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      Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota

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          Abstract

          Plants are associated with a complex microbiota that contributes to nutrient acquisition, plant growth, and plant defense. Nitrogen-fixing microbial associations are efficient and well characterized in legumes but are limited in cereals, including maize. We studied an indigenous landrace of maize grown in nitrogen-depleted soils in the Sierra Mixe region of Oaxaca, Mexico. This landrace is characterized by the extensive development of aerial roots that secrete a carbohydrate-rich mucilage. Analysis of the mucilage microbiota indicated that it was enriched in taxa for which many known species are diazotrophic, was enriched for homologs of genes encoding nitrogenase subunits, and harbored active nitrogenase activity as assessed by acetylene reduction and 15N 2 incorporation assays. Field experiments in Sierra Mixe using 15N natural abundance or 15N-enrichment assessments over 5 years indicated that atmospheric nitrogen fixation contributed 29%–82% of the nitrogen nutrition of Sierra Mixe maize.

          Author summary

          Nitrogen is an essential nutrient for plants, and for many nonlegume crops, the requirement for nitrogen is primarily met by the use of inorganic fertilizers. These fertilizers are produced from fossil fuel by energy-intensive processes that are estimated to use 1% to 2% of the total global energy supply and produce an equivalent share of greenhouse gases. Because maize ( Zea mays L.) is a significant recipient of nitrogen fertilization, a research goal for decades has been to identify or engineer mechanisms for biological fixation of atmospheric nitrogen in association with this crop. We hypothesized that isolated indigenous landraces of maize grown using traditional practices with little or no fertilizer might have evolved strategies to improve plant performance under low-nitrogen nutrient conditions. Here, we show that for one such maize landrace grown in nitrogen-depleted fields near Oaxaca, Mexico, 29%–82% of the plant nitrogen is derived from atmospheric nitrogen. High levels of nitrogen fixation are supported, at least in part, by the abundant production of a sugar-rich mucilage associated with aerial roots that provides a home to a complex nitrogen-fixing microbiome.

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          Most cited references39

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          The TIGRFAMs database of protein families.

          TIGRFAMs is a collection of manually curated protein families consisting of hidden Markov models (HMMs), multiple sequence alignments, commentary, Gene Ontology (GO) assignments, literature references and pointers to related TIGRFAMs, Pfam and InterPro models. These models are designed to support both automated and manually curated annotation of genomes. TIGRFAMs contains models of full-length proteins and shorter regions at the levels of superfamilies, subfamilies and equivalogs, where equivalogs are sets of homologous proteins conserved with respect to function since their last common ancestor. The scope of each model is set by raising or lowering cutoff scores and choosing members of the seed alignment to group proteins sharing specific function (equivalog) or more general properties. The overall goal is to provide information with maximum utility for the annotation process. TIGRFAMs is thus complementary to Pfam, whose models typically achieve broad coverage across distant homologs but end at the boundaries of conserved structural domains. The database currently contains over 1600 protein families. TIGRFAMs is available for searching or downloading at www.tigr.org/TIGRFAMs.
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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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              Algal ancestor of land plants was preadapted for symbiosis.

              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.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Methodology
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: InvestigationRole: Methodology
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                7 August 2018
                August 2018
                7 August 2018
                : 16
                : 8
                : e2006352
                Affiliations
                [1 ] Department of Plant Sciences, University of California, Davis, California, United States of America
                [2 ] Department of Agronomy, University of Wisconsin, Madison, Wisconsin, United States of America
                [3 ] Department of Bacteriology, University of Wisconsin, Madison, Wisconsin, United States of America
                [4 ] Genome Center, University of California, Davis, California, United States of America
                [5 ] Department of Population Health and Reproduction, University of California, Davis, California, United States of America
                [6 ] Instituto Tecnológico del Valle de Oaxaca, Oaxaca, Mexico
                [7 ] Mars, Incorporated, McLean, Virginia, United States of America
                University of Tübingen, Germany
                Author notes

                Howard-Yana Shapiro is affiliated with Mars, Incorporated, one of the research sponsors. Author Cristobal Heitmann was unable to confirm authorship or contributions himself, and this was carried out collectively by the other co-authors.

                ‡ These authors share first authorship on this work.

                Author information
                http://orcid.org/0000-0002-3684-4307
                Article
                pbio.2006352
                10.1371/journal.pbio.2006352
                6080747
                30086128
                3535f6f0-873b-4ec4-b368-e63d53a8803a
                © 2018 Van Deynze et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 April 2018
                : 3 July 2018
                Page count
                Figures: 5, Tables: 2, Pages: 21
                Funding
                Mars, Incorporated http://www.mars.com/global. The research was funded by an unrestricted gift and a grant to ABB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The research was funded by grants to ABB from BioN2, Incorporated. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Preliminary research was supported by a Dissertation Research Grant from UC Mexus to KS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Maize
                Research and Analysis Methods
                Model Organisms
                Maize
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Grasses
                Maize
                Research and Analysis Methods
                Experimental Organism Systems
                Plant and Algal Models
                Maize
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Nitrogen Fixation
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Diazo Compounds
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Diazo Compounds
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Rhizosphere
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Environment Interactions
                Rhizosphere
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Environment Interactions
                Rhizosphere
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Cereal Crops
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Research and Analysis Methods
                Computational Techniques
                Split-Decomposition Method
                Multiple Alignment Calculation
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Custom metadata
                All numerical data are now posted at DOI: 10.6084/m9.figshare.6534545 and all DNA/RNA sequence data at https://figshare.com/s/04997ae7f7d18b53174a.

                Life sciences
                Life sciences

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