title: Protein networks identify novel symbiogenetic genes resulting from plastid endosymbiosis.
abstract: The integration of foreign genetic information is central to the evolution of eukaryotes, as has been demonstrated for the origin of the Calvin cycle and of the heme and carotenoid biosynthesis pathways in algae and plants. For photosynthetic lineages, this coordination involved three genomes of divergent phylogenetic origins (the nucleus, plastid, and mitochondrion). Major hurdles overcome by the ancestor of these lineages were harnessing the oxygen-evolving organelle, optimizing the use of light, and stabilizing the partnership between the plastid endosymbiont and host through retargeting of proteins to the nascent organelle. Here we used protein similarity networks that can disentangle reticulate gene histories to explore how these significant challenges were met. We discovered a previously hidden component of algal and plant nuclear genomes that originated from the plastid endosymbiont: symbiogenetic genes (S genes). These composite proteins, exclusive to photosynthetic eukaryotes, encode a cyanobacterium-derived domain fused to one of cyanobacterial or another prokaryotic origin and have emerged multiple, independent times during evolution. Transcriptome data demonstrate the existence and expression of S genes across a wide swath of algae and plants, and functional data indicate their involvement in tolerance to oxidative stress, phototropism, and adaptation to nitrogen limitation. Our research demonstrates the "recycling" of genetic information by photosynthetic eukaryotes to generate novel composite genes, many of which function in plastid maintenance.
authors.affiliation: Unité Mixte de Recherche 7138 Evolution Paris Seine, Institut de Biologie Paris Seine, Université Pierre et Marie Curie, Centre National de la Recherche Scientifique, Sorbonne Universités, 75005 Paris, France;
authors.forename: Raphaël
authors.initials: R
authors.lastname: Méheust
authors.affiliation: Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08901.
authors.forename: Ehud
authors.initials: E
authors.lastname: Zelzion
authors.affiliation: Department of Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ 08901.
authors.forename: Debashish
authors.initials: D
authors.lastname: Bhattacharya
authors.affiliation: Unité Mixte de Recherche 7138 Evolution Paris Seine, Institut de Biologie Paris Seine, Université Pierre et Marie Curie, Centre National de la Recherche Scientifique, Sorbonne Universités, 75005 Paris, France;
authors.forename: Philippe
authors.initials: P
authors.lastname: Lopez
authors.affiliation: Unité Mixte de Recherche 7138 Evolution Paris Seine, Institut de Biologie Paris Seine, Université Pierre et Marie Curie, Centre National de la Recherche Scientifique, Sorbonne Universités, 75005 Paris, France; epbapteste@gmail.com.
authors.forename: Eric
authors.initials: E
authors.lastname: Bapteste
mesh_terms: D056890:Eukaryota / Q000235:genetics; D019143:Evolution, Molecular; D050939:Gene Fusion; D018745:Genome, Plant; D008957:Models, Genetic; D005810:Multigene Family; D010084:Oxidation-Reduction; D010788:Photosynthesis / Q000235:genetics; D010802:Phylogeny; D010944:Plants / Q000235:genetics; D018087:Plastids / Q000235:genetics*; D011506:Proteins / Q000235:genetics*; D017386:Sequence Homology, Amino Acid; D013559:Symbiosis / Q000235:genetics*
chemical_list: D011506:Proteins
keywords: endosymbiosis; eukaryote evolution; gene fusion; novel gene origin; photosynthesis