Novel Root-Fungus Symbiosis in Ericaceae: Sheathed Ericoid Mycorrhiza Formed by a Hitherto Undescribed Basidiomycete with Affinities to Trechisporales

Ericaceae (the heath family) are widely distributed calcifuges inhabiting soils with inherently poor nutrient status. Ericaceae overcome nutrient limitation through symbiosis with ericoid mycorrhizal (ErM) fungi that mobilize nutrients complexed in recalcitrant organic matter. At present, recognized ErM fungi include a narrow taxonomic range within the Ascomycota, and the Sebacinales, basal Hymenomycetes with unclamped hyphae and imperforate parenthesomes. Here we describe a novel type of basidiomycetous ErM symbiosis, termed ‘sheathed ericoid mycorrhiza’, discovered in two habitats in mid-Norway as a co-dominant mycorrhizal symbiosis in Vaccinium spp. The basidiomycete forming sheathed ErM possesses clamped hyphae with perforate parenthesomes, produces 1- to 3-layer sheaths around terminal parts of hair roots and colonizes their rhizodermis intracellularly forming hyphal coils typical for ErM symbiosis. Two basidiomycetous isolates were obtained from sheathed ErM and molecular and phylogenetic tools were used to determine their identity; they were also examined for the ability to form sheathed ErM and lignocellulolytic potential. Surprisingly, ITS rDNA of both conspecific isolates failed to amplify with the most commonly used primer pairs, including ITS1 and ITS1F + ITS4. Phylogenetic analysis of nuclear LSU, SSU and 5.8S rDNA indicates that the basidiomycete occupies a long branch residing in the proximity of Trechisporales and Hymenochaetales, but lacks a clear sequence relationship (>90% similarity) to fungi currently placed in these orders. The basidiomycete formed the characteristic sheathed ErM symbiosis and enhanced growth of Vaccinium spp. in vitro, and degraded a recalcitrant aromatic substrate that was left unaltered by common ErM ascomycetes. Our findings provide coherent evidence that this hitherto undescribed basidiomycete forms a morphologically distinct ErM symbiosis that may occur at significant levels under natural conditions, yet remain undetected when subject to amplification by ‘universal’ primers. The lignocellulolytic assay suggests the basidiomycete may confer host adaptations distinct from those provisioned by the so far investigated ascomycetous ErM fungi

Out of the rivers: are some aquatic hyphomycetes plant endophytes?

Ingoldian fungi, or aquatic hyphomycetes, are asexual microfungi, mostly ascomycetes, commonly occurring in running freshwater. They grow on dead plant material, such as leaves and twigs, and play a major role in nutrient flows in stream ecosystems (Bärlocher, 1992). They were discovered and first extensively studied by Ingold (1942) and were thus named "Ingoldian" fungi. Ingold described their abundant multicellular asexual spores of sigmoid or, more typically, tetraradiate shape (Fig. 1). He recognized that they probably arose from multiple convergent evolutions, by secondary adaptation to aquatic life, as recently confirmed by molecular markers (Belliveau & Bärlocher, 2005; Baschien et al., 2006). Because of their apparent lack of sexuality, Ingoldian species were placed in asexual genera, such as Tricladium or Tetracladium, based on conidial morphology and/or mode of conidiogenesis. Unexpectedly, several lines of evidence now suggest that some Ingoldian fungi are also plant endophytes, that is, they grow in plants without producing symptoms.[...

