Expansion of Signal Transduction Pathways in Fungi by Extensive Genome Duplication
Language English Country England, Great Britain Media print-electronic
Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.
Grant support
R01 AI050113
NIAID NIH HHS - United States
PubMed
27238284
PubMed Central
PMC5089372
DOI
10.1016/j.cub.2016.04.038
PII: S0960-9822(16)30361-X
Knihovny.cz E-resources
- MeSH
- Gene Duplication * MeSH
- Transcription, Genetic radiation effects MeSH
- Genome, Fungal * MeSH
- Evolution, Molecular * MeSH
- Mucor genetics radiation effects MeSH
- Multigene Family MeSH
- Perception MeSH
- Phycomyces genetics radiation effects MeSH
- Signal Transduction genetics MeSH
- Light MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
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.
Centre for Genomic Regulation 08010 Barcelona Spain
Centre for Genomic Regulation Doctor Aiguader 88 08003 Barcelona Spain
Departamento de Genética y Microbiología Universidad de Murcia 30071 Murcia Spain
Department of Agrarian Production Public University of Navarre 31006 Pamplona Spain
Department of Biology Technion Israel Institute of Technology Haifa 32000 Israel
Department of Biology University of Florida P O Box 118525 Gainesville FL 32611 8525 USA
Department of Genetics University of Seville Avenida Reina Mercedes s n 41012 Seville Spain
Genome Analysis Platform CIC bioGUNE Bizkaia Technology Park 48160 Derio Bizkaia Spain
Pacific Northwest National Laboratory 902 Battelle Boulevard Richland WA 99352 USA
US Department of Energy Joint Genome Institute 2800 Mitchell Drive Walnut Creek CA 94598 USA
See more in PubMed
Cerdá-Olmedo E. Phycomyces and the biology of light and color. FEMS Microbiol Rev. 2001;25:503–512. PubMed
Corrochano LM, Garre V. Photobiology in the Zygomycota: multiple photoreceptor genes for complex responses to light. Fungal Genet Biol. 2010;47:893–899. PubMed
Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, et al. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet. 2009;5:e1000549. PubMed PMC
Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997;387:708–713. PubMed
Dietrich FS, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S, Mohr C, Pöhlmann R, Luedi P, Choi S, et al. The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science. 2004;304:304–307. PubMed
Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004;428:617–624. PubMed
Sanz C, Rodríguez-Romero J, Idnurm A, Christie JM, Heitman J, Corrochano LM, Eslava AP. Phycomyces MADB interacts with MADA to form the primary photoreceptor complex for fungal phototropism. Proc Natl Acad Sci USA. 2009;106:7095–7100. PubMed PMC
Idnurm A, Rodríguez-Romero J, Corrochano LM, Sanz C, Iturriaga EA, Eslava AP, Heitman J. The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc Natl Acad Sci USA. 2006;103:4546–4551. PubMed PMC
Silva F, Torres-Martínez S, Garre V. Distinct white collar-1 genes control specific light responses in Mucor circinelloides. Mol Microbiol. 2006;61:1023–1037. PubMed
McLaughlin DJ, Hibbett DS, Lutzoni F, Spatafora JW, Vilgalys R. The search for the fungal tree of life. Trends Microbiol. 2009;17:488–497. PubMed
Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, et al. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature. 2008;452:88–92. PubMed
Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL, et al. Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA. 2011;108:9166–9171. PubMed PMC
Huerta-Cepas J, Gabaldón T. Assigning duplication events to relative temporal scales in genome-wide studies. Bioinformatics. 2011;27:38–45. PubMed
