“…The basic fruiting body morphology in Pezizomycotina is a cup‐like structure with asci oriented towards the concavity (apothecia). This basic body plan has become elaborated in many groups to form a bottle‐like (perithecia) or completely closed (cleistothecia) architecture (Liu & Hall, ; Schoch et al ., ; Kües et al ., ). Cleistothecia often act as both protective and dissemination structures.…”
Section: Cellular Complexitymentioning
confidence: 97%
“…This was confirmed with the discovery of sexual cycles in Penicillium (Houbraken, Frisvad & Samson, ) and Aspergillus (O'Gorman, Fuller & Dyer, ; Swilaiman et al ., ), widely studied fungi that were thought to be asexual for more than a century. Ascomata size is highly variable, ranging from less than a millimeter to several centimeters (Schmitt, ; Kües et al ., ). The relationships between phylogeny and fruiting body morphology are poorly understood in Pezizomycotina, although it is generally acknowledged that closed ascomatas (Pezizomycetes and lichen‐forming Lecanoromycetes) are derived forms (Liu & Hall, ; Schoch et al ., ; Schmitt, ).…”
Section: Cellular Complexitymentioning
confidence: 97%
“…Even in fungi that produce fruiting bodies, these structures are not indispensable for reproduction and dispersal, given the possibility to propagate asexually. Multicellular structures have evolved independently at least twice in fungi (Nguyen et al ., ; Kües et al ., ; Nagy et al ., ) and is only present in three lineages: Neolectomycetes, Pezizomycotina and Agaricomycetes.…”
The question of how phenotypic and genomic complexity are inter‐related and how they are shaped through evolution is a central question in biology that historically has been approached from the perspective of animals and plants. In recent years, however, fungi have emerged as a promising alternative system to address such questions. Key to their ecological success, fungi present a broad and diverse range of phenotypic traits. Fungal cells can adopt many different shapes, often within a single species, providing them with great adaptive potential. Fungal cellular organizations span from unicellular forms to complex, macroscopic multicellularity, with multiple transitions to higher or lower levels of cellular complexity occurring throughout the evolutionary history of fungi. Similarly, fungal genomes are very diverse in their architecture. Deep changes in genome organization can occur very quickly, and these phenomena are known to mediate rapid adaptations to environmental changes. Finally, the biochemical complexity of fungi is huge, particularly with regard to their secondary metabolites, chemical products that mediate many aspects of fungal biology, including ecological interactions. Herein, we explore how the interplay of these cellular, genomic and metabolic traits mediates the emergence of complex phenotypes, and how this complexity is shaped throughout the evolutionary history of Fungi.
“…The basic fruiting body morphology in Pezizomycotina is a cup‐like structure with asci oriented towards the concavity (apothecia). This basic body plan has become elaborated in many groups to form a bottle‐like (perithecia) or completely closed (cleistothecia) architecture (Liu & Hall, ; Schoch et al ., ; Kües et al ., ). Cleistothecia often act as both protective and dissemination structures.…”
Section: Cellular Complexitymentioning
confidence: 97%
“…This was confirmed with the discovery of sexual cycles in Penicillium (Houbraken, Frisvad & Samson, ) and Aspergillus (O'Gorman, Fuller & Dyer, ; Swilaiman et al ., ), widely studied fungi that were thought to be asexual for more than a century. Ascomata size is highly variable, ranging from less than a millimeter to several centimeters (Schmitt, ; Kües et al ., ). The relationships between phylogeny and fruiting body morphology are poorly understood in Pezizomycotina, although it is generally acknowledged that closed ascomatas (Pezizomycetes and lichen‐forming Lecanoromycetes) are derived forms (Liu & Hall, ; Schoch et al ., ; Schmitt, ).…”
Section: Cellular Complexitymentioning
confidence: 97%
“…Even in fungi that produce fruiting bodies, these structures are not indispensable for reproduction and dispersal, given the possibility to propagate asexually. Multicellular structures have evolved independently at least twice in fungi (Nguyen et al ., ; Kües et al ., ; Nagy et al ., ) and is only present in three lineages: Neolectomycetes, Pezizomycotina and Agaricomycetes.…”
The question of how phenotypic and genomic complexity are inter‐related and how they are shaped through evolution is a central question in biology that historically has been approached from the perspective of animals and plants. In recent years, however, fungi have emerged as a promising alternative system to address such questions. Key to their ecological success, fungi present a broad and diverse range of phenotypic traits. Fungal cells can adopt many different shapes, often within a single species, providing them with great adaptive potential. Fungal cellular organizations span from unicellular forms to complex, macroscopic multicellularity, with multiple transitions to higher or lower levels of cellular complexity occurring throughout the evolutionary history of fungi. Similarly, fungal genomes are very diverse in their architecture. Deep changes in genome organization can occur very quickly, and these phenomena are known to mediate rapid adaptations to environmental changes. Finally, the biochemical complexity of fungi is huge, particularly with regard to their secondary metabolites, chemical products that mediate many aspects of fungal biology, including ecological interactions. Herein, we explore how the interplay of these cellular, genomic and metabolic traits mediates the emergence of complex phenotypes, and how this complexity is shaped throughout the evolutionary history of Fungi.
