Article: Frontiers in Ecology and Evolution

The influence of contrasting microbial lifestyles on the pre-symbiotic metabolite responses of Eucalyptus grandis roots JWH Wong, A Lutz, S Natera, M Wang, V Ng, IV Grigoriev, FM Martin, … Frontiers in Ecology and Evolution 7, 10


Plant roots co-inhabit the soil with a diverse consortium of microbes of which a number attempt to enter symbiosis with the plant. These microbes may be pathogenic, mutualistic or commensal. Hence, the health and survival of plants is heavily reliant on their ability to perceive different microbial lifestyles and respond appropriately. Emerging research suggests that there is a pivotal role for plant root secondary metabolites in responding to microbial colonization. However, it is largely unknown if plants are able to differentiate between microbes of different lifestyles and respond differently during the earliest stages of pre-symbiosis (i.e. prior to physical contact). By studying, here, plant responses to a range of microbial isolates, we questioned: (1) if individual microbes of different lifestyles and species caused alterations to the plant root metabolome during pre-symbiosis, and (2) if these early metabolite responses correlate with the outcome of the symbiotic interaction in later phases of colonization.

We compared the changes of the root tip metabolite profile of the model tree Eucalyptus grandis during pre-symbiosis with two isolates of a pathogenic fungus (Armillaria luteobubalina), one isolate of a pathogenic oomycete (Phytophthora cinnamomi), two isolates of an incompatible mutualistic fungus (Suillus granulatus), and six isolates of a compatible mutualistic fungus (Pisolithus microcarpus). Untargeted metabolite profiling revealed predominantly positive root metabolite responses at the pre-symbiosis stage, prior to any observable phenotypical changes of the root tips. Metabolite responses in the host tissue that were specific to each microbial species were identified. A deeper analysis of the root metabolomic profiles during pre-symbiotic contact with six strains of P. microcarpus showed a connection between these early metabolite responses in the root with later colonization success. Further investigation using isotopic tracing revealed a portion of metabolites found in root tips originated from the fungus. RNA-sequencing also showed that the plant roots undergo complementary transcriptomic reprogramming in responses to the fungal stimuli. Taken together, our results demonstrate that the early metabolite responses of plant roots are partially selective towards the lifestyle of the interacting microbe, and that these responses can be crucial in determining the outcome of the interaction.

Article: Mycorrhiza

Influence of annual climatic variations, climate changes, and sociological factors on the production of the Périgord black truffle (Tuber melanosporum Vittad.) from …M Baragatti, PM Grollemund, P Montpied, JL Dupouey, J Gravier, C Murat, … Mycorrhiza, 1-13


From 1903–1904 to 1988–1989, the two World Wars and sociological factors as rural desertification and changes in land uses mainly explained the decline of black truffle production in the Vaucluse department, which well reflects that of the whole of France. These can be correlated with the annual climatic variations as well as, from 1924–1925 to 1948–1949, the raw production rates of the managed truffle orchard of Pernes-les-Fontaines located in Vaucluse. The two methods used (correlation coefficients and Bayesian functional linear regression with Sparse Step functions) gave consistent results: the main factor explaining the annual variations of truffle production was the summer climatic water deficit of the year n. A general model including the rural exodus and the cumulated climatic water deficit of summer months both allowed to well explain the evolution of truffle production from 1903–1904 to 1988–1989 in the Vaucluse and its huge decrease. During that period, global warming had little effect. However, in the twenty-first century, all the scenarios predict increased summer water stress for the Mediterranean region, which could greatly affect black truffle production.

Article: Molecular Ecology

Genome‐based estimates of fungal rDNA copy number variation across phylogenetic scales and ecological lifestyles LA Lofgren, JK Uehling, S Branco, TD Bruns, F Martin, PG Kennedy Molecular Ecology


Ribosomal DNA (rDNA) copy number variation (CNV) has major physiological implications for all organisms, but how it varies for fungi, an ecologically ubiquitous and important group of microorganisms, has yet to be systemically investigated. Here, we examine rDNA CNV using an in silico read depth approach for 91 fungal taxa with sequenced genomes and assess copy number conservation across phylogenetic scales and ecological lifestyles. rDNA copy number varied considerably across fungi, ranging from an estimated 14 to 1442 copies (mean = 113, median = 82), and copy number similarity was inversely correlated with phylogenetic distance. No correlations were found between rDNA CNV and fungal trophic mode, ecological guild, or genome size. Taken together, these results show that like other microorganisms, fungi exhibit substantial variation in rDNA copy number, which is linked to their phylogeny in a scale‐dependent manner.

