The genome of an organism bears the signature of its lifestyle, and organisms with similar life strategies are expected to share common genomic traits. Indeed, ectomycorrhizal and arbuscular ...mycorrhizal fungi share some genomic traits, such as the expansion of gene families encoding taxon-specific small secreted proteins, which are candidate effectors in the symbiosis, and a very small repertoire of plant cell wall-degrading enzymes. A large gene family coding for candidate effectors was also revealed in ascomycetous ericoid mycorrhizal (ERM) fungi, but these fungal genomes are characterised by a very high number of genes encoding degradative enzymes, mainly acting on plant cell wall components. We suggest that the genomic signature of ERM fungi mirrors a versatile life strategy, which allows them to occupy several ecological niches.
Abstract
Plants harbor in their external surfaces and internal tissues a highly diverse and finely structured microbial assembly, the microbiota. Each plant compartment usually represents a unique ...ecological niche hosting a distinct microbial community and niche differentiation, which may mirror distinct functions of a specialized microbiota, has been mainly investigated for bacteria. Far less is known for the fungal components of the plant-associated microbiota. Here, we applied a metabarcoding approach to describe the fungal assemblages in different organs of
Vaccinium myrtillus
plants (Ericaceae) collected in a subalpine meadow in North-West Italy, and identified specific taxa enriched in internal tissues of roots, stems, leaves and flowers. We also traced the distribution of some important fungi commonly associated with plants of the family Ericaceae, namely the ericoid mycorrhizal (ErM) fungi and the dark septate endophytes (DSE), both playing important roles in plant growth and health. Operational taxonomic units attributed to established ErM fungal species in the genus
Hyaloscypha
and to DSE species in the
Phialocephala-Acephala applanata
complex (PAC) were found in all the plant organs. Mycorrhizal fungi are thought to be strictly associated with the plant roots, and this first observation of ErM fungi in the above-ground organs of the host plant may be explained by the evolutionary closeness of ErM fungi in the genus
Hyaloscypha
with non mycorrhizal fungal endophytes. This is also witnessed by the closer similarities of the ErM fungal genomes with the genomes of plant endophytes than with those of other mycorrhizal fungi, such as arbuscular or ectomycorrhizal fungi.
The endophytic microbiota can establish mutualistic or commensalistic interactions within the host plant tissues. We investigated the bacterial endophytic microbiota in three species of Mediterranean ...orchids (
,
, and
) by metabarcoding of the 16S rRNA gene. We examined whether the different orchid species and organs, both underground and aboveground, influenced the endophytic bacterial communities. A total of 1,930 operational taxonomic units (OTUs) were obtained, mainly Proteobacteria and Actinobacteria, whose distribution model indicated that the plant organ was the main determinant of the bacterial community structure. The co-occurrence network was not modular, suggesting a relative homogeneity of the microbiota between both plant species and organs. Moreover, the decrease in species richness and diversity in the aerial vegetative organs may indicate a filtering effect by the host plant. We identified four hub OTUs, three of them already reported as plant-associated taxa (
, and
), whereas
was an unusual member of the plant microbiota. Core microbiota analysis revealed a selective and systemic ascent of bacterial communities from the vegetative to the reproductive organs. The core microbiota was also maintained in the
seeds, suggesting a potential vertical transfer of the microbiota. Surprisingly, some
seed samples displayed a very rich endophytic microbiota, with a large number of OTUs shared with the roots, a situation that may lead to a putative restoring process of the root-associated microbiota in the progeny. Our results indicate that the bacterial community has adapted to colonize the orchid organs selectively and systemically, suggesting an active involvement in the orchid holobiont.
Mycorrhizal fungi are essential for the survival of orchid seedlings under natural conditions. The distribution of these fungi in soil can constrain the establishment and resulting spatial ...arrangement of orchids at the local scale, but the actual extent of occurrence and spatial patterns of orchid mycorrhizal (OrM) fungi in soil remain largely unknown.
We addressed the fine-scale spatial distribution of OrM fungi in two orchid-rich Mediterranean grasslands by means of high-throughput sequencing of fungal ITS2 amplicons, obtained from soil samples collected either directly beneath or at a distance from adult Anacamptis morio and Ophrys sphegodes plants.
