Comparative genomics reveals a dynamic genome evolution in the ectomycorrhizal milk‐cap (Lactarius) mushrooms

Abstract

Ectomycorrhizal fungi play a key role in forests by establishing mutualistic symbioses with woody plants. Genome analyses have identified conserved symbiosis-related traits among ectomycorrhizal fungal species, but the molecular mechanisms underlying host specificity remain poorly known.We sequenced and compared the genomes of seven species of milk-cap fungi (Lactarius, Russulales) with contrasting host specificity. We also compared these genomes with those of symbiotic and saprotrophic Russulales species, aiming to identify genes involved in their ecology and host specificity.The size of Lactarius genomes is significantly larger than other Russulales species, owing to a massive accumulation of transposable elements and duplication of dispensable genes. As expected, their repertoire of genes coding for plant cell wall-degrading enzymes is restricted, but they retained a substantial set of genes involved in microbial cell wall degradation. Notably, Lactarius species showed a striking expansion of genes encoding proteases, such as secreted ectomycorrhiza-induced sedolisins. A high copy number of genes coding for small secreted LysM proteins and Lactarius-specific lectins were detected, which may be linked to host specificity.This study revealed a large diversity in the genome landscapes and gene repertoires within Russulaceae. The known host specificity of Lactarius symbionts may be related to mycorrhizainduced species-specific genes, including secreted sedolisins.

The High-quality genome assembly of Lactarius hatsudake

“…The Scaffold N(x) length distribution in L. hatsudake JH5 was also significantly higher than the length of Scaffold N(x) distribution in L. hatsudake MG20 (Figure 2). In total, this L. hatsudake genome assembly represents a significant improvement than that of other previously released Lactarius genomes (contig N50: 5.0 kb-261.3 kb) (Table 1) (Li et al 2020,Saier et al 2014,Lebreton et al 2022). Compared with L. hatsudake 109 genome assembly, JH5 genome show the considerable N50 length (223.2 kb vs 261.3 kb), and BUSCO results (89.0% vs 87.6 % ).…”

“…What is currently known is that, based on whole-genome sequencing, sexual reproduction was found to be heterotypical coordinated in Tuber melanosporum (Martin et al 2010), while Laccaria bicolor was found to possess a family of genes associated with symbiosis, called the “symbiosis toolbox” (Martin et al 2008; Martin and Selosse 2008). Studies have revealed a great diversity of genomic landscapes and gene pools within Russulaceae (Lebreton et al 2022). These results suggest that in-depth analysis of the genomic characteristics of mycorrhizal edible fungi by genome sequencing technology can help to identify and clarify the process of mycorrhiza formation and fruiting body development, thus contributing to an efficient and sustainable cultivation of this edible mycorrhizal fungi.…”

“…Deciphering the genome of L. hatsudake will provide theoretical support for the process of mycorrhiza and fruiting body formation and may guide further large-scale cultivation. Currently, twenty-four Lactarius species have undergone preliminary genomic analysis, with N50 values ranging from 5.0 kb to 261.3 kb (Li et al 2020, Lebreton et al (2022). For L. hatsudake , using Illumina sequencing technology, Li et al (2020) reported a draft genome of L. hatsudake MG20 with an N50 of 5.0 kb.…”

“…For L. hatsudake , using Illumina sequencing technology, Li et al (2020) reported a draft genome of L. hatsudake MG20 with an N50 of 5.0 kb. More recently, using PacBio sequencing platform, Lebreton et al (2022) published the genome assembly of L. hatsudake 109 with an N50 of 261.3 kb.…”

Cultivation studies of edible ectomycorrhizal mushrooms: successful establishment of ectomycorrhizal associations <i>in vitro</i> and efficient production of fruiting bodies

“…A recent study reported taxon-specific expression of small secreted proteins (SSPs) that likely function as effectors in fungus-plant interactions in Suillus , which may explain the association between the host of this fungal taxon and Pinaceae ( Lofgren et al, 2021 ). Even in saffron milk caps, specific SSPs bearing LysM have been reported ( Lebreton et al, 2022 ). The identification of specific SSPs that determine the conifer hosts of T. matsutake and control gene expressions to influence host colonization levels would dramatically facilitate T. matsutake cultivation.…”