Lipid biology in fungal stress and virulence: Entomopathogenic fungi

Broad host range insect pathogenic fungi penetrate through the host cuticle, necessitating an ability to confront and overcome surface lipids and other molecules that often include antimicrobial compounds. In this context, induction of lipid assimilatory pathways by exogenous substrates is crucial for successful infection to occur, and lipid growth substrates can have significant effects on the virulence of fungal infectious propagules, e.g. conidia. The production of lipases is a critical part of the cuticle-degrading repertoire and pathways involved in triglyceride metabolism and phospholipid homeostasis have been shown to contribute to host invasion. Mobilization of endogenous lipid stores via the activities of the caleosin and perilipin lipid storage-turnover proteins, have been linked to diverse processes including formation of penetration structures, e.g. germ tubes and appressoria, spore properties and dispersal, and the ability to respond to lipid growth substrates and virulence. Here, we summarize recent advances in our understanding of lipid assimilation and mobilization pathways in the ability of entomogenous fungi to infect and use host substrates. Host surface and internal lipids can alternatively act as antifungal barriers, inducers of pathogenesis-related pathways, and/or as fungal growth substrates. Lipids and lipid assimilation can be considered as forming a co-evolutionary web between the insect host and entomogenous fungi.     

Role of accelerated style senescence in pathogen defense

Plants, like animals, suffer from a variety of diseases that are transmitted via their sexual organs. In many species, the flowers senesce rapidly after pollination or fertilization. In ongoing studies of the impacts of a transposon insertional mutation in the gene that encodes the most abundant isoform of a major group-1 pollen allergen of maize, we found that pollen tubes with the mutant allele grow significantly slower in vivo than pollen with the wild-type allele. Here, we report that under field conditions, maize silks (styles) pollinated with pollen bearing the slower-growing mutant allele take significantly longer to senesce, and the resulting ears (infructescences) have dramatically higher incidence of "fungal ear rot" disease than silks pollinated with pollen bearing the wild-type allele. Because ear rot fungi gain access to the developing ear by growing on and through the silks, we propose that accelerated senescence of silks after fertilization is a defense against pathogens such as those causing ear rot. In addition, we divided the silks on each ear into two halves and experimentally varied the type of pollen (wild type, mutant, unpollinated) that was placed onto each half of the silks. Senescence of unpollinated silks was accelerated when ovaries on the other half of the ear were fertilized.     

The evolution of mimicry under constraints

The resemblance between mimetic organisms and their models varies from near perfect to very crude. One possible explanation, which has received surprisingly little attention, is that evolution can improve mimicry only at some cost to the mimetic organism. In this article, an evolutionary game theory model of mimicry is presented that incorporates such constraints. The model generates novel and testable predictions. First, Batesian mimics that are very common and/or mimic very weakly defended models should evolve either inaccurate mimicry (by stabilizing selection) or mimetic polymorphism. Second, Batesian mimics that are very common and/or mimic very weakly defended models are more likely to evolve mimetic polymorphism if they encounter predators at high rates and/or are bad at evading predator attacks. The model also examines how cognitive constraints acting on signal receivers may help determine evolutionarily stable levels of mimicry. Surprisingly, improved discrimination abilities among signal receivers may sometimes select for less accurate mimicry.     

食线虫真菌资源研究概况

食线虫真菌是指寄生、捕捉、定殖和毒害线虫的一类真菌,这类真菌是自然界中线虫种群控制的重要因子,也是动植物病害生物防治的重要研究材料,具有特殊的研究意义和经济价值。目前全世界共报道700余种食线虫真菌,包括捕食线虫真菌380余种,线虫内寄生真菌120余种,产毒真菌270余种和大量机会真菌。针对丰富的食线虫真菌资源,近年来世界各国尤其是中国科学家对其进行了广泛研究,在捕食线虫真菌资源的分类、系统进化、生态分布、有性无性联系等方面的研究取得了重要进展,在线虫内寄生真菌侵染宿主的方式及产毒真菌的次生代谢产物挖掘等方面也进行了广泛研究,文章综述了以上研究进展并简述了食线虫真菌资源的生物防治应用概况。     

