Scripting a new dialogue between diazotrophs and crops

The availability of nutrients such as nitrogen (N) affects crop productivity. Unfortunately, the intensive use synthetic N fertilizers has detrimental economic and environmental consequences.Engineered associative diazotrophs hold immense potential to help many crops acquire from air via biological fixation.The mechanistic understanding plant–diazotroph interactions forms basis engineering these associations increase transfer fixed plants.Biorthogonal signaling is a promising approach specific, efficient, ecofriendly interactions.The composition root exudates, physical proximity plants, their nontoxic nature, efficiency in fixing N, amenability genetic manipulations are essential for between sustainable agriculture. Diazotrophs bacteria archaea that can reduce atmospheric dinitrogen (N2) into ammonium. Plant–diazotroph have been explored over century source improve agricultural productivity sustainability. This scientific quest generated much information about molecular mechanisms underlying function, assembly, regulation nitrogenase, ammonium assimilation, interactions. review presents various approaches manipulating fixation activity, release by diazotrophs, We discuss research avenues this area, propose future routes, emphasizing at metabolic level biorthogonal signaling, conclude highlighting importance biocontrol measures public acceptance. an plant nutrient. Despite N2 comprising 78% Earth's atmosphere, it not directly available often limiting nutrient systems [1.Hawkesford M.J. et al.Functions macronutrients.in: Rengel Z. Marschner’s Mineral Nutrition Plants. Elsevier, 2023: 201-281Crossref Scopus (10) Google Scholar, 2.Robertson G.P. Vitousek P.M. Nitrogen agriculture: balancing cost resource.Annu. Rev. Environ. Resour. 2009; 34: 97-125Crossref (775) 3.Pankievicz V.C.S. al.Are we there yet? long walk towards development efficient symbiotic nitrogen-fixing non-leguminous crops.BMC Biol. 2019; 17: 99Crossref PubMed (89) Scholar]. Low physiological processes, resulting stunted growth, decline health, overall reduction yields. (NH4+), chemical reaction requires lot energy break triple bounds molecule. In industrial fixation, also known Haber–Bosch process, synthesized primarily using natural gas. Since Green Revolution, used widely agriculture overcome limitation. Synthetic highly costly growers, especially developing countries, relying on fossil fuels produce them unsustainable. Their effects, including eutrophication rivers, degradation coastal zones, greenhouse gas emissions [2.Robertson For reasons, cheap, alternatives desired Scholar,4.Fernandes M.S. Rossiello R.O.P. physiology nutrition.CRC Crit. Plant Sci. 1995; 14: 111-148Crossref (69) (henceforth diazotrophs) nitrogenase enzyme complex ATP perform [5.Bueno Batista M. Dixon R. Manipulating diazotrophic agronomic benefit.Biochem. Soc. Trans. 47: 603-614Crossref (57) However, inhibited oxygen large amounts form ATP. Diverse live soil; some associate with plants obtain photosynthesis-derived carbon. cases, even provide low-oxygen niche protects [6.Van Deynze A. al.Nitrogen landrace maize supported mucilage-associated microbiota.PLoS 2018; 16e2006352Crossref (191) return, significant host plants. Such include nodule symbioses, particularly rhizobium–legume associations. These symbioses lead new organs, nodules proper which cells infected intracellularly alpha- or beta-proteobacteria called rhizobia Frankia actinobacteria. Some rhizobia–legume extremely hosts require little no inputs add soil subsequent through rotations. occur only monophyletic ‘N-fixing’ clade, Fabale, Fagale, Cucurbitale, Rosale (FaFaCuRo) families [7.Cope K.R. al.Perception lipo-chitooligosaccharides bioenergy Populus.Plant Signal. Behav. 