Rice Science ›› 2026, Vol. 33 ›› Issue (4): 465-484.DOI: 10.1016/j.rsci.2026.04.005
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Chu Qingnan1,2,#, Li Detian1,3,#, Feng Zhihang4, Wang Mengcen5, Sha Zhimin1(
)
Received:2025-12-16
Accepted:2026-04-03
Online:2026-07-28
Published:2026-08-06
Contact:
SHA Zhimin (zhiminsha@sjtu.edu.cn)About author:#These authors contribute equally to this work
Chu Qingnan, Li Detian, Feng Zhihang, Wang Mengcen, Sha Zhimin. Breeding Rice to Recruit Diazotrophs: Plant Genetic Levers for Rhizosphere Nitrogen Fixation[J]. Rice Science, 2026, 33(4): 465-484.
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Fig. 1. Conceptual diagram illustrating structure and microbial processes of flooded rice paddy ecosystem. The figure shows the rice plant with axial and lateral roots extending through distinct soil layers, surface water, rhizosphere soil, and bulk anaerobic soil. Cyanobacteria in the surface water and diazotrophic iron (Fe)-reducing bacteria (IRB, e.g., Anaeromyxobacter, Geobacter) in the bulk soil fix atmospheric N2, contributing to biological nitrogen fixation under contrasting redox conditions. O2 released through root aerenchyma and carbon-rich exudates (e.g., sugars, flavonoids) shape rhizosphere microhabitats and drive coupled processes of N2 fixation and Fe3+ reduction. This schematic summarizes the spatial coupling of plant traits, soil microenvironments, and microbial functions that underpin associative N2 fixation in rice-paddy ecosystems.
| Class | Genus | Presumed importance | Distribution in paddy soil | Environmental preference | Reference |
|---|---|---|---|---|---|
| Cyanobacteria | Nostoc | High | Surface water and oxic topsoil layer (~5 cm) | Phototrophic, prefers oxic conditions, light availability, low nitrogen (N) input and enhanced by organic amendment | Wang et al, |
| Alphaproteobacteria | Bradyrhizobium | High | Rhizosphere and endosphere, occasionally in iron plaque (IP) | Associative, microaerophilic to anaerobic, labile carbon (C) from exudates; tolerance of low N but suppressed by high N | Saini et al, |
| Azospirillum | High | Rhizosphere hotspots, endophytic in roots | Microaerophilic, labile C from exudates, flooding, low N input and enhanced by organic amendment | Thomas et al, | |
| Gluconacetobacter | High | Rhizosphere and endosphere, microaerophilic | Labile C from root exudates, low N input, endophytic BNF, promotes biofilm formation and plant growth | Saini et al, | |
| Betaproteobacteria | Herbaspirillum | High | Rhizosphere and endosphere, root exudation hotspots | Anaerobic, labile C from exudates, flooding, low N input, immune-tolerant hosts enhance endophytic entry | Brusamarello-Santos et al, |
| Azoarcus | Medium | Endosphere and rhizosphere | Associative/endophytic, anaerobic microaerophilic, flooding, enhanced by plant geotope with high exudation | Dos Santos et al, | |
| Paraburkholderia/Burkholderia | Medium | Rhizosphere and bulk soil, occasionally in IP | Versatile, microaerophilic, high C, flooding, low-moderate N, some strains associative with roots | Dos Santos et al, | |
| Deltaproteobacteria | Geobacter | High | IP and anoxic bulk soil, plaque-associated biofilms | Anaerobic, organic C electron donors, competes with methanogens, boosted by iron additions and low N | Ding et al, |
| Myxococcia | Anaeromyxobacter | Medium | Strict anaerobic, requires Fe3+ (e.g., ferrihydrite) | IP interfaces and anoxic rhizosphere, enriched in deeper soil layers and plaque microsites | Ding et al, |
| Firmicutes | Clostridium | Medium | Strict anaerobic, suppressed by high N or O2 | Anoxic bulk soil and deeper layers, less in rhizosphere or surface, occasionally in reduced microsites | Ahmed et al, |
Table 1. Key diazotroph genera, distribution, and environmental preferences in rice paddy soils.
