Sexual attraction: on the role of fungal pheromone/receptor systems (A review)

Pheromones have been detected in all fungal phylogenetic lineages. This came as a surprise, as the general role of pheromones in mate attraction was not envisioned for some fungi. Pheromones and pheromone receptor genes have been identified, however, in members of all true fungal lineages, and even for mycelia forming organisms of plant and amoeba lineages, like oomycetes and myxomycetes. The mating systems and genes governing the mating type are different in fungi, ranging from bipolar with two opposite mating types to tetrapolar mating systems (with four possible mating outcomes, only one of which leads to fertile sexual development) in homobasidioymcetes with more than 23,000 mating types occurring in nature. Pheromones and receptors specifically recognizing these pheromones have evolved with slightly different functions in these different systems. This review is dedicated to follow the evolution of pheromone/receptor systems from simple, biallelic bipolar systems to multiallelic, tetrapolar versions and to explain the slightly different functions the pheromone recognition and subsequent signal transduction cascades within the fungal kingdom. The biotechnological implications of a detailed understanding of mating systems for biological control and plant protection, in medicine, and in mushroom breeding are discussed.     

Having sex,yes, but with whom? Inferences from fungi on the evolution of anisogamy and mating types

The advantage of sex has been among the most debated issues in biology. Surprisingly, the question of why sexual reproduction generally requires the combination of distinct gamete classes, such as small and large gametes, or gametes with different mating types, has been much less investigated. Why do systems with alternative gamete classes (i.e. systems with either anisogamy or mating types or both) appear even though they restrict the probability of finding a compatible mating partner? Why does the number of gamete classes vary from zero to thousands, with most often only two classes? We review here the hypotheses proposed to explain the origin, maintenance, number, and loss of gamete classes. We argue that fungi represent highly suitable models to help resolve issues related to the evolution of distinct gamete classes, because the number of mating types vary from zero to thousands across taxa, anisogamy is present or not, and because there are frequent transitions between these conditions. We review the nature and number of gamete classes in fungi, and we attempt to draw inferences from these data on the evolutionary forces responsible for their appearance, loss or maintenance, and number.     

Sex in fungi: lessons of gene regulation

Fungi have been very useful for gene regulation studies. Mating implicates in a series of events influenced by many types of environmental input that are interpreted into regulatory pathways, including signal transduction. Although various aspects of mating and signal transduction in the yeast Saccharomyces cerevisiae have long been characterized, recent findings in filamentous fungi indicate that pheromones and pheromone receptors may be essential for mating partner recognition and also for nucleus recognition in sorting before meiosis. A brief overview on mating-type genes of ascomycete fungi and recent contributions to the understanding of their role in the regulation of multicellularity and sexual dimorphism is presented in this review.     

Lymphokine signal transduction

Lymphokines are a group of signalling molecules involved in communication between cells, mainly those of the immune system. The lymphokines are multi-functional and most of them have mitogenic or co-mitogenic activity. An understanding of lymphokine biology is essential to understand how the immune system develops and functions and to provide a rationale for their use in immunotherapy.The potential to understand the cell biology of the lymphokines has recently become more apparent as molecular biological techniques have first of all produced recombinant factors and secondly have provided clues to the signal transduction pathways by cloning receptors, applying site-directed mutational analysis and also probing for specific promoters and enhancers that are activated along the signal pathway.This review discusses the information that has come from these recent analyses which blends with the biochemical analysis of the second messenger systems in an effort to understand the signalling pathways of the lymphokines.     

