Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius–Pinus Symbioses

Abstract

Ectomycorrhizal fungi establish a mutualistic symbiosis in roots of most woody plants. The molecular underpinning of ectomycorrhizal development was only explored in a few lineages. Here, we characterized the symbiotic transcriptomes of several milkcap species (Lactarius, Russulales) in association with different pine hosts. A time-course study of changes in gene expression during the development of L. deliciosus–Pinus taeda symbiosis identified 6 to 594 differentially expressed fungal genes at various developmental stages. Up- or down-regulated genes are involved in signaling pathways, nutrient transport, cell wall modifications, and plant defenses. A high number of genes coding for secreted proteases, especially sedolisins, were induced during root colonization. In contrast, only a few genes encoding mycorrhiza-induced small secreted proteins were identified. This feature was confirmed in several other Lactarius species in association with various pines. Further comparison among all these species revealed that each Lactarius species encodes a highly specific symbiotic gene repertoire, a feature possibly related to their host-specificity. This study provides insights on the genetic basis of symbiosis in an ectomycorrhizal order, the Russulales, which was not investigated so far.

Functional genomics gives new insights into the ectomycorrhizal degradation of chitin

“…The gene repertoire for chitin degradation varied among EcM species, as already reported for PCWDEs, secreted lipases, and proteases (Martino et al ., 2018; Miyauchi et al ., 2020; Lebreton et al ., 2021; Tang et al ., 2021; Looney et al ., 2022; Wu et al ., 2022). The studied genomes often lacked the chitosanase ( GH75 ) gene required for chitosan degradation, a key step in the alternate pathway involving chitin deacetylation to chitosan and genes encoding for LPMO participating in chitin oxidation.…”

“…proteases in combination with Fenton reaction) to scavenge organic N (Bödeker et al ., 2014; Rineau et al ., 2016; Shah et al ., 2016; Nicolás et al ., 2018; Op De Beeck et al ., 2018). In parallel with ecological and physiological research, large‐scale comparative genomic studies have shown that the genomes of most EcM fungi encode a restricted set of secreted plant cell wall–degrading enzymes (PCWDEs; Mycorrhizal Genomics Initiative Consortium et al ., 2015; Miyauchi et al ., 2020; Lebreton et al ., 2021; Tang et al ., 2021; Looney et al ., 2022; Wu et al ., 2022). Still, various lineages of EcM fungi have retained large sets of microbial cell wall degradation enzymes (MCWDEs) participating in fungal glucan, mannan, and chitin depolymerization (Miyauchi et al ., 2020).…”

Dual transcriptomic and metabolomic analyses provide novel insights into the role of vitamins A and B metabolism in ectomycorrhizal symbiosis between Pinus yunnanensis and Lactarius deliciosus

“…High-quality sections were stained with 5 μg mL À1 WGA (wheat germ agglutinin) conjugated with FITC (fluorescein isothiocyanate) (L4895, Sigma-Aldrich) to better observe EM structures (Tang et al, 2021).…”

How to reconnect mycorrhizal research with natural environments

“…Transcriptomics revealed thousands of differentially expressed plant genes in AM roots: as an example, 5215 genes of Lotus japonicus have been found to be impacted by the AM Gigaspora margarita (Venice et al, 2021) out of its 27,991 annotated genes (Li et al, 2020). By contrast, in ECM roots, fungal gene expression has been mostly investigated, resulting in the detection of a higher percentage of fungal gene regulation than the plant partner (Tang et al, 2021; Tarkka et al, 2013). These data offer us a snapshot of the different cellular and molecular mechanisms behind the two main types of mycorrhizas under lab conditions: in AMs the impressive reprogramming of root cells following the AM fungal entry requires an intense transcriptional activity and protein synthesis, while in ECM roots, plant cellular changes are much more limited and mostly involve the expansion of the apoplast to accommodate the intercellular hyphae (Bonfante, 2018).…”