The rust fungus Melampsora larici-populina expresses a conserved genetic program and distinct sets of secreted protein genes during infection of its two host plants,…C Lorrain, C Marchal, S Hacquard, C Delaruelle, J Pétrowski, B Petre, …Molecular Plant-Microbe Interactions

Abstract

Mechanisms required for broad spectrum or specific host colonization of plant parasites are poorly understood. As a perfect illustration, heteroecious rust fungi require two alternate host plants to complete their life cycles. Melampsora larici populina infects two taxonomically unrelated plants, larch on which sexual reproduction is achieved and poplar on which clonal multiplication occurs leading to severe epidemics in plantations. We applied deep RNA sequencing to three key developmental stages of M. larici-populina infection on larch: basidia, pycnia and aecia; and we performed comparative transcriptomics of infection on poplar and larch hosts using available expression data. Secreted protein was the only significantly over-represented category among differentially expressed M. larici-populina genes between the basidial, the pycnial and the aecial stages, highlighting their probable involvement in the infection process. Comparison of fungal transcriptomes in larch and poplar revealed a majority of rust genes commonly expressed on the two hosts and a fraction exhibiting host-specific expression. More particularly, gene families encoding small secreted proteins presented striking expression profiles that highlight probable candidate effectors specialized on each host. Our results bring valuable new information about the biological cycle of rust fungi and identify genes that may contribute to host specificity.

High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis ECH Chen, E Morin, D Beaudet, J Noel, G Yildirir, S Ndikumana, … New Phytologist

Roles and maturation of iron–sulfur proteins in plastids J Przybyla-Toscano, M Roland, F Gaymard, J Couturier, N Rouhier JBIC Journal of Biological Inorganic Chemistry, 1-2

One reason why iron is an essential element for most organisms is its presence in prosthetic groups such as hemes or iron–sulfur (Fe–S) clusters, which are notably required for electron transfer reactions. As an organelle with an intense metabolism in plants, chloroplast relies on many Fe–S proteins. This includes those present in the electron transfer chain which will be, in fact, essential for most other metabolic processes occurring in chloroplasts, e.g., carbon fixation, nitrogen and sulfur assimilation, pigment, amino acid, and vitamin biosynthetic pathways to cite only a few examples. The maturation of these Fe–S proteins requires a complex and specific machinery named SUF (sulfur mobilisation). The assembly process can be split in two major steps, (1) the de novo assembly on scaffold proteins which requires ATP, iron and sulfur atoms, electrons, and thus the concerted action of several proteins forming early acting assembly complexes, and (2) the transfer of the preformed Fe–S cluster to client proteins using a set of late-acting maturation factors. Similar machineries, having in common these basic principles, are present in the cytosol and in mitochondria. This review focuses on the currently known molecular details concerning the assembly and roles of Fe–S proteins in plastids.

Secretome analysis from the ectomycorrhizal ascomycete Cenococcum geophilum MDF Pereira, C Veneault-Fourrey, P Vion, F Guinet, E Morin, K Barry, … Frontiers in Microbiology 9, 141

Abstract

Cenococcum geophilum is an ectomycorrhizal fungus with global distribution in numerous habitats and associates with a large range of host species including gymnosperm and angiosperm trees. Moreover, C. geophilum is the unique ectomycorrhizal species within the clade Dothideomycetes, the largest class of Ascomycetes containing predominantly saprotrophic and many devastating phytopathogenic fungi. Recent studies highlight that mycorrhizal fungi, as pathogenic ones, use effectors in form of Small Secreted Proteins (SSPs) as molecular keys to promote symbiosis. In order to better understand the biotic interaction of C. geophilum with its host plants, the goal of this work was to characterize mycorrhiza-induced small-secreted proteins (MiSSPs) that potentially play a role in the ectomycorrhiza formation and functioning of this ecologically very important species. We combined different approaches such as gene expression profiling, genome localization and conservation of MiSSP genes in different C. geophilum strains and closely related species as well as protein subcellular localization studies of potential targets of MiSSPs in interacting plants using in tobacco leaf cells. Gene expression analyses of C. geophilum interacting with Pinus sylvestris and Populus sp. showed that similar sets of genes coding for secreted proteins were up-regulated and only few were specific to each host. Whereas pine induced more carbohydrate active enzymes (CAZymes), the interaction with poplar induced the expression of specific SSPs.
We identified a set of 22 MiSSPs, which are located in both, gene-rich, repeat-poor or gene-sparse, repeat-rich regions of the C. geophilum genome, a genome showing a bipartite architecture as seen for some pathogens but not yet for an ectomycorrhizal fungus. Genome re-sequencing data of 15 C. geophilum strains and two close relatives Glonium stellatum and Lepidopterella palustris were used to study sequence conservation of MiSSP-encoding genes. The 22 MiSSPs showed a high presence-absence polymorphism among the studied C. geophilum strains suggesting an evolution through gene gain/gene loss. Finally, we showed that six CgMiSSPs target four distinct sub-cellular compartments such as endoplasmic reticulum, plasma membrane, cytosol and tonoplast. Overall, this work presents a comprehensive analysis of secreted proteins and MiSSPs in different genetic level of C. geophilum opening a valuable resource to future functional analysis.

Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. E Martino, E Morin, GA Grelet, A Kuo, A Kohler, S Daghino, KW Barry, … New Phytologist

Abstract

• Some soil fungi in the Leotiomycetes form ericoid mycorrhizal (ERM) symbioses with Ericaceae. In the harsh habitats in which they occur, ERM plant survival relies on nutrient mobilization from soil organic matter (SOM) by their fungal partners. The characterization of the fungal genetic machinery underpinning both the symbiotic lifestyle and SOM degradation is needed to understand ERM symbiosis functioning and evolution, and its impact on soil carbon (C) turnover.
• We sequenced the genomes of the ERM fungi Meliniomyces bicolor, M. variabilis,Oidiodendron maius and Rhizoscyphus ericae, and compared their gene repertoires with those of fungi with different lifestyles (ecto- and orchid mycorrhiza, endophytes, saprotrophs, pathogens). We also identified fungal transcripts induced in symbiosis.
• The ERM fungal gene contents for polysaccharide-degrading enzymes, lipases, proteases and enzymes involved in secondary metabolism are closer to those of saprotrophs and pathogens than to those of ectomycorrhizal symbionts. The fungal genes most highly upregulated in symbiosis are those coding for fungal and plant cell wall-degrading enzymes (CWDEs), lipases, proteases, transporters and mycorrhiza-induced small secreted proteins (MiSSPs).
• The ERM fungal gene repertoire reveals a capacity for a dual saprotrophic and biotrophic lifestyle. This may reflect an incomplete transition from saprotrophy to the mycorrhizal habit, or a versatile life strategy similar to fungal endophytes.

Know your Enemy, Embrace your Friend: Using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms JM Plett, FM Martin. The Plant Journal

Summary

Micro-organisms, or ‘microbes’, have formed intimate associations with plants throughout the length of their evolutionary history. In extant plant systems microbes still remain an integral part of the ecological landscape impacting plant health, productivity, and long-term fitness. Therefore, to properly understand the genetic wiring of plants, we must first determine what perception systems plants have evolved to parse beneficial from commensal from pathogenic microbes. In this review, we consider some of the most recent advances in how plants respond at the molecular level to different microbial lifestyles. Further, we cover some of the means by which microbes are able to manipulate plant signaling pathways through altered destructiveness and nutrient sinks as well as the use of effector proteins and miRNA’s. We conclude by highlighting some of the major questions still to be answered in the field of plant-microbe research and suggest some of key areas that most need further research investment. The results of these proposed studies will have impacts in a wide range of plant research disciplines and will, ultimately, translate into stronger agronomic crops and forestry stock whose immune perception and response system is bred to foster beneficial microbial symbioses while repudiating pathogenic symbioses.

Erv1 of Arabidopsis thaliana can directly oxidize mitochondrial intermembrane space proteins in the absence of redox-active Mia40 V Peleh, F Zannini, S Backes, N Rouhier, JM Herrmann. BMC biology 15 (1), 106

Conclusions

We observed that plant Erv1, unlike its homologs in fungi and animals, can promote protein import and oxidative protein folding in the IMS independently of the oxidoreductase Mia40. In accordance to the absence of Mia40 in many protists, our study suggests that the mitochondrial disulfide relay evolved in a stepwise reaction from an Erv1-only system to which Mia40 was added in order to improve substrate specificity.

Phylogenetics and Phylogenomics of Rust Fungi MC Aime, AR McTaggart, SJ Mondo, S Duplessis. Advances in Genetics

Abstract

The Fungal Tree of Life: from Molecular Systematics to Genome-Scale Phylogenies. JW Spatafora, MC Aime, IV Grigoriev, F Martin, JE Stajich, M Blackwell. Microbiology spectrum 5 (5)

Abstract:

The kingdom Fungi is one of the more diverse clades of eukaryotes in terrestrial ecosystems, where they provide numerous ecological services ranging from decomposition of organic matter and nutrient cycling to beneficial and antagonistic associations with plants and animals. The evolutionary relationships of the kingdom have represented some of the more recalcitrant problems in systematics and phylogenetics. The advent of molecular phylogenetics, and more recently phylogenomics, has greatly advanced our understanding of the patterns and processes associated with fungal evolution, however. In this article, we review the major phyla, subphyla, and classes of the kingdom Fungi and provide brief summaries of ecologies, morphologies, and exemplar taxa. We also provide examples of how molecular phylogenetics and evolutionary genomics have advanced our understanding of fungal evolution within each of the phyla and some of the major classes. In the current classification we recognize 8 phyla, 12 subphyla, and 46 classes within the kingdom. The ancestor of fungi is inferred to be zoosporic, and zoosporic fungi comprise three lineages that are paraphyletic to the remainder of fungi. Fungi historically classified as zygomycetes do not form a monophyletic group and are paraphyletic to Ascomycota and Basidiomycota. Ascomycota and Basidiomycota are each monophyletic and collectively form the subkingdom Dikarya.

Regulatory networks underlying mycorrhizal development delineated by genome-wide expression profiling and functional analysis of the transcription factor repertoire of the plant symbiotic fungus Laccaria bicolor. Y Daguerre, E Levati, J Ruytinx, E Tisserant, E Morin, A Kohler, … BMC genomics 18 (1), 737

Abstract