Journal Articles

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    Reconstruction of gene innovation associated with major evolutionary transitions in the kingdom Fungi
    (BioMed Central Ltd, 2022-12) Wu B; Hao W; Cox MP
    BACKGROUND: Fungi exhibit astonishing diversity with multiple major phenotypic transitions over the kingdom's evolutionary history. As part of this process, fungi developed hyphae, adapted to land environments (terrestrialization), and innovated their sexual structures. These changes also helped fungi establish ecological relationships with other organisms (animals and plants), but the genomic basis of these changes remains largely unknown. RESULTS: By systematically analyzing 304 genomes from all major fungal groups, together with a broad range of eukaryotic outgroups, we have identified 188 novel orthogroups associated with major changes during the evolution of fungi. Functional annotations suggest that many of these orthogroups were involved in the formation of key trait innovations in extant fungi and are functionally connected. These innovations include components for cell wall formation, functioning of the spindle pole body, polarisome formation, hyphal growth, and mating group signaling. Innovation of mitochondria-localized proteins occurred widely during fungal transitions, indicating their previously unrecognized importance. We also find that prokaryote-derived horizontal gene transfer provided a small source of evolutionary novelty with such genes involved in key metabolic pathways. CONCLUSIONS: The overall picture is one of a relatively small number of novel genes appearing at major evolutionary transitions in the phylogeny of fungi, with most arising de novo and horizontal gene transfer providing only a small additional source of evolutionary novelty. Our findings contribute to an increasingly detailed portrait of the gene families that define fungal phyla and underpin core features of extant fungi.
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    Recurrent horizontal transfer identifies mitochondrial positive selection in a transmissible cancer.
    (Springer Nature Limited, 2020-06-16) Strakova A; Nicholls TJ; Baez-Ortega A; Ní Leathlobhair M; Sampson AT; Hughes K; Bolton IAG; Gori K; Wang J; Airikkala-Otter I; Allen JL; Allum KM; Arnold CL; Bansse-Issa L; Bhutia TN; Bisson JL; Blank K; Briceño C; Castillo Domracheva A; Corrigan AM; Cran HR; Crawford JT; Cutter SM; Davis E; de Castro KF; De Nardi AB; de Vos AP; Delgadillo Keenan L; Donelan EM; Espinoza Huerta AR; Faramade IA; Fazil M; Fotopoulou E; Fruean SN; Gallardo-Arrieta F; Glebova O; Gouletsou PG; Häfelin Manrique RF; Henriques JJGP; Horta RS; Ignatenko N; Kane Y; King C; Koenig D; Krupa A; Kruzeniski SJ; Lanza-Perea M; Lazyan M; Lopez Quintana AM; Losfelt T; Marino G; Martínez Castañeda S; Martínez-López MF; Masuruli BM; Meyer M; Migneco EJ; Nakanwagi B; Neal KB; Neunzig W; Nixon SJ; Ortega-Pacheco A; Pedraza-Ordoñez F; Peleteiro MC; Polak K; Pye RJ; Ramirez-Ante JC; Reece JF; Rojas Gutierrez J; Sadia H; Schmeling SK; Shamanova O; Sherlock AG; Steenland-Smit AE; Svitich A; Tapia Martínez LJ; Thoya Ngoka I; Torres CG; Tudor EM; van der Wel MG; Vițălaru BA; Vural SA; Walkinton O; Wehrle-Martinez AS; Widdowson SAE; Zvarich I; Chinnery PF; Falkenberg M; Gustafsson CM; Murchison EP
    Autonomous replication and segregation of mitochondrial DNA (mtDNA) creates the potential for evolutionary conflict driven by emergence of haplotypes under positive selection for 'selfish' traits, such as replicative advantage. However, few cases of this phenomenon arising within natural populations have been described. Here, we survey the frequency of mtDNA horizontal transfer within the canine transmissible venereal tumour (CTVT), a contagious cancer clone that occasionally acquires mtDNA from its hosts. Remarkably, one canine mtDNA haplotype, A1d1a, has repeatedly and recently colonised CTVT cells, recurrently replacing incumbent CTVT haplotypes. An A1d1a control region polymorphism predicted to influence transcription is fixed in the products of an A1d1a recombination event and occurs somatically on other CTVT mtDNA backgrounds. We present a model whereby 'selfish' positive selection acting on a regulatory variant drives repeated fixation of A1d1a within CTVT cells.