Dataset Information

Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication.

ABSTRACT: Plants and fungi use light and other signals to regulate development, growth, and metabolism. The fruiting bodies of the fungus Phycomyces blakesleeanus are single cells that react to environmental cues, including light, but the mechanisms are largely unknown [1]. The related fungus Mucor circinelloides is an opportunistic human pathogen that changes its mode of growth upon receipt of signals from the environment to facilitate pathogenesis [2]. Understanding how these organisms respond to environmental cues should provide insights into the mechanisms of sensory perception and signal transduction by a single eukaryotic cell, and their role in pathogenesis. We sequenced the genomes of P. blakesleeanus and M. circinelloides and show that they have been shaped by an extensive genome duplication or, most likely, a whole-genome duplication (WGD), which is rarely observed in fungi [3-6]. We show that the genome duplication has expanded gene families, including those involved in signal transduction, and that duplicated genes have specialized, as evidenced by differences in their regulation by light. The transcriptional response to light varies with the developmental stage and is still observed in a photoreceptor mutant of P. blakesleeanus. A phototropic mutant of P. blakesleeanus with a heterozygous mutation in the photoreceptor gene madA demonstrates that photosensor dosage is important for the magnitude of signal transduction. We conclude that the genome duplication provided the means to improve signal transduction for enhanced perception of environmental signals. Our results will help to understand the role of genome dynamics in the evolution of sensory perception in eukaryotes.

SUBMITTER: Corrochano LM

PROVIDER: S-EPMC5089372 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication.

Corrochano Luis M LM Kuo Alan A Marcet-Houben Marina M Polaino Silvia S Salamov Asaf A Villalobos-Escobedo José M JM Grimwood Jane J Álvarez M Isabel MI Avalos Javier J Bauer Diane D Benito Ernesto P EP Benoit Isabelle I Burger Gertraud G Camino Lola P LP Cánovas David D Cerdá-Olmedo Enrique E Cheng Jan-Fang JF Domínguez Angel A Eliáš Marek M Eslava Arturo P AP Glaser Fabian F Gutiérrez Gabriel G Heitman Joseph J Henrissat Bernard B Iturriaga Enrique A EA Lang B Franz BF Lavín José L JL Lee Soo Chan SC Li Wenjun W Lindquist Erika E López-García Sergio S Luque Eva M EM Marcos Ana T AT Martin Joel J McCluskey Kevin K Medina Humberto R HR Miralles-Durán Alejandro A Miyazaki Atsushi A Muñoz-Torres Elisa E Oguiza José A JA Ohm Robin A RA Olmedo María M Orejas Margarita M Ortiz-Castellanos Lucila L Pisabarro Antonio G AG Rodríguez-Romero Julio J Ruiz-Herrera José J Ruiz-Vázquez Rosa R Sanz Catalina C Schackwitz Wendy W Shahriari Mahdi M Shelest Ekaterina E Silva-Franco Fátima F Soanes Darren D Syed Khajamohiddin K Tagua Víctor G VG Talbot Nicholas J NJ Thon Michael R MR Tice Hope H de Vries Ronald P RP Wiebenga Ad A Yadav Jagjit S JS Braun Edward L EL Baker Scott E SE Garre Victoriano V Schmutz Jeremy J Horwitz Benjamin A BA Torres-Martínez Santiago S Idnurm Alexander A Herrera-Estrella Alfredo A Gabaldón Toni T Grigoriev Igor V IV

Current biology : CB 20160526 12

Plants and fungi use light and other signals to regulate development, growth, and metabolism. The fruiting bodies of the fungus Phycomyces blakesleeanus are single cells that react to environmental cues, including light, but the mechanisms are largely unknown [1]. The related fungus Mucor circinelloides is an opportunistic human pathogen that changes its mode of growth upon receipt of signals from the environment to facilitate pathogenesis [2]. Understanding how these organisms respond to enviro ...[more]

PMID: 27238284

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Project description:BackgroundRecent genomic studies have revealed a teleost-specific third-round whole genome duplication (3R-WGD) event occurred in a common ancestor of teleost fishes. However, it is unclear how the genes duplicated in this event were lost or persisted during the diversification of teleosts, and therefore, how many of the duplicated genes contribute to the genetic differences among teleosts. This subject is also important for understanding the process of vertebrate evolution through WGD events. We applied a comparative evolutionary approach to this question by focusing on the genes involved in long-term potentiation, taste and olfactory transduction, and the tricarboxylic acid cycle, based on the whole genome sequences of four teleosts; zebrafish, medaka, stickleback, and green spotted puffer fish.ResultsWe applied a state-of-the-art method of maximum-likelihood phylogenetic inference and conserved synteny analyses to each of 130 genes involved in the above biological systems of human. These analyses identified 116 orthologous gene groups between teleosts and tetrapods, and 45 pairs of 3R-WGD-derived duplicate genes among them. This suggests that more than half [(45x2)/(116+45)] = 56.5%) of the loci, probably more than ten thousand genes, present in a common ancestor of the four teleosts were still duplicated after the 3R-WGD. The estimated temporal pattern of gene loss suggested that, after the 3R-WGD, many (71/116) of the duplicated genes were rapidly lost during the initial 75 million years (MY), whereas on average more than half (27.3/45) of the duplicated genes remaining in the ancestor of the four teleosts (45/116) have persisted for about 275 MY. The 3R-WGD-derived duplicates that have persisted for a long evolutionary periods of time had significantly larger number of interacting partners and longer length of protein coding sequence, implying that they tend to be more multifunctional than the singletons after the 3R-WGD.ConclusionWe have shown firstly the temporal pattern of gene loss process after 3R-WGD on the basis of teleost phylogeny and divergence time frameworks. The 3R-WGD-derived duplicates have not undergone constant exponential decay, suggesting that selection favoured the long-term persistence of a subset of duplicates that tend to be multi-functional. On the basis of these results obtained from the analysis of 116 orthologous gene groups, we propose that more than ten thousand of 3R-WGD-derived duplicates have experienced lineage-specific evolution, that is, the differential sub-/neo-functionalization or secondary loss between lineages, and contributed to teleost diversity.

Dataset Information

Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication.

Publications

Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication.

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