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CPOP1 is the key heme synthesis enzyme required for nodule microenvironment control and successful symbiotic nitrogen fixation in Lotus japonicus

ABSTRACT: Heme is utilized as the cofactor of diverse proteins and plays critical roles in different redox reactions. The fixation active nodules of legumes are abundant with heme-containing leghemoglobin to buffer the oxygen concentration. Symbiotic rhizobia could also synthesize heme, and employ heme for efficient respiration and iron uptake regulation. However, the role and regulation of host-controlled heme production during symbiotic nitrogen fixation have not been directly investigated and experimentally proved. Here, we identified the coproporphyrinogen III oxidase plastid related 1 (CPOP1) as a key regulator of symbiotic heme synthesis enzyme in Lotus japonicus. CPOP1 is specifically highly expressed in nitrogen-fixing nodules, and knocking out CPOP1 alone causes leaf etiolation and dwarfism which could be fully recovered by the exogenous application of nitrogen source, indicating nitrogen fixation defect. The cpop1 mutant shows significantly increased nodule oxygen level and decreased nitrogen fixation activity compared to the wild type (WT). Moreover, cell division and related gene expression of bacteroids are also affected upon CPOP1 knockout. We conclude that CPOP1 is essential for the microaerophilic environment control of infected cells and the activation of rhizobial nitrogenase required for symbiotic nitrogen fixation, through host-regulated nodule heme synthesis.

ORGANISM(S): Lotus japonicus

PROVIDER: GSE262662 | GEO | 2025/09/01

REPOSITORIES: GEO

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Project description:During the legume-rhizobium symbiosis, free-living soil bacteria known as rhizobia trigger the formation of root nodules. The rhizobia infect these organs and adopt an intracellular lifestyle within the symbiotic nodule cells where they become nitrogen-fixing bacteroids. Several legume lineages enforce their symbionts into an extreme cellular differentiation, comprising cell enlargement and genome endoreduplication. The antimicrobial peptide transporter BclA is a major determinant of this differentiation process in Bradyrhizobium sp. ORS285, a symbiont of Aeschynomene spp.. In the absence of BclA, Bradyrhizobium sp. ORS285 proceeds until the intracellular infection of nodule cells but the bacteria cannot differentiate into enlarged polyploid bacteroids and fix nitrogen. The nodule bacteria of the bclA mutant constitute thus an intermediate stage between the free-living soil bacteria and the intracellular nitrogen-fixing bacteroids. Metabolomics on whole nodules of Aeschynomene afraspera and Aeschynomene indica infected with the ORS285 wild type or the bclA mutant revealed 47 metabolites that differentially accumulated concomitantly with bacteroid differentiation. Bacterial transcriptome analysis of these nodules discriminated nodule-induced genes that are specific to differentiated and nitrogen-fixing bacteroids and others that are activated in the host microenvironment irrespective of bacterial differentiation and nitrogen fixation. These analyses demonstrated that the intracellular settling of the rhizobia in the symbiotic nodule cells is accompanied with a first transcriptome switch involving several hundreds of upregulated and downregulated genes and a second switch accompanying the bacteroid differentiation, involving less genes but that are expressed to extremely elevated levels. The transcriptomes further highlighted the dynamics of oxygen and redox regulation of gene expression during nodule formation and we discovered that bclA represses the expression of non-ribosomal peptide synthetase gene clusters suggesting a non-symbiotic function of BclA. Together, our data uncover the metabolic and gene expression changes that accompany the transition from intracellular bacteria into differentiated nitrogen-fixing bacteroids.

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CPOP1 is the key heme synthesis enzyme required for nodule microenvironment control and successful symbiotic nitrogen fixation in Lotus japonicus

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