Arbuscular mycorrhizas and dark septate endophytes in bromeliads from South American arid environment

Most plant roots are associated with glomalean fungi forming arbuscular mycorrhizas (AM) and a wide range are also colonized by ascomycetous dark septate endophytes (DSE). Bromeliaceae species can be epiphytic, rupicolous or terrestrial but their mycorrhizal status is poorly studied. We examined the AM and DSE status of 5 epiphytic and 4 terrestrial Bromeliaceae from an arid area of Central Argentina. The terrestrial species were either dually associated (AM and DSE) or non-associated whereas the epiphytes were only DSE colonized. Terrestrial Bromeliaceae that formed AM-DSE associations were likely responding to the arid conditions of the area and the availability of AM fungal (AMF) spores in the soil. The terrestrialBromelia ubaniana was not colonized either by AMF or DSE. This could reflect its root morphology and high number of root hairs. DSE are endosymbiotic in the stressful ecosystems experienced by canopy epiphytes in the studied environment. The different fungal associations are discussed in relation to the three Bromeliaceae subfamiles and we suggest that environmental features determinethe type of association formed by species in this plant family.     

The Co-occurrence and Morphological Continuum Between Ericoid Mycorrhiza and Dark Septate Endophytes in Roots of Six European Rhododendron Species

Ericaceae associate with a wide spectrum of root mycobionts, but the most common are ascomycetous ericoid mycorrhizal fungi and dark septate endophytes (DSE), followed by basidiomycetous fungi and glomeracean arbuscular mycorrhizal fungi. We investigated distribution and morphological diversity of ericoid mycorrhizae (ErM), DSE associations, ectomycorrhizae (EcM) and arbuscular mycorrhizae (AM) in hair roots of six European native Rhododendron species and found that i) while EcM and AM were absent, ErM and DSE associations were simultaneously present in all screened plants; ii) their levels were negatively correlated, suggesting Ericaceae preference for certain root-fungus association in certain habitats; iii) the highest ErM colonization occurred at sites in southern and central Europe, while the highest DSE colonization was found in a subarctic site in northern Finland and in a subalpine site in the Carpathians, suggesting a latitudinal/altitudinal shift in Ericaceae root-fungus associations; iv) some mycelia could simultaneously form structures corresponding to ErM and DSE association, which occasionally resulted in a unique ectendomycorrhizal colonization comprising an intercellular parenchymatous net and intracellular hyphal coils. These results indicate frequent interactions between ErM fungi and DSE in roots of European rhododendrons and a morphological continuum between ErM and DSE associations. The new ectendomycorrhizal type deserves further investigation.     

Medicinal plants as hosts of arbuscular mycorrhizal fungi and dark septate endophytes

Arbuscular mycorrhizal and dark septate endophyte associations of 31 medicinal plant species collected from the Garden of Medicinal Plants of the Faculty of Pharmacy, Jagiellonian University, Collegium Medicum in Kraków were investigated. Arbuscular mycorrhiza (AM) was found in 30 species; 23 were of the Arum-type, 5—Paris and 2 taxa revealed intermediate morphology. Many plants were strongly colonized by arbuscular mycorrhizal fungi (AMF). The mycelium of dark septate endophytes (DSE) was observed in 21 taxa. However, the percentage of root colonization by these fungi was low. Spores of 15 species of AMF (Glomeromycota) were found in the rhizosphere of the investigated plants. Our results are the first detailed report of both AMF and DSE associations of these plant species. The use of AMF and DSE during the process of medicinal plant cultivation for pharmaceutical purposes is discussed.     

Arbuscular mycorrhizal morphology and dark septate fungal associations in medicinal and aromatic plants of Western Ghats, Southern India

We investigated roots of 107 medicinal and aromatic plants (MAPs) in the Western Ghats region of Southern India for arbuscular mycorrhizal (AM) and dark septate endophyte (DSE) associations. Of the 107 MAPs belonging to 98 genera in 52 families examined, 79 were AM and 38 harbored a DSE association. Typical Arum- and Paris-type mycorrhizas are first reported in the presumed nonmycorrhizal family Amaranthaceae. Similarly, DSE associations are recorded for the first time in nine plant families and 37 plant species. Thirty MAPs had both AM and DSE associations. The number of MAPs having Arum-type mycorrhiza was greater than those having Paris-type. This was more prominent among herbaceous plants than in trees where the Paris-type was predominant. Similarly, the Arum-type was more prevalent in annuals than in perennials. DSE associations were more frequent in herbs and perennials compared to other MAPs.     