真菌有性生殖调控与进化

以真菌为对象的有性生殖机制研究揭示了普遍存在于真核生物中的生物学现象及规律,包括染色体倍性变化、减数分裂形成配子、交配对象识别及细胞一细胞融合形成合子等．真菌的有性生殖由交配型位点控制,除了类似其他真核生物两性生殖的异宗配合外,还包括同宗配合和次级同宗配合,部分物种的单倍体还具有交配型互换的能力．互补交配型的单倍体通过荷尔蒙及其受体进行相互识别,再经过G蛋白偶联受体介导的信号途径调控有性生殖过程及子实体发育,这一过程受多种胞内调控因子及外界环境条件的影响．不同真菌类群生殖方式的演化与物种进化仍缺少统一的规律．进一步研究揭示,真菌有性生殖的调控机制及环境诱导因子,不仅具有重要的理论意义,也有利于促进不同经济真菌子实体的人工培养及高效利用．     

Capability of polychlorinated biophenyl (PCBs) degrading fungi segregated from sediments

Four strains of fungi isolated from the sediments of badly contaminated Li-Cun River were studied to investigate their ability to remove 6 target PCBs with and without sodium dodecyl sulfate as the surfactant. Having different viability at different conditions, these four fungi all showed relatively better PCB degradation capability and higher efficiency for total PCB removal in the absence of the ligninolytic enzymes. The findings that chloride concentration changes and some acids are generated as the metabolic products contribute to our understanding of PCBs degradation pathways. Combinations of different PCB concentrations and fresh fungi weight inoculated were attempted to achieve maximum efficiency. After the bio-treatment, the concentrations of PCBs are significantly reduced with the chloride ion concentration increasing slightly. Not only in the PCB degradation process but also in the total PCB removed did these four fungi show high capability, but no apparent effect of SDS on the performance of the fungi is found.     

Sex, outcrossing and mating types: unsolved questions in fungi and beyond

Variability in the way organisms reproduce raises numerous, and still unsolved, questions in evolutionary biology. In this study, we emphasize that fungi deserve a much greater emphasis in efforts to address these questions because of their multiple advantages as model eukaryotes. A tremendous diversity of reproductive modes and mating systems can be found in fungi, with many evolutionary transitions among closely related species. In addition, fungi show some peculiarities in their mating systems that have received little attention so far, despite the potential for providing insights into important evolutionary questions. In particular, selfing can occur at the haploid stage in addition to the diploid stage in many fungi, which is generally not possible in animals and plants but has a dramatic influence upon the structure of genetic systems. Fungi also present several advantages that make them tractable models for studies in experimental evolution. Here, we briefly review the unsolved questions and extant hypotheses about the evolution and maintenance of asexual vs. sexual reproduction and of selfing vs. outcrossing, focusing on fungal life cycles. We then propose how fungi can be used to address these long-standing questions and advance our understanding of sexual reproduction and mating systems across all eukaryotes.     

The RAM network in pathogenic fungi

The regulation of Ace2 and morphogenesis (RAM) network is a protein kinase signaling pathway conserved among eukaryotes from yeasts to humans. Among fungi, the RAM network has been most extensively studied in the model yeast Saccharomyces cerevisiae and has been shown to regulate a range of cellular processes, including daughter cell-specific gene expression, cell cycle regulation, cell separation, mating, polarized growth, maintenance of cell wall integrity, and stress signaling. Increasing numbers of recent studies on the role of the RAM network in pathogenic fungal species have revealed that this network also plays an important role in the biology and pathogenesis of these organisms. In addition to providing a brief overview of the RAM network in S. cerevisiae, we summarize recent developments in the understanding of RAM network function in the human fungal pathogens Candida albicans, Candida glabrata, Cryptococcus neoformans, Aspergillus fumigatus, and Pneumocystis spp.     

Orchestration of sexual reproduction and virulence by the fungal mating-type locus

The mating-type locus (MAT) orchestrates sexual reproduction in fungi. Sexual reproduction is related not only to fitness of an organism, but also correlated with virulence in certain pathogens. In the dandruff-associated fungus Malassesia globosa, although the sexual cycle remains to be discovered, whole genome analysis has led to the hypothesis that mating may occur on host skin. Furthermore, the MAT locus of M. globosa and U. hordei provides evidence that transitions between tetrapolar and bipolar systems have independently occurred. These results, together with studies recapitulating the ancestral tetrapolar mating system in Cryptococcus and the structure of MAT in related smut fungi, have furthered understanding on transitions between different mating systems and the evolution of MAT in the Basidiomycota.     