Article: New Phytologist

Advances in understanding obligate biotrophy in rust fungi C Lorrain, KC Gonçalves dos Santos, H Germain, A Hecker, S Duplessis New Phytologist


Rust fungi (Pucciniales) are the largest group of plant pathogens and represent one of the most devastating threats to agricultural crops worldwide. Despite the economic importance of these highly specialized pathogens, many aspects of their biology remain obscure largely because rust fungi are obligate biotrophs. The rise of genomics and advances in high‐throughput sequencing technology have presented new options for identifying candidate effector genes involved in pathogenicity mechanisms of rust fungi. Transcriptome analysis and integrated bioinformatics tools have led to the identification of key genetic determinants of host susceptibility to infection by rusts. Thousands of genes encoding secreted proteins highly expressed during host infection have been reported for different rust species, which represents significant potential towards understanding rust effector function. Recent high‐throughput in planta expression screen approaches (effectoromics) have pushed the field ahead even further towards predicting high‐priority effectors and identifying avirulence genes. These new insights into rust effector biology promise to inform future research and spur the development of effective and sustainable strategies for managing rust diseases.

Article: Microbial Ecology

Microbial Enzymatic Activities and Community-Level Physiological Profiles (CLPP) in Subsoil Layers Are Altered by Harvest Residue Management Practices in a Tropical Eucalyptus … F Maillard, V Leduc, C Bach, JL de Moraes Gonçalves, FD Androte, … Microbial Ecology, 1-6


Harvest residue management is a key issue for the sustainability of Eucalyptus plantations established on poor soils. Soil microbial communities contribute to soil fertility by the decomposition of the organic matter (OM), but little is known about the effect of whole-tree harvesting (WTH) in comparison to stem only harvesting (SOH) on soil microbial functional diversity in Eucalyptus plantations. We studied the effects of harvest residue management (branches, leaves, bark) of Eucalyptus grandis trees on soil enzymatic activities and community-level physiological profiles in a Brazilian plantation. We measured soil microbial enzymatic activities involved in OM decomposition and we compared the community level physiological profiles (CLPP) of the soil microbes in WTH and SOH plots. WTH decreased enzyme activities and catabolic potential of the soil microbial community. Furthermore, these negative effects on soil functional diversity were mainly observed below the 0–5 cm layer (5–10 and 10–20 cm), suggesting that WTH can be harmful to the soil health in these plantations.

Article: New Phytologist

Phylogenomics of Endogonaceae and evolution of mycorrhizas within Mucoromycota. Y Chang, A Desiro, H Na, L Sandor, A Lipzen,…New Phytologist


Endogonales (Mucoromycotina), composed of Endogonaceae and Densosporaceae, is the only known non‐Dikarya order with ectomycorrhizal members. They also form mycorrhizal‐like association with some non‐Spermatophyte plants. It has been recently proposed that Endogonales were among the earliest mycorrhizal partners with land plants. It remains unknown whether Endogonales possess genomes with mycorrhizal‐lifestyle signatures and whether Endogonales originated around the same time as land plants did.

We sampled sporocarp tissue from four Endogonaceae collections and performed shotgun genome sequencing. After binning the metagenome data, we assembled and annotated the Endogonaceae genomes. We performed comparative analysis on plant‐cell‐wall‐degrading‐enzymes (PCWDEs) and small secreted proteins (SSPs). We inferred phylogenetic placement of Endogonaceae and estimated the ages of Endogonaceae and Endogonales with expanded taxon sampling.

Endogonaceae have large genomes with high repeat content, low diversity of PCWDEs, but without elevated SSP/secretome ratios. Dating analysis estimated that Endogonaceae originated in the Permian‐Triassic boundary and Endogonales originated in the mid‐late Silurian. Mycoplasma‐related endobacterium sequences were identified in three Endogonaceae genomes.

Endogonaceae genomes possess typical signatures of mycorrhizal lifestyle. The early origin of Endogonales suggests that the mycorrhizal association between Endogonales and plants might have played an important role during the colonization of land by plants.

Article: Biochimica et Biophysica Acta

The thioredoxin-mediated recycling of Arabidopsis thaliana GRXS16 relies on a conserved C-terminal cysteine F Zannini, A Moseler, R Bchini, T Dhalleine, AJ Meyer, N Rouhier, … Biochimica et Biophysica Acta (BBA)-General Subjects



Glutaredoxins (GRXs) are oxidoreductases involved in diverse cellular processes through their capacity to reduce glutathionylated proteins and/or to coordinate iron‑sulfur (FeS) clusters. Among class II GRXs, the plant-specific GRXS16 is a bimodular protein formed by an N-terminal endonuclease domain fused to a GRX domain containing a 158CGFS signature.


