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Increasing temperature and decreasing precipitation has led to more frequent and extreme drought events in many regions throughout the world. In the western United States, multi‐year drought events have led to widespread plant mortality and extreme wildfires (Asner et al. 2016, Pickrell and Pennisi 2020). Communities of ectomycorrhizal fungi (EMF) ‐ root symbionts which play a critical role in forest health ‐ are also thought to be threatened by these climatic changes (Fernandez et al. 2017, Steidinger et al. 2019). However, altered soil moisture conditions have complex direct and indirect effects on both fungi and ecosystem processes, such as nutrient availability (Schimel 2018), making it difficult to elucidate the primary drivers of community composition based on field observations or experiments (Pena and Polle 2014). As a result, efforts to identify the genes or traits involved in response to drought events are critical for accurate prediction of future EMF composition and function (Allison and Treseder 2008, Romero‐Olivares et al. 2019). Despite this fact, we are not aware of any studies that have used gene expression analyses to measure the response of individual EMF to drought events or other climatic stressors.
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... 2003(Fu et al., -2017, to induce shifts in aboveground microbial assemblages (Debray et al., 2022(Debray et al., , in this issue pp. 2018(Debray et al., -2031 and to trigger transcriptional acclimation in the etomycorrhizal fungus Suillus pungens (Erlandson et al., 2022(Erlandson et al., , in this issue pp. 1910(Erlandson et al., -1913. ...
Earth’s temperature is rising, and with this increase, fungal communities are responding and affecting soil carbon processes. At a long-term soil-warming experiment in a boreal forest in interior Alaska, warming and warming-associated drying alters the function of microbes, and thus, decomposition of carbon. But what genetic mechanisms and resource allocation strategies are behind these community shifts and soil carbon changes? Here, we evaluate fungal resource allocation efforts under long-term experimental warming (including associated drying) using soil metatranscriptomics. We profiled resource allocation efforts toward decomposition and cell metabolic maintenance, and we characterized community composition. We found that under the warming treatment, fungi allocate resources to cell metabolic maintenance at the expense of allocating resources to decomposition. In addition, we found that fungal orders that house taxa with stress-tolerant traits were more abundant under the warmed treatment compared to control conditions. Our results suggest that the warming treatment elicits an ecological tradeoff in resource allocation in the fungal communities, with potential to change ecosystem-scale carbon dynamics. Fungi preferentially invest in mechanisms that will ensure survival under warming and drying, such as cell metabolic maintenance, rather than in decomposition. Through metatranscriptomes, we provide mechanistic insight behind the response of fungi to climate change and consequences to soil carbon processes.
A spatially explicit global map of tree symbioses with nitrogen-fixing bacteria and mycorrhizal fungi reveals that climate variables are the primary drivers of the distribution of different types of symbiosis.
Peroxisomes are ubiquitous organelles in eukaryotic cells that fulfill a variety of biochemical functions. The biogenesis of peroxisomes requires a variety of proteins named peroxins, which are encoded by PEX genes. Pex14/17 is a putative peroxin recently identified, specifically present in filamentous fungal species. Its function in peroxisomal biogenesis is still obscure and its roles in fungal pathogenicity are yet undocumented. Here, we demonstrated the contributions of Pex14/17 in the rice blast fungus Magnaporthe oryzae (Mopex14/17) to peroxisomal biogenesis and fungal pathogenicity by targeting gene replacement strategies. Mopex14/17 has properties of both Pex14 and Pex17 in protein sequence. Mopex14/17 is distributed at the peroxisomal membrane and is essential for efficient peroxisomal targeting of proteins containing peroxisomal targeting signal 1. The MoPEX19 deletion led to the cytoplasmic distribution of Mopex14/17, indicating the peroxisomal import of Pex14/17 depends on Pex19. The knockout mutants of MoPEX14/17 were reduced in fatty acids utilization, reactive oxygen species (ROS) degradation and cell wall integrity. Moreover, the Δmopex14/17 mutants were delayed in conidial generation and appressorial formation, and reduced in appressorial turgor accumulation and penetration ability into host plants. These defects resulted in a significant reduction of the virulence of the mutant. These data indicated that MoPEX14/17 plays crucial roles in peroxisome biogenesis and contributes to fungal development and pathogenicity. This article is protected by copyright. All rights reserved.
In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html.
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The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.
Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine
the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature
regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as
adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years,
acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations
for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate
resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
Mycorrhizal fungi have a key role in nitrogen (N) cycling, particularly in boreal and temperate ecosystems. However, the significance of ectomycorrhizal fungal (EMF) diversity for this important ecosystem function is unknown. Here, EMF taxon-specific N uptake was analyzed via (15)N isotope enrichment in complex root-associated assemblages and non-mycorrhizal root tips in controlled experiments. Specific (15)N enrichment in ectomycorrhizas, which represents the N influx and export, as well as the exchange of (15)N with the N pool of the root tip, was dependent on the fungal identity. Light or water deprivation revealed interspecific response diversity for N uptake. Partial taxon-specific N fluxes for ectomycorrhizas were assessed, and the benefits of EMF assemblages for plant N nutrition were estimated. We demonstrated that ectomycorrhizal assemblages provide advantages for inorganic N uptake compared with non-mycorrhizal roots under environmental constraints but not for unstressed plants. These benefits were realized via stress activation of distinct EMF taxa, which suggests significant functional diversity within EMF assemblages. We developed and validated a model that predicts net N flux into the plant based on taxon-specific (15)N enrichment in ectomycorrhizal root tips. These results open a new avenue to characterize the functional traits of EMF taxa in complex communities.
Climate changes have important consequences for plant communities and their root symbionts. The distribution of tree species within temperate, boreal and tropical biomes will be altered, as palaeoecological studies have demonstrated for previous climate change events. Predicted effects on ectomycorrhizal (ECM) associations include migration of host and symbiont, modification of interactions between plant and fungal species, and changes in the contribution of both partners to the global carbon cycle. Anthropogenic factors introduce new variables, affecting the ability of tree species and their fungal associates to disperse in response to climate change. Here we focus on how ECM fungi and their hosts respond to atmospheric CO2 enrichment, increasing temperatures, nutrient addition, species invasions, loss of biodiversity and anthropogenic land-use changes, particularly silviculture. All of these factors are key to understanding the impacts of climate change on the ECM symbiosis, and relevant future topics of research are presented.
The outcome of species interactions often depends on the environmental conditions under which they occur. In this study, we
tested how different soil moisture conditions affected the outcome of the ectomycorrhizal symbiosis between three Rhizopogon species and Pinus muricata in a factorial growth chamber experiment. We found that when grown in 7% soil moisture conditions, ectomycorrhizal plants
had similar biomass, photosynthesis, conductance, and total leaf nitrogen as non-mycorrhizal plants. However, when grown at
13% soil moisture, ectomycorrhizal plants had significantly greater shoot biomass, higher photosynthetic and conductance rates,
and higher total leaf nitrogen than non-mycorrhizal plants. The differences in plant response by mycorrhizal status in the
two soil moisture treatments corresponded with evidence of water limitation experienced by the fungi, which had much lower
colonization at 7% compared to 13% soil moisture. Our results suggest that the outcome of the ectomycorrhizal symbiosis can
be context-dependent and that fluctuating environmental conditions may strongly affect the way plants and fungi interact.
Microorganisms are often covered by a proteinaceous surface layer that serves as a sieve for external molecular influx, as a shield to protect microbes from external aggression, or as an aid to help microbial dispersion. In bacteria, the latter is called the S-layer, in Actinomycetes, the rod-like fibrillar layer, and in fungi, the rodlet layer . The self-assembly properties and remarkable structural and physicochemical characteristics of hydrophobin proteins underlie the multiple roles played by these unique proteins in fungal biology.
Through Earth’s history, drought has been a common crisis in terrestrial ecosystems; in human societies, it has caused famines and become one of the Four Horsemen of the apocalypse. As the global hydrological cycle intensifies with global warming, deeper droughts and rewetting will alter, and possibly transform, ecosystems. Soil communities, however, seem more tolerant than plants or animals are to water stress—the main effects, in fact, on soil processes appear to be limited diffusion and the limited supply of resources to soil organisms. Thus, the rains that end a drought not only release soil microbes from stress but also create a resource pulse that fuels soil microbial activity. It remains unclear whether the effects of drought on soil processes result from drying or rewetting. It is also unclear whether the flush of activity on rewetting is driven by microbial growth or by the physical/ chemical processes that mobilize organic matter. In this review, I discuss how soil water, and the lack of it, regulates microbial life and biogeochemical processes. I first focus on organismal-level responses and then consider how these influence whole-soil organic matter dynamics. A final focus is on how to incorporate these effects into Earth System models that can effectively capture dry–wet cycling. Expected final online publication date for the Annual Review of Ecology, Evolution, and Systematics Volume 49 is November 2, 2018. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Rising temperatures associated with climate change have been shown to negatively affect the photosynthetic rates of boreal forest tree saplings at their southern range limits. To quantify the responses of ectomycorrhizal (EM) fungal communities associated with poorly performing hosts, we sampled the roots of Betula papyrifera and Abies balsamea saplings growing in the B4Warmed (Boreal Forest Warming at an Ecotone in Danger) experiment. EM fungi on the root systems of both hosts were compared from ambient and +3.4 °C air and soil warmed plots at two sites in northern Minnesota. EM fungal communities were assessed with high-throughput sequencing along with measures of plant photosynthesis, soil temperature, moisture, and nitrogen. Warming selectively altered EM fungal community composition at both the phylum and genus levels, but had no significant effect on EM fungal operational taxonomic unit (OTU) diversity. Notably, warming strongly favored EM Ascomycetes and EM fungi with short-contact hyphal exploration types. Declining host photosynthetic rates were also significantly inversely correlated with EM Ascomycete and EM short-contact exploration type abundance, which may reflect a shift to less carbon demanding fungi due to lower photosynthetic capacity. Given the variation in EM host responses to warming, both within and between ecosystems, better understanding the link between host performance and EM fungal community structure will to clarify how climate change effects cascade belowground.
