Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi

Lofgren, Lotus A.; Nguyen, Nhu; Vilgalys, Rytas; Ruytinx, Joske; Liao, Hui; Branco, Sara; Kuo, Alan; LaButti, Kurt; Lipzen, Anna; Andreopoulos, William; Pangilinan, Jasmyn; Riley, Robert; Hundley, Hope; Na, Hyunsoo; Barry, Kerrie; Grigoriev, Igor V.; Stajich, Jason E.; Kennedy, Peter G.

doi:10.1111/nph.17160

Cited by 54 publications

(65 citation statements)

References 178 publications

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“…The evolution of ECM genomes within a single lineage has been investigated for the Amanitaceae, which showed a rapid expansion and contraction of functionally relevant genes early in the evolution of the ECM habit (Hess et al ., 2018). Another study focusing on the Pinaceae‐associated genus Suillus found dynamic gene evolution within the lineage, with secondary metabolites linked to host specificity (Lofgren et al ., 2021).…”

Section: Introductionmentioning

confidence: 99%

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom‐forming fungi

et al. 2022

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The ectomycorrhizal (ECM) symbiosis has independently evolved from diverse types of saprotrophic ancestors. In this study, we seek to identify genomic signatures of the transition to the ECM habit within the hyperdiverse Russulaceae.We present comparative analyses of the genomic architecture and the total and secreted gene repertoires of 18 species across the order Russulales, of which 13 are newly sequenced, including a representative of a saprotrophic member of Russulaceae, Gloeopeniophorella convolvens.The genomes of ECM Russulaceae are characterized by a loss of genes for plant cell walldegrading enzymes (PCWDEs), an expansion of genome size through increased transposable element (TE) content, a reduction in secondary metabolism clusters, and an association of small secreted proteins (SSPs) with TE 'nests', or dense aggregations of TEs. Some PCWDEs have been retained or even expanded, mostly in a species-specific manner. The genome of G. convolvens possesses some characteristics of ECM genomes (e.g. loss of some PCWDEs, TE expansion, reduction in secondary metabolism clusters).Functional specialization in ECM decomposition may drive diversification. Accelerated gene evolution predates the evolution of the ECM habit, indicating that changes in genome architecture and gene content may be necessary to prime the evolutionary switch.

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Section: Introductionmentioning

confidence: 99%

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom‐forming fungi

et al. 2022

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“…Functional traitssuch as gene copy numbers for PCWDEs, N and phosphate acquisition pathways, MiSSPs, and TEswithin a fungal family across functional guilds (e.g. saprotrophs vs symbiotrophs) have been investigated within the Amanitaceae, Endogonaceae, Russulaceae, Suillaceae, and Tuberaceae (Hess et al, 2018;Murat et al, 2018;Chang et al, 2019;Lofgren et al, 2021;Looney et al, 2021). These studies have shown that the aforementioned hallmarks of the ectomycorrhizal ecology are recapitulated at the family level, although idiosyncrasies have been identified in each of these fungal families, e.g.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales

Miyauchi

Morin

et al. 2021

New Phytologist

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We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives.Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae.Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay.This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes.

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“…How host specificity may be encoded into EcM fungal genomes and driven by gene expression remains poorly understood. In their global analysis of gene family dynamics for 23 Suillus species, Lofgren et al (2021) found that host specialist Suillus genomes encode numerous rapidly evolving gene families, representing both gene family expansions and contractions. Gene families coding for terpene- and non-ribosomal peptide synthetase-like secondary metabolite clusters, known to play a role in the structuring of host specificity relationships for fungi, are significantly enriched in Suillus species.…”

Section: Introductionmentioning

confidence: 99%

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

Tang

Lebreton

et al. 2021

Front. Plant Sci.

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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.

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Comparative genomics reveals dynamic genome evolution in host specialist ectomycorrhizal fungi

Cited by 54 publications

References 178 publications

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom‐forming fungi

Evolutionary transition to the ectomycorrhizal habit in the genomes of a hyperdiverse lineage of mushroom‐forming fungi

Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales

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

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