A meta-analysis of plant responses to dark septate root endophytes
TL;DR: It is suggested that DSE enhance plant performance under controlled conditions, particularly when all, or the majority, of N is available in organic form.
Abstract: Summary
•Dark septate endophytes (DSE) frequently colonize roots in the natural environment, but the effects of these fungi on plants are obscure, with previous studies indicating negative, neutral or positive effects on plant performance
•In order to reach a consensus for how DSE influence plant performance, meta-analyses were performed on data from 18 research articles, in which plants had been inoculated with DSE in sterile substrates
•Negative effects of DSE on plant performance were not recorded Positive effects were identified on total, shoot and root biomass, and on shoot nitrogen (N) and phosphorus contents, with increases of 26–103% in these parameters for plants inoculated with DSE, relative to uninoculated controls Inoculation increased total, shoot and root biomass by 52–138% when plants had not been supplied with additional inorganic N, or when all, or the majority, of N was supplied in organic form Inoculation with the DSE Phialocephala fortinii was found to increase shoot and root biomass, shoot P concentration and shoot N content by 44–116%, relative to uninoculated controls
•The analyses here suggest that DSE enhance plant performance under controlled conditions, particularly when all, or the majority, of N is available in organic form
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TL;DR: This review focuses on microbe-mediated plant salt tolerance, in particular on the physiological and molecular mechanisms underlying root-microbe symbiosis, and opens a new avenue for capitalizing on the cultivable microbiome to strengthen plant saltolerance and thus to refine agricultural practices and production under saline conditions.
238 citations
TL;DR: In all global change scenarios, except elevated CO2, fungal symbionts significantly altered plant responses to global change, and the results show that considering plant-fungal symbioses is critical to predicting ecosystem response toglobal change.
Abstract: While direct plant responses to global change have been well characterized, indirect plant responses to global change, via altered species interactions, have received less attention. Here, we examined how plants associated with four classes of fungal symbionts (class I leaf endophytes [EF], arbuscular mycorrhizal fungi [AMF], ectomycorrhizal fungi [ECM], and dark septate endophytes [DSE]) responded to four global change factors (enriched CO2, drought, N deposition, and warming). We performed a meta-analysis of 434 studies spanning 174 publications to search for generalizable trends in responses of plant-fungal symbioses to future environments. Specifically, we addressed the following questions: (1) Can fungal symbionts ameliorate responses of plants to global change? (2) Do fungal symbiont groups differ in the degree to which they modify plant response to global change? (3) Do particular global change factors affect plant-fungal symbioses more than others? In all global change scenarios, except elevated CO2, fungal symbionts significantly altered plant responses to global change. In most cases, fungal symbionts increased plant biomass in response to global change. However, increased N deposition reduced the benefits of symbiosis. Of the global change factors we considered, drought and N deposition resulted in the strongest fungal mediation of plant responses. Our analysis highlighted gaps in current knowledge for responses of particular fungal groups and revealed the importance of considering not only the nonadditive effects of multiple global change factors, but also the interactive effects of multiple fungal symbioses. Our results show that considering plant-fungal symbioses is critical to predicting ecosystem response to global change.
229 citations
TL;DR: It is suggested that long-term nitrogen and phosphorous fertilizer regimes reduced fungal biodiversity and changed community composition in black soil in northeast China.
Abstract: Black soil is one of the main soil types in northeast China, and plays an important role in Chinese crop production. However, nitrogen inputs over 50 years have led to reduced black soil fertility. It is unclear how N affects the fungal community in this soil type, so a long-term fertilizer experiment was begun in 1980 and we applied 454 pyrosequencing and quantitative PCR to targeted fungal ITS genes. There were five treatments: control (no fertilizer), N1 (low nitrogen fertilizer), N2 (high nitrogen fertilizer), N1P1 (low nitrogen plus low phosphorus fertilizers) and N2P2 (high nitrogen plus high phosphorus fertilizers). Soil nutrient concentrations (Total N, Avail N, NO3−, NH4+, etc.) and ITS gene copy numbers increased, whereas soil pH and fungal diversity decreased in all the fertilized treatments. Relationships between soil parameters and fungal communities were evaluated. Dothideomycetes, Eurotiomycetes, Leotiomycetes, Sordariomycetes, and Agaricomycetes were the most abundant classes in all soils. Principal coordinates analysis showed that the fungal communities in the control and lower-fertilizer treatments clustered closely and were separated from communities where more concentrated fertilizers were used. Fungal diversity and ITS gene copy number were dependent on soil pH. Our findings suggested that long-term nitrogen and phosphorous fertilizer regimes reduced fungal biodiversity and changed community composition. The influence of the more concentrated fertilizer treatments was greater than the lower concentrations.
