The Natural Histories of Species and Their Genomes

Hess, Jaqueline; Pringle, Anne

doi:10.1016/b978-0-12-397940-7.00008-2

Cited by 10 publications

(4 citation statements)

References 76 publications

(98 reference statements)

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“…Amanita inopinata closely resembles the EM Amanita with respect to its set of PCW degrading enzymes, although this species is not associated with EM hosts, does not form EM structures in nature or in culture, and appears nested within a clade of litter degraders ( Wolfe, Tulloss, et al. 2012 ; Hess and Pringle 2014 ). While losses and reductions of PCW-degrading enzymes define the EM Amanita , an EM Amanita cannot be defined by the absence of PCW degrading enzymes.…”

Section: Resultsmentioning

confidence: 99%

“…guessowii (from this point forward discussed as “ A. muscaria ”), the AS species Amanita inopinata and Amanita thiersii , and the AS outgroup Volvariella volvaceae . The natural history of each species is described more fully by ( Hess and Pringle 2014 ). We have previously shown transposable element (TE) expansions in two out of three of these EM species (but also the asymbiotic A. thiersii ), suggesting that even within this single genus, distinct evolutionary processes may be influencing the architecture of different genomes ( Hess et al.…”

Section: Introductionmentioning

confidence: 99%

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Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita

Hess

Skrede

Mares

et al. 2018

Molecular Biology and Evolution

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Fungi are evolutionary shape shifters and adapt quickly to new environments. Ectomycorrhizal (EM) symbioses are mutualistic associations between fungi and plants and have evolved repeatedly and independently across the fungal tree of life, suggesting lineages frequently reconfigure genome content to take advantage of open ecological niches. To date analyses of genomic mechanisms facilitating EM symbioses have involved comparisons of distantly related species, but here, we use the genomes of three EM and two asymbiotic (AS) fungi from the genus Amanita as well as an AS outgroup to study genome evolution following a single origin of symbiosis. Our aim was to identify the defining features of EM genomes, but our analyses suggest no clear differentiation of genome size, gene repertoire size, or transposable element content between EM and AS species. Phylogenetic inference of gene gains and losses suggests the transition to symbiosis was dominated by the loss of plant cell wall decomposition genes, a confirmation of previous findings. However, the same dynamic defines the AS species A. inopinata, suggesting loss is not strictly associated with origin of symbiosis. Gene expansions in the common ancestor of EM Amanita were modest, but lineage specific and large gene family expansions are found in two of the three EM extant species. Even closely related EM genomes appear to share few common features. The genetic toolkit required for symbiosis appears already encoded in the genomes of saprotrophic species, and this dynamic may explain the pervasive, recurrent evolution of ectomycorrhizal associations.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita

Hess

Skrede

Mares

et al. 2018

Molecular Biology and Evolution

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“…in the genus Epipactis (Selosse et al, 2004; see references above). Yet, phylogenies support that ECM fungi have evolved from soil saprotrophic fungi (Hess & Pringle, 2014;Kohler et al, 2015), but: (1) these analyses did not consider endophytic species or status; and (2) endophytism may just be the intermediary step on the way from saprotrophic to ECM conditions. From this step, endophytism may either secondarily disappear or persist in extant ECM species.…”

Section: Endophytism In Other Ecm Fungimentioning

confidence: 99%

Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, endophytically colonise roots of non‐ectomycorrhizal plants in natural environments

et al. 2019

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Summary Serendipitous findings and studies on Tuber species suggest that some ectomycorrhizal fungi, beyond their complex interaction with ectomycorrhizal hosts, also colonise roots of nonectomycorrhizal plants in a loose way called endophytism. Here, we investigate endophytism of T. melanosporum and T. aestivum. We visualised endophytic T. melanosporum hyphae by fluorescent in situ hybridisation on nonectomycorrhizal plants. For the two Tuber species, microsatellite genotyping investigated the endophytic presence of the individuals whose mating produced nearby ascocarps. We quantified the expression of four T. aestivum genes in roots of endophyted, non‐ectomycorrhizal plants. Tuber melanosporum hyphae colonised the apoplast of healthy roots, confirming endophytism. Endophytic Tuber melanosporum and T. aestivum contributed to nearby ascocarps, but only as maternal parents (forming the flesh). Paternal individuals (giving only genes found in meiotic spores of ascocarps) were not detected. Gene expression of T. aestivum in non‐ectomycorrhizal plants confirmed a living status. Tuber species, and likely other ectomycorrhizal fungi found in nonectomycorrhizal plant roots in this study, can be root endophytes. This is relevant for the ecology (brûlé formation) and commercial production of truffles. Evolutionarily speaking, endophytism may be an ancestral trait in some ectomycorrhizal fungi that evolved from root endophytes.

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“…A recent phylogeny documents a single origin of symbiosis within the Amanita ; asymbiotic Amanita form a strongly supported clade basal to a monophyletic clade of symbiotic species (Wolfe et al ., ). Comparative genomics of EM and SAP Amanita reveal large‐scale losses of carbohydrate‐active enzymes from symbiotic genomes (Nagendran et al ., ; Wolfe et al ., ; Chaib De Mares et al ., ; Hess & Pringle, ). The result appears to be a general one; plant cell wall degrading enzymes are frequently lost after fungi become obligately dependent on plants for carbon (Martin et al ., , ).…”

Section: Introductionmentioning

confidence: 99%

Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita

et al. 2014

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SummaryThe genus Amanita encompasses both symbiotic, ectomycorrhizal fungi and asymbiotic litter decomposers; all species are derived from asymbiotic ancestors. Symbiotic species are no longer able to degrade plant cell walls. The carbohydrate esterases family 1 (CE1s) is a diverse group of enzymes involved in carbon metabolism, including decomposition and carbon storage. CE1 genes of the ectomycorrhizal A. muscaria appear diverged from all other fungal homologues, and more similar to CE1s of bacteria, suggesting a horizontal gene transfer (HGT) event.In order to test whether Amanita CE1s were acquired horizontally, we built a phylogeny of CE1s collected from across the tree of life, and describe the evolution of CE1 genes among Amanita and relevant lineages of bacteria.CE1s of symbiotic Amanita were very different from CE1s of asymbiotic Amanita, and are more similar to bacterial CE1s. The protein structure of one CE1 gene of A. muscaria matched a depolymerase that degrades the carbon storage molecule poly((R)-3-hydroxybutyrate) (PHB). Asymbiotic Amanita do not carry sequence or structural homologues of these genes.The CE1s acquired through HGT may enable novel metabolisms, or play roles in signaling or defense. This is the first evidence for the horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal fungi.

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The Natural Histories of Species and Their Genomes

Cited by 10 publications

References 76 publications

Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita

Rapid Divergence of Genome Architectures Following the Origin of an Ectomycorrhizal Symbiosis in the Genus Amanita

Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, endophytically colonise roots of non‐ectomycorrhizal plants in natural environments

Horizontal transfer of carbohydrate metabolism genes into ectomycorrhizal Amanita

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