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Genetic modification of flavone biosynthesis in rice enhances biofilm formation of soil diazotrophic bacteria and biological nitrogen fixation.

ABSTRACT: Improving biological nitrogen fixation (BNF) in cereal crops is a long-sought objective; however, no successful modification of cereal crops showing increased BNF has been reported. Here, we described a novel approach in which rice plants were modified to increase the production of compounds that stimulated biofilm formation in soil diazotrophic bacteria, promoted bacterial colonization of plant tissues and improved BNF with increased grain yield at limiting soil nitrogen contents. We first used a chemical screening to identify plant-produced compounds that induced biofilm formation in nitrogen-fixing bacteria and demonstrated that apigenin and other flavones induced BNF. We then used CRISPR-based gene editing targeting apigenin breakdown in rice, increasing plant apigenin contents and apigenin root exudation. When grown at limiting soil nitrogen conditions, modified rice plants displayed increased grain yield. Biofilm production also modified the root microbiome structure, favouring the enrichment of diazotrophic bacteria recruitment. Our results support the manipulation of the flavone biosynthetic pathway as a feasible strategy for the induction of biological nitrogen fixation in cereals and a reduction in the use of inorganic nitrogen fertilizers.

SUBMITTER: Yan D

PROVIDER: S-EPMC9616522 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Genetic modification of flavone biosynthesis in rice enhances biofilm formation of soil diazotrophic bacteria and biological nitrogen fixation.

Yan Dawei D Tajima Hiromi H Cline Lauren C LC Fong Reedmond Y RY Ottaviani Javier I JI Shapiro Howard-Yana HY Blumwald Eduardo E

Plant biotechnology journal 20220808 11

Improving biological nitrogen fixation (BNF) in cereal crops is a long-sought objective; however, no successful modification of cereal crops showing increased BNF has been reported. Here, we described a novel approach in which rice plants were modified to increase the production of compounds that stimulated biofilm formation in soil diazotrophic bacteria, promoted bacterial colonization of plant tissues and improved BNF with increased grain yield at limiting soil nitrogen contents. We first used ...[more]

PMID: 35869808

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Project description:BackgroundNitrogen-fixing prokaryotes (diazotrophs) contribute substantially to nitrogen input in mangrove sediments, and their structure and nitrogen fixation rate (NFR) are significantly controlled by environmental conditions. Despite the well-known studies on diazotrophs in surficial sediments, the diversity, structure, and ecological functions of diazotrophic communities along environmental gradients of mangrove sediment across different depths are largely unknown. Here, we investigated how biological nitrogen fixation varied with the depth of mangrove sediments from the perspectives of both NFR and diazotrophic communities.ResultsThrough acetylene reduction assay, nifH gene amplicon and metagenomic sequencing, we found that the NFR increased but the diversity of diazotrophic communities decreased with the depth of mangrove sediments. The structure of diazotrophic communities at different depths was largely driven by salinity and exhibited a clear divergence at the partitioning depth of 50 cm. Among diazotrophic genera correlated with NFR, Agrobacterium and Azotobacter were specifically enriched at 50-100 cm sediments, while Anaeromyxobacter, Rubrivivax, Methylocystis, Dickeya, and Methylomonas were more abundant at 0-50 cm. Consistent with the higher NFR, metagenomic analysis demonstrated the elevated abundance of nitrogen fixation genes (nifH/D/K) in deep sediments, where nitrification genes (amoA/B/C) and denitrification genes (nirK and norB) became less abundant. Three metagenome-assembled genomes (MAGs) of diazotrophs from deep mangrove sediments indicated their facultatively anaerobic and mixotrophic lifestyles as they contained genes for low-oxygen-dependent metabolism, hydrogenotrophic respiration, carbon fixation, and pyruvate fermentation.ConclusionsThis study demonstrates the depth-dependent variability of biological nitrogen fixation in terms of NFR and diazotrophic communities, which to a certain extent relieves the degree of nitrogen limitation in deep mangrove sediments. Video Abstract.

Project description:Nitrogen gas (N2) fixation driven by diazotrophs is a crucial process for supplying nitrogen to paddy soil ecosystems. The genus Geomonas has been considered to be an important potential diazotroph in paddy soils, but direct experimental evidence of the nitrogen-fixing ability of Geomonas in pure culture is still lacking. Hence, we aimed to demonstrate this nitrogen-fixing capability and shed light on how this process was regulated in response to ammonium (NH4 +) in Geomonas. In this study, we determined that a key nitrogenase gene (nifH) was present in 50 isolates from paddy soils. Members of Geomonas contained the minimum nitrogen fixation gene cluster (nifBHDKEN) based on genomic analysis, implying Geomonas species had the potential to fix nitrogen. Acetylene reduction assay (ARA), 15N2 isotope labeling, and total nitrogen accumulation assays validated that Geomonas was, indeed, able to fix nitrogen in pure culture. Under nitrogen-fixing conditions, the cell morphology of Geomonas changed from short rod-shaped (with NH4 +) to long rod-shaped and flagella became longer and thicker. The expression of genes correlated to nitrogen fixation in the Geomonas transcriptome was quantified in response to NH4 +. Expression of genes associated with nitrogenase, flavin-based electron bifurcation complexes (such as the FixAB system), NH4 + uptake, and transformation (e.g., glutamine and glutamate synthetases) were significantly upregulated under nitrogen-fixing conditions, suggesting these mechanisms might be involved in N2 fixation in Geomonas. These results were verified by RT-qPCR. Taken together, our results demonstrate that Geomonas species possess the ability to fix N2 and expand our understanding on the ecological significance and potential applications of Geomonas in paddy soil ecosystems. IMPORTANCE The ability of Geomonas species to fix nitrogen gas (N2) is an important metabolic feature for its application as a plant growth-promoting rhizobacterium. This research is of great importance as it provides the first comprehensive direct experimental evidence of nitrogen fixation by the genus Geomonas in pure culture. We isolated a number of Geomonas strains from paddy soils and determined that nifH was present in these strains. This study demonstrated that these Geomonas species harbored genes encoding nitrogenase, as do Geobacter and Anaeromyxobacter in the same class of Deltaproteobacteria. We demonstrated N2-dependent growth of Geomonas and determined regulation of gene expression associated with nitrogen fixation. The research establishes and advances our understanding of nitrogen fixation in Geomonas.

Dataset Information

Genetic modification of flavone biosynthesis in rice enhances biofilm formation of soil diazotrophic bacteria and biological nitrogen fixation.

Publications

Genetic modification of flavone biosynthesis in rice enhances biofilm formation of soil diazotrophic bacteria and biological nitrogen fixation.

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