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Salt Stress Tolerance of Dark Septate Endophytes Is Independent of Melanin Accumulation.

ABSTRACT: Dark septate endophytes (DSEs) represent a diverse group of root-endophytic fungi that have been isolated from plant roots in many different natural and anthropogenic ecosystems. Melanin is widespread in eukaryotic organisms and possesses various functions such as protecting human skin from UV radiation, affecting the virulence of pathogens, and playing a role in development and physiology of insects. Melanin is a distinctive feature of the cell walls of DSEs and has been thought to protect these fungi from abiotic stress. Melanin in DSEs is assumed to be synthesized via the 1,8-dihydroxynaphthalene (DHN) pathway. Its function in alleviation of salt stress is not yet known. The aims of this study were: (i) investigating the growth responses of three DSEs (Periconia macrospinosa, Cadophora sp., and Leptodontidium sp.) to salt stress, (ii) analyzing melanin production under salt stress and, (iii) testing the role of melanin in salt stress tolerance of DSEs. The study shows that the three DSE species can tolerate high salt concentrations. Melanin content increased in the hyphae of all DSEs at 100 mM salt, but decreased at 500 mM. This was not reflected in the RNA accumulation of the gene encoding scytalone dehydratase which is involved in melanin biosynthesis. The application of tricyclazole, a DHN-melanin biosynthesis inhibitor, did not affect either salt stress tolerance or the accumulation of sodium in the hyphae. In addition, melanin biosynthesis mutants of Leptodontidium sp. did not show decreased growth performance compared to the wild-type, especially not at high salt concentrations. This indicates that DSEs can live under salt stress and withstand these conditions regardless of melanin accumulation.

SUBMITTER: Gaber DA

PROVIDER: S-EPMC7758464 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Salt Stress Tolerance of Dark Septate Endophytes Is Independent of Melanin Accumulation.

Gaber Dalia A DA Berthelot Charlotte C Camehl Iris I Kovács Gábor M GM Blaudez Damien D Franken Philipp P

Frontiers in microbiology 20201210

Dark septate endophytes (DSEs) represent a diverse group of root-endophytic fungi that have been isolated from plant roots in many different natural and anthropogenic ecosystems. Melanin is widespread in eukaryotic organisms and possesses various functions such as protecting human skin from UV radiation, affecting the virulence of pathogens, and playing a role in development and physiology of insects. Melanin is a distinctive feature of the cell walls of DSEs and has been thought to protect thes ...[more]

PMID: 33362727

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Project description:Fungal endophytes can improve plant tolerance to abiotic stress conditions. Dark septate endophytes (DSEs) belong to phylogenetically non-related groups of root colonizing fungi among the Ascomycota with high melanin-producing activities. They can be isolated from roots of more than 600 plant species in diverse ecosystems. Still the knowledge about their interaction with host plants and their contribution to stress alleviation is limited. The current work aimed to test the abilities of three DSEs (Periconia macrospinosa, Cadophora sp., Leptodontidium sp.) to alleviate moderate and high salt stress in tomato plants. By including an albino mutant, the role of melanin for the interaction with plants and salt stress alleviation could also be tested. P. macrospinosa and Cadophora sp. improved shoot and root growth 6 weeks after inoculation under moderate and high salt stress conditions. No matter how much salt stress was applied, macroelement (P, N, and C) contents were unaffected by DSE inoculation. The four tested DSE strains successfully colonized the roots of tomato, but the colonization level was clearly reduced in the albino mutant of Leptodontidium sp. Any difference in the effects on plant growth between the Leptodontidium sp. wild type strain and the albino mutant could, however, not be observed. These results show that particular DSEs are able to increase salt tolerance as they promote plant growth specifically under stress condition. Increased plant biomasses combined with stable nutrient contents resulted in higher P uptake in shoots of inoculated plants at moderate and high salt conditions and higher N uptake in the absence of salt stress in all inoculated plants, in P. macrospinosa-inoculated plants at moderate salt condition and in all inoculated plants except the albino mutants at high salt condition. In summary, melanin in DSEs seems to be important for the colonization process, but does not influence growth, nutrient uptake or salt tolerance of plants.