“…Hyphae might have also facilitated the transition of fungi to terrestrial life, by bridging nutrient-rich and nutrient-poor habitats 23 and confer immense medical relevance to pathogenic species 24 . Hyphae of extant fungi rarely stick to each other in vegetative mycelia and adhesion becomes key only in fruiting bodies 25,26 —which, in terms of complexity level, resemble multicellular metazoans and plants 7,27 —or in the attachment to host surfaces 28 . Thus, whereas in most multicellular lineages adhesion, cell–cell cooperation, communication and differentiation represent the main hurdles to the emergence of multicellular precursors 3,6,29,30 , fungi might have had different obstacles to overcome.…”
Hyphae represent a hallmark structure of multicellular fungi. The evolutionary origins of hyphae and of the underlying genes are, however, hardly known. By systematically analyzing 72 complete genomes, we here show that hyphae evolved early in fungal evolution probably via diverse genetic changes, including co-option and exaptation of ancient eukaryotic (e.g. phagocytosis-related) genes, the origin of new gene families, gene duplications and alterations of gene structure, among others. Contrary to most multicellular lineages, the origin of filamentous fungi did not correlate with expansions of kinases, receptors or adhesive proteins. Co-option was probably the dominant mechanism for recruiting genes for hypha morphogenesis, while gene duplication was apparently less prevalent, except in transcriptional regulators and cell wall - related genes. We identified 414 novel gene families that show correlated evolution with hyphae and that may have contributed to its evolution. Our results suggest that hyphae represent a unique multicellular organization that evolved by limited fungal-specific innovations and gene duplication but pervasive co-option and modification of ancient eukaryotic functions.
“…These Principles form the warp and weft of the canvas upon which fungal developmental biology has been built by the cell and molecular biologists of the pre-genomics era. It is now up to the genomic systems analysts to paint the rest of the individual details of the stories on that canvas (Kües & Navarro-González, 2015;Kües et al, 2018;Halbwachs et al, 2016;Pelkmans et al, 2016;Hibbett et al, 2017;Stajich, 2017).…”
Section: Basic Principles Of Fungal Developmental Biologymentioning
We review the most recent developments in understanding the nature of development and morphogenesis in fungi and suggest how it might be applied to biotechnological manipulation of some cultivated mushrooms. We believe that it is essential to match the deductions of the molecular observations of the genomics generation with the inductive reasoning of the in vivo experiments and observations of the pregenomics generations to take full advantage of the synergism between the approaches to illuminate better the living biology of the system. As specific examples we show how model mushroom fungi (Coprinopsis and Volvariella) make hymenia and gills (not forgetting how the polypore Phellinus makes tubes), developmental commitment and pattern formation. The Coprinopsis sporophore also provides examples for the construction of mushroom stems and the coordination of cell behaviour throughout the maturing sporophore and the timing process that achieves that. This leads us to consider the mechanics of the mushroom and its dependence on the biochemistry and regulation of metabolism in relation to morphogenesis, and how it varies between species. We finish with our summary of the basic principles of fungal developmental biology. Having demonstrated how classic approaches allowed progress to be made in the study of fungal development we show how this has been accelerated by genomics and other aspects of global analysis of macromolecules. We also include work on some cultivated mushrooms to illustrate how the generalisations from research on model organisms might be applied in mushroom farming.
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