham/USB Cleveland) under conditions recommended by Bacterialand fungal strains: S. macrospora strain k-hell the manufacturer. An ordered set of deletion clones was pre- (3346) from our laboratory collection has a wild-type pheno- pared using a nested deletion kit (Pharmacia, Freiburg, Ger- type (ESSERand STRAUB1958). Genomic DNA from strain many). Clones were sequenced on both strands using the 3346 was used for construction of the indexed S. macrospma universal or reverse sequencing primer. Individual sequenc- cosmid library (POGGELERet al. 1997). TheP. anserina strains ing primers (Table 2) were synthesized in regions whereclone a A I Sm tA-3 SmtA-2SmtA-3 SmtA-l S,B H EV EV EV HBSEV S SH B I II I I I I I I 1 t 4 pS3-20 I I pB63 FIGURE1.-Physical map of the S. macrospma mating-type locus. The line showing restriction enzyme sites covers the 8810-bp
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