Project description:Although the ecological function of dark septate endophytes (DSEs) is well studied, little is known about the responses of the host plant to DSEs obtained from other plants, especially under conditions of heavy metal stress. This study aimed to investigate how DSEs from a heavy-metal habitat affect non-host plants in cadmium (Cd) stress soils, which then provides a basis for the application of DSEs in the cultivation of different plant and soil remediation strategies for polluted ecosystems. We isolated and identified two species of DSE (Acrocalymma vagum and Scytalidium lignicola) inhabiting the roots of Ilex chinensis (host plant) which are grown in metal-polluted habitats. Then, the Cd stress tolerance of the DSEs was tested using a pure culture of which the Cd concentration has been adjusted. Subsequently, we examined the performance of non-host plants (Medicago sativa and Ammopiptanthus mongolicus) which were inoculated with DSEs under Cd stress in a growth chamber. The results indicated that the two DSEs could grow under Cd stress in vitro, even when not exhibiting high levels of tolerance to Cd. The superoxide dismutase (SOD), malondialdehyde (MDA), glutathione (GSH), soluble protein, and melanin of the DSE fungi reached maximal levels at concentrations of 30-60 mg Cd/L, indicating the important preventive strategies adopted by the DSE fungi in environments contaminated by Cd. Despite a decreased biomass of DSE hyphae with enhanced Cd concentrations, the accumulation of Cd in the DSE hyphae tended to show an increasing trend. Both DSEs were effective colonizers of the non-host plants. A. vagum and S. lignicola inoculation significantly promoted the biomass and the root architecture of the two non-host plants under Cd stress. A. vagum inoculation increased the total nitrogen (TN) of A. mongolicus, whereas inoculation with S. lignicola significantly increased the organic carbon (OC) of M. sativa. In particular, the DSE inoculation significantly improved the accumulation of Cd in plant tissues under Cd stress, demonstrating a potential application in the bio-remediation of heavy-metal-pollution areas. Our findings suggest that the DSE inoculation improved the root growth and nutrient absorption of non-host plants, altered the soil Cd concentration, and facilitated plant growth and survival under Cd stress. These results contribute to a better understanding of DSE-plant interactions in habitats contaminated by heavy metals.

Project description:BACKGROUND: Fungi are asexually and sexually reproducing organisms that can combine the evolutionary advantages of the two reproductive modes. However, for many fungi the sexual cycle has never been observed in the field or in vitro and it remains unclear whether sexual reproduction is absent or cryptic. Nevertheless, there are indirect approaches to assess the occurrence of sex in a species, such as population studies, expression analysis of genes involved in mating processes and analysis of their selective constraints. The members of the Phialocephala fortinii s. l. - Acephala applanata species complex (PAC) are ascomycetes and the predominant dark septate endophytes that colonize woody plant roots. Despite their abundance in many ecosystems of the northern hemisphere, no sexual state has been identified to date and little is known about their reproductive biology, and how it shaped their evolutionary history and contributes to their ecological role in forest ecosystems. We therefore aimed at assessing the importance of sexual reproduction by indirect approaches that included molecular analyses of the mating type (MAT) genes involved in reproductive processes. RESULTS: The study included 19 PAC species and > 3, 000 strains that represented populations from different hosts, continents and ecosystems. Whereas A. applanata had a homothallic (self-fertile) MAT locus structure, all other species were structurally heterothallic (self-sterile). Compatible mating types were observed to co-occur more frequently than expected by chance. Moreover, in > 80% of the populations a 1:1 mating type ratio and gametic equilibrium were found. MAT genes were shown to evolve under strong purifying selection. CONCLUSIONS: The signature of sex was found in worldwide populations of PAC species and functionality of MAT genes is likely preserved by purifying selection. We hypothesize that cryptic sex regularely occurs in the PAC and that further field studies and in vitro crosses will lead to the discovery of the sexual state. Although structurally heterothallic species prevail, it cannot be excluded that homothallism represents the ancestral breeding system in the PAC.