2021; 161903758Crossref (5) Multiple being benefits crops, cereals, achieve maximal One exciting aims expressing Progress was made different components organelles, chloroplasts mitochondria regarded most suitable sites engineering, due ability necessary reducing power fixation. challenges remain, undesired instability proteins [8.López-Torrejón G. al.Expression functional oxygen-labile component mitochondrial matrix aerobically grown yeast.Nat. Commun. 2016; 7: 11426Crossref (84) Scholar,9.Burén S. Rubio L.M. State art eukaryotic engineering.FEMS Microbiol. Lett. 365fnx274Crossref (81) Scholar] (Figure 1). Another engineer outside FaFaCuRo clade. progress past decades genes controlling early recognition, organogenesis, evolution symbiosis, mechanisms, those governing intracellular infection, remain poorly understood [3.Pankievicz Scholar,10.de Bruijn F.J. cereals: perspective prospective.in: Biological Fixation. John Wiley & Sons, 2015: 1087-1101Crossref A third identifying better nonleguminous diversity. Maize landraces develop aerial roots abundant mucilage half atmosphere hosting mucilage. trait be transferred conventional accessions classical breeding without transgenic Scholar,11.Bennett A.B. al.A model cereal crops.Trends 2020; 25: 226-235Abstract Full Text PDF (30) Scholar,12.Pankievicz production controlled border cell functions.Front. 2022; 13977056Crossref (1) fourth approach, nodule-independent cereals involves secrete specific metabolite, would selectively enhance competitiveness selected rhizosphere, instance, acting [13.Geddes B.A. al.Engineering transkingdom signalling control gene expression rhizosphere bacteria.Nat. 10: 3430Crossref (70) zone chemical, biological, influence growth activity [14.McNear Jr., D.H. – roots, everything between.Nat. Educ. Knowl. 2013; 4: 1Google make free-living do altruistically share they need manipulated so access [15.Mus F. al.Symbiotic its extension nonlegumes.Appl. 82: 3698-3710Crossref (339) 16.Oger P. al.Genetically engineered producing opines alter environment.Nat. Biotechnol. 1997; 15: 369-372Crossref 17.Rosenblueth cereals.Front. 9: 1794Crossref (145) Engineering ammonia excretion achieved disrupting tight negative regulatory circuits required biosynthesis general focus approach. interface microbes represents region bidirectional flow metabolites. soil, exudates select providing carbon sources, mostly carbohydrates, dicarboxylic acids, amino acids. exudate varies species depends plant's developmental status. While acids generally observed high levels other metabolites auxins, coumaric salicylic acid vary across genotypes environments [18.Dundas C.M. Dinneny J.R. Genetic circuit design rhizobacteria.BioDes. Res. 20229858049Crossref 19.Khorassani al.Citramalic sugar beet solubilize phosphorus.BMC 2011; 11: 121Crossref (87) 20.Li X.-G. al.The two resistant peanut cultivars effects soil-borne pathogen.Int. J. 164-173Crossref (112) Specific metabolites, flavonoids, legumes but low abundance Plants actively take nitrate unlike modest, makes relatively environment favors microbiota influences content direct consumption development, defense reactions [21.Jacoby R.P. al.Recent advances role shaping microbiome.F1000Res. 9Crossref (42) Flavonoids sensed Bacillus subtilis Herbaspirillum seropedicae [22.Tadra-Sfeir M.Z. al.Naringenin regulates involved wall synthesis seropedicae.Appl. 77: 2180-2183Crossref (36) Scholar,23.Hirooka K. al.Regulation divergent yetL yetM transcriptional repressor, YetL, response flavonoids.J. Bacteriol. 