Interakce v rhizosféře erikoidně mykorhizních rostlin

This doctonl dissertation focuses on selected intemctions, which take place in the rhizosphere of ericoid myconhial (ErM) plmts' These include (i) interactions betwren ErM fungi and dark scptate endophýic (DsE) fungi; (ii) intenctions among ericaceous plmts md ErM and EcM fungi, and fungi with yet unresolved myconhial status; (iii) int€nctions among ErM and DSE fungi md soil testate ammbae' Main findings achieved in the frame ofthe doctoral dissertation are: Ericoid mycorrhlza rnd DsE-association simultaneously occur in roots of 8ll screened European Rhotlotkrulron species across the continent. However, their proportlons differ depending mainly on htitude. DsE.coloniation is negrtiv€|y corr€lsted with ErM colonization in roots of rl| screned rbododendrons. DsE fungi form intmcellu|ar structuÍes, which moÍphologicr||y resemble ericoid mycorrhizs. Colonization witb selected DSE stmins has neutral to negative influence on the groMh of ericaceous plants in vitro, whereas th€ eff€ct of the t}?ica| ErM fungus Rhizoscyphus ericae is neutml to positive. Effects of both types of fungi on the grosth of host plrnts are correlated with the |eve| of ErM rnd DsE co|onization. ErM fungi crn r|teÍ the negrtive effect of DSE fungi when presnt in the same root system in vitro. ErM frlngus Oidiodendron n aius..

Interakce v rhizosféře erikoidně mykorhizních rostlin

This doctonl dissertation focuses on selected intemctions, which take place in the rhizosphere of ericoid myconhial (ErM) plmts' These include (i) interactions betwren ErM fungi and dark scptate endophýic (DsE) fungi; (ii) intenctions among ericaceous plmts md ErM and EcM fungi, and fungi with yet unresolved myconhial status; (iii) int€nctions among ErM and DSE fungi md soil testate ammbae' Main findings achieved in the frame ofthe doctoral dissertation are: Ericoid mycorrhlza rnd DsE-association simultaneously occur in roots of 8ll screened European Rhotlotkrulron species across the continent. However, their proportlons differ depending mainly on htitude. DsE.coloniation is negrtiv€|y corr€lsted with ErM colonization in roots of rl| screned rbododendrons. DsE fungi form intmcellu|ar structuÍes, which moÍphologicr||y resemble ericoid mycorrhizs. Colonization witb selected DSE stmins has neutral to negative influence on the groMh of ericaceous plants in vitro, whereas th€ eff€ct of the t}?ica| ErM fungus Rhizoscyphus ericae is neutml to positive. Effects of both types of fungi on the grosth of host plrnts are correlated with the |eve| of ErM rnd DsE co|onization. ErM fungi crn r|teÍ the negrtive effect of DSE fungi when presnt in the same root system in vitro. ErM frlngus Oidiodendron n aius..

Testate Amoebae Communities in the Rhizosphere of Rhododendron ponticum (Ericaceae) in an Evergreen Broadleaf Forest in Southern Spain

Testate amoebae (TA) are an important part of soil microbial communities and in certain ecosystems they may represent a substantial proportion of total microbial biomass. Their distribution and abundance is driven by various abiotic factors (e.g. pH, organic matter, soil moisture, soil/water chemistry) but comparatively less is known about the role of biotic interactions. TA often co-occur with Ericaceae, a ubiquitous plant family inhabiting acidic soils with poor nutrient status. Ericaceae can significantly change soil properties through production of recalcitrant litter and possibly also due to root exudates and activities of root-inhabiting fungi; this may result in profound modifications of microbial communities. A recent study from northwest England shows that the invasive ericaceous shrub Rhododendron ponticum may significantly modify communities of soil TA. Here, we investigate the effect of pH, organic matter, soil moisture and R. ponticum presence on TA communities within the native range of the ericaceous shrub at two sites in south Spain and compare our results with the previous study from NW England. At the Spanish sites, organic matter content, R. ponticum presence and pH affected occurrence and abundance of several TA species; R. ponticum presence and organic matter content were highly correlated and explained most of the observed variability in TA communities (= the effect of the R. ponticum rhizosphere). R. ponticum rhizosphere affected especially TA with relatively large tests, i.e. Cyclopyxis eurystoma, Phryganella acropodia and Trigonopyxis arcula. Interestingly, T. arcula was also positively associated with R. ponticum in the previously studied British sites. The rhizosphere of the ericaceous shrub appears to have a positive effect on testate amoebae taxon richness at the two studied autochthonous Spanish sites but may reduce taxon richness in the sites in Britain where R. ponticum is an introduced species. Such possible positive/negative effects of native/invasive species, as well as other plant guilds, on TA communities clearly deserve further investigation