| Class | Genus | Presumed importance | Distribution in paddy soil | Environmental preference | Reference |
|---|---|---|---|---|---|
| Cyanobacteria | Nostoc | High | Surface water and oxic topsoil layer (~5 cm) | Phototrophic, prefers oxic conditions, light availability, low nitrogen (N) input and enhanced by organic amendment | Wang et al, |
| Alphaproteobacteria | Bradyrhizobium | High | Rhizosphere and endosphere, occasionally in iron plaque (IP) | Associative, microaerophilic to anaerobic, labile carbon (C) from exudates; tolerance of low N but suppressed by high N | Saini et al, |
| Azospirillum | High | Rhizosphere hotspots, endophytic in roots | Microaerophilic, labile C from exudates, flooding, low N input and enhanced by organic amendment | Thomas et al, | |
| Gluconacetobacter | High | Rhizosphere and endosphere, microaerophilic | Labile C from root exudates, low N input, endophytic BNF, promotes biofilm formation and plant growth | Saini et al, | |
| Betaproteobacteria | Herbaspirillum | High | Rhizosphere and endosphere, root exudation hotspots | Anaerobic, labile C from exudates, flooding, low N input, immune-tolerant hosts enhance endophytic entry | Brusamarello-Santos et al, |
| Azoarcus | Medium | Endosphere and rhizosphere | Associative/endophytic, anaerobic microaerophilic, flooding, enhanced by plant geotope with high exudation | Dos Santos et al, | |
| Paraburkholderia/Burkholderia | Medium | Rhizosphere and bulk soil, occasionally in IP | Versatile, microaerophilic, high C, flooding, low-moderate N, some strains associative with roots | Dos Santos et al, | |
| Deltaproteobacteria | Geobacter | High | IP and anoxic bulk soil, plaque-associated biofilms | Anaerobic, organic C electron donors, competes with methanogens, boosted by iron additions and low N | Ding et al, |
| Myxococcia | Anaeromyxobacter | Medium | Strict anaerobic, requires Fe3+ (e.g., ferrihydrite) | IP interfaces and anoxic rhizosphere, enriched in deeper soil layers and plaque microsites | Ding et al, |
| Firmicutes | Clostridium | Medium | Strict anaerobic, suppressed by high N or O2 | Anoxic bulk soil and deeper layers, less in rhizosphere or surface, occasionally in reduced microsites | Ahmed et al, |
| Method | Directly measure item | Strength | Main limitation/bias | Best use-case |
|---|---|---|---|---|
| 15N (nitrogen) isotope dilution | Estimated fraction of plant/soil N derived from fixation under labelled-fertilizer conditions | Field-relevant, links to plant N pools | Requires suitable non-fixing reference and assumptions about comparable N uptake and label uniformity | Quantifying N contribution across treatments/sites |
| 15N2 incorporation | Direct incorporation of labelled N2 into biomass (microbial and/or plant pools) | Strong evidence for fixation, can be paired with stable isotope probing to identify active taxa | Low-throughput, enclosure artifacts, technical complexity/cost | Mechanistic confirmation, benchmarking key genotypes |
| Natural-abundance 15N | Integrated isotopic signal over time (often subtle in cereal systems) | Non-invasive, field-friendly | Low sensitivity, baseline and fractionation uncertainty | Long-term/large-scale surveys with strong controls |
| Acetylene reduction assay | Nitrogenase activity potential under assay conditions | Fast, inexpensive, scalable | Conversion to N fixed uncertain, sensitive to assay conditions, does not directly quantify plant N gain | Screening and treatment comparisons within a standardized protocol |
| nifH qPCR/nifH amplicon sequencing | Diazotroph abundance/ composition (potential) | High-throughput, sensitive, community tracking | Potential ≠ flux, primer/gene-copy biases, presence does not guarantee activity | Community shifts, early-stage ranking of genotypes/treatments |
| Metagenomics | Functional gene repertoire (capacity) | Broad functional context, hypothesis generation | Cost, capacity not rate, bioinformatic complexity | Trait-microbiome links, candidate pathway discovery |
| Metatranscriptomics/ nifH expression | Functional activity proxy (transcriptional engagement) | Captures responses to genotype/ environment | Expression not always proportional to flux, sampling time sensitivity, cost | Mechanistic studies paired with isotope/activity validation |
| Stable isotope probing (DNA/RNA-stable isotope probing with 15N2) | Identifies taxa actively incorporating labelled N during fixation | Links function to specific organisms in situ | Technical complexity, low-throughput, enclosure artifacts possible | Attribution of active diazotrophs and niches, validating mechanistic hypotheses |
Table 2. Comparative summary of methods used in quantifying rice biological nitrogen fixation and diazotroph studies.