Like ectomycorrhizal and arbuscular mycobionts, OrM fungi (tulasnelloid, ceratobasidioid, sebacinoid and pezizoid fungi) exhibited significant horizontal spatial autocorrelation in soil. However, OrM fungal read numbers did not correlate with distance from adult orchid plants, and several of these fungi were extremely sporadic or undetected even in the soil samples containing the orchid roots.
Orchid mycorrhizal ‘rhizoctonias’ are commonly regarded as unspecialized saprotrophs. The sporadic occurrence of mycobionts of grassland orchids in host-rich stands questions the view of these mycorrhizal fungi as capable of sustained growth in soil.
Several studies have investigated soil microbial biodiversity, but understanding of the mechanisms underlying plant responses to soil microbiota remains in its infancy. Here, we focused on tomato ...(Solanum lycopersicum), testing the hypothesis that plants grown on native soils display different responses to soil microbiotas.
Using transcriptomics, proteomics, and biochemistry, we describe the responses of two tomato genotypes (susceptible or resistant to Fusarium oxysporum f. sp. lycopersici) grown on an artificial growth substrate and two native soils (conducive and suppressive to Fusarium).
Native soils affected tomato responses by modulating pathways involved in responses to oxidative stress, phenol biosynthesis, lignin deposition, and innate immunity, particularly in the suppressive soil. In tomato plants grown on steam-disinfected soils, total phenols and lignin decreased significantly. The inoculation of a mycorrhizal fungus partly rescued this response locally and systemically. Plants inoculated with the fungal pathogen showed reduced disease symptoms in the resistant genotype in both soils, but the susceptible genotype was partially protected from the pathogen only when grown on the suppressive soil.
The ‘state of alert’ detected in tomatoes reveals novel mechanisms operating in plants in native soils and the soil microbiota appears to be one of the drivers of these plant responses.
Orchids are highly dependent on their mycorrhizal fungal partners for nutrient supply, especially during early developmental stages. In addition to organic carbon, nitrogen (N) is probably a major ...nutrient transferred to the plant because orchid tissues are highly N-enriched. We know almost nothing about the N form preferentially transferred to the plant or about the key molecular determinants required for N uptake and transfer.
We identified, in the genome of the orchid mycorrhizal fungus Tulasnella calospora, two functional ammonium transporters and several amino acid transporters but found no evidence of a nitrate assimilation system, in agreement with the N preference of the free-living mycelium grown on different N sources.
Differential expression in symbiosis of a repertoire of fungal and plant genes involved in the transport and metabolism of N compounds suggested that organic N may be the main form transferred to the orchid host and that ammonium is taken up by the intracellular fungus from the apoplatic symbiotic interface.
This is the first study addressing the genetic determinants of N uptake and transport in orchid mycorrhizas, and provides a model for nutrient exchanges at the symbiotic interface, which may guide future experiments.
Earth's life may have originated as self-replicating RNA, and it has been argued that RNA viruses and viroid-like elements are remnants of such pre-cellular RNA world. RNA viruses are defined by ...linear RNA genomes encoding an RNA-dependent RNA polymerase (RdRp), whereas viroid-like elements consist of small, single-stranded, circular RNA genomes that, in some cases, encode paired self-cleaving ribozymes. Here we show that the number of candidate viroid-like elements occurring in geographically and ecologically diverse niches is much higher than previously thought. We report that, amongst these circular genomes, fungal ambiviruses are viroid-like elements that undergo rolling circle replication and encode their own viral RdRp. Thus, ambiviruses are distinct infectious RNAs showing hybrid features of viroid-like RNAs and viruses. We also detected similar circular RNAs, containing active ribozymes and encoding RdRps, related to mitochondrial-like fungal viruses, highlighting fungi as an evolutionary hub for RNA viruses and viroid-like elements. Our findings point to a deep co-evolutionary history between RNA viruses and subviral elements and offer new perspectives in the origin and evolution of primordial infectious agents, and RNA life.
