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16 Fruiting-Body Development in Ascomycetes 16 Fruiting-Body Development in Ascomycetes S. Pöggeler1,M.Nowrousian1,U.Kück1 CONTENTS I. Introduction I. Introduction ......................... 325 A. Induction of Sexual Development andFruiting-BodyMorphology........ 326 The primary morphological character that dis- B. Model Organisms to Study Fruiting-Body tinguishes members of the phylum Ascomycota Development...................... 327 1. Neurospora crassa ................. 327 from all other fungi is the ascus. This sac-like 2. Sordaria macrospora .............. 331 meiosporangium contains the meiospores (as- 3. Aspergillus nidulans ............... 331 cospores) and is produced only during the sexual II. Physiological Factors Influencing life cycle. The taxonomic classification of members Fruiting-Body Development ............. 333 A.EnvironmentalFactors............... 333 of the phylum Ascomycota is complex, because 1.NutrientsandRelatedFactors....... 333 these comprise a multitude of species showing 2.PhysicalFactors.................. 334 high diversity in morphology, habitat and life B.EndogenousFactors................. 336 history. However, the ability to produce a dikaryon 1.MetabolicProcesses............... 336 separates members of the Ascomycota into two 2.Pheromones..................... 338 III. Signal Transduction Cascades ............ 339 distinct groups: (1) the saccharomycetes, which are A. Perception of Environmental mostly unicellular, and (2) mycelial ascomycetes, andEndogenousSignals............. 339 the majority of which share several characteristics B.SignalTransductionPathways......... 341 including certain cell wall constituents, septal 1.HeterotrimericGProteins.......... 342 2.RASandRAS-LikeProteins......... 342 pores with Woronin bodies, and a dikaryotic phase 3. cAMP Activated Protein Kinases PKA . 343 as part of their life cycle. Mycelial ascomycetes 4. Mitogen-Activated Protein Kinase typically form fruiting bodies called ascomata (MAPK)Pathways................ 343 or ascocarps (Alexopoulos et al. 1996; Barr 5. Other Putative Signaling Proteins . 344 2001). These are highly complex, multicellular C.TranscriptionFactors................ 344 IV. Structural Components Involved structures composed of many different cell types in Fruiting-Body Development ........... 345 that surround the asci in a characteristic manner A. The Cytoskeleton (Bistis et al. 2003). Whereas ascospores arise inFruiting-BodyDevelopment........ 346 from dikaryotic hyphae after karyogamy and B. The Cell Wall inFruiting-BodyDevelopment........ 346 meiosis, all fruiting body-forming tissues rise 1.Chitin.......................... 346 from haploid, non-dikaryotic hyphae. This feature 2.Carbohydrates................... 346 clearly distinguishes fruiting-body formation in 3.Pigments ....................... 347 ascomycetes from that in basidiomycetous fungi, 4.CellWallProteins................. 347 in which dikaryotic hyphae are involved in both 5. Are Multiple Genes with Overlapping Functions Involved the meiotic cycle and fruiting-body formation inCellWallMetabolism?........... 348 (for review, see Moore 1998). Fruiting-body V. C o n c lu s i o n s .......................... 348 development in filamentous ascomycetes is a com- References........................... 348 plex cellular differentiation process that requires special environmental conditions and is controlled by many developmentally regulated genes. This chapter gives a concise overview on the basics of fruiting-body development in hyphal ascomycetes, 1 Lehrstuhl für Allgemeine und Molekulare Botanik, Ruhr-Univer- focusing on aspects relevant for taxonomy and sität Bochum, 44780 Bochum, Germany morphology, and it summarizes environmental The Mycota I Growth, Differentation and Sexuality Kües/Fischer (Eds.) © Springer-Verlag Berlin Heidelberg 2006 326 S. Pöggeler et al. as well as intrinsic signals influencing ascocarp ers), and divide mitotically in synchrony. The two formation. Finally, we highlight recent molec- nuclei remain in close association and undergo suc- ular genetic datasets from forward and reverse cessive divisions that result in dikaryotic cells (as- genetic approaches, which give further insight cogenous hyphae), in which each cell has two sexu- into presumptive signal transduction pathways ally compatible haploid nuclei. During the dikary- determining this multicellular differentiation otic phase, a dikaryotic mycelium grows within, process. and draws nourishment from, the haploid ascoma tissue. Inside the ultimate branches of the dikary- otic hyphae (the young asci), of which there may A. InductionofSexualDevelopment be millions in larger ascomata, fusion of the male and Fruiting-Body Morphology and female nucleus takes place. Immediately after karyogamy, the diploid nucleus