* The contribution of hyphae to water transport in ectomycorrhizal (ECM) white spruce (Picea glauca) seedlings was examined by altering expression of a major water-transporting aquaporin in Laccaria ...bicolor. * Picea glauca was inoculated with wild-type (WT), mock transgenic or L. bicolor aquaporin JQ585595-overexpressing (OE) strains and exposed to root temperatures ranging from 5 to 20 degree C to examine the root water transport properties, physiological responses and plasma membrane intrinsic protein (PIP) expression in colonized plants. * Mycorrhization increased shoot water potential, transpiration, net photosynthetic rates, root hydraulic conductivity and root cortical cell hydraulic conductivity in seedlings. At 20 degree C, OE plants had higher root hydraulic conductivity compared with WT plants and the increases were accompanied by higher expression of P. glauca PIP GQ03401_M18.1 in roots. In contrast to WT L. bicolor, the effects of OE fungi on root and root cortical cell hydraulic conductivities were abolished at 10 and 5 degree C in the absence of major changes in the examined transcript levels of P. glauca root PIPs. * The results provide evidence for the importance of fungal aquaporins in root water transport of mycorrhizal plants. They also demonstrate links between hyphal water transport, root aquaporin expression and root water transport in ECM plants.
SUMMARY
Tree growth and survival are dependent on their ability to perceive signals, integrate them, and trigger timely and fitted molecular and growth responses. While ectomycorrhizal symbiosis is a ...predominant tree‐microbe interaction in forest ecosystems, little is known about how and to what extent it helps trees cope with environmental changes. We hypothesized that the presence of
Laccaria bicolor
influences abiotic cue perception by
Populus trichocarpa
and the ensuing signaling cascade. We submitted ectomycorrhizal or non‐ectomycorrhizal
P. trichocarpa
cuttings to short‐term cessation of watering or ozone fumigation to focus on signaling networks before the onset of any physiological damage. Poplar gene expression, metabolite levels, and hormone levels were measured in several organs (roots, leaves, mycorrhizas) and integrated into networks. We discriminated the signal responses modified or maintained by ectomycorrhization. Ectomycorrhizas buffered hormonal changes in response to short‐term environmental variations systemically prepared the root system for further fungal colonization and alleviated part of the root abscisic acid (ABA) signaling. The presence of ectomycorrhizas in the roots also modified the leaf multi‐omics landscape and ozone responses, most likely through rewiring of the molecular drivers of photosynthesis and the calcium signaling pathway. In conclusion,
P. trichocarpa‐L. bicolor
symbiosis results in a systemic remodeling of the host's signaling networks in response to abiotic changes. In addition, ectomycorrhizal, hormonal, metabolic, and transcriptomic blueprints are maintained in response to abiotic cues, suggesting that ectomycorrhizas are less responsive than non‐mycorrhizal roots to abiotic challenges.
• Here we characterized the effect of the ectomycorrhizal symbiosis on the genotypic and functional diversity of soil Pseudomonas fluorescens populations and analysed its possible consequences in ...terms of plant nutrition, development and health. • Sixty strains of P. fluorescens were isolated from the bulk soil of a forest nursery, the ectomycorrhizosphere and the ectomycorrhizas of the Douglas fir (Pseudostuga menziesii) seedlings-Laccaria bicolor S238N. They were characterized in vitro with the following criteria: ARDRA, phosphate solubilization, siderophore, HCN and AIA production, genes of N2-fixation and antibiotic synthesis, in vitro confrontation with a range of phytopathogenic and ectomycorrhizal fungi, effect on the Douglas fir-L. bicolor symbiosis. • For most of these criteria, we demonstrated that the ectomycorrhizosphere significantly structures the P. fluorescens populations and selects strains potentially beneficial to the symbiosis and to the plant. • This prompts us to propose the ectomycorrhizal symbiosis as a true microbial complex where multitrophic interactions take place. Moreover it underlines the fact that this symbiosis has an indirect positive effect on plant growth, via its selective pressure on bacterial communities, in addition to its known direct positive effect.
