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Nitrate restricts nodule organogenesis through inhibition of cytokinin biosynthesis in Lotus japonicus

ABSTRACT: Legumes balance nitrogen acquisition from soil nitrate with symbiotic nitrogen fixation. Nitrogen fixation requires establishment of a new organ, which is a cytokinin dependent developmental process in the root. We found cytokinin biosynthesis is a central integrator, balancing nitrate signalling with symbiotic acquired nitrogen. Low nitrate conditions provide a permissive state for induction of cytokinin by symbiotic signalling and thus nodule development. In contrast, high nitrate is inhibitory to cytokinin accumulation and nodule establishment in the root zone susceptible to nodule formation. This reduction of symbiotic cytokinin accumulation was further exacerbated in cytokinin biosynthesis mutants, which display hypersensitivity to nitrate inhibition of nodule development, maturation and nitrogen fixation. Consistent with this, cytokinin application rescues nodulation and nitrogen fixation of biosynthesis mutants in a concentration dependent manner. These inhibitory impacts of nitrate on symbiosis occur in a Nlp1 and Nlp4 dependent manner and contrast with the positive influence of nitrate on cytokinin biosynthesis that occurs in species that do not form symbiotic root nodules. Altogether this shows that legumes, as exemplified by Lotus japonicus, have evolved a different cytokinin response to nitrate compared to non-legumes. Nodule development in legumes is a cytokinin dependent process. Here the authors show that high nitrate supply, which limits nodulation, suppresses cytokinin biosynthesis in Lotus japonicus which contrasts with the positive effect of nitrate on cytokinin biosynthesis in non-legumes

SUBMITTER: Lin J

PROVIDER: S-EPMC8585978 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Correction: Cytokinin biosynthesis genes expressed during nodule organogenesis are directly regulated by the KNOX3 protein in Medicago truncatula.

Project description:[This corrects the article DOI: 10.1371/journal.pone.0232352.].

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Ectopic expression of NAC094 induces premature nodule senescence in Lotus japonicus.

Project description:To investigate the function of NAC094 in vivo, we overexpressed NAC094 in the infected cells of nodules using an L. japonicus Lb2 expression cassette. To this end, we used a GUS overexpression construct as control and analysed stably transformed plants to detect symbiotic phenotypes. Results show that overexpression of NAC094 causes premature senescence of nodules. To identify the mechanism by which NAC094 regulates nodule senescence, we performed a transcriptome profiling analysis of nodules at 3 wpi. Around 13,850 differentially expressed genes (DEGs) were identified by comparing NAC-OE with control nodules (Log2FC > 1, FDR < 0.05). Of these, 7,516 were up-regulated (NAC-OE-UP) and 6,334 were down-regulated (NAC-OE-DOWN).

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Project description:Lotus japonicus has been used for decades as a model legume to study the establishment of binary symbiotic relationships with nitrogen-fixing rhizobia that trigger root nodule organogenesis for bacterial accommodation. Using community profiling of 16S rRNA gene amplicons, we reveal that in Lotus, distinctive nodule- and root-inhabiting communities are established by parallel, rather than consecutive, selection of bacteria from the rhizosphere and root compartments. Comparative analyses of wild-type (WT) and symbiotic mutants in Nod factor receptor5 (nfr5), Nodule inception (nin) and Lotus histidine kinase1 (lhk1) genes identified a previously unsuspected role of the nodulation pathway in the establishment of different bacterial assemblages in the root and rhizosphere. We found that the loss of nitrogen-fixing symbiosis dramatically alters community structure in the latter two compartments, affecting at least 14 bacterial orders. The differential plant growth phenotypes seen between WT and the symbiotic mutants in nonsupplemented soil were retained under nitrogen-supplemented conditions that blocked the formation of functional nodules in WT, whereas the symbiosis-impaired mutants maintain an altered community structure in the nitrogen-supplemented soil. This finding provides strong evidence that the root-associated community shift in the symbiotic mutants is a direct consequence of the disabled symbiosis pathway rather than an indirect effect resulting from abolished symbiotic nitrogen fixation. Our findings imply a role of the legume host in selecting a broad taxonomic range of root-associated bacteria that, in addition to rhizobia, likely contribute to plant growth and ecological performance.

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