We present kallisto, an RNA-seq quantification program that is two orders of magnitude faster than previous approaches and achieves similar accuracy. Kallisto pseudoaligns reads to a reference, producing a list of transcripts that are compatible with each read while avoiding alignment of individual bases. We use kallisto to analyze 30 million unaligned paired-end RNA-seq reads in <10 min on a standard laptop computer. This removes a major computational bottleneck in RNA-seq analysis.
The 2012-2015 drought has left California with severely reduced snowpack, soil moisture, ground water, and reservoir stocks, but the impact of this estimated millennial-scale event on forest health is unknown. We used airborne laser-guided spectroscopy and satellite-based models to assess losses in canopy water content of California's forests between 2011 and 2015. Approximately 10.6 million ha of forest containing up to 888 million large trees experienced measurable loss in canopy water content during this drought period. Severe canopy water losses of greater than 30% occurred over 1 million ha, affecting up to 58 million large trees. Our measurements exclude forests affected by fire between 2011 and 2015. If drought conditions continue or reoccur, even with temporary reprieves such as El Niño, we predict substantial future forest change.
Ectomycorrhizal (EM) fungi form symbiotic associations with plant roots that regulate nutrient exchange between forest plants and soil. Environmental metagenomics approaches that employ next-generation sequencing show great promise for studying EM symbioses, however, metatranscriptomic studies have been constrained by the inherent difficulties associated with isolation and sequencing of RNA from mycorrhizae. Here we apply an optimized method for combined DNA/RNA extraction using field-collected EM fungal-pine root clusters, together with protocols for taxonomic identification of expressed ribosomal RNA, and inference of EM function based on plant and fungal metatranscriptomics. We used transcribed portions of ribosomal RNA genes to identify several transcriptionally dominant fungal taxa associated with loblolly pine including Amphinema, Russula, and Piloderma spp. One taxon, Piloderma croceum, has a publically available genome that allowed us to identify patterns of gene content and transcript abundance. Over 1500 abundantly expressed Piloderma genes were detected from mycorrhizal roots, including genes for protein metabolism, cell signaling, electron transport, terpene synthesis, and other extracellular activities. In contrast, Piloderma gene encoding an ammonia transporter showed highest transcript abundance in soil samples. Our methodology highlights the potential of metatranscriptomics to identify genes associated with symbiosis and ecosystem function using field-collected samples.
Climate warming is expected to have particularly strong effects on tundra and boreal ecosystems, yet relatively few studies have examined soil responses to temperature change in these systems. We used closed-top greenhouses to examine the response of soil respiration, nutrient availability, microbial abundance, and active fungal communities to soil warming in an Alaskan boreal forest dominated by mature black spruce. This treatment raised soil temperature by 0.5 °C and also resulted in a 22% decline in soil water content. We hypothesized that microbial abundance and activity would increase with the greenhouse treatment. Instead, we found that bacterial and fungal abundance declined by over 50%, and there was a trend toward lower activity of the chitin-degrading enzyme N-acetyl-glucosaminidase. Soil respiration also declined by up to 50%, but only late in the growing season. These changes were accompanied by significant shifts in the community structure of active fungi, with decreased relative abundance of a dominant Thelephoroid fungus and increased relative abundance of Ascomycetes and Zygomycetes in response to warming. In line with our hypothesis, we found that warming marginally increased soil ammonium and nitrate availability as well as the overall diversity of active fungi. Our results indicate that rising temperatures in northern-latitude ecosystems may not always cause a positive feedback to the soil carbon cycle, particularly in boreal forests with drier soils. Models of carbon cycle-climate feedbacks could increase their predictive power by incorporating heterogeneity in soil properties and microbial communities across the boreal zone.