Fungi of the genus
are economically important due to their plant growth- and performance-promoting effects, such as improved nutrient supply, mycoparasitism of plant-pathogens and priming of plant ...defense. Due to their mycotrophic lifestyle, however, they might also be antagonistic to other plant-beneficial fungi, such as mycorrhiza-forming species.
spp. release a high diversity of volatile organic compounds (VOCs), which likely play a decisive role in the inter-species communication. It has been shown that
VOCs can inhibit growth of some plant pathogens, but their inhibition potentials during early interactions with mutualistic fungi remain unknown.
is a common ectomycorrhizal fungus which in symbiotic relationship is well known to facilitate plant performance. Here, we investigated the VOC profiles of three strains of
species,
, and
, as well as
by stir bar sorptive extraction and gas chromatography - mass spectrometry (SBSE-GC-MS). We further examined the fungal performance and the VOC emission profiles during confrontation of the
species with
in different co-cultivation scenarios. The VOC profiles of the three
species were highly species-dependent.
was the strongest VOC emitter with the most diverse compound pattern, followed by
and
. Co-cultivation of
spp. and
altered the VOC emission patterns dramatically in some scenarios. The co-cultivations also revealed contact degree-dependent inhibition of one of the fungal partners.
growth was at least partially inhibited when sharing the same headspace with
. In direct contact between both mycelia, however,
growth was impaired, indicating that
and
apply different effectors when defending their territory. Multivariate analysis demonstrated that all examined individual fungal species in axenic cultures, as well as their co-cultivations were characterized by a distinct VOC emission pattern. The results underline the importance of VOCs in fungal interactions and reveal unexpected adjustability of the VOC emissions according to the specific biotic environments.
Ectomycorrhizal fungi, such as Laccaria bicolor, support forest growth and sustainability by providing growth-limiting nutrients to their plant host through a mutualistic symbiotic relationship with ...host roots. We have previously shown that the effector protein MiSSP7 (Mycorrhiza-induced Small Secreted Protein 7) encoded by L. bicolor is necessary for the establishment of symbiosis with host trees, although the mechanistic reasoning behind this role was unknown. We demonstrate here that MiSSP7 interacts with the host protein PtJAZ6, a negative regulator of jasmonic acid (JA)-induced gene regulation in Populus. As with other characterized JASMONATE ZIM-DOMAIN (JAZ) proteins, PtJAZ6 interacts with PtCOI1 in the presence of the JA mimic coronatine, and PtJAZ6 is degraded in plant tissues after JA treatment. The association between MiSSP7 and PtJAZ6 is able to protect PtJAZ6 from this JA-induced degradation. Furthermore, MiSSP7 is able to block—or mitigate—the impact of JA on L. bicolor colonization of host roots. We show that the loss of MiSSP7 production by L. bicolor can be complemented by transgenically varying the transcription of PtJAZ6 or through inhibition of JA-induced gene regulation. We conclude that L. bicolor, in contrast to arbuscular mycorrhizal fungi and biotrophic pathogens, promotes mutualism by blocking JA action through the interaction of MiSSP7 with PtJAZ6.
Agaricus bisporus is the model fungus for the adaptation, persistence, and growth in the humic-rich leaf-litter environment. Aside from its ecological role, A. bisporus has been an important ...component of the human diet for over 200 y and worldwide cultivation of the “button mushroom” forms a multibillion dollar industry. We present two A. bisporus genomes, their gene repertoires and transcript profiles on compost and during mushroom formation. The genomes encode a full repertoire of polysaccharide-degrading enzymes similar to that of wood-decayers. Comparative transcriptomics of mycelium grown on defined medium, casing-soil, and compost revealed genes encoding enzymes involved in xylan, cellulose, pectin, and protein degradation are more highly expressed in compost. The striking expansion of heme-thiolate peroxidases and β-etherases is distinctive from Agaricomycotina wood-decayers and suggests a broad attack on decaying lignin and related metabolites found in humic acid-rich environment. Similarly, up-regulation of these genes together with a lignolytic manganese peroxidase, multiple copper radical oxidases, and cytochrome P450s is consistent with challenges posed by complex humic-rich substrates. The gene repertoire and expression of hydrolytic enzymes in A. bisporus is substantially different from the taxonomically related ectomycorrhizal symbiont Laccaria bicolor . A common promoter motif was also identified in genes very highly expressed in humic-rich substrates. These observations reveal genetic and enzymatic mechanisms governing adaptation to the humic-rich ecological niche formed during plant degradation, further defining the critical role such fungi contribute to soil structure and carbon sequestration in terrestrial ecosystems. Genome sequence will expedite mushroom breeding for improved agronomic characteristics.