191: 3685-3697Crossref (19) Chemoreceptors diazotroph Azospirillum brasilense, discovered allow perceive [24.O’Neal L. al.Specific compounds dedicated chemoreceptors shape brasilense chemotaxis rhizosphere.Appl. 86e01026–20PubMed mutual provides several Physical matters (root exudates), (plant respiration), uptake) environment. Proximity facilitates uptake preventing loss (see later). Associative epiphytes surfaces, endophytes tissues. elicit more robust chemotactic endophytic than [25.Bacilio-Jiménez al.Chemical characterization rice (Oryza sativa) bacteria.Plant Soil. 2003; 249: 271-277Crossref (0) Azoarcus sp. strain BH72, H. express nif during association [26.Broek A.V. al.Spatial-temporal colonization patterns wheat surface bacterial nifH association.Mol. Plant-Microbe Interact. 1993; 6: 592-600Crossref 27.Steenhoudt O. Vanderleyden Azospirillum, bacterium closely associated grasses: genetic, biochemical ecological aspects.FEMS 2000; 24: 487-506Crossref 28.Roncato-Maccari L.D.B. al.Endophytic expresses gramineous plants.FEMS Ecol. 45: 39-47Crossref (118) BH72 found stele, suggesting colonize systemically [29.Hurek T. Reinhold-Hurek B. grass endophytes.J. 106: 169-178Crossref (157) comparison wild-type mutant nifK, lacked enzyme, revealed associating resulted enhanced increased accumulation mutant. seems rely significantly survival, making biocontainment simple classification certain debated [30.Cocking E.C. al.Intracellular Arabidopsis Gluconacetobacter diazotrophicus.In Vitro Cell. Dev. Plant. 2006; 42: 74-82Crossref (39) Scholar,31.White al.Rhizophagy cycle: oxidative process extraction microbes.Microorganisms. 95Crossref (79) present leaves, amount mechanism needs quantified precisely [32.Kandel S.L. al.Bacterial endophyte distribution within plants.Microorganisms. 2017; 5: 77Crossref excellent N-fixers thrive deposits absence independence limits benefit rate could challenges. addition benefits, plant-associated promote phytohormone (e.g., auxin, cytokinin, gibberellic acid), ethylene precursor 1-aminocyclopropane-1-carboxylate (ACC), phosphorus solubilization, iron acquisition, protection against pathogens [33.Dobbelaere al.Plant growth-promoting rhizosphere.CRC 22: 107-149Crossref (722) Due environment, plant-growth-promoting rhizobacteria (PGPR) diazotrophs. PGPRs act synergistically increasing biomass [34.Pankievicz al.Diazotrophic interact cereals.Mol. 491-498Crossref (23) How N-fixing associations? There factors should, ideally, collectively considered. Epi- preferred targets plant. Particular attention should given may prefer Metabolites source, chemoattractants protective compounds. betaines studied extensively contexts symbiosis [35.Phillips D.A. al.Trigonelline stachydrine released alfalfa seeds activate NodD2 protein Rhizobium meliloti.Plant Physiol. 1992; 99: 1526-1531Crossref 36.Roy al.Celebrating 20 years discoveries legume nodulation fixation.Plant 32: 15-41Crossref (288) 37.Boncompagni E. al.Occurrence choline glycine betaine metabolism family rhizobiaceae roles osmoprotection.Appl. 1999; 65: 2072-2077Crossref Strigolactones, important mycorrhizal associations, rhizobial motility likely broadly [38.López-Ráez J.A. al.Strigolactones beneficial organisms: Yin Yang.Trends 527-537Abstract (128) Scholar,39.Lanfranco cross kingdoms: fungi, arbuscular symbiosis.J. Exp. Bot. 69: 2175-2188Crossref (83) consistency mucilages above- underground enrich engineered, diversity exploited, identify ones preferentially higher Similarly, respond metabolite. Ideally, generic bacteria; able respond. rare desirable specificity plant–microbe barley synthesize rhizopine scyllo-inosamine naturally produced context range sense means Scholar,40.Jiang al.Optimization p-coumaric biosensor system versatile dynamic performance.ACS Synth. 