Photosynthetic orchids associate with mycorrhizal fungi that can be mostly ascribed to the "rhizoctonia" species complex. Rhizoctonias' phylogenetic diversity covers a variety of ...ecological/nutritional strategies that include, beside the symbiosis establishment with host plants, endophytic and pathogenic associations with non-orchid plants or saprotrophic soil colonization. In addition, orchid mycorrhizal fungi (OMF) that establish a symbiotic relationship with an orchid host can later proliferate in browning and rotting orchid tissues. Environmental triggers and molecular mechanisms governing the switch leading to either a saprotrophic or a mycorrhizal behavior in OMF remain unclear. As the sequenced OMF genomes feature a wide range of genes putatively involved in the degradation of plant cell wall (PCW) components, we tested if these transitions may be correlated with a change in the expression of some PCW degrading enzymes. Regulation of several genes encoding PCW degrading enzymes was evaluated during saprotrophic growth of the OMF
on different substrates and under successful and unsuccessful mycorrhizal symbioses. Fungal gene expression
was investigated in two orchid species, the terrestrial Mediterranean
and the epiphytic tropical
. Although we only tested a subset of the CAZyme genes identified in the
genome, and we cannot exclude therefore a role for different CAZyme families or members inside a family, the results showed that the degradative potential of
is finely regulated during saprotrophic growth and in symbiosis, often with a different regulation in the two orchid species. These data pose novel questions about the role of fungal PCW degrading enzymes in the development of unsuccessful and successful interactions.
MAIN CONCLUSION : Orchid mycorrhiza has been often interpreted as an antagonistic relationship. Our data on mycorrhizal protocorms do not support this view as plant defence genes were not induced, ...whereas some nodulin-like genes were significantly up-regulated. Orchids fully depend on symbiotic interactions with specific soil fungi for seed germination and early development. Germinated seeds give rise to a protocorm, a heterotrophic organ that acquires nutrients, including organic carbon, from the mycorrhizal partner. It has long been debated if this interaction is mutualistic or antagonistic. To investigate the molecular bases of the orchid response to mycorrhizal invasion, we developed a symbiotic in vitro system between Serapias vomeracea, a Mediterranean green meadow orchid, and the rhizoctonia-like fungus Tulasnella calospora. 454 pyrosequencing was used to generate an inventory of plant and fungal genes expressed in mycorrhizal protocorms, and plant genes could be reliably identified with a customized bioinformatic pipeline. A small panel of plant genes was selected and expression was assessed by real-time quantitative PCR in mycorrhizal and non-mycorrhizal protocorm tissues. Among these genes were some markers of mutualistic (e.g. nodulins) as well as antagonistic (e.g. pathogenesis-related and wound/stress-induced) genes. None of the pathogenesis or wound/stress-related genes were significantly up-regulated in mycorrhizal tissues, suggesting that fungal colonization does not trigger strong plant defence responses. In addition, the highest expression fold change in mycorrhizal tissues was found for a nodulin-like gene similar to the plastocyanin domain-containing ENOD55. Another nodulin-like gene significantly more expressed in the symbiotic tissues of mycorrhizal protocorms was similar to a sugar transporter of the SWEET family. Two genes coding for mannose-binding lectins were significantly up-regulated in the presence of the mycorrhizal fungus, but their role in the symbiosis is unclear.
Many adult orchids, especially photoautotrophic species, associate with a diverse range of mycorrhizal fungi, but little is known about the temporal changes that might occur in the diversity and ...functioning of orchid mycorrhiza during vegetative and reproductive plant growth. Temporal variations in the spectrum of mycorrhizal fungi and in stable isotope natural abundance were investigated in adult plants of Anacamptis morio, a wintergreen meadow orchid. Anacamptis morio associated with mycorrhizal fungi belonging to Tulasnella, Ceratobasidium and a clade of Pezizaceae (Ascomycetes). When a complete growing season was investigated, multivariate analyses indicated significant differences in the mycorrhizal fungal community. Among fungi identified from manually isolated pelotons, Tulasnella was more common in autumn and winter, the pezizacean clade was very frequent in spring, and Ceratobasidium was more frequent in summer. By contrast, relatively small variations were found in carbon (C) and nitrogen (N) stable isotope natural abundance, A. morio samples showing similar¹⁵N enrichment and¹³C depletion at the different sampling times. These observations suggest that, irrespective of differences in the seasonal environmental conditions, the plant phenological stages and the associated fungi, the isotopic content in mycorrhizal A. morio remains fairly constant over time.
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