of the zygote un- The sexual life cycle of ascomycetes can be ei- dergoes meiosis, which is in many species followed ther heterothallic (self-incompatible) or homothal- by a post-meiotic mitosis, resulting in the forma- lic (self-compatible). Heterothallic fungi exist in tionofeightnucleithatwillbecomeincorporated two mating types, designated, for example, A and into eight ascospores (see Zickler, Chap. 20, this a (or + and −), and mating occurs only between volume). sexual structures of opposite mating type. In a ho- Depending on the number of post-meiotic mi- mothallic fungus, every strain is able to complete toses and the degeneration of nuclei after meiosis, the sexual cycle without a mating partner. thenumberofascosporeswithinanascusvaries Sexual reproduction is typically controlled by between one and many thousands. The sizes and genes that reside in the mating-type locus. Mating shapes of ascospores and asci vary in a species- type-encoded proteins are putative transcription specific manner (Esser 1982; Alexopoulos et al. factors that are thought to act as transcriptional 1996). Based on light microscope studies, and ir- regulators on pheromone and pheromone recep- respective of size and shape, different types of asci tor genes (see Sect. III.C, and Debuchy and Tur- can be defined (Kirk et al. 2001). In a large number geon, Chap. 15, this volume). In most cases, the sin- of hyphal ascomycetes, the spores are discharged gle mating-type locus conferring mating behavior fromtheascus.Insidetheascoma(fruitingbody), consists of dissimilar DNA sequences (idiomorphs) the asci may be arranged in a scattered fashion or in the mating partners (Coppin et al. 1997; Kron- within a definite layer, which is called the hyme- stad and Staben 1997; Pöggeler 2001). nium. The first step in the sexual reproduction of Four major types of the multicellular asco- mycelial fungi is to combine two compatible nu- mata (fruiting bodies) can be distinguished: cleis- cleiinthesamecell.Thisoccursbyfusionofmor- tothecia, perithecia, apothecia and pseudothecia phologically similar or morphologically differenti- (Fig. 16.1). These produce the asci, and act as the ated gametangia, the male antheridia and female platformsfromwhichthemeiosporesarelaunched. ascogonia. In some species, the ascogonium is sur- The cleistothecium is a completely closed fruit- rounded by sterile hyphae to form a pre-fruiting ing body, whereas the perithecium is a more or body. It then bears a specialized hypha, the trichog- less closed, globose or flask-like fruiting body with yne, which receives the male nucleus. A functional a pore (ostiole) through which the ascospores es- male gamete may be a uninucleate spermatium cape. The apothecium is a cup- or saucer-like as- or microconidium or a multinucleate macroconid- coma in which the hymenium is exposed at ma- ium,whichcanbeformedonthemyceliumorin turity. In ascomycetes with a pseudothecium (or specialized structures called spermogonia. Subse- ascostroma), the fruiting body is initiated by the quenttocontactwithamalegamete,thetrichog- formation of a locule within a stroma, which is yne recruits a fertilizing nucleus from the male a matrix of vegetative hyphae, with or without tis- gamete, which migrates to the ascogonium (Bis- sue of a host. In contrast to cleistothecia, perithecia tis 1981). An alternative method of fertilization, and apothecia, the sexual organs of fungi produc- referred to as somatogamy, involves the fusion of ing pseudothecia are formed from hyphae already unspecialized somatic hyphae of two compatible within the developing ascocarp. In addition to asci, mycelia. Fertilization is not immediately followed many fruiting bodies contain sterile hyphae of var- by karyogamy. The nuclei migrate in pairs to the de- ious types that are important taxonomic charac- veloping, hook-shaped ascogenous hyphae (croiz- ters. Amongst these are paraphyses, elongated hy- Fruiting Bodies in Ascomycetes 327 Fig. 16.1. Fruiting bodies of fila- mentous ascomycetes phae originating from the base of an ascocarp, pe- pyrenomycetes Neurospora crassa and Sordaria riphyses, short unbranched hyphae in the ostiolar macrospora,andtheplectomyceteAspergillus canal of perithecia, and pseudoparaphyses, sterile nidulans, which will be described in detail in the hyphae originating above the level of asci in a pseu- following sections. However, molecular genetic dothecium (Alexopoulos et al. 1996). analyses of many other hyphal ascomycetes, Traditionally, fruiting-body morphology and including the pyrenomycetes Podospora anserina, the ascus structure have been used for a general Magnaporthe grisea and Cryphonectria parasitica taxonomic classification of the hyphal ascomycetes, as well as the loculoascomycete Cochliobolus which have thereby been grouped into four
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