Perspectives and Debates: Mimicry,Signalling and Co‐Evolution (Commentary on Wolfgang Wickler – Understanding Mimicry – With special reference to vocal mimicry)

In his stimulating discussion, Wolfgang Wickler criticizes fuzzy usage of term mimicry by drawing attention to its original definition by H. Bates. Mimicry refers to functional ‘model–mimic–selecting agent’ trinity (with varying number of species involved) when the selecting agent (i.e. signal receiver) responds similarly to mimic and model to the advantage of the mimic. Concurring with Wickler I argue that convergence is neither necessary nor sufficient to support similarity as evidence for mimicry and that it is artificial and unproductive to classify mimicry with respect to ontogeny (innate vs. learned similarity) or model species identity (learning from conspecifics vs. heterospecifics). Using butterfly ‘eye’‐spots, I argue that just identifying each of the supposed model, the mimic and the selective agent, and even demonstrating that mimic‐model similarity affects the agent's behaviour, provides no conclusive evidence for mimicry. Even a demonstration that the mimic benefits from receiver response may not provide conclusive evidence for mimicry. Using avian brood parasite–host egg and nestling mimicry, I emphasize that without experimental manipulation of the hypothesized mimetic traits, it is impossible to test the mimicry hypothesis robustly. Due to fundamental constraints on human perception, some cases of mimicry may in fact be just a by‐product of human inability to perceive relevant differences between animal phenotypes (what is similar for human eye, nose or ear may not be viewed, smelled or heard as similar for relevant animal observers), whereas many cases of real mimicry may escape our attention from the same reason (‘hidden’ mimicry). Surprisingly, the same mimetic phenotype may show completely different effects on selective agents under different ecological circumstances. Finally, relatively dissimilar species may be more mimetic than highly similar model–mimic pairs because mimicry may be more fruitfully understood as a co‐evolutionary process rather than a similarity.     

C and N stable isotope signatures reveal constraints to nutritional modes in orchids from the Mediterranean and Macaronesia

We compared the nutritional modes and habitats of orchids (e.g., autotrophic, partially or fully mycoheterotrophic) of the Mediterranean region and adjacent islands of Macaronesia. We hypothesized that ecological factors (e.g., relative light availability, surrounding vegetation) determine the nutritional modes of orchids and thus impose restrictions upon orchid distribution. Covering habitats from dark forests to open sites, orchid samples of 35 species from 14 genera were collected from 20 locations in the Mediterranean and Macaronesia to test for mycoheterotrophy. Mycorrhizal fungi were identified via molecular analyses, and stable isotope analyses were applied to test whether organic nutrients are gained from the fungal associates. Our results show that orchids with partial or full mycoheterotrophy among the investigated species are found exclusively in Neottieae thriving in light-limited forests. Neottioid orchids are missing in Macaronesia, possibly because mycoheterotrophy is constrained by the lack of suitable ectomycorrhizal fungi. Furthermore, most adult orchids of open habitats in the Mediterranean and Macaronesia show weak or no N gains from fungi and no C gain through mycoheterotrophy. Instead isotope signatures of some of these species indicate net plant-to-fungus C transfer.     

Termite-egg mimicry by a sclerotium-forming fungus

Mimicry has evolved in a wide range of organisms and encompasses diverse tactics for defence, foraging, pollination and social parasitism. Here, I report an extraordinary case of egg mimicry by a fungus, whereby the fungus gains competitor-free habitat in termite nests. Brown fungal balls, called 'termite balls', are frequently found in egg piles of Reticulitermes termites. Phylogenetic analysis illustrated that termite-ball fungi isolated from different hosts (Reticulitermes speratus, Reticulitermes flavipes and Reticulitermes virginicus) were all very similar, with no significant molecular differences among host species or geographical locations. I found no significant effect of termite balls on egg survivorship. The termite-ball fungus rarely kills termite eggs in natural colonies. Even a termite species (Reticulitermes okinawanus) with no natural association with the fungus tended termite balls along with its eggs when it was experimentally provided with termite balls. Dummy-egg bioassays using glass beads showed that both morphological and chemical camouflage were necessary to induce tending by termites. Termites almost exclusively tended termite balls with diameters that exactly matched their egg size. Moreover, scanning electron microscopic observations revealed sophisticated mimicry of the smooth surface texture of eggs. These results provide clear evidence that this interaction is beneficial only for the fungus, i.e. termite balls parasitically mimic termite eggs.     