Arbuscular mycorrhizal and dark septate endophytic fungi at 5,500 m on a glacier forefront in the Qinghai-Tibet Plateau, China

Arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi are rarely studied at extremely high elevations. Here, AM and DSE colonization in two dominant plant species (Melandrium apetalum and Poa litwinowiana) were microscopically observed on the forefront of Zhadang Glacier (5,500 m above sea level) in the Qinghai-Tibet Plateau, China. The AM fungal taxa were also identified by molecular methods. Both AM and DSE fungi synchronously colonized these two plant species, but AM dominated in M. apetalum and DSE dominated in P. litwinowiana. A total of five AM fungal spore morphotypes (Acaulospora capsicula, Diversispora sp., Glomus constrictum, G. eburneum and Glomus sp.) were found in the rhizosphere soils. Molecular identification revealed two AM fungal phylotypes: one Claroideoglomus phylotype from roots and one Diversispora phylotype from spores. These results extend the elevation at which both AM and DSE are known to occur.     

Mycorrhizal status of plant species in the Chaco Serrano Woodland from central Argentina

We examined the mycorrhizal type of 128 plant species in two patches of native vegetation of the Chaco Serrano Woodland, central Argentina, the largest dry forest area in South America. Of the 128 plant species investigated (belonging to 111 genera in 53 families), 114 were colonized by arbuscular mycorrhizal fungi (AM), orchid mycorrhizal associations were present in the five terrestrial orchid species analyzed, one ectomycorrhiza was only present in Salix humboldtiana Willd., and 96 harbored a dark septate endophyte (DSE) association. Co-occurrence of AM and DSE was observed in 88 plant species. We determine morphological types of arbuscular mycorrhizal fungi (Arum, Paris, and intermediate AM structures) and report the mycorrhizal status in 106 new species, 12 of which are endemic to central Argentina and two, Aa achalensis Schltr. and Buddleja cordobensis Griseb., are declared to be vulnerable species. Root colonization in the Chaco Serrano Woodland is widespread and should be considered in revegetation programs due to the deterioration of this particular ecosystem. Considering the predominance of AM and DSE associations and the various potential benefits that these associations may bring to plant establishment, they should receive special attention in conservation and reforestation of these woodlands.     

Mycorrhizal colonisation in plants from intermittent aquatic habitats

Several plant species with amphibious characteristics from intermittent aquatic habitats were examined for colonisation with arbuscular mycorrhizal fungi (AM), dark septate endophytes (DSE) and the ratio of aerenchyma in root tissue. We studied submerged specimens of Alisma plantago-aquatica, Mentha aquatica, Myosotis scorpioides, Oenanthe fistulosa, Gratiola officinalis, Glyceria fluitans, Sium latifolium and Teucrium scordium. In the first four, we also examined the emerged growth forms, which were grown under experimental conditions. Roots of all species were mycorrhizal and showed AM and DSE colonisation. The results suggest that AM colonisation may also be abundant in plants of aquatic environment. Arbuscules were not found in submerged specimens of M. aquatica, O. fistulosa and S. latifolium. The AM colonisation was generally higher in emerged specimens as compared to submerged ones. The aerenchyma ratio in root cross-sections ranged from 10 to 50% and in most cases did not differ between submerged and emerged specimens. No clear relationship between AM colonisation and aerenchyma ratio was recognized, while a positive correlation between AM and plant available phosphorous was established.     