Marcet-Houben M, Gabaldón T. Beyond the whole-genome duplication: phylogenetic evidence for an ancient interspecies hybridization in the baker's yeast lineage. PLoS Biol. 2015;13:e1002220. PubMed PMC
Marcet-Houben M, Marceddu G, Gabaldón T. Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. BMC Evol Biol. 2009;9:295. PubMed PMC
Schwartze VU, Winter S, Shelest E, Marcet-Houben M, Horn F, Wehner S, Linde J, Valiante V, Sammeth M, Riege K, et al. Gene expansion shapes genome architecture in the human pathogen Lichtheimia corymbifera: an evolutionary genomics analysis in the ancient terrestrial mucorales (Mucoromycotina) PLoS Genet. 2014;10:e1004496. PubMed PMC
Lafon A, Han KH, Seo JA, Yu JH, d'Enfert C. G-protein and cAMP-mediated signaling in aspergilli: a genomic perspective. Fungal Genet Biol. 2006;43:490–502. PubMed
Li L, Wright SJ, Krystofova S, Park G, Borkovich KA. Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol. 2007;61:423–452. PubMed
Müller P, Leibbrandt A, Teunissen H, Cubasch S, Aichinger C, Kahmann R. The Gβ-subunit-encoding gene bpp1 controls cyclic-AMP signaling in Ustilago maydis. Eukaryot Cell. 2004;3:806–814. PubMed PMC
Wang P, Perfect JR, Heitman J. The G-protein β subunit GPB1 is required for mating and haploid fruiting in Cryptococcus neoformans. Mol Cell Biol. 2000;20:352–362. PubMed PMC
Xue C, Hsueh YP, Heitman J. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiol Rev. 2008;32:1010–1032. PubMed PMC
Idnurm A, Verma S, Corrochano LM. A glimpse into the basis of vision in the kingdom Mycota. Fungal Genet Biol. 2010;47:881–892. PubMed PMC
Peñalva MA, Tilburn J, Bignell E, Arst HN., Jr. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 2008;16:291–300. PubMed
Nicolás FE, Moxon S, de Haro JP, Calo S, Grigoriev IV, Torres-Martínez S, Moulton V, Ruiz-Vázquez RM, Dalmay T. Endogenous short RNAs generated by Dicer 2 and RNA-dependent RNA polymerase 1 regulate mRNAs in the basal fungus Mucor circinelloides. Nucleic Acids Res. 2010;38:5535–5541. PubMed PMC
Ruiz-Roldán MC, Garre V, Guarro J, Mariné M, Roncero MI. Role of the white collar 1 photoreceptor in carotenogenesis, UV resistance, hydrophobicity, and virulence of Fusarium oxysporum. Eukaryot Cell. 2008;7:1227–1230. PubMed PMC
Idnurm A, Heitman J. Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol. 2005;3:e95. PubMed PMC
Lee SC, Li A, Calo S, Heitman J. Calcineurin plays key roles in the dimorphic transition and virulence of the human pathogenic zygomycete Mucor circinelloides. PLoS Pathog. 2013;9:e1003625. PubMed PMC
Lipson ED, Terasaka DT. Photogeotropism in Phycomyces double mutants. Exp Mycol. 1981;5:101–111.
Sanz C, Benito EP, Orejas M, Alvarez MI, Eslava AP. Protein-DNA interactions in the promoter region of the Phycomyces carB and carRA genes correlate with the kinetics of their mRNA accumulation in response to light. Fungal Genet Biol. 2010;47:773–781. PubMed
Larhammar D, Nordström K, Larsson TA. Evolution of vertebrate rod and cone phototransduction genes. Philos Trans R Soc Lond B Biol Sci. 2009;364:2867–2880. PubMed PMC
Campuzano V, Díaz-Mínguez JM, Eslava AP, Alvarez MI. A new gene (madI) involved in the phototropic response of Phycomyces. Mol Gen Genet. 1990;223:148–151. PubMed
Alvarez MI, Eslava AP, Lipson ED. Phototropism mutants of Phycomyces blakesleeanus isolated at low light intensity. Exp Mycol. 1989;13:38–48.
Chaudhary S, Polaino S, Shakya VP, Idnurm A. A new genetic linkage map of the zygomycete fungus Phycomyces blakesleeanus. PLoS One. 2013;8:e58931. PubMed PMC