The Périgord black truffle (Tuber melanosporum Vittad.) and the Piedmont white truffle dominate today's truffle market. The hypogeous fruiting body of T. melanosporum is a gastronomic delicacy ...produced by an ectomycorrhizal symbiont endemic to calcareous soils in southern Europe. The worldwide demand for this truffle has fuelled intense efforts at cultivation. Identification of processes that condition and trigger fruit body and symbiosis formation, ultimately leading to efficient crop production, will be facilitated by a thorough analysis of truffle genomic traits. In the ectomycorrhizal Laccaria bicolor, the expansion of gene families may have acted as a 'symbiosis toolbox'. This feature may however reflect evolution of this particular taxon and not a general trait shared by all ectomycorrhizal species. To get a better understanding of the biology and evolution of the ectomycorrhizal symbiosis, we report here the sequence of the haploid genome of T. melanosporum, which at ∼125 megabases is the largest and most complex fungal genome sequenced so far. This expansion results from a proliferation of transposable elements accounting for ∼58% of the genome. In contrast, this genome only contains ∼7,500 protein-coding genes with very rare multigene families. It lacks large sets of carbohydrate cleaving enzymes, but a few of them involved in degradation of plant cell walls are induced in symbiotic tissues. The latter feature and the upregulation of genes encoding for lipases and multicopper oxidases suggest that T. melanosporum degrades its host cell walls during colonization. Symbiosis induces an increased expression of carbohydrate and amino acid transporters in both L. bicolor and T. melanosporum, but the comparison of genomic traits in the two ectomycorrhizal fungi showed that genetic predispositions for symbiosis-'the symbiosis toolbox'-evolved along different ways in ascomycetes and basidiomycetes.
Forest soils constitute a major carbon pool in the context of the global carbon cycle. Although ectomycorrhizal fungi (EMF) are responsible for a large part of the input of carbon into this pool, ...information on the transformation of EMF biomass into soil organic matter (SOM) is scarce. In order to quantitatively analyze the contribution of EMF biomass to SOM formation, we incubated a typical forest arenosol with 13C-labeled fungal biomass from the ectomycorrhizal basidiomycete Laccaria bicolor in a closed bioreactor system for 231 d, enabling the establishment of a full mass balance for the turnover. rDNA fragments specific for the genus Laccaria disappeared after 28 d, indicating death and decay of the organism. The amount of 13C PLFA as a proxy for living biomass decreased to roughly 10% of the initial value in the course of the experiment, again suggesting efficient disintegration of the fungal organism. After 231 d, however, 63.5% of the initially added 13C had been converted to SOM and 52% belonged to the non-living fraction. The analysis of 13CO2 formation (36.5% of the initially added label) suggested two-pool exponential kinetics with k1 = 0.0615 d−1 for the easily degradable and k2 = 0.0005 d−1 for the stable fraction (pool sizes 74% and 26% of the initially added label, respectively). When compared to the degradation of bacterial biomass in agricultural soils, the pool of readily degradable fungal biomass was considerably smaller and the half-lives of both pools (readily degradable and persistent C) were markedly higher for fungal biomass. In summary, our data allow the conclusion that EMF biomass is a significant source of SOM in forest ecosystems.
•A full mass balance for EMF-derived 13C in a forest soil was set up.•After 231 d, 64% of the added C remained in soil and 36% were mineralized.•The degradation kinetics differed from studies with bacterial derived biomass.•EMF necromass is a potential significant contributor to SOM formation.
Summary
Ectomycorrhizas are an intrinsic component of tree nutrition and responses to environmental variations. How epigenetic mechanisms might regulate these mutualistic interactions is unknown.
By ...manipulating the level of expression of the chromatin remodeler DECREASE IN DNA METHYLATION 1 (DDM1) and two demethylases DEMETER‐LIKE (DML) in Populus tremula × Populus alba lines, we examined how host DNA methylation modulates multiple parameters of the responses to root colonization with the mutualistic fungus Laccaria bicolor. We compared the ectomycorrhizas formed between transgenic and wild‐type (WT) trees and analyzed their methylomes and transcriptomes.
The poplar lines displaying lower mycorrhiza formation rate corresponded to hypomethylated overexpressing DML or RNAi‐ddm1 lines. We found 86 genes and 288 transposable elements (TEs) differentially methylated between WT and hypomethylated lines (common to both OX‐dml and RNAi‐ddm1) and 120 genes/1441 TEs in the fungal genome suggesting a host‐induced remodeling of the fungal methylome. Hypomethylated poplar lines displayed 205 differentially expressed genes (cis and trans effects) in common with 17 being differentially methylated (cis).
Our findings suggest a central role of host and fungal DNA methylation in the ability to form ectomycorrhizas including not only poplar genes involved in root initiation, ethylene and jasmonate‐mediated pathways, and immune response but also terpenoid metabolism.
See also the Commentary on this article by Zimmermann & Gaillard, 238: 2259–2260.
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