Common and contrasting themes in host cell-targeted effectors from bacterial,fungal, oomycete and nematode plant symbionts described using the Gene Ontology

A wide diversity of plant-associated symbionts, including microbes, produce proteins that can enter host cells, or are injected into host cells in order to modify the physiology of the host to promote colonization. These molecules, termed effectors, commonly target the host defense signaling pathways in order to suppress the defense response. Others target the gene expression machinery or trigger specific modifications to host morphology or physiology that promote the nutrition and proliferation of the symbiont. When recognized by the host's surveillance machinery, which includes cognate resistance (R) gene products, defense responses are engaged to restrict pathogen proliferation. Effectors from diverse symbionts may be delivered into plant cells via varied mechanisms, including whole organism cellular entry (viruses, some bacteria and fungi), type III and IV secretion (in bacteria), physical injection (nematodes and insects) and protein translocation signal sequences (oomycetes and fungi). This mini-review will summarize both similarities and differences in effectors and effector delivery systems found in diverse plant-associated symbionts as well as how these are described with Plant-Associated Microbe Gene Ontology (PAMGO) terms.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

真菌铜离子内稳态（homeostasis）调节的多样性

摘要：铜是生物体中必需的微量元素之一,作为多种氧化酶的辅助因子参与不同的生物反应,对于维持生命活动起到重要的作用。但在过量的情况下,无论是一价铜离子还是二价铜离子对于生物体都具有很强的细胞毒性,因此铜的代谢是受细胞严格调控的。以酿酒酵母(Saccharomyces cerevisiae)为模式生物对铜代谢的研究已取得了很大进展,对其它高等生物体内铜代谢及其重要生理功能提供了重要信息。本文对酿酒酵母中铜离子的吸收、转运以及在细胞内的代谢调控的新进展进行了归纳,并结合自己的研究综述了真菌铜代谢调节的共性与差异。     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

Egg phenotype differentiation in sympatric cuckoo Cuculus canorus gentes

The brood parasitic common cuckoo Cuculus canorus consists of gentes, which typically parasitize only a single host species whose eggs they often mimic. Where multiple cuckoo gentes co‐exist in sympatry, we may expect variable but generally poorer mimicry because of host switches or inter‐gens gene flow via males if these also contribute to egg phenotypes. Here, we investigated egg trait differentiation and mimicry in three cuckoo gentes parasitizing great reed warblers Acrocephalus arundinaceus, marsh warblers Acrocephalus palustris and corn buntings Miliaria calandra breeding in close sympatry in partially overlapping habitat types. The three cuckoo gentes showed a remarkable degree of mimicry to their three host species in some but not all egg features, including egg size, a hitherto largely ignored feature of egg mimicry. Egg phenotype matching for both background and spot colours as well as for egg size has been maintained in close sympatry despite the possibility for gene flow.     

