Six Key Traits of Fungi: Their Evolutionary Origins and Genetic Bases LÁSZLÓ G. NAGY,1 RENÁTA TÓTH,2 ENIKŐ KISS,1 JASON SLOT,3 ATTILA GÁCSER,2 and GÁBOR M. KOVÁCS4,5 1Synthetic and Systems Biology Unit, Institute of Biochemistry, HAS, Szeged, Hungary; 2Department of Microbiology, University of Szeged, Szeged, Hungary; 3Department of Plant Pathology, Ohio State University, Columbus, OH 43210; 4Department of Plant Anatomy, Institute of Biology, Eötvös Loránd University, Budapest, Hungary; 5Plant Protection Institute, Center for Agricultural Research, Hungarian Academy of Sciences, Budapest, Hungary ABSTRACT The fungal lineage is one of the three large provides an overview of some of the most important eukaryotic lineages that dominate terrestrial ecosystems. fungal traits, how they evolve, and what major genes They share a common ancestor with animals in the eukaryotic and gene families contribute to their development. The supergroup Opisthokonta and have a deeper common ancestry traits highlighted here represent just a sample of the with plants, yet several phenotypes, such as morphological, physiological, or nutritional traits, make them unique among characteristics that have evolved in fungi, including po- all living organisms. This article provides an overview of some of larized multicellular growth, fruiting body development, the most important fungal traits, how they evolve, and what dimorphism, secondary metabolism, wood decay, and major genes and gene families contribute to their development. mycorrhizae. However, a great deal of other important The traits highlighted here represent just a sample of the traits also underlie the evolution of the taxonomically characteristics that have evolved in fungi, including polarized and phenotypically hyperdiverse fungal kingdom, which multicellular growth, fruiting body development, dimorphism, could fill up a volume on its own. After reviewing the secondary metabolism, wood decay, and mycorrhizae. However, a great number of other important traits also evolution of these six well-studied traits in fungi, we underlie the evolution of the taxonomically and phenotypically discuss how the recurrent evolution of phenotypic sim- hyperdiverse fungal kingdom, which could fill up a volume on its ilarity, that is, convergent evolution in the broad sense, own. After reviewing the evolution of these six well-studied traits has shaped their phylogenetic distribution in extant in fungi, we discuss how the recurrent evolution of phenotypic species. similarity, that is, convergent evolution in the broad sense, has shaped their phylogenetic distribution in extant species. Received: 29 November 2016, Accepted: 31 May 2017, Published: 18 August 2017 INTRODUCTION Editors: Joseph Heitman, Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710; The fungal lineage is one of the three large eukaryotic Neil A. R. Gow, School of Medical Sciences, University of Aberdeen, lineages that dominate terrestrial ecosystems. They share Fosterhill, Aberdeen, AB25 2ZD, United Kingdom Citation: Nagy LG, Tóth R, Kiss E, Slot J, Gácser A, Kovács GM. 2017. a common ancestor with animals in the eukaryotic Six key traits of fungi: their evolutionary origins and genetic bases. supergroup Opisthokonta and have a deeper common Microbiol Spectrum 5(4):FUNK-0036-2016. doi:10.1128 ancestry with plants, yet several phenotypes such as /microbiolspec.FUNK-0036-2016. morphological, physiological, or nutritional traits make Correspondence: László Nagy, [email protected] © 2017 American Society for Microbiology. All rights reserved. them unique among all living organisms. This article ASMscience.org/MicrobiolSpectrum 1 Downloaded from www.asmscience.org by IP: 141.211.4.224 On: Fri, 01 Sep 2017 17:47:38 Nagy et al. THE EVOLUTION AND DE-EVOLUTION Mucoromycota mucoralean fungi such as the bread OF MULTICELLULARITY mold Rhizopus stolonifer. Early filamentous species Multicellular life dominates most ecosystems on Earth, have relatively simple, little-differentiated mycelia of and its evolution is considered to be one of the major tube-like cells that are not (or are minimally) compart- transitions in the history of life. Multicellularity confers mentalized by septa. More derived fungi evolved vari- several competitive advantages. Among others, it allows ous solutions to block the free diffusion of materials the division of labor between cells, increased size and in hyphae, which would also minimize the risk of the complexity, a longer life span, or an advantage in avoid- free passage of external invaders (5). Specialized struc- ing predation. It has been estimated that multicellularity tures around septa, including Woronin bodies and the evolved in some form 25 to 30 times both in the pro- dolipore septum among others, serve