228 citations
TL;DR: It is argued that practices used in plant breeding, seed treatments and agriculture are among the reasons for the loss of fungal endophytes diversity in domesticated plants and accounts for the reduced effectiveness of some endophyte strains to confer plant benefits.
227 citations
Cites background from "A meta-analysis of plant responses ..."
...Metaanalyses performed by Newsham (2011) on data from 18 research articles, in which plants had been inoculated with DSE species indicated that they can enhance plant performance under controlled conditions, particularly when most of the nitrogen is available in an organic form such as proteins,…...
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...…cold- and water-stressed environments, arbuscular mycorrhizal fungi, the typical mutualists of grass roots at lower altitudes and latitudes, are essentially absent (Newsham, 2011) and it has been suggested that DSE species might act as surrogate mycorrhiza in these habitats (Bledsoe et al., 1990)....
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...Plants apparently do not benefit from DSE species when roots can readily access inorganic nitrogen (Newsham, 2011). by guest on Septem ber 15, 2016 http://fem sec.oxfordjournals.org/ D ow nloaded from...
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TL;DR: New innovative methods and the associated new insights into plant–fungal interactions are reviewed and the potential of fungi in preventing plant diseases, improving plant productivity and understanding ecosystem stability is understood.
Abstract: Fungi interact with plants in various ways, with each interaction giving rise to different alterations in both partners. While fungal pathogens have detrimental effects on plant physiology, mutualistic fungi augment host defence responses to pathogens and/or improve plant nutrient uptake. Tropic growth towards plant roots or stomata, mediated by chemical and topographical signals, has been described for several fungi, with evidence of species-specific signals and sensing mechanisms. Fungal partners secrete bioactive molecules such as small peptide effectors, enzymes and secondary metabolites which facilitate colonization and contribute to both symbiotic and pathogenic relationships. There has been tremendous advancement in fungal molecular biology, omics sciences and microscopy in recent years, opening up new possibilities for the identification of key molecular mechanisms in plant–fungal interactions, the power of which is often borne out in their combination. Our fragmentary knowledge on the interactions between plants and fungi must be made whole to understand the potential of fungi in preventing plant diseases, improving plant productivity and understanding ecosystem stability. Here, we review innovative methods and the associated new insights into plant–fungal interactions.
220 citations
Cites background from "A meta-analysis of plant responses ..."
...In contrast, dark septate endophytes evoked an overall increase in root biomass (Alberton et al. 2010), shoot, root and total biomass as well as nitrogen and phosphorus content in the host plant (Newsham 2011)....
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References
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TL;DR: The approximate sampling distribution of the log response ratio is given, why it is a particularly useful metric for many applications in ecology, and how to use it in meta-analysis are discussed.
Abstract: Meta-analysis provides formal statistical techniques for summarizing the results of independent experiments and is increasingly being used in ecology. The response ratio (the ratio of mean outcome in the experimental group to that in the control group) and closely related measures of proportionate change are often used as measures of effect magnitude in ecology. Using these metrics for meta-analysis requires knowledge of their statistical properties, but these have not been previously derived. We give the approximate sampling distribution of the log response ratio, discuss why it is a particularly useful metric for many applications in ecology, and demonstrate how to use it in meta-analysis. The meta-analysis of response-ratio data is illustrated using experimental data on the effects of increased atmospheric CO2 on plant biomass responses.