Dark septate endophyte and arbuscular mycorrhizal status of vegetation colonizing a bottomland hardwood forest after a 100 year flood

Levels of arbuscular mycorrhizal (AM) colonization and dark septate endophyte (DSE) colonization were assessed in the vegetation recolonizing a remnant bottomland hardwood forest in north central Texas following a 100 year flood. Thirty seven plant species representing 21 dicotyledonous and 2 montocotyledonous families established following floodwater recession. AM and/or DSE were found in all species. AM colonization was found in 31 out of the 37 species assessed including both monocotyledonous families (Poaceae and Cyperaceae) and 17 out of 21 dicotyledonous families (Acanthaceae, Asteraceae, Boraginaceae, Cucurbitaceae, Euphorbiaceae, Lamiaceae, Loganiaceae, Lythraceae, Malvaceae, Onagraceae, Pedaliaceae, Ranunculaceae, Sapindaceae, Scrophulariaceae, Solanaceae, Verbanaceae and Violaceae). DSE were found in 31 out of 37 species assessed including both monocotyledonous families and 15 out of 21 dicotyledonous families (Amaranthaceae, Asteraceae, Boraginaceae, Brassicaceae, Cucurbitaceae, Euphorbiaceae, Lamiaceae, Lythraceae, Malvaceae, Pedaliaceae, Phytolaccaceae, Polygonaceae, Ranunculaceae, Sapindaceae, Scrophulariaceae and Violaceae). There were no detectable differences in AM or DSE colonization levels among wetland indicator groups (p > 0.05). Levels of DSE colonization were negatively correlated with vesicular colonization and hyphal colonization for the obligate wetland species. There were no other significant relationships between AM and DSE colonization detected. Spearman rank order correlation coefficients did not differ significantly among wetland indicatory category for any level of AM or DSE colonization.     

Mycorrhizal and dark septate fungal associations in shola species of Western Ghats, southern India

We analyzed mycorrhizal types and dark septate endophyte (DSE) fungal associations in a shola vegetation of Western Ghats region, southern India. Plants belonging to 29 species of 19 families were assessed for mycorrhizal type and DSE fungal association. Five mycorrhizal classes were classified based on morphological traits: arbuscular, ecto-, ectendo-, ericoid-, and orchid mycorrhizas. Arbuscular mycorrhizal (AM) association was the most predominant mycorrhizal type, occurring in 16 plant species, followed by orchid (3 species), ericoid- (2 species), and ecto- and ectendomycorrhizas (1 species each). Mycorrhizal association is reported for the first time in 19 plant species. DSE fungal association was found in six plant species. Arum- and Paris-type AM morphology was found, respectively, in 10 and 5 plant species, with intermediate type recorded in one species. In this study, some new records on the morphological types of AM in some plant families were obtained. Further occurrence of ectendomycorrhizas in Pinus oocarpa and dark septate fungal association in Eleaocarpus munronii, Symplocos cochinchiensis, Daphniphyllum neilgherrense, Euodia roxburghiana, Syzygium arnottianum, and Syzygium montanum are reported for the first time. Roots of Berberis tinctoria, Mahonia leschenaultii (Berberidaceae), Elaeagnus latifolia (Elaeagnaceae), and Elaeocarpus oblongus (Elaeocarpaceae) lacked any fungal structures.     

Contrasting preferences of arbuscular mycorrhizal and dark septate fungi colonizing boreal and subarctic Avenella flexuosa

Arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi are ubiquitous in grass roots, but their colonizations may vary according to latitudinal gradient and site conditions. We investigated how vegetation zone (boreal vs. subarctic), humus thickness, and site openness affect root fungal colonizations of the grass Avenella flexuosa. More precisely, we hypothesized that AM and DSE fungal colonizations would have different responses to environmental conditions such that AM fungi could be more common in boreal zone, whereas we expected DSE fungi to be more affected by the amount of humus. We found site openness to affect AM and DSE fungi in a contrasting manner, in interaction with the vegetation zone. AM colonization was high at open coastal dunes, whereas DSE fungi were more common at forested sites, in the boreal zone. Humus thickness affected AM fungi negatively and DSE fungi positively. To conclude, the observed AM and DSE fungal colonization patterns were largely contrasting. AM fungi were favored in seashore conditions characterized by thin humus layer, whereas DSE fungi were favored in conditions of higher humus availability.     