Understanding Mimicry – with Special Reference to Vocal Mimicry

The term mimicry was introduced to biology in 1862 by Henry Walter Bates in his evolutionary explanation of deceptive communication in nature, based on a three‐part interaction system of a mimicked organism or object (called model), a mimicking organism (called mimic), and one or more organisms as selecting agents. Bates gave two incongruous definitions of mimicry: one from the viewpoint of a natural agent that selects for, and in consequence is deceived by, the close resemblance of a toxic model's warning signal and the similar appearance of a palatable mimic, and another one from the viewpoint of a human taxonomist who under an evolutionary aspect focuses on convergent resemblance between model and mimic. Later definitions of Müllerian (F. Müller), arithmetic (A. Wallace) and social (M. Moynihan) mimicry abolish deception in the natural selecting agent, rely on the convergence criterion alone, fuse the roles of model and mimic but have to accept a mix of homologous and convergent resemblance amongst them for a functional explanation. The definition of vocal mimicry (E. Armstrong) refers to a learned resemblance between mimic and heterospecific model by character duplication (no convergence), so far without known (deceived or not deceived) natural selecting agents. It excludes Batesian vocal mimicry. The functional ethological understanding of mimicry as a tripartite communication system (W. Wickler) is consistent with Bates' concept and accepts deception as key element of Batesian mimicry beyond homologous and convergent resemblances. Deception is seen as caused by the divergence between a sign and its meaning for the natural selecting agent. This understanding covers mimicry in all behaviour domains, provides a generally applicable definition of mimic and model so far missing in any mimicry concept, and it distinguishes – still in line with Henry Bates – cultural from genetically determined model‐mimic‐resemblance; this applies to vocal mimicry in particular. Convergently evolved model‐mimic‐resemblance, not essential in Batesian mimicry but mandatory for its alternatives, marks a fundamental distinction between Batesian mimicry (including Mimesis) and all other conceptualized mimicries and accounts for the non‐existence of a unified meaning of the term mimicry. However, character convergence does not help to explain the mere existence of mimicry phenomena and is irrelevant for their permanence in nature. I therefore propose to remove the convergence argument from any mimicry definition.     

Laboratory investigations of trichomycete prevalence, abundance and fecundity in a Smittium-simuliid model

Smittium, the most speciose genus of the "gut fungi" (Zygomycota: Trichomycetes), is found attached to the hindgut cuticle of larval aquatic Diptera. Smittium spp. colonize several host families (e.g., Smittium culisetae in Chironomidae, Culicidae and Simuliidae), but some species appear to be specific to a single host family (e.g., Smittium morbosum Sweeney in Culicidae). The specificity of Smittium spp. within a host family has been difficult to resolve. This research presents evidence that certain Smittium spp. differentially colonize particular species of black fly (Diptera: Simuliidae) hosts as measured by differences in prevalence, abundance and fecundity. Reasons for this differential occurrence and fecundity in hosts are unclear but might include fungal responses to variations in host morphology, physiology, distribution or behavior. Variable fitness of Smittium spp., within a suite of available hosts, could be a factor in the diversity of this fungal group.     

Circadian orchestration of host and gut microbiota in infection

Circadian rhythms are present in almost every organism and regulate multiple aspects of biological and physiological processes (e.g. metabolism, immune responses, and microbial exposure). There exists a bidirectional circadian interaction between the host and its gut microbiota, and potential circadian orchestration of both host and gut microbiota in response to invading pathogens. In this review, we summarize what is known about these intestinal microbial oscillations and the relationships between host circadian clocks and various infectious agents (bacteria, fungi, parasites, and viruses), and discuss how host circadian clocks prime the immune system to fight pathogen infections as well as the direct effects of circadian clocks on viral activity (e.g. SARS-CoV-2 entry and replication). Finally, we consider strategies employed to realign normal circadian rhythmicity for host health, such as chronotherapy, dietary intervention, good sleep hygiene, and gut microbiota-targeted therapy. We propose that targeting circadian rhythmicity may provide therapeutic opportunities for the treatment of infectious diseases.     

Live-cell imaging of conidial fusion in the bean pathogen, Colletotrichum lindemuthianum

Fusion of conidia and conidial germlings by means of conidial anastomosis tubes (CATs) is a common phenomenon in filamentous fungi, including many plant pathogens. It has a number of different roles, and has been speculated to facilitate parasexual recombination and horizontal gene transfer between species. The bean pathogen Colletotrichum lindemuthianum naturally undergoes CAT fusion on the host surface and within asexual fruiting bodies in anthracnose lesions on its host. It has not been previously possible to analyze the whole process of CAT fusion in this or any other pathogen using live-cell imaging techniques. Here we report the development of a robust protocol for doing this with C. lindemuthianum in vitro. The percentage of conidial germination and CAT fusion was found to be dependent on culture age, media and the fungal strain used. Increased CAT fusion was correlated with reduced germ tube formation. We show time-lapse imaging of the whole process of CAT fusion in C. lindemuthianum for the first time and monitored nuclear migration through fused CATs using nuclei labelled with GFP. CAT fusion in this pathogen was found to exhibit significant differences to that in the model system Neurospora crassa. In contrast to N. crassa, CAT fusion in C. lindemuthianum is inhibited by nutrients (it only occurs in water) and the process takes considerably longer.     

