Fungal genes in the innovation and evolution of land plants.

Although fungal association has been instrumental to the evolution of land plants, how genes of fungal origin might have contributed to major plant innovations remains unclear. In a recent study, we showed that a macro2 domain-containing gene likely acquired from mycorrhiza-like fungi is important in gametophore development of mosses, suggesting a role of fungi-derived genes in the three-dimensional growth of land plants.

Asperimides A-D, anti-inflammatory aromatic butenolides from a tropical endophytic fungus Aspergillus terreus.

Four new aromatic butenolides, asperimides A-D (1-4), together with a known analogue, butyrolactone I (5), were isolated from solid cultures of a tropical endophytic fungus Aspergillus terreus. The structures of these compounds were elucidated on the basis of spectroscopic methods and electronic circular dichroism calculations. Compounds 1-4 represent the first examples of butenolides with a maleimide core isolated from Aspergillus sp. Inhibitory effects of the isolated compounds on nitric oxide production were investigated in lipopolysaccaride (LPS)-mediated RAW 264.7 cells. Compounds 3 and 4 exhibited potent anti-inflammatory with IC50 values of 0.78 ±â€¯0.06 and 1.26 ±â€¯0.11 µM, respectively.

Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification.

Mycorrhizal symbiosis between soil fungi and land plants is one of the most widespread and ecologically important mutualisms on earth. It has long been hypothesized that the Glomeromycotina, the mycorrhizal symbionts of the majority of plants, facilitated colonization of land by plants in the Ordovician. This view was recently challenged by the discovery of mycorrhiza-like associations with Mucoromycotina in several early diverging lineages of land plants. Utilizing a large, species-level database of plants' mycorrhiza-like associations and a Bayesian approach to state transition dynamics we here show that the recruitment of Mucoromycotina is the best supported transition from a non-mycorrhizal state. We further found that transitions between different combinations of either or both of Mucoromycotina and Glomeromycotina occur at high rates, and found similar promiscuity among combinations that include either or both of Glomeromycotina and Ascomycota with a nearly fixed association with Basidiomycota. Our results portray an evolutionary scenario of evolution of mycorrhizal symbiosis with a prominent role for Mucoromycotina in the early stages of land plant diversification.

Fungi and fungal interactions in the Rhynie chert: a review of the evidence, with the description of Perexiflasca tayloriana gen. et sp. nov.†.

The Lower Devonian Rhynie chert is one of the most important rock deposits yielding comprehensive information on early continental plant, animal and microbial life. Fungi are especially abundant among the microbial remains, and include representatives of all major fungal lineages except Basidiomycota. This paper surveys the evidence assembled to date of fungal hyphae, mycelial cords and reproductive units (e.g. spores, sporangia, sporocarps), and presents examples of fungal associations and interactions with land plants, other fungi, algae, cyanobacteria and animals from the Rhynie chert. Moreover, a small, chytrid-like organism that occurs singly, in chain-like, linear arrangements, planar assemblages and three-dimensional aggregates of less than 10 to [Formula: see text] individuals in degrading land plant tissue in the Rhynie chert is formally described, and the name Perexiflasca tayloriana proposed for the organism. Perexiflasca tayloriana probably colonized senescent or atrophied plant parts and participated in the process of biological degradation. The fungal fossils described to date from the Rhynie chert constitute the largest body of structurally preserved evidence of fungi and fungal interactions from any rock deposit, and strongly suggest that fungi played important roles in the functioning of the Early Devonian Rhynie ecosystem.This article is part of a discussion meeting issue 'The Rhynie cherts: our earliest terrestrial ecosystem revisited'.

Evolutionary History of Subtilases in Land Plants and Their Involvement in Symbiotic Interactions.

Subtilases, a family of proteases involved in a variety of developmental processes in land plants, are also involved in both mutualistic symbiosis and host-pathogen interactions in different angiosperm lineages. We examined the evolutionary history of subtilase genes across land plants through a phylogenetic analysis integrating amino acid sequence data from full genomes, transcriptomes, and characterized subtilases of 341 species of diverse green algae and land plants along with subtilases from 12 species of other eukaryotes, archaea, and bacteria. Our analysis reconstructs the subtilase gene phylogeny and identifies 11 new gene lineages, six of which have no previously characterized members. Two large, previously unnamed, subtilase gene lineages that diverged before the origin of angiosperms accounted for the majority of subtilases shown to be associated with symbiotic interactions. These lineages expanded through both whole-genome and tandem duplication, with differential neofunctionalization and subfunctionalization creating paralogs associated with different symbioses, including nodulation with nitrogen-fixing bacteria, arbuscular mycorrhizae, and pathogenesis in different plant clades. This study demonstrates for the first time that a key gene family involved in plant-microbe interactions proliferated in size and functional diversity before the explosive radiation of angiosperms.