Contrasting impacts of defoliation on root colonization by arbuscular mycorrhizal and dark septate endophytic fungi of Medicago sativa

Individual plants typically interact with multiple mutualists and enemies simultaneously. Plant roots encounter both arbuscular mycorrhizal (AM) and dark septate endophytic (DSE) fungi, while the leaves are exposed to herbivores. AMF are usually beneficial symbionts, while the functional role of DSE is largely unknown. Leaf herbivory may have a negative effect on root symbiotic fungi due to decreased carbon availability. However, evidence for this is ambiguous and no inoculation-based experiment on joint effects of herbivory on AM and DSE has been done to date. We investigated how artificial defoliation impacts root colonization by AM (Glomus intraradices) and DSE (Phialocephala fortinii) fungi and growth of Medicago sativa host in a factorial laboratory experiment. Defoliation affected fungi differentially, causing a decrease in arbuscular colonization and a slight increase in DSE-type colonization. However, the presence of one fungal species had no effect on colonization by the other or on plant growth. Defoliation reduced plant biomass, with this effect independent of the fungal treatments. Inoculation by either fungal species reduced root/shoot ratios, with this effect independent of the defoliation treatments. These results suggest AM colonization is limited by host carbon availability, while DSE may benefit from root dieback or exudation associated with defoliation. Reductions in root allocation associated with fungal inoculation combined with a lack of effect of fungi on plant biomass suggest DSE and AMF may be functional equivalent to the plant within this study. Combined, our results indicate different controls of colonization, but no apparent functional consequences between AM and DSE association in plant roots in this experimental setup.     

Fungal root endophyte associations of plants endemic to the Pamir Alay Mountains of Central Asia

The fungal root endophyte associations of 16 species from 12 families of plants endemic to the Pamir Alay Mountains of Central Asia are presented. The plants and soil samples were collected in Zeravshan and Hissar ranges within the central Pamir Alay mountain system. Colonization by arbuscular mycorrhizal fungi (AMF) was found in 15 plant species; in 8 species it was of the Arum type and in 4 of the Paris type, while 3 taxa revealed intermediate arbuscular mycorrhiza (AM) morphology. AMF colonization was found to be absent only in Matthiola integrifolia, the representative of the Brassicaceae family. The AM status and morphology are reported for the first time for all the species analyzed and for the genera Asyneuma, Clementsia, and Eremostachys. Mycelia of dark septate endophytes (DSE) accompanied the AMF colonization in ten plant species. The frequency of DSE occurrence in the roots was low in all the plants, with the exception of Spiraea baldschuanica. However, in the case of both low and higher occurrence, the percentage of DSE root colonization was low. Moreover, the sporangia of Olpidium spp. were sporadically found inside the root epidermal cells of three plant species. Seven AMF species (Glomeromycota) found in the trap cultures established with soils surrounding roots of the plants being studied were reported for the first time from this region of Asia. Our results provide information that might well be of use to the conservation and restoration programmes of these valuable plant species. The potential application of beneficial root-inhabiting fungi in active plant protection projects of rare, endemic and endangered plants is discussed.     

荒漠沙蒿根围AM真菌和DSE的空间分布

2009年7月在内蒙古黑城子北、多伦县城东和正蓝旗元上都遗址3个样地分别从0-10 cm、10-20 cm、20-30cm、30-40 cm和40-50 cm 5个土层采集沙蒿(Artemisia sphaerocephala)根围土壤和根样,系统研究了沙蒿根围AM真菌和DSE(Dark septate endophytes)的空间分布及与土壤因子的相关性。结果表明,沙蒿根系能被AM真菌高度侵染形成典型的I-型(Intermediate type)丛枝菌根,并发育形成泡囊和丛枝结构, 并与DSE形成良好的共生关系,样地生态条件和采样深度对AM真菌分布和活动有显著影响。黑城子样地孢子密度最高,元上都样地泡囊定殖率最高,不同样地间丛枝、菌丝、总定殖率和DSE定殖率无显著差异。孢子密度峰值出现在0-10cm表层土,并随土壤剖面深度增加而降低;泡囊定殖率峰值出现在10-20cm土层;AM真菌其他结构定殖率及DSE定殖率在各土层间差异不显著或变化无规律。孢子密度与AM真菌不同结构定殖率无显著相关性,与各土壤因子极显著正相关。泡囊定殖率与脲酶和碱性磷酸酶极显著负相关,与酸性磷酸酶显著负相关。菌丝定殖率、总定殖率及DSE定殖率与各土壤因子均无显著相关性。土壤碱解N和有机C与脲酶、酸性磷酸酶和碱性磷酸酶极显著正相关;土壤速效P与碱性磷酸酶极显著正相关,与脲酶显著正相关。对沙蒿根系AM真菌和DSE真菌分布和定殖规律的研究,可进一步明确AM真菌和DSE的生态功能,为利用菌根生物技术促进荒漠植被恢复和生态重建提供依据。     

