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Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.

Within the plant microbiota, mutualistic fungal and bacterial symbionts are striking examples of microorganisms playing crucial roles in nutrient acquisition. They have coevolved with their hosts since initial plant adaptation to land. Despite the evolutionary distances that separate mycorrhizal and nitrogen-fixing symbioses, these associations share a number of highly conserved features, including specific plant symbiotic signaling pathways, root colonization strategies that circumvent plant immune responses, functional host-microbe interface formation, and the central role of phytohormones in symbiosis-associated root developmental pathways. We highlight recent and emerging areas of investigation relating to these evolutionarily conserved mechanisms, with an emphasis on the more ancestral mycorrhizal associations, and consider to what extent this knowledge can contribute to an understanding of plant-microbiota associations as a whole.

Fungi and bacteria are found living together in a wide variety of environments. Their interactions are significant drivers of many ecosystem functions and are important for the health of plants and animals. A large number of fungal and bacterial families engage in complex interactions that lead to critical behavioural shifts of the microorganisms ranging from mutualism to antagonism. The importance of bacterial-fungal interactions (BFI) in environmental science, medicine and biotechnology has led to the emergence of a dynamic and multidisciplinary research field that combines highly diverse approaches including molecular biology, genomics, geochemistry, chemical and microbial ecology, biophysics and ecological modelling. In this review, we discuss recent advances that underscore the roles of BFI across relevant habitats and ecosystems. A particular focus is placed on the understanding of BFI within complex microbial communities and in regard of the metaorganism concept. We also discuss recent discoveries that clarify the (molecular) mechanisms involved in bacterial-fungal relationships, and the contribution of new technologies to decipher generic principles of BFI in terms of physical associations and molecular dialogues. Finally, we discuss future directions for research in order to stimulate synergy within the BFI research area and to resolve outstanding questions.

Contents Summary 1190 I. Introduction 1190 II. Rust fungi: a diverse and serious threat to agriculture 1191 III. The different facets of rust life cycles and unresolved questions about their evolution 1191 IV. The biology of rust infection 1192 V. Rusts in the genomics era: the ever-expanding list of candidate effector genes 1195 VI. Functional characterization of rust effectors 1197 VII. Putting rusts to sleep: Pucciniales research outlooks 1201 Acknowledgements 1202 References 1202 SUMMARY: 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.

The mycorrhizal symbiosis at the dawn and rise of the land flora 1014 III. From early land plants to early trees: the origin of roots and true mycorrhizas 1016 IV. The diversification of the AM symbiosis 1019 V. The ECM symbiosis 1021 VI. The recently evolved ericoid and orchid mycorrhizas 1023 VII. Limits of paleontological vs genetic approaches and perspectives 1023 Acknowledgements 1025 References 1025 SUMMARY: The ability of fungi to form mycorrhizas with plants is one of the most remarkable and enduring adaptations to life on land. The occurrence of mycorrhizas is now well established in c. 85% of extant plants, yet the geological record of these associations is sparse. Fossils preserved under exceptional conditions provide tantalizing glimpses into the evolutionary history of mycorrhizas, showing the extent of their occurrence and aspects of their evolution in extinct plants. The fossil record has important roles to play in establishing a chronology of when key fungal associations evolved and in understanding their importance in ecosystems through time. Together with calibrated phylogenetic trees, these approaches extend our understanding of when and how groups evolved in the context of major environmental change on a global scale. Phylogenomics furthers this understanding into the evolution of different types of mycorrhizal associations, and genomic studies of both plants and fungi are shedding light on how the complex set of symbiotic traits evolved. Here we present a review of the main phases of the evolution of mycorrhizal interactions from palaeontological, phylogenetic and genomic perspectives, with the aim of highlighting the potential of fossil material and a geological perspective in a cross-disciplinary approach.

Significance Plant genomes encode hundreds of genes controlling the detection, signaling pathways, and immune responses necessary to defend against pathogens. Pathogens, in turn, continually evolve to evade these defenses. Small RNAs, such as microRNAs (miRNAs), are one mechanism used by pathogens to overcome plant defenses and facilitate plant colonization. Mounting evidence would suggest that beneficial microbes, likewise, use miRNAs to facilitate symbiosis. Here, we demonstrate that the beneficial fungus Pisolithus microcarpus encodes a miRNA that enters plant cells and stabilizes the symbiotic interaction. These results demonstrate that beneficial fungi may regulate host gene expression through the use of miRNAs and sheds light on how beneficial microbes have evolved mechanisms to colonize plant tissues.