Range expansion of Marinomyxa marina, a phytomyxid parasite of the invasive seagrass Halophila stipulacea, to the Caribbean

Halophila stipulacea, a small seagrass species native to the Indo-Pacific, is a Lessepsian migrant and a high-profile invader that has successfully colonized two exotic regions, the Mediterranean (first observed in 1894) and the Caribbean (2002). In 1961, an intracellular phytomyxid parasite, Marinomyxa marina (SAR: Rhizaria: Endomyxa: Phytomyxea) was discovered in the petioles of H. stipulacea in the Red Sea, and three decades later, it was reported off the coast of Sicily (Mediterranean), suggesting parallel migration of the two organisms. In 2018, infected petioles of H. stipulacea were also observed in St. Eustatius (Caribbean), but the identity of the causative agent remained unresolved. Here, we provide information on four new localities of phytomyxid-infested populations of H. stipulacea in Greece (Mediterranean), and Bonaire and Martinique (Caribbean), including notes on infection prevalence and seasonal dynamics. Using the 18S rRNA barcoding gene, we bring molecular evidence that the disease is caused by a genetically uniform variant of M. marina at all the examined sites. We conclude that the parasite is now widespread throughout both invaded regions and has been present in the Caribbean since 2013 at the latest. For the first time, the production of fruits in infected plants is observed, indicating a non-lethal nature of the symbiosis. While the arrival of M. marina to the Caribbean is unlikely to alleviate the current invasiveness of H. stipulacea, we emphasize the need for its further monitoring since the host-specificity and general biology of seagrass-associated phytomyxids are still poorly understood

The Potential of Dark Septate Endophytes to Form Root Symbioses with Ectomycorrhizal and Ericoid Mycorrhizal Middle European Forest Plants

<div><p>The unresolved ecophysiological significance of Dark Septate Endophytes (DSE) may be in part due to existence of morphologically indistinguishable cryptic species in the most common <i>Phialocephala fortinii</i> s. l.—<i>Acephala applanata</i> species complex (PAC). We inoculated three middle European forest plants (European blueberry, Norway spruce and silver birch) with 16 strains of eight PAC cryptic species and other DSE and ectomycorrhizal/ericoid mycorrhizal fungi and focused on intraradical structures possibly representing interfaces for plant-fungus nutrient transfer and on host growth response. The PAC species <i>Acephala applanata</i> simultaneously formed structures resembling ericoid mycorrhiza (ErM) and DSE microsclerotia in blueberry. <i>A</i>. <i>macrosclerotiorum</i>, a close relative to PAC, formed ectomycorrhizae with spruce but not with birch, and structures resembling ErM in blueberry. <i>Phialocephala glacialis</i>, another close relative to PAC, formed structures resembling ErM in blueberry. In blueberry, six PAC strains significantly decreased dry shoot biomass compared to ErM control. In birch, one <i>A</i>. <i>macrosclerotiorum</i> strain increased root biomass and the other shoot biomass in comparison with non-inoculated control. The dual mycorrhizal ability of <i>A</i>. <i>macrosclerotiorum</i> suggested that it may form mycorrhizal links between Ericaceae and Pinaceae. However, we were unable to detect this species in Ericaceae roots growing in a forest with presence of <i>A</i>. <i>macrosclerotiorum</i> ectomycorrhizae. Nevertheless, the diversity of Ericaceae mycobionts was high (380 OTUs) with individual sites often dominated by hitherto unreported helotialean and chaetothyrialean/verrucarialean species; in contrast, typical ErM fungi were either absent or low in abundance. Some DSE apparently have a potential to form mycorrhizae with typical middle European forest plants. However, except <i>A</i>. <i>applanata</i>, the tested representatives of all hitherto described PAC cryptic species formed typical DSE colonization without specific structures necessary for mycorrhizal nutrient transport. <i>A</i>. <i>macrosclerotiorum</i> forms ectomycorrhiza with conifers but not with broadleaves and probably does not form common mycorrhizal networks between conifers with Ericaceae.</p></div