Harnessing atmospheric nitrogen for cereal crop production

Borlaug, 1972, Nobel lecture, December 11, 1970 Searchinger, 2018, Creating a sustainable food future: a menu of solutions to feed nearly 10 billion people by 2050 Griffiths, 2014, Food for thought: infographic reveals what the world consumes - with China being the biggest meat eaters and Germany drinking the most alcohol Erisman, 2008, Reduced nitrogen in ecology and the environment: special issue of the ESF-FWF Conference in partnership with LFUI, October 2006, Environ Pollut, 154, 357, 10.1016/j.envpol.2008.05.001 Glendining, 2009, Is it possible to increase the sustainability of arable and ruminant agriculture by reducing inputs?, Agric Syst, 99, 117, 10.1016/j.agsy.2008.11.001 Lassaletta, 2014, 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland, Environ Res Lett, 9, 10.1088/1748-9326/9/10/105011 Zhang, 2015, Managing nitrogen for sustainable development, Nature, 528, 51, 10.1038/nature15743 Reed, 2011, Functional ecology of free-living nitrogen fixation: a contemporary perspective, Ann Rev Ecol Evol Syst, 42, 489, 10.1146/annurev-ecolsys-102710-145034 Mus, 2016, Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes, Appl Environ Microbiol, 82, 3698, 10.1128/AEM.01055-16 Santi, 2013, Biological nitrogen fixation in non-legume plants, Ann Bot, 111, 743, 10.1093/aob/mct048 Smercina, 2019, To fix or not to fix: controls on free-living nitrogen fixation in the rhizosphere, Appl Environ Microbiol, 85 Van Deynze, 2018, Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota, PLoS Biol, 16, 10.1371/journal.pbio.2006352 Dixon, 2004, Genetic regulation of biological nitrogen fixation, Nat Rev Microbiol, 2, 621, 10.1038/nrmicro954 Dixon, 1972, Genetic transfer of nitrogen fixation from Klebsiella pneumoniae to Escherichia coli, Nature, 237, 102, 10.1038/237102a0 Clua, 2018, Compatibility between legumes and rhizobia for the establishment of a successful nitrogen-fixing symbiosis, Genes (Basel), 9, 10.3390/genes9030125 Folberth, 2013, Modeling maize yield responses to improvement in nutrient, water and cultivar inputs in sub-Saharan Africa, Agric Syst, 119, 22, 10.1016/j.agsy.2013.04.002 Rogers, 2014, Synthetic biology approaches to engineering the nitrogen symbiosis in cereals, J Exp Bot, 65, 1939, 10.1093/jxb/eru098 Pankievicz, 2015, Robust biological nitrogen fixation in a model grass-bacterial association, Plant J, 81, 907, 10.1111/tpj.12777 Garcia de Salamone, 1996, Biological nitrogen fixation in Azospirillum strain-maize genotype associations as evaluated by the 15N isotope dilution technique, Biol Fertil Soils, 23, 249, 10.1007/BF00335952 Montañez, 2009, Biological nitrogen fixation in maize (Zea mays L.) by 15N isotope-dilution and identification of associated culturable diazotrophs, Biol Fertil Soils, 45, 253, 10.1007/s00374-008-0322-2 Fox, 2016, Major cereal crops benefit from biological nitrogen fixation when inoculated with the nitrogen-fixing bacterium Pseudomonas protegens Pf-5 X940, Environ Microbiol, 18, 3522, 10.1111/1462-2920.13376 Lima, 1987, Quantification of biological nitrogen fixation associated with sugar cane using a 15N aided nitrogen balance, Soil Biol Biochem, 19, 165, 10.1016/0038-0717(87)90077-0 Boddey, 2001, Use of the 15N natural abundance technique for the quantification of the contribution of N2 fixation to sugar cane and other grasses, Aust J Plant Physiol, 28, 889 Iniguez, 2004, Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342, Mol Plant Microbe Interact, 17, 1078, 10.1094/MPMI.2004.17.10.1078 Ohta, 1991, Metabolic engineering of Klebsiella oxytoca M5A1 for ethanol production from xylose and glucose, Appl Environ Microbiol, 57, 2810, 10.1128/AEM.57.10.2810-2815.1991 Dixon, 2004, Development of nif genetics and regulation in Klebsiella pneumoniae Ausubel, 2018, Tracing my roots: how I became a plant biologist, Annu Rev Genet, 52, 1, 10.1146/annurev-genet-120417-031722 Wang, 2013, A minimal nitrogen fixation gene cluster from Paenibacillus