The genome of an organism bears the signature of its lifestyle, and organisms with similar life strategies are expected to share common genomic traits. Indeed, ectomycorrhizal and arbuscular mycorrhizal fungi share some genomic traits, such as the expansion of gene families encoding taxon‐specific small secreted proteins, which are candidate effectors in the symbiosis, and a very small repertoire of plant cell wall‐degrading enzymes. A large gene family coding for candidate effectors was also revealed in ascomycetous ericoid mycorrhizal (ERM) fungi, but these fungal genomes are characterised by a very high number of genes encoding degradative enzymes, mainly acting on plant cell wall components. We suggest that the genomic signature of ERM fungi mirrors a versatile life strategy, which allows them to occupy several ecological niches.

Arbuscular mycorrhizal fungi (AMF) are known to improve plant fitness through the establishment of mycorrhizal symbioses. Genetic and phenotypic variations among closely related AMF isolates can significantly affect plant growth, but the genomic changes underlying this variability are unclear. To address this issue, we improved the genome assembly and gene annotation of the model strain Rhizophagus irregularis DAOM197198, and compared its gene content with five isolates of R. irregularis sampled in the same field. All isolates harbor striking genome variations, with large numbers of isolate-specific genes, gene family expansions, and evidence of interisolate genetic exchange. The observed variability affects all gene ontology terms and PFAM protein domains, as well as putative mycorrhiza-induced small secreted effector-like proteins and other symbiosis differentially expressed genes. High variability is also found in active transposable elements. Overall, these findings indicate a substantial divergence in the functioning capacity of isolates harvested from the same field, and thus their genetic potential for adaptation to biotic and abiotic changes. Our data also provide a first glimpse into the genome diversity that resides within natural populations of these symbionts, and open avenues for future analyses of plant-AMF interactions that link AMF genome variation with plant phenotype and fitness.

Basidiomycota (basidiomycetes) make up 32% of the described fungi and include most wood-decaying species, as well as pathogens and mutualistic symbionts. Wood-decaying basidiomycetes have typically been classified as either white rot or brown rot, based on the ability (in white rot only) to degrade lignin along with cellulose and hemicellulose. Prior genomic comparisons suggested that the two decay modes can be distinguished based on the presence or absence of ligninolytic class II peroxidases (PODs), as well as the abundance of enzymes acting directly on crystalline cellulose (reduced in brown rot). To assess the generality of the white-rot/brown-rot classification paradigm, we compared the genomes of 33 basidiomycetes, including four newly sequenced wood decayers, and performed phylogenetically informed principal-components analysis (PCA) of a broad range of gene families encoding plant biomass-degrading enzymes. The newly sequenced Botryobasidium botryosum and Jaapia argillacea genomes lack PODs but possess diverse enzymes acting on crystalline cellulose, and they group close to the model white-rot species Phanerochaete chrysosporium in the PCA. Furthermore, laboratory assays showed that both B. botryosum and J. argillacea can degrade all polymeric components of woody plant cell walls, a characteristic of white rot. We also found expansions in reducing polyketide synthase genes specific to the brown-rot fungi. Our results suggest a continuum rather than a dichotomy between the white-rot and brown-rot modes of wood decay. A more nuanced categorization of rot types is needed, based on an improved understanding of the genomics and biochemistry of wood decay.

Iron (Fe) is a major micronutrient and is required for plant growth and development. Nongrass species have evolved a reduction-based strategy to solubilize and take up Fe. The secretion of Fe-mobilizing coumarins (e.g. fraxetin, esculetin and sideretin) by plant roots plays an important role in this process. Although the biochemical mechanisms leading to their biosynthesis have been well described, very little is known about their cellular and subcellular localization or their mobility within plant tissues. Spectral imaging was used to monitor, in Arabidopsis thaliana, the in planta localization of Fe-mobilizing coumarins and scopolin. Molecular, genetic and biochemical approaches were also used to investigate the dynamics of coumarin accumulation in roots. These approaches showed that root hairs play a major role in scopoletin secretion, whereas fraxetin and esculetin secretion occurs through all epidermis cells. The findings of this study also showed that the transport of coumarins from the cortex to the rhizosphere relies on the PDR9 transporter under Fe-deficient conditions. Additional experiments support the idea that coumarins move throughout the plant body via the xylem sap and that several plant species can take up coumarins present in the surrounding media. Altogether, the data presented here demonstrate that coumarin storage and accumulation in roots is a highly complex and dynamic process.