Sebacinales - one thousand and one interactions with land plants.

20 I 21 II 21 III 23 IV 29 V 33 VI 35 36 36 References 36 SUMMARY: Root endophytism and mycorrhizal associations are complex derived traits in fungi that shape plant physiology. Sebacinales (Agaricomycetes, Basidiomycota) display highly diverse interactions with plants. Although early-diverging Sebacinales lineages are root endophytes and/or have saprotrophic abilities, several more derived clades harbour obligate biotrophs forming mycorrhizal associations. Sebacinales thus display transitions from saprotrophy to endophytism and to mycorrhizal nutrition within one fungal order. This review discusses the genomic traits possibly associated with these transitions. We also show how molecular ecology revealed the hyperdiversity of Sebacinales and their evolutionary diversification into two sister families: Sebacinaceae encompasses mainly ectomycorrhizal and early-diverging saprotrophic species; the second family includes endophytes and lineages that repeatedly evolved ericoid, orchid and ectomycorrhizal abilities. We propose the name Serendipitaceae for this family and, within it, we transfer to the genus Serendipita the endophytic cultivable species Piriformospora indica and P. williamsii. Such cultivable Serendipitaceae species provide excellent models for root endophytism, especially because of available genomes, genetic tractability, and broad host plant range including important crop plants and the model plant Arabidopsis thaliana. We review insights gained with endophytic Serendipitaceae species into the molecular mechanisms of endophytism and of beneficial effects on host plants, including enhanced resistance to abiotic and pathogen stress.

Symbiotic options for the conquest of land.

The domination of the landmasses of Earth by plants starting during the Ordovician Period drastically altered the development of the biosphere and the composition of the atmosphere, with far-reaching consequences for all life ever since. It is widely thought that symbiotic soil fungi facilitated the colonization of the terrestrial environment by plants. However, recent discoveries in molecular ecology, physiology, cytology, and paleontology have brought into question the hitherto-assumed identity and biology of the fungi engaged in symbiosis with the earliest-diverging lineages of extant land plants. Here, we reconsider the existing paradigm and show that the symbiotic options available to the first plants emerging onto the land were more varied than previously thought.

Nostopeptolide plays a governing role during cellular differentiation of the symbiotic cyanobacterium Nostoc punctiforme.

Nostoc punctiforme is a versatile cyanobacterium that can live either independently or in symbiosis with plants from distinct taxa. Chemical cues from plants and N. punctiforme were shown to stimulate or repress, respectively, the differentiation of infectious motile filaments known as hormogonia. We have used a polyketide synthase mutant that accumulates an elevated amount of hormogonia as a tool to understand the effect of secondary metabolites on cellular differentiation of N. punctiforme. Applying MALDI imaging to illustrate the reprogramming of the secondary metabolome, nostopeptolides were identified as the predominant difference in the pks2(-) mutant secretome. Subsequent differentiation assays and visualization of cell-type-specific expression of nostopeptolides via a transcriptional reporter strain provided evidence for a multifaceted role of nostopeptolides, either as an autogenic hormogonium-repressing factor or as a chemoattractant, depending on its extracellular concentration. Although nostopeptolide is constitutively expressed in the free-living state, secreted levels dynamically change before, during, and after the hormogonium differentiation phase. The metabolite was found to be strictly down-regulated in symbiosis with Gunnera manicata and Blasia pusilla, whereas other metabolites are up-regulated, as demonstrated via MALDI imaging, suggesting plants modulate the fine-balanced cross-talk network of secondary metabolites within N. punctiforme.

Across-habitat comparison of diazotroph activity in the subarctic.

Nitrogen (N) fixation by N2-fixing bacteria (diazotrophs) is the primary N input to pristine ecosystems like boreal forests and subarctic and arctic tundra. However, the contribution by the various diazotrophs to habitat N2 fixation remains unclear. We present results from in situ assessments of N2 fixation of five diazotroph associations (with a legume, lichen, feather moss, Sphagnum moss and free-living) incorporating the ground cover of the associations in five typical habitats in the subarctic (wet and dry heath, polygon-heath, birch forest, mire). Further, we assessed the importance of soil and air temperature, as well as moisture conditions for N2 fixation. Across the growing season, the legume had the highest total as well as the highest fraction of N2 fixation rates at habitat level in the heaths (>85 % of habitat N2 fixation), whereas the free-living diazotrophs had the highest N2 fixation rates in the polygon heath (56 %), the lichen in the birch forest (87 %) and Sphagnum in the mire (100 %). The feather moss did not contribute more than 15 % to habitat N2 fixation in any of the habitats despite its high ground cover. Moisture content seemed to be a major driver of N2 fixation in the lichen, feather moss and free-living diazotrophs. Our results show that the range of N2 fixers found in pristine habitats contribute differently to habitat N2 fixation and that ground cover of the associates does not necessarily mirror contribution.