3,042 citations
TL;DR: It is suggested that global standing stocks of mycorrhizal fungi may increase substantially under elevated CO2 but decline moderately under P additions, and effects of N deposition may be difficult to predict for individual ecosystems, with a slightly negative influence overall.
Abstract: Summary • Numerous field studies have measured mycorrhizal dynamics under additions of nitrogen (N), phosphorus (P), or atmospheric CO 2 to test the hypothesis that plants should invest in mycorrhizal fungi when soil nutrients are limiting. • Here meta-analyses were used to integrate nutrient responses across independent field-based studies. Responses were compared between ecto- and arbuscular mycorrhizal fungi, and among fertilizer types, methods of measurement, biomes, and lead investigators. Relationships between degree of response and study length, fertilization rates, total amounts of nutrients applied, and numbers of replicates were also tested. • Across studies, mycorrhizal abundance decreased 15% under N fertilization and 32% under P fertilization. Elevated CO 2 elicited a 47% increase. Nitrogen effects varied significantly among studies, and P effects varied significantly among lead investigators. Most other factors did not affect mycorrhizal responses. • These results support the plant investment hypothesis, and suggest that global standing stocks of mycorrhizal fungi may increase substantially under elevated CO 2 but decline moderately under P additions. Effects of N deposition may be difficult to predict for individual ecosystems, with a slightly negative influence overall.
1,066 citations
TL;DR: The current literature on DSE and the ecology is reviewed, the need for and direction of future research are discussed, and clear generalizations on their ecological role are drawn.
Abstract: Dark septate root endophytes (DSE) are conidial or sterile fungi (Deuteromycotina, Fungi Imperfecti) likely to be ascomycetous and colonizing plant roots. They have been reported for nearly 600 plant species representing about 320 genera and 100 families. DSE fungi occur from the tropics to arctic and alpine habitats and comprise a heterogeneous group that functionally and ecologically overlaps with soil fungi, saprotrophic rhizoplane-inhabiting fungi, obligately and facultatively pathogenic fungi and mycorrhizal fungi. Numerous species of undescribed sterile and anamorphic taxa may also await discovery. Although DSE are abundant in washed root and soil samples from various habitats, and are easily isolated from surface-sterilized roots of ecto-, ectendo-, endo- and non-mycorrhizal host species, their ecological functions are little understood. Studies of DSE thus far have yielded inconsistent results and only poorly illustrate the role of DSE in their natural habitats. These inconsistencies are largely due to the uncertain taxonomic affinities of the strains of DSE used. In addition, because different strains of a single anamorph taxon seem to vary greatly in function, no clear generalizations on their ecological role have been drawn. This paper reviews the current literature on DSE and the ecology and discusses the need for and direction of future research.
842 citations
TL;DR: It is concluded that DSE are capable of forming mutualistic associations functionally similar to mycorrhizas, and must be considered my Corrhizal, at least under some conditions.
Abstract: Dark septate endophytes (DSE) are a miscellaneous group of ascomycetous anamorphic fungi that colonize root tissues intracellularly and intercellularly. The limited selection of studies quoted here exemplifies the range of host responses to symbiotic DSE fungi. Like mycorrhizal associations, DSE associations vary from negative to neutral and positive when measured by host performance or host tissue nutrient concentrations. This range of host responses is partially attributable to variation between different fungus taxa and strains. Similarly, hosts differ in their responses to a single DSE strain. Experimental conditions may also govern the nature of the symbiotic association. It is concluded that DSE are capable of forming mutualistic associations functionally similar to mycorrhizas. If the variation in host response to mycorrhizal fungi is considered to represent a continuum ranging from parasitism to mutualism, DSE symbiosis must be considered mycorrhizal, at least under some conditions.
544 citations
TL;DR: The most likely functions of this poorly understood group of root-associated fungi are reviewed and it is proposed that, like mycorrhizal symbioses, DSE-plant Symbioses should be considered multifunctional and not limited to nutrient acquisition and resultant positive host growth responses.
544 citations