sp. WLY78 enables expression of active nitrogenase in Escherichia coli, PLoS Genet, 9, 10.1371/annotation/1e9bcb70-265a-4383-abf4-3466d144d56e Geddes, 2015, Use of plant colonizing bacteria as chassis for transfer of N(2)-fixation to cereals, Curr Opin Biotechnol, 32, 216, 10.1016/j.copbio.2015.01.004 Smanski, 2014, Functional optimization of gene clusters by combinatorial design and assembly, Nat Biotechnol, 32, 1241, 10.1038/nbt.3063 Temme, 2012, Refactoring the nitrogen fixation gene cluster from Klebsiella oxytoca, Proc Natl Acad Sci U S A, 109, 7085, 10.1073/pnas.1120788109 Boehm, 2019, Recent advances and current challenges in synthetic biology of the plastid genetic system and metabolism, Plant Physiol, 179, 794, 10.1104/pp.18.00767 Piatek, 2018, Advanced editing of the nuclear and plastid genomes in plants, Plant Sci, 273, 42, 10.1016/j.plantsci.2018.02.025 Liu, 2019, Combined assembly and targeted integration of multigene for nitrogenase biosynthetic pathway in Saccharomyces cerevisiae, ACS Synth Biol, 8, 1766, 10.1021/acssynbio.9b00060 Curatti, 2014, Challenges to develop nitrogen-fixing cereals by direct nif-gene transfer, Plant Sci, 225, 130, 10.1016/j.plantsci.2014.06.003 Buren, 2018, State of the art in eukaryotic nitrogenase engineering, FEMS Microbiol Lett, 365, 10.1093/femsle/fnx274 Meyers, 2010, Nuclear and plastid genetic engineering of plants: comparison of opportunities and challenges, Biotechnol Adv, 28, 747, 10.1016/j.biotechadv.2010.05.022 Buren, 2017, Formation of nitrogenase NifDK tetramers in the mitochondria of Saccharomyces cerevisiae, ACS Synth Biol, 6, 1043, 10.1021/acssynbio.6b00371 Lopez-Torrejon, 2016, Expression of a functional oxygen-labile nitrogenase component in the mitochondrial matrix of aerobically grown yeast, Nat Commun, 7, 10.1038/ncomms11426 Buren, 2017, Purification and in vitro activity of mitochondria targeted nitrogenase cofactor maturase NifB, Front Plant Sci, 8, 10.3389/fpls.2017.01567 Allen, 2017, Expression of 16 nitrogenase proteins within the plant mitochondrial matrix, Front Plant Sci, 8, 287, 10.3389/fpls.2017.00287 Yang, 2018, Polyprotein strategy for stoichiometric assembly of nitrogen fixation components for synthetic biology, Proc Natl Acad Sci U S A, 115, E8509, 10.1073/pnas.1804992115 Ivleva, 2016, Expression of active subunit of nitrogenase via integration into plant organelle genome, PLoS One, 11, 10.1371/journal.pone.0160951 Yang, 2017, Modular electron-transport chains from eukaryotic organelles function to support nitrogenase activity, Proc Natl Acad Sci U S A, 114, E2460, 10.1073/pnas.1620058114 Long, 2018, Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts, Nat Commun, 9, 3570, 10.1038/s41467-018-06044-0 Henriques, 2018, Circadian regulation of plant growth, Annu Plant Rev, 1 Desbrosses, 2011, Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways, Cell Host Microbe, 10, 348, 10.1016/j.chom.2011.09.005 Madsen, 2010, The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus, Nat Commun, 1, 10, 10.1038/ncomms1009 Held, 2014, Lotus japonicus cytokinin receptors work partially redundantly to mediate nodule formation, Plant Cell, 26, 678, 10.1105/tpc.113.119362 Maillet, 2011, Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza, Nature, 469, 58, 10.1038/nature09622 Oldroyd, 2013, Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants, Nat Rev Microbiol, 11, 252, 10.1038/nrmicro2990 Rocha, 2007, Signal transduction-related responses to phytohormones and environmental challenges in sugarcane, BMC Genomics, 8, 71, 10.1186/1471-2164-8-71 Alberton, 2013, Comparative proteomics analysis of the rice roots colonized by Herbaspirillum seropedicae strain SmR1 reveals induction of the methionine recycling in the plant host, J Proteome Res, 12, 4757, 10.1021/pr400425f Brusamarello-Santos, 2017, Metabolic profiling of two maize (Zea mays L.) inbred lines inoculated with the nitrogen fixing plant-interacting bacteria Herbaspirillum seropedicae and Azospirillum brasilense, PLoS