Biocontrol potential of endophytes harbored in Radula marginata (liverwort) from the New Zealand ecosystem.

Radula marginata and Cannabis sativa L. are two phylogenetically unrelated plant species containing structurally similar secondary metabolites like cannabinoids. The major objective of our work was the isolation, identification, biocontrol efficacies, biofilm forming potential and anti-biofilm ability of endophytic microbial community of the liverwort R. marginata, as compared to bacterial endophytic isolates harbored in C. sativa plants. A total of 15 endophytic fungal and 4 endophytic bacterial isolates were identified, including the presence of a bacterial endosymbiont within an endophytic fungal isolate. The endosymbiont was visible only when the fungus containing it was challenged with two phytopathogens Botrytis cinerea and Trichothecium roseum, highlighting a tripartite microbe-microbe interaction and biocontrol potency of endophytes under biotic stress. We also observed sixteen types of endophytic fungal-pathogen and twelve types of endophytic bacterial-pathogen interactions coupled to varying degree of growth inhibitions of either the pathogen or endophyte or both. This showed the magnitude of biocontrol efficacies of endophytes in aiding plant fitness benefits under different media (environmental) conditions. Additionally, it was ecologically noteworthy to find the presence of similar endophytic bacterial genera in both Radula and Cannabis plants, which exhibited similar functional traits like biofilm formation and general anti-biofilm activities. Thus far, our work underlines the biocontrol potency and defensive functional traits (in terms of antagonism and biofilm formation) of endophytes harbored in liverwort R. marginata as compared to the endophytic community of phylogenetically unrelated but phytochemically similar plant C. sativa.

Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 million year old) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses.

Fungi (Eumycota) form close associations with plants, with which they have co-existed since the dawn of life on land, but their diversity in early terrestrial ecosystems is still poorly understood. We studied petrographic sections of exceptionally well-preserved petrified plants from the 407 million yr-old Rhynie Chert (Scotland, UK). For comparative purposes, we illustrate fungal associations in four extant lower land plants. We document two new endophytes in the plant Horneophyton lignieri: Palaeoglomus boullardii (sp. nov. Glomeromycota) colonizes parenchyma in a discontinuous zone of the outer cortex of the aerial axes, forming arbuscule-like structures, vesicles and spores; Palaeoendogone gwynne-vaughaniae (gen. nov., sp. nov. Mucoromycotina) colonizes parenchyma in the basal part of the plant, where it is present in intercellular spaces and as intracellular coils but absent from rhizoids. Critical comparisons between the newly discovered Horneophyton endophytes, fungi previously described from the Rhynie Chert and fungal colonization in extant lower land plants reveal several features characteristic of both Mucoromycotina and Glomeromycota. A reappraisal of fungal associations in early land plants indicates that they are more diverse than assumed hitherto, overturning the long-held paradigm that the early endophytes were exclusively Glomeromycota.

A trait-based framework to understand life history of mycorrhizal fungi.

Despite the growing appreciation for the functional diversity of arbuscular mycorrhizal (AM) fungi, our understanding of the causes and consequences of this diversity is still poor. In this opinion article, we review published data on AM fungal functional traits and attempt to identify major axes of life history variation. We propose that a life history classification system based on the grouping of functional traits, such as Grime's C-S-R (competitor, stress tolerator, ruderal) framework, can help to explain life history diversification in AM fungi, successional dynamics, and the spatial structure of AM fungal assemblages. Using a common life history classification framework for both plants and AM fungi could also help in predicting probable species associations in natural communities and increase our fundamental understanding of the interaction between land plants and AM fungi.

Pullularins E and F, two new peptides from the endophytic fungus Bionectria ochroleuca isolated from the mangrove plant Sonneratia caseolaris.