Seasonal and temporal dynamics of arbuscular mycorrhizal and dark septate endophytic fungi in a tallgrass prairie ecosystem are minimally affected by nitrogen enrichment

Root colonization by arbuscular mycorrhizae (AM) and dark septate endophytic (DSE) fungi in nitrogen amended and unamended mixed tallgrass prairie communities were analyzed monthly over two growing seasons. Roots were stained with Trypan blue and Sudan IV and fungal structures quantified using the modified magnified intersections method. Root length colonized (RLC) by DSE exceeded AM colonization during early part of the growing season. Fungal colonization varied among the years and was greater in 2003 than in 2002. Seasonal variation among the months within a growing season was observed in 2002 but not in 2003 for both AM and DSE. AM fungi were most abundant during the peak growing season of dominant C₄ vegetation while DSE were most abundant during the early part of the growing season. Hyperparasitism of AM hyphal coils by melanized septate fungi was frequently observed and increased with AM coil frequency. Although nitrogen amendment had altered the plant community composition, it had no impact on the colonization by AM or DSE fungi.     

Species composition and colonization of dark septate endophytes are affected by host plant species and soil depth in the Mu Us sandland,northwest China

Investigations into the edaphic associations, host affiliations and soil depth of dark septate endophytes (DSE) in arid desert environments can help explain their spatial distribution and the response mechanisms in desert ecosystems. Soils were sampled to a depth of 50 cm in the rhizospheres of Psammochloa villosa, Hedysarum laeve and Artemisia ordosica in the Mu Us sandland of northwest China in July 2015. The plant species and soil depth significantly influenced the distribution and colonization of DSE. Hyphal and total root colonization were significantly higher under P. villosa than the others in the 0–20 cm layer. The maximum colonization of P. villosa and H. laeve occurred in the 10–20 cm and 20–30 cm soil layers, respectively, while 30–40 cm soil layer under A. ordosica. Of twelve DSE species isolated from the roots of these plants, Phoma radicina and Bipolaris zeae were reported in desert ecosystems for the first time. Hyphal colonization was significantly and positively correlated with soil total nitrogen (TN) and significantly and negatively correlated with the soil carbon/nitrogen (C/N) ratio. Microsclerotial colonization was significantly and positively correlated with soil organic carbon (SOC), and total colonization was significantly and positively correlated with soil TN and total phosphorus (TP) and significantly and negatively correlated with soil C/N. Variation of DSE colonization was mostly attributed to effects of plant species. We concluded that the species composition and colonization of the DSE fungi were influenced by the plant species, soil depth and soil nutrient availability in this desert ecosystem. This research provides a basis for further understanding the ecological adaptability of DSE and their roles in promoting vegetation restoration and reducing desertification in arid ecosystems.     

Arbuscular mycorrhizal fungi as (agro)ecosystem engineers

Symbiotic interactions have been shown to facilitate shifts in the structure and function of host plant communities. For example, parasitic plants can induce changes in plant diversity through the suppression of competitive community dominants. Arbuscular mycorrhizal (AM) fungi have also be shown to induce shifts in host communities by increasing host plant nutrient uptake and growth while suppressing non-mycorrhizal species. AM fungi can therefore function as ecosystem engineers facilitating shifts in host plant communities though the presumed physiological suppression of non-contributing or non-mycorrhizal plant species. This dichotomy in plant response to AM fungi has been suggested as a tool to suppress weed species (many of which are non-mycorrhizal) in agro-ecosystems where mycorrhizal crop species are cultivated. Rinaudo et al. (2010), this issue, have demonstrated that AM fungi can suppress pernicious non-mycorrhizal weed species including Chenopodium album (fat hen) while benefiting the crop plant Helianthus annuus (sunflower). These findings now suggest a future for harnessing AM fungi as agro-ecosystem engineers representing potential alternatives to costly and environmentally damaging herbicides.     