The evolution of mating type switching

Predictions about the evolution of sex determination mechanisms have mainly focused on animals and plants, whereas unicellular eukaryotes such as fungi and ciliates have received little attention. Many taxa within the latter groups can stochastically switch their mating type identity during vegetative growth. Here, we investigate the hypothesis that mating type switching overcomes distortions in the distribution of mating types due to drift during asexual growth. Using a computational model, we show that smaller population size, longer vegetative periods and more mating types lead to greater distortions in the distribution of mating types. However, the impact of these parameters on optimal switching rates is not straightforward. We find that longer vegetative periods cause reductions and considerable fluctuations in the switching rate over time. Smaller population size increases the strength of selection for switching but has little impact on the switching rate itself. The number of mating types decreases switching rates when gametes can freely sample each other, but increases switching rates when there is selection for speedy mating. We discuss our results in light of empirical work and propose new experiments that could further our understanding of sexuality in isogamous eukaryotes.     

Males,but not females,mate with multiple partners: a laboratory study of a primitively eusocial wasp <Emphasis Type="Italic">Ropalidia marginata</Emphasis>

The intense interest in social Hymenoptera, on account of their elaborate sociality and the paradox of altruism, has often suffered from considerable gender imbalance. This is partly due to the fact that worker behaviour and altruism are restricted to the females and partly because males often live off the nest. Yet, understanding the males, especially in the context of mating biology is essential even for understanding the evolution of sociality. Mating patterns have a direct bearing on the levels of intra-colony genetic relatedness, which in turn, along with the associated costs and benefits of worker behaviour, are central to our understanding of the evolution of sociality. Although mating takes place away from the nest in natural colonies of the primitively eusocial wasp Ropalidia marginata, mating can be observed in the laboratory if a male and a female are placed in a transparent, aerated plastic container, and both wasps are in the range of 5–20 days of age. Here, we use this setup and show that males, but not females, mate serially with multiple partners. The multiple mating behaviour of the males is not surprising because in nature males have to mate with a number of females, only a few of whom will go on to lay eggs. The reluctance of R. marginata females to mate with multiple partners is consistent with the expectation of monogamy in primitively eusocial species with totipotent females, although the apparent discrepancy with a previous work with allozyme markers in natural colonies suggesting that females may sometimes mate with two or three different males remains to be resolved.     

The a and b loci of Ustilago maydis hybridize with DNA sequences from other smut fungi.

The smut fungi are obligately parasitic during the sexual phase of their life cycle, and the mating-type genes of these fungi play key roles in both sexual development and pathogenicity. Among species of smut fungi it is common to find a bipolar mating system in which one locus with two alternate alleles is believed to control cell fusion and establishment of the infectious cell type. Alternatively, several species have a tetrapolar mating system in which two different genetic loci, one of which has multiple alleles, control fusion and subsequent development of the infection hyphae. Cloned sequences from the a and b mating-type loci of the tetrapolar smut fungus Ustilago maydis were used as hybridization probes to DNAs from 23 different fungal strains, including smut fungi with both tetrapolar and bipolar mating systems. In general, all of the smut fungi hybridized with the mating-type genes from U. maydis, suggesting conservation of the sequences involved in mating interactions. A selection of DNAs from other ascomycete and basidiomycete fungi failed to hybridize with the U. maydis mating-type sequences. Exceptions to this finding include hybridization of DNA from the a1 idiomorph of U. maydis to DNA from one strain of U. violacea and hybridization of both a idiomorphs to DNA from Saccharomyces cerevisiae.     

