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Curr Biol. 2016 Jun 20;26(12):1577-1584. doi: 10.1016/j.cub.2016.04.038. Epub 2016 May 26.

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

Author information

1
Department of Genetics, University of Seville, Avenida Reina Mercedes s/n, 41012 Seville, Spain. Electronic address: corrochano@us.es.
2
US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA.
3
Centre for Genomic Regulation (CRG), Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain.
4
School of Biological Sciences, University of Missouri-Kansas City, 5007 Rockhill Road, Kansas City, MO 64110, USA.
5
Laboratorio Nacional de Genómica para la Biodiversidad (LANGEBIO), Centro de Investigación y Estudios Avanzados, Kilómetro 9.6 Libramiento Norte, Carretera Irapuato-León, 36821 Irapuato, Guanajuato, México.
6
US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, CA 94598, USA; HudsonAlpha Institute of Biotechnology, 601 Genome Way Northwest, Huntsville, AL 35806, USA.
7
Departamento de Microbiología y Genética, Universidad de Salamanca, Plaza de los doctores de la Reina s/n, 37007 Salamanca, Spain.
8
Department of Genetics, University of Seville, Avenida Reina Mercedes s/n, 41012 Seville, Spain.
9
Departamento de Microbiología y Genética, Universidad de Salamanca, Plaza de los doctores de la Reina s/n, 37007 Salamanca, Spain; Instituto Hispano-Luso de Investigaciones Agrarias (CIALE), Universidad de Salamanca, Río Duero 12, 37185 Salamanca, Spain.
10
CBS-KNAW Fungal Biodiversity Centre and Fungal Molecular Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht, the Netherlands.
11
Universite de Montreal, Pavillon Roger-Gaudry, Biochimie, CP 6128, Succursale Centre-Ville, Montreal QC, H3C 3J7, Canada.
12
Department of Biology and Ecology, Faculty of Science, University of Ostrava, Chittussiho 10, 710 00 Ostrava, Czech Republic.
13
Lokey Interdisciplinary Center for Life Sciences and Engineering, Technion - Israel Institute of Technology, Haifa 3200003, Israel.
14
Department of Molecular Genetics and Microbiology, Duke University Medical Center, Research Drive, Durham, NC 27710, USA.
15
Centre National de la Recherche Scientifique (CNRS), UMR7257, Université Aix-Marseille, 163 Avenue de Luminy, 13288 Marseille, France; Department of Biological Sciences, King Abdulaziz University, P.O. Box 80203, Jeddah 21589, Saudi Arabia.
16
Genome Analysis Platform, CIC bioGUNE, Bizkaia Technology Park, 48160 Derio, Bizkaia, Spain.
17
Departamento de Genética y Microbiología, Universidad de Murcia, 30071 Murcia, Spain.
18
Department of Plant Pathology, Kansas State University, 4024 Throckmorton Plant Sciences Center, Manhattan, KS 66506, USA.
19
Department of Biological Sciences, Faculty of Science and Engineering, Ishinomaki Senshu University, Ishinomaki 986-8580, Japan.
20
Departamento de Biología Celular y Patología, Facultad de Medicina, Universidad de Salamanca, Avenida Campus Miguel de Unamuno, 37007 Salamanca, Spain.
21
Department of Agrarian Production, Public University of Navarre, 31006 Pamplona, Spain.
22
Instituto de Agroquímica y Tecnología de Alimentos, Consejo Superior de Investigaciones Científicas (IATA-CSIC), Avenida Catedrático Agustín Escardino 7, 46980 Paterna, Valencia, Spain.
23
Departamento de Ingeniería Genética, Unidad Irapuato, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Kilómetro 9.6 Libramiento Norte, Carretera Irapuato-León, 36821 Irapuato, Guanajuato, Mexico.
24
Leibniz Institute for Natural Product Research and Infection Biology (Hans Knoell Institute), Beutenbergstrasse 11a, 07745 Jena, Germany.
25
Biosciences, College of Life and Environmental Sciences, University of Exeter, Stocker Road, Exeter EX4 4QD, UK.
26
Department of Environmental Health, University of Cincinnati College of Medicine, 160 Panzeca Way, Cincinnati, OH 45267-0056, USA.
27
Department of Biology, University of Florida, P.O. Box 118525, Gainesville, FL 32611-8525, USA.
28
Pacific Northwest National Laboratory, 902 Battelle Boulevard, Richland, WA 99352, USA.
29
Department of Biology, Technion - Israel Institute of Technology, Haifa 32000, Israel.
30
School of Biological Sciences, University of Missouri-Kansas City, 5007 Rockhill Road, Kansas City, MO 64110, USA; School of BioSciences, University of Melbourne, Melbourne, VIC 3010, Australia.
31
Centre for Genomic Regulation (CRG), Doctor Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), Doctor Aiguader 88, 08003 Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), 08010 Barcelona, Spain.

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.

PMID:
27238284
PMCID:
PMC5089372
DOI:
10.1016/j.cub.2016.04.038
[Indexed for MEDLINE]
Free PMC Article

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