| Method | Directly measure item | Strength | Main limitation/bias | Best use-case |
|---|---|---|---|---|
| 15N (nitrogen) isotope dilution | Estimated fraction of plant/soil N derived from fixation under labelled-fertilizer conditions | Field-relevant, links to plant N pools | Requires suitable non-fixing reference and assumptions about comparable N uptake and label uniformity | Quantifying N contribution across treatments/sites |
| 15N2 incorporation | Direct incorporation of labelled N2 into biomass (microbial and/or plant pools) | Strong evidence for fixation, can be paired with stable isotope probing to identify active taxa | Low-throughput, enclosure artifacts, technical complexity/cost | Mechanistic confirmation, benchmarking key genotypes |
| Natural-abundance 15N | Integrated isotopic signal over time (often subtle in cereal systems) | Non-invasive, field-friendly | Low sensitivity, baseline and fractionation uncertainty | Long-term/large-scale surveys with strong controls |
| Acetylene reduction assay | Nitrogenase activity potential under assay conditions | Fast, inexpensive, scalable | Conversion to N fixed uncertain, sensitive to assay conditions, does not directly quantify plant N gain | Screening and treatment comparisons within a standardized protocol |
| nifH qPCR/nifH amplicon sequencing | Diazotroph abundance/ composition (potential) | High-throughput, sensitive, community tracking | Potential ≠ flux, primer/gene-copy biases, presence does not guarantee activity | Community shifts, early-stage ranking of genotypes/treatments |
| Metagenomics | Functional gene repertoire (capacity) | Broad functional context, hypothesis generation | Cost, capacity not rate, bioinformatic complexity | Trait-microbiome links, candidate pathway discovery |
| Metatranscriptomics/ nifH expression | Functional activity proxy (transcriptional engagement) | Captures responses to genotype/ environment | Expression not always proportional to flux, sampling time sensitivity, cost | Mechanistic studies paired with isotope/activity validation |
| Stable isotope probing (DNA/RNA-stable isotope probing with 15N2) | Identifies taxa actively incorporating labelled N during fixation | Links function to specific organisms in situ | Technical complexity, low-throughput, enclosure artifacts possible | Attribution of active diazotrophs and niches, validating mechanistic hypotheses |
Fig. 2. Four genetic ‘levers’ of plants that help rice recruit diazotrophs, shaping activity of N2-fixers in flooded paddies. Root system architecture (depth, angle, lateral density) that places carbon where microbes forage. Root exudates (e.g., flavonoids, sugars, LMWOAs) that attract and feed diazotrophs. Aerenchyma-mediated radial O2 loss that sculpts oxic-anoxic microsites along roots. Iron plaque on root surfaces that provides Fe3+ for IRB and a catalytic oxic-anoxic interface supporting biological nitrogen fixation. Together, these levers determine where and which diazotrophs thrive around rice roots. IRB, Iron-reducing bacterium; LMWOAs, Low-molecular-weight organic acids.
Fig. 3. Workflow for breeding and validating biological nitrogen fixation-supportive rice. The figure summarizes the stepwise pipeline (trait/locus discovery, validation, multi-environment test, and deployment) and is intended as a navigational schematic that visualizes the text rather than a comparison of measurement methods. BILs, Backcross inbred lines; BNF, Biological nitrogen fixation; CSSLs, Chromosome segment substitution lines; GWAS, Genome-wide association study; eco-GWAS, Ecological GWAS; FACE, Free air CO2 enrichment; MAS, Marker-assisted selection; NILs, Near-isogenic lines; RILs, Recombinant inbred lines.
| Gene | Known/proposed function | Effect on diazotroph recruitment | Reference |
|---|---|---|---|
| DRO1 | Influence root gravitropic angle | Promote deeper rooting and extend rhizosphere into anaerobic layers to support anaerobic diazotrophs like iron-reducing bacterium (IRB) | Kitomi et al, |
| OsMADS50 | MADS-box transcription factor | Suppress crown root growth when overexpressed, and may influence root architecture to enhance surface area for IRB interaction and nutrient absorption | Lin et al, |
| ARF16 | Auxin response factor regulating root hair development | Suppress root hair elongation. Reduced activity could increase root hairs, providing more attachment sites for diazotroph biofilms | Gao et al, |
| FLR7 | Receptor-like kinase regulating radial O2 loss | Alter O2 leakage patterns, enrich anaerobic diazotrophs such as Anaeromyxobacter, and improve submergence tolerance and biological nitrogen fixation (BNF) under flooded conditions | Liu et al, |
| FLS | Flavonol synthase involved in flavonoid biosynthesis | Increase flavonoid exudation, attracting and signaling diazotrophs, linked to higher IRB abundance | Lu and Zhu et al, |
| CYP75B3/ CYP75B4 | Flavonoid 3’-hydroxylase genes in flavonoid biosynthesis pathway | Disruption diverts pathway to increase apigenin and luteolin production, enhance biofilm formation and nitrogenase activity in diazotrophs like Gluconacetobacter | Yan et al, |
| GS3 (gs3) | G-protein γ subunit 3; pleiotropic effects on development of roots | Field multi-omics evidence links a gs3 loss-of-function allele to enrichment of BNF genes (nifH, nifD, and nifK) in the rhizosphere microbiome under low-N conditions | Kwon et al, |
| AMT1.1/ AMT1.2 | Ammonium uptake coupling | High-affinity ammonium uptake allows host to capture fixed N and support partnership, and indirectly stabilizes diazotroph association | Li et al, |
| OsFRO2 | Ferric reductase involved in iron homeostasis | Promote iron plaque formation by supplying Fe2+, provide a scaffold for IRB, and enhance BNF at the root-soil interface | Paul et al, |
| NRT1.1B | Nitrate transporter influencing nitrogen (N) uptake and signaling | Natural allelic variation affects N use efficiency and is associated with distinct root microbiome profiles in field-grown rice | Lu and Zhu, |
Table 3. Genes of rice plants identified throughout literature directly or potentially influencing diazotroph enrichment in rice rhizosphere.
