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Proc Natl Acad Sci U S A. 2015 Oct 27;112(43):13390-5. doi: 10.1073/pnas.1515426112. Epub 2015 Oct 5.

Algal ancestor of land plants was preadapted for symbiosis.

Author information

1
Department of Agronomy, University of Wisconsin, Madison, WI 53706; John Innes Centre, Norwich NR4 7UH, United Kingdom; pierre-marc.delaux@lrsv.ups-tlse.fr.
2
John Innes Centre, Norwich NR4 7UH, United Kingdom;
3
Department of Agronomy, University of Wisconsin, Madison, WI 53706; Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
4
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;
5
Biotechnology Center, University of Wisconsin, Madison, WI 53706; Department of Biochemistry, University of Wisconsin, Madison, WI 53706;
6
Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, 2-8-1 Mejirodai, Bunkyo-ku, Tokyo, 112-8681 Japan;
7
Advanced Science Research Center, Kanazawa University, 13-1 Takara-machi, Kanazawa, 920-0934, Japan;
8
Botany Department, Cologne Biocenter, University of Cologne, 50674 Cologne, Germany;
9
Real Jardín Botánico, 28014 Madrid, Spain;
10
Department of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
11
Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695;
12
New York Botanical Garden, Bronx, NY 10458;
13
Beijing Genomics Institute-Shenzhen, Shenzhen 518083, China;
14
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.

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.

KEYWORDS:

algae; phylogeny; plant evolution; plant–microbe interactions; symbiosis

PMID:
26438870
PMCID:
PMC4629359
DOI:
10.1073/pnas.1515426112
[Indexed for MEDLINE]
Free PMC Article

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