The osmoadaptation of most micro-organisms involves the accumulation of K+ ions and one or more of a restricted range of low molecular mass organic solutes, collectively termed ‘compatible solutes’. These solutes are accumulated to high intracellular concentrations, in order to balance the osmotic pressure of the growth medium and maintain cell turgor pressure, which provides the driving force for cell extension growth. In this review, I discuss the alternative roles which compatible solutes may also play as intracellular reserves of carbon, energy and nitrogen, and as more general stress metabolites involved in protection of cells against other environmental stresses including heat, desiccation and freezing. Thus, the evolutionary selection for the accumulation of a specific compatible solute may not depend solely upon its function during osmoadaptation, but also upon the secondary benefits its accumulation provides, such as increased tolerance of other environmental stresses prevalent in the organism's niche or even anti-herbivory or dispersal functions in the case of dimethylsulfoniopropionate (DMSP). In the second part of the review, I discuss the ecological consequences of the release of compatible solutes to the environment, where they can provide sources of compatible solutes, carbon, nitrogen and energy for other members of the micro-flora. Finally, at the global scale the metabolism of specific compatible solutes (betaines and DMSP) in brackish water, marine and hypersaline environments may influence global climate, due to the production of the trace gases, methane and dimethylsulfide (DMS) and in the case of DMS, also couple the marine and terrestrial sulfur cycles.
Physiological studies can help predict effects of climate change through determining which species currently live closest to their upper thermal tolerance limits, which physiological systems set these limits, and how species differ in acclimatization capacities for modifying their thermal tolerances. Reductionist studies at the molecular level can contribute to this analysis by revealing how much change in sequence is needed to adapt proteins to warmer temperatures--thus providing insights into potential rates of adaptive evolution--and determining how the contents of genomes--protein-coding genes and gene regulatory mechanisms--influence capacities for adapting to acute and long-term increases in temperature. Studies of congeneric invertebrates from thermally stressful rocky intertidal habitats have shown that warm-adapted congeners are most susceptible to local extinctions because their acute upper thermal limits (LT(50) values) lie near current thermal maxima and their abilities to increase thermal tolerance through acclimation are limited. Collapse of cardiac function may underlie acute and longer-term thermal limits. Local extinctions from heat death may be offset by in-migration of genetically warm-adapted conspecifics from mid-latitude 'hot spots', where midday low tides in summer select for heat tolerance. A single amino acid replacement is sufficient to adapt a protein to a new thermal range. More challenging to adaptive evolution are lesions in genomes of stenotherms like Antarctic marine ectotherms, which have lost protein-coding genes and gene regulatory mechanisms needed for coping with rising temperature. These extreme stenotherms, along with warm-adapted eurytherms living near their thermal limits, may be the major 'losers' from climate change.
Increasing evidence suggests a major role for phosphatidylcholine (PC) in plant stress adaptation. The present work investigated the regulation of choline, PC and interconnected phosphatidylethanolamine biosynthesis in Arabidopsis thaliana L. as a function of cold- and salt- or mannitol-mediated hyperosmotic stresses. While PC synthesis is accelerated in both salt- and cold-treated plants, the choline kinase (CK) and phosphocholine cytidylyltransferase genes are oppositely regulated with respect to these abiotic treatments. Salt stress also stimulates CK activity in vitro. A possible regulatory role of CK in stimulating PC biosynthesis rate in salt-stressed plants is discussed.
Functional compartmentation of the extramatrical mycelium of ectomycorrhizal (ECM) fungi is considered important for the operation of ECM associations, although the molecular basis is poorly characterized. Global gene expression profiles of mycelium colonizing an ammonium sulphate ((NH4)2SO4) nutrient patch, rhizomorphs and ECM root tips of the Betula pendula-Paxillus involutus association were compared by cDNA microarray analysis. The expression profiles of rhizomorphs and nutrient patch mycelium were similar to each other but distinctly different from that of mycorrhizal tips. Statistical analyses revealed 337 of 1075 fungal genes differentially regulated among these three tissues. Clusters of genes exhibiting distinct expression patterns within specific tissues were identified. Genes implicated in the glutamine synthetase/glutamate synthase (GS/GOGAT) and urea cycles, and the provision of carbon skeletons for ammonium assimilation via beta-oxidation and the glyoxylate cycle, were highly expressed in rhizomorph and nutrient patch mycelium. Genes implicated in vesicular transport, cytoskeleton organization and morphogenesis and protein degradation were also differentially expressed. Differential expression of genes among the extramatrical mycelium and mycorrhizal tips indicates functional specialization of tissues forming ECM associations.
Conservation and discreteness of the atromentin gene cluster in fungi