Chromatin-mediated Candida albicans virulence

Candida albicans is the most prevalent human fungal pathogen. To successfully propagate an infection, this organism relies on the ability to change morphology, express virulence-associated genes and resist DNA damage caused by the host immune system. Many of these events involve chromatin alterations that are crucial for virulence. This review will focus on the studies that have been conducted on how chromatin function affects pathogenicity of C. albicans and other fungi. This article is part of a Special Issue entitled: Histone chaperones and Chromatin assembly.     

Abnormal germling development by brown rust and powdery mildew on cer barley mutants

The barley leaf rust fungus forms appressoria over host leaf stomata and penetrates via the stomatal pore. High levels of avoidance to leaf rust fungi have been described in some wild accessions of Hordeum species where a prominent wax layer on the stomata inhibits triggering of fungal appressorium differentiation. Leaf rust avoidance has not yet been found in H. vulgare. Since cuticular leaf waxes are implicated in the avoidance trait, we screened 27 eceriferum (cer) mutant lines of H. vulgare for avoidance to barley leaf rust. These mutations affect leaf waxes. Reduction in numbers of germ tubes forming appressoria over stomata was found in some lines, but the greatest reduction (ca 30%) was less than previously found in wild barley spp. or in an accession of H. chilense used here as a check. In one line (cer-zh654), avoidance was due to a combination of factors. Firstly, fewer germ tubes oriented towards stomata and so failed to contact them. Secondly, some germ tubes that encountered stomata did not form appressoria but over-grew them. In this line, therefore, the fungus tended to fail both to locate and to respond to stomata. The appressoria of barley powdery mildew form on leaf epidermal cells that they penetrate directly. On certain cer lines, a proportion of germlings of the barley powdery mildew fungus developed abnormally, suggesting that germlings failed to recognise and/or respond to the leaf surface waxes on these mutants.     

Artificial neural networks in models of specialization, guild evolution and sympatric speciation

Sympatric speciation can arise as a result of disruptive selection with assortative mating as a pleiotropic by-product. Studies on host choice, employing artificial neural networks as models for the host recognition system in exploiters, illustrate how disruptive selection on host choice coupled with assortative mating can arise as a consequence of selection for specialization. Our studies demonstrate that a generalist exploiter population can evolve into a guild of specialists with an 'ideal free' frequency distribution across hosts. The ideal free distribution arises from variability in host suitability and density-dependent exploiter fitness on different host species. Specialists are less subject to inter-phenotypic competition than generalists and to harmful mutations that are common in generalists exploiting multiple hosts.When host signals used as cues by exploiters coevolve with exploiter recognition systems, our studies show that evolutionary changes may be continuous and cyclic. Selection changes back and forth between specialization and generalization in the exploiters, and weak and strong mimicry in the hosts, where non-defended hosts use the host investing in defence as a model. Thus, host signals and exploiter responses are engaged in a red-queen mimicry process that is ultimately cyclic rather then directional. In one phase, evolving signals of exploitable hosts mimic those of hosts less suitable for exploitation (i.e. the model). Signals in the model hosts also evolve through selection to escape the mimic and its exploiters. Response saturation constraints in the model hosts lead to the mimic hosts finally perfecting its mimicry, after which specialization in the exploiter guild is lost. This loss of exploiter specialization provides an opportunity for the model hosts to escape their mimics. Therefore, this cycle then repeats.We suggest that a species can readily evolve sympatrically when disruptive selection for specialization on hosts is the first step. In a sexual reproduction setting, partial reproductive isolation may first evolve by mate choice being confined to individuals on the same host. Secondly, this disruptive selection will favour assortative mate choice on genotype, thereby leading to increased reproductive isolation.