Dark Septate Root Endophytic Fungus <Emphasis Type="Italic">Nectria haematococca</Emphasis> Improves Tomato Growth Under Water Limiting Conditions

The ascomycetous dark septate endophytic (DSE) fungi characterized by their melanized hyphae can confer abiotic stress tolerance in their associated plants in addition to improving plant growth and health. In this study inoculation of the DSE fungus Nectria haematococca Berk. & Broome significantly improved all the plant growth parameters like the plant height, stem girth, leaf characteristics and plant biomass of drought-stressed tomato. Root characters like the total root length, primary root diameter, 2nd order root number and diameter, root hair number and length were also significantly influenced by the fungal inoculation. Nevertheless, N. haematococca inoculation did not affect root colonization by native arbuscular mycorrhizal (AM) fungi and no significant correlation existed between the AM and DSE fungal variables examined. The proline accumulation in shoots of N. haematococca inoculated plants was significantly higher than uninoculated plants. The present study clearly indicates for the first time the ability of the DSE fungus, N. haematococca in inducing the drought stress tolerance and promoting the growth of the host plant under water stress.     

Indigenous arbuscular mycorrhizal fungal assemblages protect grassland host plants from pathogens

Plant roots can establish associations with neutral, beneficial and pathogenic groups of soil organisms. Although it has been recognized from the study of individual isolates that these associations are individually important for plant growth, little is known about interactions of whole assemblages of beneficial and pathogenic microorganisms associating with plants.We investigated the influence of an interaction between local arbuscular mycorrhizal (AM) fungal and pathogenic/saprobic microbial assemblages on the growth of two different plant species from semi-arid grasslands in NE Germany (Mallnow near Berlin). In a greenhouse experiment each plant species was grown for six months in either sterile soil or in sterile soil with one of three different treatments: 1) an AM fungal spore fraction isolated from field soil from Mallnow; 2) a soil pathogen/saprobe fraction consisting of a microbial community prepared with field soil from Mallnow and; 3) the combined AM fungal and pathogen/saprobe fractions. While both plant species grew significantly larger in the presence of AM fungi, they responded negatively to the pathogen/saprobe treatment. For both plant species, we found evidence of pathogen protection effects provided by the AM fungal assemblages. These results indicate that interactions between assemblages of beneficial and pathogenic microorganisms can influence the growth of host plants, but that the magnitude of these effects is plant species-specific.     

Mycorrhizas and dark septate root endophytes in polar regions

We review the distributions and functions of mycorrhizas and dark septate root endophytes in polar regions. Arbuscular mycorrhizas (AM) are present in the Arctic and Antarctic to 82 °N and 63 °S, respectively, with fine endophyte being the dominant form of AM in roots at higher latitudes. Ecto- (ECM) and ericoid (ERM) mycorrhizas both occur in the Arctic to 79 °N, owing to the presence of species of Salix, Dryas, Vaccinium and Cassiope to this latitude. ECM and ERM are not present in Antarctic ecosystems, owing to an absence of suitable hosts. Arbutoid and orchid mycorrhizas are infrequent in the Arctic, whilst the latter are present at one location in the sub-Antarctic. Data from studies of AM, ECM and ERM colonisation along a latitudinal transect through the Arctic indicate that the frequency of plant species not colonised by mycorrhizas increases at higher latitudes, largely owing to an increase in non-mycorrhizal and a decrease in obligately mycorrhizal plant families at more northerly locations. A separate group of root- and rhizoid-associated fungi, the dark septate root endophytes (DSE), are widespread to 82 °N and 77 °S, and are apparently more frequent than mycorrhizal fungi in polar regions. The functions of DSE are largely unclear, but studies suggest beneficial effects on plant growth under defined conditions. We advocate further research into the effects of DSE on their host plants in polar regions.