title: Algal ancestor of land plants was preadapted for symbiosis.
abstract: Colonization of land by plants was a major transition on Earth, but the developmental and genetic innovations required for this transition remain unknown. Physiological studies and the fossil record strongly suggest that the ability of the first land plants to form symbiotic associations with beneficial fungi was one of these critical innovations. In angiosperms, genes required for the perception and transduction of diffusible fungal signals for root colonization and for nutrient exchange have been characterized. However, the origin of these genes and their potential correlation with land colonization remain elusive. A comprehensive phylogenetic analysis of 259 transcriptomes and 10 green algal and basal land plant genomes, coupled with the characterization of the evolutionary path leading to the appearance of a key regulator, a calcium- and calmodulin-dependent protein kinase, showed that the symbiotic signaling pathway predated the first land plants. In contrast, downstream genes required for root colonization and their specific expression pattern probably appeared subsequent to the colonization of land. We conclude that the most recent common ancestor of extant land plants and green algae was preadapted for symbiotic associations. Subsequent improvement of this precursor stage in early land plants through rounds of gene duplication led to the acquisition of additional pathways and the ability to form a fully functional arbuscular mycorrhizal symbiosis.
authors.affiliation: Department of Agronomy, University of Wisconsin, Madison, WI 53706; John Innes Centre, Norwich NR4 7UH, United Kingdom; pierre-marc.delaux@lrsv.ups-tlse.fr.
authors.forename: Pierre-Marc
authors.initials: PM
authors.lastname: Delaux
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom;
authors.forename: Guru V
authors.initials: GV
authors.lastname: Radhakrishnan
authors.affiliation: Department of Agronomy, University of Wisconsin, Madison, WI 53706; Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
authors.forename: Dhileepkumar
authors.initials: D
authors.lastname: Jayaraman
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom;
authors.forename: Jitender
authors.initials: J
authors.lastname: Cheema
authors.affiliation: Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, Université Paul Sabatier, Unité Mixte de Recherche UMR5546, 31326 Castanet-Tolosan CEDEX, France; Centre National de la Recherche Scientifique, UMR5546, 31326 Castanet-Tolosan CEDEX, France;
authors.forename: Mathilde
authors.initials: M
authors.lastname: Malbreil
authors.affiliation: Biotechnology Center, University of Wisconsin, Madison, WI 53706; Department of Biochemistry, University of Wisconsin, Madison, WI 53706;
authors.forename: Jeremy D
authors.initials: JD
authors.lastname: Volkening
authors.affiliation: Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, 2-8-1 Mejirodai, Bunkyo-ku, Tokyo, 112-8681 Japan;
authors.forename: Hiroyuki
authors.initials: H
authors.lastname: Sekimoto
authors.affiliation: Advanced Science Research Center, Kanazawa University, 13-1 Takara-machi, Kanazawa, 920-0934, Japan;
authors.forename: Tomoaki
authors.initials: T
authors.lastname: Nishiyama
authors.affiliation: Botany Department, Cologne Biocenter, University of Cologne, 50674 Cologne, Germany;
authors.forename: Michael
authors.initials: M
authors.lastname: Melkonian
authors.affiliation: Real Jardín Botánico, 28014 Madrid, Spain;
authors.forename: Lisa
authors.initials: L
authors.lastname: Pokorny
authors.affiliation: Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
authors.forename: Carl J
authors.initials: CJ
authors.lastname: Rothfels
authors.affiliation: Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695;
authors.forename: Heike Winter
authors.initials: HW
authors.lastname: Sederoff
authors.affiliation: New York Botanical Garden, Bronx, NY 10458;
authors.forename: Dennis W
authors.initials: DW
authors.lastname: Stevenson
authors.affiliation: Botany Department, Cologne Biocenter, University of Cologne, 50674 Cologne, Germany;
authors.forename: Barbara
authors.initials: B
authors.lastname: Surek
authors.affiliation: Beijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
authors.forename: Yong
authors.initials: Y
authors.lastname: Zhang
authors.affiliation: Biotechnology Center, University of Wisconsin, Madison, WI 53706; Department of Biochemistry, University of Wisconsin, Madison, WI 53706;
authors.forename: Michael R
authors.initials: MR
authors.lastname: Sussman
authors.affiliation: Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, Université Paul Sabatier, Unité Mixte de Recherche UMR5546, 31326 Castanet-Tolosan CEDEX, France; Centre National de la Recherche Scientifique, UMR5546, 31326 Castanet-Tolosan CEDEX, France;
authors.forename: Christophe
authors.initials: C
authors.lastname: Dunand
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom;
authors.forename: Richard J
authors.initials: RJ
authors.lastname: Morris
authors.affiliation: Laboratoire de Recherche en Sciences Végétales, Université de Toulouse, Université Paul Sabatier, Unité Mixte de Recherche UMR5546, 31326 Castanet-Tolosan CEDEX, France; Centre National de la Recherche Scientifique, UMR5546, 31326 Castanet-Tolosan CEDEX, France;
authors.forename: Christophe
authors.identifier: http://orcid.org/0000-0001-5688-5379
authors.initials: C
authors.lastname: Roux
authors.affiliation: Beijing Genomics Institute-Shenzhen, Shenzhen 518083, China; Department of Biological Sciences, University of Alberta, Edmonton AB, T6G 2E9, Canada; Department of Medicine, University of Alberta, Edmonton AB, T6G 2E, Canada.
authors.forename: Gane Ka-Shu
authors.initials: GK
authors.lastname: Wong
authors.affiliation: John Innes Centre, Norwich NR4 7UH, United Kingdom;
authors.forename: Giles E D
authors.initials: GE
authors.lastname: Oldroyd
authors.affiliation: Department of Agronomy, University of Wisconsin, Madison, WI 53706; Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Ané
mesh_terms: D000220:Adaptation, Biological / Q000235:genetics* / Q000502:physiology; D001483:Base Sequence; D005075:Biological Evolution; D000460:Chlorophyta / Q000235:genetics* / Q000502:physiology; D058119:Closterium / Q000235:genetics / Q000254:growth & development; D017931:DNA Primers / Q000235:genetics; D019669:Embryophyta / Q000235:genetics* / Q000502:physiology; D005658:Fungi / Q000502:physiology; D035926:Hepatophyta / Q000235:genetics / Q000254:growth & development; D016013:Likelihood Functions; D046913:Medicago truncatula / Q000382:microbiology; D008957:Models, Genetic; D008969:Molecular Sequence Data; D038821:Mycorrhizae / Q000502:physiology; D010802:Phylogeny; D010940:Plant Proteins / Q000235:genetics; D018517:Plant Roots / Q000382:microbiology; D018749:RNA, Plant / Q000235:genetics; D020133:Reverse Transcriptase Polymerase Chain Reaction; D017423:Sequence Analysis, RNA; D058131:Spirogyra / Q000235:genetics / Q000254:growth & development; D013559:Symbiosis / Q000235:genetics* / Q000502:physiology
chemical_list: D017931:DNA Primers; D010940:Plant Proteins; D018749:RNA, Plant
keywords: algae; phylogeny; plant evolution; plant–microbe interactions; symbiosis