to regulate trans- karyotes and the eukaryotes, but most of those lineages port between cells in the hyphae of Asco- and Basidio- are simple aggregates or colonies of cells that show little mycota, respectively, although exceptions to this rule phenotypic or functional differentiation. Fungi repre- exist. Neolecta vitellina, a basal ascomycete (Taphrino- sent one of the few lineages that have achieved higher mycotina), produces crystalline bodies analogous to levels of multicellular complexity. Like animals and Woronin bodies but which are of vacuolar origin and plants, fungi evolved integrated multicellular structures only loosely bound to the membrane (6). Although struc- that enable them to adapt to diverse ecological niches. turally different, all three solutions provide the means However, unlike animals and plants, fungi evolved to finely coordinate the transport of goods and to block complex multicellularity through filamentous inter- the diffusion of organelles from one cell to the other. mediate stages. Fungal filaments (hyphae), unlike fila- mentous forms in other lineages, develop by polarized Polarized Growth and the apical growth, and individual cells are divided from Underlying Cellular Components the elongating hypha by developing cross-walls (septa), Polarized hyphal growth of fungi is a unique innova- a unique solution for filamentous growth seen mostly tion in the history of life, with similar solutions seen in higher fungi (1). Hyphae have been hypothesized to only in a few other groups such as Oomycota and the have emerged through gradual elongation of substrate- pollen tubes of seed plants and axons of some neurons. anchoring rhizoids of ancestral unicellular fungi such as The orchestration of hyphal growth involves several chytrids (2). cellular pathways and entailed the evolution of several Similar, apically growing hyphae have evolved in the novel traits, including the establishment of polarity, Oomycetes (Stramenopila), but oomycete hyphae are apical extension, the coordinated transport of mate- not septate, allowing the transport of compounds and rial to the sites of active growth, the establishment of organelles along the hyphae. Such aseptate hyphae are a branching, and septation patterns. In hyphae, growth multinucleate, coenocytic architecture, similar to hyphae occurs in the apical zone, coincident with a strong gra- of early-diverging fungal groups (e.g., Mucoromycota). dient of cell wall material deposition toward the tip. Within fungi, hyphae evolved convergently in multiple Apical growth is achieved by the expansion of the hy- groups (Fig. 1A,B), one of them comprising most of the phal tip, which is predominantly driven by turgor pres- well-known filamentous fungi. Other hyphal groups sure within the cell that, in turn, is regulated by the include the Monoblepharidomycetes, an early-diverging osmotic mitogen-activated protein kinase cascade (7). lineage of aquatic fungi in which several species have Cell wall materials are transported by secretory vesi- switched to filamentous growth (3), and certain chytrid- cles to the growing tip along cytoskeletal structures (7). like fungi. One of the core signal transduction pathways connected Fungal mycelia—intricate branching networks of to polarity establishment is the Ras/Rho GTPase path- hyphae—are adapted to efficiently explore the available way described in Saccharomyces cerevisiae, which is space in the substrate. Foraging for nutrients may have also conserved in filamentous fungi. This pathway is driven the emergence of multicellularity in fungi, al- responsible for polarity establishment and maintenance though transition to terrestrial habitats and exploitation by the formation of a stable polarity axis that specifies of prokaryotic biofilms have also been proposed as the the site of germ tube emergence. This positional infor- necessary selection pressures for their emergence (4). mation is generated by the recruitment of cell polarity The first multicellular hyphae evolved in the common proteins (Bud4, Axl2, swoC in Aspergillus nidulans)at ancestor of the Zoopagomycota, Mucoromycota, and the site of polarized growth (8) and then is transduced the Dikarya and were probably similar to those of extant via regulatory Rho GTPases (RacA A. nidulans, CDC42 2 ASMscience.org/MicrobiolSpectrum Downloaded from www.asmscience.org by IP: 141.211.4.224 On: Fri, 01 Sep 2017 17:47:38 Six Key Traits of Fungi: Evolutionary Origins and Genetic Bases FIGURE 1 Overview of the phylogenetic distribution of the traits presented in this article. (A) Phylogeny of the major fungal groups and the phylogenetic distribution of the traits discussed in this article. Tree modified and redrawn from MycoCosm (http://genome.jgi.doe.gov/programs/fungi/index.jsf).