132-144Crossref (13) Several fix degrees [41.Setten Pseudomonas protegens Pf-5 application under nitrogen-deficient conditions.PLoS One. 8e63666Crossref 42.Tatemichi Y. al.Construction recombinant Escherichia coli nitrogenase-related Azotobacter vinelandii.Biosci. Biochem. 85: 2209-2216Crossref 43.Ji C. al.Effects Enterobacter cloacae HG-1 community structure salt tolerance.Front. 1094Crossref (18) 44.Neilson A.H. biotype Erwinia herbicola resembling coli.J. Appl. 1979; 46: 483-491Crossref (6) 45.Gupta al.Natural occurrence aeruginosa, dominant cultivable colonizing Pennisetum glaucum (L.) Br.Appl. Soil 64: 252-261Crossref (60) 46.Vesga al.Transcriptome plasticity insect invasion protegens.ISME 2766-2782Crossref 47.Warriner al.Interaction growing salad spinach plants.J. Food Prot. 66: 1790-1797Crossref 48.Balsanelli al.Herbaspirillum rfbB rfbC colonization.Environ. 2010; 12: 2233-2244Crossref 49.Wachtel M.R. al.Association O157:H7 preharvest leaf lettuce upon exposure contaminated irrigation water.J. 2002; 18-25Crossref (187) 50.Shankar al.Root promoting cloacae.J. Basic 51: 523-530Crossref 51.Handelsman Brill W.J. isolates play meliloti.Appl. 1985; 49: 818-821Crossref (22) Figure 2 ranks acquisition At same time, restricted single species. Engineered consortia developed where individual taxa occupy spatial temporal niches [52.Liang microbial consortia: based principles.Front. 13829717Crossref (11) Together, work cooperatively nearby access. described previously. Candidate must amenable transformations well culturable laboratory conditions. adhere industry safety regulations gain traction broader ultimately nonpathogenic strains limited antibiotic resistance prevent biohazard concerns. large-scale bioreactors meet demands usage. Additionally, sporulating effective shelf life bioactive products [53.Toyota Bacillus-related spore formers: attractive agents promotion.Microbes 2015; 30: 205-207Crossref Therefore gamma-proteobacteria Klebsiella, Kosakonia, seem prime engineering. technologies high-throughput Proteobacteria Firmicutes Paenibacillus offers opportunities too [54.Elmore al.High-throughput nonmodel undomesticated iterative site-specific genome integration.Sci. Adv. 2023; 9eade1285Crossref hugely energy-intensive requiring 16 molecules per molecule produced. Therefore, tightly regulated [55.Alberty R.A. Thermodynamics reaction.Biophys. Chem. 2005; 114: 115-120Crossref (33) gamma-proteobacteria, key regulator (nifL) precedes activator (nifA) operon. common strategy ergo replacement nifL constitutive promoter. change removes while simultaneously N-rich [56.Ortiz-Marquez J.C.F. al.Metabolic multispecies cell-factories.Metab. Eng. 2014; 23: 154-164Crossref 57.Barney B.M. al.Gene deletions vinelandii: novel biosensor.Appl. 81: 4316-4328Crossref (41) 58.Bali al.Excretion vinelandii nitrogen.Appl. 58: 1711-1718Crossref successful overexpression nifA lethal drawbacks toxicity [59.Mus al.Genetic determinants mutants vinelandii.Appl. 88e01876-21Crossref (7) modifications nifLA operon decoupling current cellular 3). since modification symbionts [60.Martinez-Argudo I. NifL-NifA system: multidomain integrates signals.J. 2004; 186: 601-610Crossref Ammonia-secreting previously point mutation post-translational inactivation glutamine synthetase (glnA), both slow incorporation [61.Schnabel Sattely posttranslational controllable symbiont brasilense.Appl. 87e0058221Crossref (8) Scholar,62.Van Dommelen al.Phenotypic changes distinct mutations glnA gene, encoding synthetase.Appl. 5699-5701Crossref (17) Affecting extend modifying PII measuring glnB, glnK) signal transduction shuts off overlap facets central adverse consequences fitness [63.Michel