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      Complete Genomes of Symbiotic Cyanobacteria Clarify the Evolution of Vanadium-Nitrogenase

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          Abstract

          Plant endosymbiosis with nitrogen-fixing cyanobacteria has independently evolved in diverse plant lineages, offering a unique window to study the evolution and genetics of plant–microbe interaction. However, very few complete genomes exist for plant cyanobionts, and therefore little is known about their genomic and functional diversity. Here, we present four complete genomes of cyanobacteria isolated from bryophytes. Nanopore long-read sequencing allowed us to obtain circular contigs for all the main chromosomes and most of the plasmids. We found that despite having a low 16S rRNA sequence divergence, the four isolates exhibit considerable genome reorganizations and variation in gene content. Furthermore, three of the four isolates possess genes encoding vanadium (V)-nitrogenase ( vnf), which is uncommon among diazotrophs and has not been previously reported in plant cyanobionts. In two cases, the vnf genes were found on plasmids, implying possible plasmid-mediated horizontal gene transfers. Comparative genomic analysis of vnf-containing cyanobacteria further identified a conserved gene cluster. Many genes in this cluster have not been functionally characterized and would be promising candidates for future studies to elucidate V-nitrogenase function and regulation.

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          Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps.

          Large-scale (segmental or whole) genome duplication has been recurring in angiosperm evolution. Subsequent gene loss and rearrangements further affect gene copy numbers and fractionate ancestral gene linkages across multiple chromosomes. The fragmented "multiple-to-multiple" correspondences resulting from this distinguishing feature of angiosperm evolution complicates comparative genomic studies. Using a robust computational framework that combines information from multiple orthologous and duplicated regions to construct local syntenic networks, we show that a shared ancient hexaploidy event (or perhaps two roughly concurrent genome fusions) can be inferred based on the sequences from several divergent plant genomes. This "paleo-hexaploidy" clearly preceded the rosid-asterid split, but it remains equivocal whether it also affected monocots. The model resulting from our multi-alignments lays the foundation for approximating the number and arrangement of genes in the last universal common ancestor of angiosperms. Comparative analysis of inferred homologous genes derived from this model shows patterns of preferential gene retention or loss after polyploidy and reveals large variability of nucleotide substitution rates among plant nuclear genomes.
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            Fern genomes elucidate land plant evolution and cyanobacterial symbioses

            Ferns are the closest sister group to all seed plants, yet little is known about their genomes other than that they are generally colossal. Here, we report on the genomes of Azolla filiculoides and Salvinia cucullata (Salviniales) and present evidence for episodic whole-genome duplication in ferns—one at the base of ‘core leptosporangiates’ and one specific to Azolla. One fern-specific gene that we identified, recently shown to confer high insect resistance, seems to have been derived from bacteria through horizontal gene transfer. Azolla coexists in a unique symbiosis with N2-fixing cyanobacteria, and we demonstrate a clear pattern of cospeciation between the two partners. Furthermore, the Azolla genome lacks genes that are common to arbuscular mycorrhizal and root nodule symbioses, and we identify several putative transporter genes specific to Azolla–cyanobacterial symbiosis. These genomic resources will help in exploring the biotechnological potential of Azolla and address fundamental questions in the evolution of plant life.
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              Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes

              Access to fixed or available forms of nitrogen limits the productivity of crop plants and thus food production. Nitrogenous fertilizer production currently represents a significant expense for the efficient growth of various crops in the developed world. There are significant potential gains to be had from reducing dependence on nitrogenous fertilizers in agriculture in the developed world and in developing countries, and there is significant interest in research on biological nitrogen fixation and prospects for increasing its importance in an agricultural setting. Biological nitrogen fixation is the conversion of atmospheric N2 to NH3, a form that can be used by plants. However, the process is restricted to bacteria and archaea and does not occur in eukaryotes. Symbiotic nitrogen fixation is part of a mutualistic relationship in which plants provide a niche and fixed carbon to bacteria in exchange for fixed nitrogen. This process is restricted mainly to legumes in agricultural systems, and there is considerable interest in exploring whether similar symbioses can be developed in nonlegumes, which produce the bulk of human food. We are at a juncture at which the fundamental understanding of biological nitrogen fixation has matured to a level that we can think about engineering symbiotic relationships using synthetic biology approaches. This minireview highlights the fundamental advances in our understanding of biological nitrogen fixation in the context of a blueprint for expanding symbiotic nitrogen fixation to a greater diversity of crop plants through synthetic biology.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                July 2019
                27 June 2019
                27 June 2019
                : 11
                : 7
                : 1959-1964
                Affiliations
                [1 ]Boyce Thompson Institute, Ithaca, New York
                [2 ]Plant Biology Section, Cornell University, Ithaca, New York
                [3 ]Smithsonian Tropical Research Institute, Panama City, Panama
                [4 ]Department of Microbiology and Molecular Genetics, University of California, Davis, California
                [5 ]Department of Biology, Laval University, Quebec City, Quebec, Canada
                Author notes

                These authors Nelson and Hauser contributed equally to this work.

                Corresponding author: E-mail: fl329@ 123456cornell.edu .
                Author information
                http://orcid.org/0000-0002-0076-0152
                Article
                evz137
                10.1093/gbe/evz137
                6645180
                31243438
                0215382b-e1ac-4475-ac7f-cf7e689c6afc
                © The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 June 2019
                Page count
                Pages: 6
                Funding
                Funded by: Simons Foundation 10.13039/100000893
                Award ID: 429440
                Funded by: Smithsonian Tropical Research Institute 10.13039/100009201
                Funded by: National Science Foundation Dimensions of Biodiversity
                Award ID: 1831428
                Categories
                Genome Report

                Genetics
                nostoc,blasia,hornworts,liverworts,phylogenomics,nanopore
                Genetics
                nostoc, blasia, hornworts, liverworts, phylogenomics, nanopore

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