The biochemical properties (redox activity, sensitivity to oxidation, pKa of cysteine residues, midpoint redox potential) of Arabidopsis thaliana GRXS16 were investigated by coupling oxidative treatments to alkylation shift assays, activity measurements and mass spectrometry analyses.


Activity measurements using redox-sensitive GFP2 (roGFP2) did not reveal any significant glutathione-dependent reductase activity of A. thaliana GRXS16 whereas it was able to catalyze its oxidation in the presence of glutathione disulfide. Accordingly, Arabidopsis GRXS16 reacted efficiently with oxidized forms of glutathione, leading to the formation of an intramolecular disulfide between Cys158 and the semi-conserved Cys215, which has a midpoint redox potential of – 298 mV at pH 7.0 and is reduced by plastidial thioredoxins (TRXs) but not GSH. By promoting the formation of this disulfide, Cys215 modulates GRXS16 oxidoreductase activity.


The reduction of AtGRXS16, which is mandatory for its oxidoreductase activity and the binding of FeS clusters, depends on light through the plastidial FTR/TRX system. Hence, disulfide formation may constitute a redox switch mechanism controlling GRXS16 function in response to day/night transition or oxidizing conditions.

General significance.

From the in vitro data obtained with roGFP2, one can postulate that GRXS16 would mediate protein glutathionylation/oxidation in plastids but not their deglutathionylation.

Article: Antioxidants and Redox signaling

Redox homeostasis in photosynthetic organisms: novel and established thiol-based molecular mechanisms. M Zaffagnini, S Fermani, CH Marchand, A Costa, F Sparla, N Rouhier, … Antioxidants and Redox Signaling

Redox homeostasis consists of an intricate network in which reactive molecular species (RMS), redox modifications and redox proteins act in concert to allow both physiological responses and adaptation to stress conditions. This review highlights established and novel thiol-based regulatory pathways underlying the functional facets and significance of redox biology in photosynthetic organisms. This cannot be all-encompassing, but is intended to provide a comprehensive overview on the structural/molecular mechanisms governing the most relevant thiol switching modifications with emphasis on the large genetic and functional diversity of redox controllers (i.e. redoxins). We also summarize the different proteomic-based approaches aimed at investigating the dynamics of redox modifications and the recent evidence that extends the possibility to monitor the cellular redox state in vivo. Lastly, the physiological relevance of redox transitions is discussed based on reverse genetic studies confirming the importance of redox homeostasis in plant growth, development, and stress responses.

Article: Nature Ecology & Evolution

  1. C Murat, T Payen, B Noel, A Kuo, E Morin, J Chen, A Kohler, K Krizsán, … Nature Ecology & Evolution, 1


    Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.

Article: Oecologia

Aboveground overyielding in a mixed temperate forest is not explained by belowground processes A Fruleux, MB Bogeat-Triboulot, C Collet, A Deveau, L Saint-André, … Oecologia, 1-11


The relationship between forest productivity and tree species diversity has been described in detail, but the underlying processes have yet to be identified. One important issue is to understand which processes are at the origin of observed aboveground overyielding in some mixed forests. We used a beech–maple plantation exhibiting aboveground overyielding to test whether belowground processes could explain this pattern. Soil cores were collected to determine fine root (FR) biomass and vertical distribution. Correlograms were used to detect spatial arrangement. Near-infrared reflectance spectroscopy was used to identify the tree species proportion in the FR samples and spatial root segregation. An isotopic approach was used to identify water acquisition patterns. The structure and the composition of the ectomycorrhizal fungal community were determined by high-throughput sequencing of DNA in the soil samples. We found no spatial pattern for FR biomass or for its vertical distribution along the gradients. No vertical root segregation was found, as FR density for both species decreased with depth in a similar way. The two species displayed similar vertical water acquisition profiles as well, mainly absorbing water from shallow soil layers; hence, niche differentiation for water acquisition was not highlighted here. Significant alterations in the fungal community compositions were detected in function of the percentage of maple in the vicinity of beech. Our findings do not support the commonly suggested drivers of aboveground overyielding in species-diverse forests and suggest that competition reduction or between-species facilitation of belowground resource acquisition may not explain the observed aboveground overyielding.