One, 12, 10.1371/journal.pone.0174576 Kost, 2014, Oxalotrophy, a widespread trait of plant-associated Burkholderia species, is involved in successful root colonization of lupin and maize by Burkholderia phytofirmans, Front Microbiol, 4, 421, 10.3389/fmicb.2013.00421 Johnston-Monje, 2011, Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology, PLoS One, 6, 10.1371/journal.pone.0020396 Ikeda, 2013, Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes, Microb Ecol, 65, 154, 10.1007/s00248-012-0104-0 Hungria, 2010, Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil, Plant Soil, 331, 413, 10.1007/s11104-009-0262-0 Kifle, 2016, Effects of selected diazotrophs on maize growth, Front Plant Sci, 7, 1429, 10.3389/fpls.2016.01429 Oliveira, 2017, Maize inoculation with Azospirillum brasilense Ab-V5 cells enriched with exopolysaccharides and polyhydroxybutyrate results in high productivity under low N fertilizer input, Front Microbiol, 8, 1873, 10.3389/fmicb.2017.01873 Compant, 2019, A review on the plant microbiome: ecology, functions, and emerging trends in microbial application, J Adv Res, 19, 29, 10.1016/j.jare.2019.03.004 Yang, 2014, Reconstruction and minimal gene requirements for the alternative iron-only nitrogenase in Escherichia coli, Proc Natl Acad Sci U S A, 111, E3718, 10.1073/pnas.1411185111 Han, 2015, Interspecies transfer and regulation of Pseudomonas stutzeri A1501 nitrogen fixation island in Escherichia coli, J Microbiol Biotechnol, 25, 1339, 10.4014/jmb.1502.02027 Yang, 2018, Global investigation of an engineered nitrogen-fixing Escherichia coli strain reveals regulatory coupling between host and heterologous nitrogen-fixation genes, Sci Rep, 8 Lehtinen, 1981, Transfer of nitrogen fixation genes into Pseudomonas putida isolated from Finnish tundra soil, Antonie Van Leeuwenhoek, 47, 405, 10.1007/BF00426002 Chen, 1983, Transfer and expression of Klebsiella nif genes in Alcaligenes faecalis, a nitrogen-fixing bacterium associated with rice root, Plasmid, 10, 290, 10.1016/0147-619X(83)90043-4 Setten, 2013, Engineering Pseudomonas protegens Pf-5 for nitrogen fixation and its application to improve plant growth under nitrogen-deficient conditions, PLoS One, 8, 10.1371/annotation/279fe0d7-d9b1-4d05-a45a-5ff00b4606b7 Brophy, 2018, Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria, Nat Microbiol, 3, 1043, 10.1038/s41564-018-0216-5 Li, 2016, Using synthetic biology to increase nitrogenase activity, Microb Cell Fact, 15, 43, 10.1186/s12934-016-0442-6 Okon, 1983, N(2) fixation by Azospirillum brasilense and its incorporation into host Setaria italica, Appl Environ Microbiol, 46, 694, 10.1128/AEM.46.3.694-697.1983 Ortiz-Marquez, 2014, Metabolic engineering of ammonium release for nitrogen-fixing multispecies microbial cell-factories, Metab Eng, 23, 154, 10.1016/j.ymben.2014.03.002 Barney, 2015, Gene deletions resulting in increased nitrogen release by Azotobacter vinelandii: application of a novel nitrogen biosensor, Appl Environ Microbiol, 81, 4316, 10.1128/AEM.00554-15 Ambrosio, 2017, Metabolic engineering of a diazotrophic bacterium improves ammonium release and biofertilization of plants and microalgae, Metab Eng, 40, 59, 10.1016/j.ymben.2017.01.002 Bageshwar, 2017, An environment friendly engineered Azotobacter can replace substantial amount of urea fertilizer and yet sustain same wheat yield, Appl Environ Microbiol, 83, 10.1128/AEM.00590-17 Kanter, 2018, Nitrogen pollution: a key building block for addressing climate change, Clim Change, 147, 11, 10.1007/s10584-017-2126-6 Robertson, 2009, Nitrogen in agriculture: balancing the cost of an essential resource, Annu Rev Environ Resour, 34, 97, 10.1146/annurev.environ.032108.105046 Kanter, 2015, Reducing nitrogen pollution while decreasing farmers’ costs and increasing fertilizer industry profits, J Environ Qual, 44, 325, 10.2134/jeq2014.04.0173 Oren, 2014, Transfer of noncoding DNA drives regulatory rewiring in bacteria, Proc Natl Acad Sci U S A, 111, 16112, 10.1073/pnas.1413272111