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Bacterial Indole-3-Acetic Acid Influences Soil Nitrogen Acquisition in Barley and Chickpea.

ABSTRACT: Farming of barley and chickpea is nitrogen (N) fertilizer dependent. Using strategies that increase the nitrogen use efficiency (NUE) and its components, nitrogen uptake efficiency (NUpE) and nitrogen utilization efficiency (NUtE) would reduce the N fertilizer application in the soil and its adverse environmental effects. We evaluated the effects of three different strains of diazotroph Klebsiella (K.p. SSN1, K.q. SGM81, and K.o. M5a1) to understand the role of biological nitrogen fixation (BNF) and bacterial indole-3-acetic acid (IAA) on NUE of the plants. A field study revealed that K.p. SSN1 results in profound increment of root surface area by eightfold and threefold compared to uninoculated (control) in barley and chickpea, respectively. We measured significant increase in the plant tissue nitrogen, chlorophyll content, protein content, nitrate reductase activity, and nitrate concentration in the inoculated plants (p ≤ 0.05). Treated barley and chickpea exhibited higher NUE and the components compared to the control plants (K.p. SSN1 ≥ K.q. SGM81> K.o. M5a1). Specifically, K.q. SGM81 treatment in barley increased NUpE by 72%, while in chickpea, K.p. SSN1 increased it by 187%. The substantial improvement in the NUpE and NUE by the auxin producers K.p. SSN1 and K.q. SGM81 compared with non-auxin producer K.o. M5a1 was accompanied by an augmented root architecture suggesting larger contribution of IAA over marginal contribution of BNF in nitrogen acquisition from the soil.

SUBMITTER: Gang S

PROVIDER: S-EPMC8071533 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:We show for soil bacterium Enterobacter soli LF7 that the possession of an indole-3-acetic acid catabolic (iac) gene cluster is causatively linked to the ability to utilize the plant hormone indole-3-acetic acid (IAA) as a carbon and energy source. Genome-wide transcriptional profiling by mRNA sequencing revealed that these iac genes, chromosomally arranged as iacHABICDEFG and coding for the transformation of IAA to catechol, were the most highly induced (>29-fold) among the relatively few (<1%) differentially expressed genes in response to IAA. Also highly induced and immediately downstream of the iac cluster were genes for a major facilitator superfamily protein (mfs) and enzymes of the ?-ketoadipate pathway (pcaIJD-catBCA), which channels catechol into central metabolism. This entire iacHABICDEFG-mfs-pcaIJD-catBCA gene set was constitutively expressed in an iacR deletion mutant, confirming the role of iacR, annotated as coding for a MarR-type regulator and located upstream of iacH, as a repressor of iac gene expression. In E. soli LF7 carrying the DNA region upstream of iacH fused to a promoterless gfp gene, green fluorescence accumulated in response to IAA at concentrations as low as 1.6 ?M. The iacH promoter region also responded to chlorinated IAA, but not other aromatics tested, indicating a narrow substrate specificity. In an iacR deletion mutant, gfp expression from the iacH promoter region was constitutive, consistent with the predicted role of iacR as a repressor. A deletion analysis revealed putative -35/-10 promoter sequences upstream of iacH, as well as a possible binding site for the IacR repressor.IMPORTANCE Bacterial iac genes code for the enzymatic conversion of the plant hormone indole-3-acetic acid (IAA) to catechol. Here, we demonstrate that the iac genes of soil bacterium Enterobacter soli LF7 enable growth on IAA by coarrangement and coexpression with a set of pca and cat genes that code for complete conversion of catechol to central metabolites. This work contributes in a number of novel and significant ways to our understanding of iac gene biology in bacteria from (non-)plant environments. More specifically, we show that LF7's response to IAA involves derepression of the MarR-type transcriptional regulator IacR, which is quite fast (less than 25 min upon IAA exposure), highly specific (only in response to IAA and chlorinated IAA, and with few genes other than iac, cat, and pca induced), relatively sensitive (low micromolar range), and seemingly tailored to exploit IAA as a source of carbon and energy.

Project description:Background: The overproduction of the main auxin indole-3-acetic acid (IAA) in Sinorhizobium meliloti RD64 leads to beneficial effects both in free-living rhizobium and in host plant during symbiosis. These effects could be related to alteration in gene expression induced by IAA. Preliminary studies of these alterations induced in free-living cells have already started. In this work the transcriptional profiles of free-living S. meliloti wild type 1021 and RD64 strains obtained by RNA-seq analysis were used to better investigate this issue. Results: Transcriptome analysis by next-generation sequencing (RNA-seq) allowed the identification of the genes differentially expressed in RD64 cells, grown in a rich medium under aerobic conditions. Most of the up-regulated genes can be classified into two main categories. The first class comprised the main regulator fixJ and the two intermediate regulators fixK and nifA, which control the expression of genes involved in nitrogen-fixation. For these two latter genes the highest expression levels were observed. Several other genes, known to be FixJ targets, such as those involved in denitrification process and proline metabolism, were also identified. The second class of up-regulated genes comprised the gene coding for the sigma factor RpoH1 and other genes regulated in RpoH1-dependent manner in S. meliloti and involved in stress response. The main category of genes negatively affected can be classified in transport of sugars and other small molecules, chemotaxis and cell envelope functions. Under microaerobic condition, quantitative real-time PCR analysis of genes coding for the two-component regulatory system FixJL and for the regulator NifA showed that for all three genes the induction levels measured in RD64 cells were even higher when compared to aerobic conditions. In particular, for the fixJ gene the expression level increased more than tenfold. The up-regulation of nifA gene was also observed under aerobic conditions both when nitrogen level in the medium was limiting and when it was high. Conclusion: This work provided evidence that the overexpression of the auxin IAA in S. meliloti free-living cells triggers the induction of many genes involved in bacterial response to different abiotic stresses and allows the expression of key genes involved in nitrogen fixation.

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Bacterial Indole-3-Acetic Acid Influences Soil Nitrogen Acquisition in Barley and Chickpea.

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