Sexual selection in fungi

The significance of sexual selection, the component of natural selection associated with variation in mating success, is well established for the evolution of animals and plants, but not for the evolution of fungi. Even though fungi do not have separate sexes, most filamentous fungi mate in a hermaphroditic fashion, with distinct sex roles, that is, investment in large gametes (female role) and fertilization by other small gametes (male role). Fungi compete to fertilize, analogous to ‘male‐male’ competition, whereas they can be selective when being fertilized, analogous to female choice. Mating types, which determine genetic compatibility among fungal gametes, are important for sexual selection in two respects. First, genes at the mating‐type loci regulate different aspects of mating and thus can be subject to sexual selection. Second, for sexual selection, not only the two sexes (or sex roles) but also the mating types can form the classes, the members of which compete for access to members of the other class. This is significant if mating‐type gene products are costly, thus signalling genetic quality according to Zahavi's handicap principle. We propose that sexual selection explains various fungal characteristics such as the observed high redundancy of pheromones at the B mating‐type locus of Agaricomycotina, the occurrence of multiple types of spores in Ascomycotina or the strong pheromone signalling in yeasts. Furthermore, we argue that fungi are good model systems to experimentally study fundamental aspects of sexual selection, due to their fast generation times and high diversity of life cycles and mating systems.     

Integrated morphodynamic signalling of the mammary gland

The mammary gland undergoes a spectacular series of changes as it develops, and maintains a remarkable capacity to remodel and regenerate for several decades. Mammary morphogenesis has been investigated for over 100 years, motivated by the dairy industry and cancer biologists. Over the past decade, the gland has emerged as a major model system in its own right for understanding the cell biology of tissue morphogenesis. Multiple signalling pathways from several cell types are orchestrated together with mechanical cues and cell rearrangements to establish the pattern of the mammary gland. The integrated mechanical and molecular pathways that control mammary morphogenesis have implications for the developmental regulation of other epithelial organs.     

Patterning mechanisms and morphological diversity of spider appendages and their importance for spider evolution

The prosoma of spiders bears different gnathal (labrum, chelicerae, pedipalps) and locomotory appendages (legs). In most species these appendages are also used for additional functions, e.g. sensing, mating, and courtship. The opisthosoma is equipped with four pairs of highly specialized appendages. Two pairs of spinnerets are used for silk production and manipulation. The other two pairs of appendages are internalized during development and give rise to a complex respiratory system of book lungs and tracheae. Thus spiders have a number of different appendage types with radically different adult morphologies. Furthermore, all these appendage types display significant additional species specific diversity correlating with a large spectrum of functions of the appendages. Despite this importance of appendage diversity for the evolution of the spiders we know relatively little about the genetic patterning mechanisms producing this diversity of morphology. We review recent advances concerning the developmental genetics of spider appendage diversification, mainly concentrating on open questions and future directions of research. We conclude that the deeper understanding of appendage development and diversity in spiders can contribute significantly not only to evolutionary developmental biology, but also to behavioral biology, speciation research and population genetics, and the study of sexually dimorphic traits.     

Guides to the final frontier of the cytoskeleton: septins in filamentous fungi

Recent investigations have established core principles by which septins can form non-polar filaments in vitro. How cells then assemble, regulate and use septin polymers is still only beginning to be understood. It is clear that there is plasticity and variability in septin organization across diverse species and cell types. Work in the filamentous fungi has been invaluable in discovering this variation in form and function. In particular filamentous fungi display many forms of higher order septin structures and study of septins in these systems has led to insights into septin assembly, dynamics and regulation. Importantly in many cases work in these alternative systems reveal differences to how septins may be organized, functioning or regulated in Saccharomyces cerevisiae. Here I review the novel aspects of septin biology found in filamentous fungi and raise many open questions about these enigmatic polymers that should guide future study.     

Regulating the reapers: activating metacaspases for programmed cell death

Research during the past two decades has revealed that specialized cysteine proteases act as conserved initiators or executioners for programmed cell death (PCD) in eukaryotes. Caspases were first identified as common regulators of PCD in metazoans, whereas the role of metacaspases (MCs) as regulators of cellular suicide in plants has only been shown genetically in the past several years. Together with recent biochemical and molecular characterizations of some of the representative MCs from different model systems, multiple mechanisms that can mediate the post-translational regulation of these proteases are beginning to emerge. Further elucidation of these regulatory pathways and definition of the downstream degradomes targeted by MCs should lead to a better understanding of cell death control in plants, protozoans, and fungi.