Chemical investigation of the EtOAc extract of the endophytic fungus Bionectria ochroleuca, isolated from the inner leaf tissues of the plant Sonneratia caseolaris (Sonneratiaceae) from Hainan island (China), yielded two new peptides, pullularins E and F (1 and 2) together with three known compounds (3-5). The structures of the new compounds were unambiguously determined on the basis of one- and two-dimensional NMR spectroscopy as well as by high-resolution mass spectrometry. The absolute configurations of amino acids were determined by HPLC analysis of acid hydrolysates using Marfey's method. The isolated compounds exhibited pronounced to moderate cytotoxic activity against the mouse lymphoma cells (L5178Y) with EC50 values ranging between 0.1 and 6.7 µg/mL.

Endophytic fungus-vascular plant-insect interactions.

Insect association with fungi has a long history. Theories dealing with the evolution of insect herbivory indicate that insects used microbes including fungi as their principal food materials before flowering plants evolved. Subtlety and the level of intricacy in the interactions between insects and fungi indicate symbiosis as the predominant ecological pattern. The nature of the symbiotic interaction that occurs between two organisms (the insect and the fungus), may be either mutualistic or parasitic, or between these two extremes. However, the triangular relationship involving three organisms, viz., an insect, a fungus, and a vascular plant is a relationship that is more complicated than what can be described as either mutualism or parasitism, and may represent facets of both. Recent research has revealed such a complex relationship in the vertically transmitted type-I endophytes living within agriculturally important grasses and the pestiferous insects that attack them. The intricacy of the association depends on the endophytic fungus-grass association and the insect present. Secondary compounds produced in the endophytic fungus-grass association can provide grasses with resistance to herbivores resulting in mutualistic relationship between the fungus and the plant that has negative consequences for herbivorous insects. The horizontally transmitted nongrass type-II endophytes are far less well studied and as such their ecological roles are not fully understood. This forum article explores the intricacy of dependence in such complex triangular relationships drawing from well-established examples from the fungi that live as endophytes in vascular plants and how they impact on the biology and evolution of free-living as well as concealed (e.g., gall-inducing, gall-inhabiting) insects. Recent developments with the inoculation of strains of type-I fungal endophytes into grasses and their commercialization are discussed, along with the possible roles the endophytic fungi play in the galls induced by the Cecidomyiidae (Diptera).

Macrophyte species drive the variation of bacterioplankton community composition in a shallow freshwater lake.

Macrophytes play an important role in structuring aquatic ecosystems. In this study, we explored whether macrophyte species are involved in determining the bacterioplankton community composition (BCC) in shallow freshwater lakes. The BCC in field areas dominated by different macrophyte species in Taihu Lake, a large, shallow freshwater lake, was investigated over a 1-year period. Subsequently, microcosm experiments were conducted to determine if single species of different types of macrophytes in an isolated environment would alter the BCC. Denaturing gradient gel electrophoresis (DGGE), followed by cloning and sequence analysis of selected samples, was employed to analyze the BCC. The DGGE results of the field investigations indicated that the BCC changed significantly from season to season and that the presence of different macrophyte species resulted in lower BCC similarities in the summer and fall. LIBSHUFF analysis of selected clone libraries from the summer demonstrated different BCCs in the water column surrounding different macrophytes. Relative to the field observations, the microcosm studies indicated that the BCC differed more pronouncedly when associated with different species of macrophytes, which was also supported by LIBSHUFF analysis of the selected clone libraries. Overall, this study suggested that macrophyte species might be an important factor in determining the composition of bacterial communities in this shallow freshwater lake and that the species-specific influence of macrophytes on BCC is variable with the season and distance.

Differential hypogeous sporocarp production from Nothofagus dombeyi and N. pumilio forests in southern Argentina.

Mycorrhizal fungi that form hypogeous sporocarps are an important component of the temperate forest soil community. In many regions, such as the Nothofagus forest in the Patagonian Andes, this group of fungi has been poorly studied. Here we examined the spring and autumn community composition of "sequestrate fungi", based on sporocarp production in pure forests of Nothofagus dombeyi (evergreen) and N. pumilio (deciduous). We investigated the possible relationships between these communities and environmental factors over 2 y. The rarefaction curves and the minimal richness estimates converged at nearly the same level for each forest type, and the asymptotes suggested that the sampling effort was sufficient to capture most of the hypogeous sporocarp richness in these forest stands. In total 27 species were recovered. Basidiomycota, Ascomycota and Glomeromycota respectively accounted for nine, two and one genera. Species richness of hypogeous sporocarps varied in relation to forest type but not to season (fall and spring), whereas sporocarp biomass varied according to an interaction between season and forest type. Species richness and sporocarp biomass were positively correlated with rainfall and negatively correlated with altitude. In addition sporocarp species richness was positively related to number of trees per transect. We found that two different forest stands, each dominated by different species of Nothofagus, exhibited different hypogeous sporocarp communities.