Project description:This study mainly aimed to investigate the effects of dark septate endophytes (DSE) (Acrocalymma vagum, Paraboeremia putaminum, and Fusarium acuminatum) on the growth and microbial community composition in the rhizosphere soil of a medicinal plant, licorice (Glycyrrhiza uralensis), grown in the non-sterile soil under drought stress. The results showed that three DSE strains could effectively colonize the plant roots and form a strain-dependent symbiosis with licorice. Although drought stress declined the growth of licorice plants, these decreases were partly recovered by DSE inoculation. Specifically, the inoculation of A. vagum and P. putaminum significantly increased the biomass and glycyrrhizin content, whereas A. vagum and F. acuminatum increased glycyrrhizic acid content of host plants under drought stress. However, the inoculation of F. acuminatum showed significant negative effects on the shoot, root, and total biomass of licorice plants. In addition, the effects of DSE inoculation on the morphological, photosynthetic, and antioxidant parameters of licorice plants, and mineral nutrient and microbial community composition in the rhizosphere soil were dependent on the DSE species as well as water regime. Interestingly, DSE inoculation significantly increased AM fungi content under drought stress. In addition, DSE associated with water had a significant positive influence on soil organic matter, available phosphorus (P), AM fungi, leaf number, soluble protein, SOD activity, total root length, root branch, and glycyrrhizic acid content. Based on the results of variance partitioning analysis, 17.0, 34.0, 14.9, 40.1, 28.2, and 18.0% variations in shoot morphology, root morphology, plant biomass, active ingredient, photosynthetic parameters, and antioxidant parameters, respectively, were attributable to the presence of certain soil microorganisms. These findings suggest the possibility that DSE inoculation improved the root development and nutrient absorption of host plants, altered the soil microbiota, and might also contribute to plant growth and survival under drought conditions. As A. vagum exhibited positive effects on the plant biomass, morphological and physiological parameters, and active ingredient content in licorice plants under drought stress, it was considered to be the best fungus for licorice cultivation. These results contribute to the understanding of the ecological function of DSE fungi in dryland agriculture.

Project description:Drought is a major abiotic stress factor affecting plant growth and production, while utilizing beneficial endophytic fungi is one of the most promising strategies for enhancing plant growth and drought tolerance. In the current study, a pot experiment was conducted to investigate the beneficial effects of dark septate endophyte (DSE) (Macrophomina pseudophaseolina, Paraphoma radicina) and Trichoderma (Trichoderma&nbsp;afroharzianum, Trichoderma&nbsp;longibrachiatum) inoculum on Astragalus mongholicus grown in sterile soil under drought stress, alone, or in combination. The addition of Trichoderma enhanced the DSE colonization in roots regardless of the water condition. Under well-watered conditions, M. pseudophaseolina inoculation significantly enhanced the biomass and root length of A. mongholicus. The two DSE and Trichoderma inoculum significantly improved calycosin-7-O-β-D-glucoside content. However, M.&nbsp;pseudophaseolina + T.&nbsp;afroharzianum inoculation better promoted root growth, whereas co-inoculation had higher active ingredient contents compared with single inoculation, except for P. radicina + T.&nbsp;afroharzianum. Under drought stress, DSE and Trichoderma inoculum significantly improved root biomass, root length, calycosin-7-O-β-D-glucoside content, and activities of nitrate reductase and soil urease. P. radicina + T.&nbsp;afroharzianum and P. radicina + T.&nbsp;longibrachiatum better increased root length, and all combinations of DSE and Trichoderma had a greater impact on the increase in formononetin content compared with the single treatments. Additionally, Trichoderma relies on antioxidant enzymes, growth hormones, and the redox system (ascorbic acid-glutathione) to resist drought, while DSE strains have an additional osmotic regulation system in addition to the drought resistance function possessed by Trichoderma, and the effect of co-inoculation (especially M. pseudophaseolina + T.&nbsp;longibrachiatum and P. radicina + T.&nbsp;afroharzianum) on plant physiological parameters was greater than that of single inoculation. This study provides a new research direction for the effects of DSE and Trichoderma on medicinal plant cultivated in dryland.

Dataset Information

Salt Stress Tolerance of Dark Septate Endophytes Is Independent of Melanin Accumulation.

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Salt Stress Tolerance of Dark Septate Endophytes Is Independent of Melanin Accumulation.

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