| Gene | Known/proposed function | Effect on diazotroph recruitment | Reference |
|---|---|---|---|
| DRO1 | Influence root gravitropic angle | Promote deeper rooting and extend rhizosphere into anaerobic layers to support anaerobic diazotrophs like iron-reducing bacterium (IRB) | Kitomi et al, |
| OsMADS50 | MADS-box transcription factor | Suppress crown root growth when overexpressed, and may influence root architecture to enhance surface area for IRB interaction and nutrient absorption | Lin et al, |
| ARF16 | Auxin response factor regulating root hair development | Suppress root hair elongation. Reduced activity could increase root hairs, providing more attachment sites for diazotroph biofilms | Gao et al, |
| FLR7 | Receptor-like kinase regulating radial O2 loss | Alter O2 leakage patterns, enrich anaerobic diazotrophs such as Anaeromyxobacter, and improve submergence tolerance and biological nitrogen fixation (BNF) under flooded conditions | Liu et al, |
| FLS | Flavonol synthase involved in flavonoid biosynthesis | Increase flavonoid exudation, attracting and signaling diazotrophs, linked to higher IRB abundance | Lu and Zhu et al, |
| CYP75B3/ CYP75B4 | Flavonoid 3’-hydroxylase genes in flavonoid biosynthesis pathway | Disruption diverts pathway to increase apigenin and luteolin production, enhance biofilm formation and nitrogenase activity in diazotrophs like Gluconacetobacter | Yan et al, |
| GS3 (gs3) | G-protein γ subunit 3; pleiotropic effects on development of roots | Field multi-omics evidence links a gs3 loss-of-function allele to enrichment of BNF genes (nifH, nifD, and nifK) in the rhizosphere microbiome under low-N conditions | Kwon et al, |
| AMT1.1/ AMT1.2 | Ammonium uptake coupling | High-affinity ammonium uptake allows host to capture fixed N and support partnership, and indirectly stabilizes diazotroph association | Li et al, |
| OsFRO2 | Ferric reductase involved in iron homeostasis | Promote iron plaque formation by supplying Fe2+, provide a scaffold for IRB, and enhance BNF at the root-soil interface | Paul et al, |
| NRT1.1B | Nitrate transporter influencing nitrogen (N) uptake and signaling | Natural allelic variation affects N use efficiency and is associated with distinct root microbiome profiles in field-grown rice | Lu and Zhu, |
Fig. 4. Ideotype for biological nitrogen fixation (BNF)-supportive rice. A rice plant with dual root architecture, deep, steep roots plus dense shallow laterals and long root hairs, to increase root-soil contact across reduced (generally anoxic) soil volumes below the thin oxic surface layer; controlled aerenchyma/ROL and iron plaque to generate oxic-anoxic interfaces for IRB; exudate signals (flavonoids; measured LMWOAs) to recruit/energize diazotrophs; and root IP to improve the Fe-N-C cycling and provide IRB-supportive niches. IRB, Iron-reducing bacterium; LMWOAs, Low-molecular-weight organic acids; ROL, Radial oxygen loss.
Fig. 5. A tiered breeding pipeline to enhance rice recruitment of N2-fixing microbiome. The pipeline links discovery to deployment: (1) Discovery. GWAS/QTL, wild introgressions, and multi-omics to find loci/alleles associated with diazotroph recruitment and BNF (e.g., flavonoids, root architectures, O2-leakage regulators); (2) Validation. CRISPR/Cas edits, NILs/CSSLs, transcriptomics, and phenotyping (e.g. nifH, 15N2, exudate profiles) across environments to prove causality; (3) Deployment. MAS and GS to pyramid validated alleles into elite backgrounds and hybrids while safeguarding yield/quality; (4) Ecosystem testing. Multi-site, low-N field trials (optionally with inoculants) to quantify fertilizer replacement, stability across soils/climates, and compatibility with agronomy. BNF, Biological nitrogen fixation; CSSLs, Chromosome segment substitution lines; GWAS, Genome-wide association study; eco-GWAS, Ecological GWAS; GS, Genomic selection; MAS, Marker-assisted selection; NILs, Near-isogenic lines.
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