l e t t e r sTo elucidate the genetic bases of mycorrhizal lifestyle evolution, we sequenced new fungal genomes, including 13 ectomycorrhizal (ECM), orchid (ORM) and ericoid (ERM) species, and five saprotrophs, which we analyzed along with other fungal genomes. Ectomycorrhizal fungi have a reduced complement of genes encoding plant cell walldegrading enzymes (PCWDEs), as compared to their ancestral wood decayers. Nevertheless, they have retained a unique array of PCWDEs, thus suggesting that they possess diverse abilities to decompose lignocellulose. Similar functional categories of nonorthologous genes are induced in symbiosis. Of induced genes, 7-38% are orphan genes, including genes that encode secreted effector-like proteins. Convergent evolution of the mycorrhizal habit in fungi occurred via the repeated evolution of a 'symbiosis toolkit', with reduced numbers of PCWDEs and lineage-specific suites of mycorrhiza-induced genes.Fungi are often described as either saprotrophs, which degrade complex organic substrates, or biotrophs, which obtain carbon compounds from living hosts. Among the latter, ECM fungi provide crucial ecological services in interacting with forest trees. They are portrayed as mutualists trading host photoassimilates for nutrients and having limited capacity to decompose soil lignocellulose 1-3 , as a result of their reduced repertoire of PCWDEs 4-6 . However, recent studies are challenging this view [7][8][9][10] . An improved understanding of the ability of ECM fungi to decompose lignocellulose is needed to resolve mechanisms of nutrient cycling in forests. The ECM lifestyle in Laccaria bicolor is associated with the expression of new mycorrhizainduced small secreted proteins (MiSSPs) that are required for establishment of symbiosis 11,12 . Mycorrhizal symbioses have arisen repeatedly during fungal evolution and include not only ECM associations but also those with ERM and ORM mycorrhizae 13 . It is not known whether these symbioses share the genomic features found in L. bicolor 4 and Tuber melanosporum 5 . Here we assess whether there Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists

Rust fungi are some of the most devastating pathogens of crop plants. They are obligate biotrophs, which extract nutrients only from living plant tissues and cannot grow apart from their hosts. Their lifestyle has slowed the dissection of molecular mechanisms underlying host invasion and avoidance or suppression of plant innate immunity. We sequenced the 101-Mb genome of Melampsora laricipopulina, the causal agent of poplar leaf rust, and the 89-Mb genome of Puccinia graminis f. sp. tritici, the causal agent of wheat and barley stem rust. We then compared the 16,399 predicted proteins of M. larici-populina with the 17,773 predicted proteins of P. graminis f. sp tritici. Genomic features related to their obligate biotrophic lifestyle include expanded lineage-specific gene families, a large repertoire of effector-like small secreted proteins, impaired nitrogen and sulfur assimilation pathways, and expanded families of amino acid and oligopeptide membrane transporters. The dramatic up-regulation of transcripts coding for small secreted proteins, secreted hydrolytic enzymes, and transporters in planta suggests that they play a role in host infection and nutrient acquisition. Some of these genomic hallmarks are mirrored in the genomes of other microbial eukaryotes that have independently evolved to infect plants, indicating convergent adaptation to a biotrophic existence inside plant cells.comparative genomics | plant pathogen | basidiomycete | evolution | rust disease

Rice blast is caused by the fungus Magnaporthe grisea, which elaborates specialized infection cells called appressoria to penetrate the tough outer cuticle of the rice plant Oryza sativa. We found that the formation of an appressorium required, sequentially, the completion of mitosis, nuclear migration, and death of the conidium (fungal spore) from which the infection originated. Genetic intervention during mitosis prevented both appressorium development and conidium death. Impairment of autophagy, by the targeted mutation of the MgATG8 gene, arrested conidial cell death but rendered the fungus nonpathogenic. Thus, the initiation of rice blast requires autophagic cell death of the conidium.

During the diversification of Fungi and the rise of conifer-dominated and angiosperm- dominated forests, mutualistic symbioses developed between certain trees and ectomycorrhizal fungi that enabled these trees to colonize boreal and temperate regions. The evolutionary success of these symbioses is evident from phylogenomic analyses that suggest that ectomycorrhizal fungi have arisen in approximately 60 independent saprotrophic lineages, which has led to the wide range of ectomycorrhizal associations that exist today. In this Review, we discuss recent genomic studies that have revealed the adaptations that seem to be fundamental to the convergent evolution of ectomycorrhizal fungi, including the loss of some metabolic functions and the acquisition of effectors that facilitate mutualistic interactions with host plants. Finally, we consider how these insights can be integrated into a model of the development of ectomycorrhizal symbioses.

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.ectomycorrhizal fungus | defense | tree nutrition | host immunity | plant hormone

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.

Fungi are major players in the carbon cycle in forest ecosystems due to the wide range of interactions they have with plants either through soil degradation processes by litter decayers or biotrophic interactions with pathogenic and ectomycorrhizal symbionts. Secretion of fungal proteins mediates these interactions by allowing the fungus to interact with its environment and/or host. Ectomycorrhizal (ECM) symbiosis independently appeared several times throughout evolution and involves approximately 80% of trees. Despite extensive physiological studies on ECM symbionts, little is known about the composition and specificities of their secretomes. In this study, we used a bioinformatics pipeline to predict and analyze the secretomes of 49 fungal species, including 11 ECM fungi, wood and soil decayers and pathogenic fungi to tackle the following questions: (1) Are there differences between the secretomes of saprophytic and ECM fungi? (2) Are small-secreted proteins (SSPs) more abundant in biotrophic fungi than in saprophytic fungi? and (3) Are there SSPs shared between ECM, saprotrophic and pathogenic fungi? We showed that the number of predicted secreted proteins is similar in the surveyed species, independently of their lifestyle. The secretome from ECM fungi is characterized by a restricted number of secreted CAZymes, but their repertoires of secreted proteases and lipases are similar to those of saprotrophic fungi. Focusing on SSPs, we showed that the secretome of ECM fungi is enriched in SSPs compared with other species. Most of the SSPs are coded by orphan genes with no known PFAM domain or similarities to known sequences in databases. Finally, based on the clustering analysis, we identified shared- and lifestyle-specific SSPs between saprotrophic and ECM fungi. The presence of SSPs is not limited to fungi interacting with living plants as the genome of saprotrophic fungi also code for numerous SSPs. ECM fungi shared lifestyle-specific SSPs likely involved in symbiosis that are good candidates for further functional analyses.

Understanding the mechanisms that underlie nutrient use efficiency and carbon allocation along with mycorrhizal interactions is critical for managing croplands and forests soundly. Indeed, nutrient availability, uptake and exchange in biotrophic interactions drive plant growth and modulate biomass allocation. These parameters are crucial for plant yield, a major issue in the context of high biomass production. Transport processes across the polarized membrane interfaces are of major importance in the functioning of the established mycorrhizal association as the symbiotic relationship is based on a 'fair trade' between the fungus and the host plant. Nutrient and/or metabolite uptake and exchanges, at biotrophic interfaces, are controlled by membrane transporters whose regulation patterns are essential for determining the outcome of plant-fungus interactions and adapting to changes in soil nutrient quantity and/or quality. In the present review, we summarize the current state of the art regarding transport systems in the two major forms of mycorrhiza, namely ecto- and arbuscular mycorrhiza.