Dataset Information

A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants.

ABSTRACT: Microbiomes are important for crop performance. However, a deeper knowledge of crop-associated microbial communities is needed to harness beneficial host-microbe interactions. Here, by assessing the assembly and functions of maize microbiomes across soil types, climate zones, and genotypes, we found that the stem xylem selectively recruits highly conserved microbes dominated by Gammaproteobacteria. We showed that the proportion of bacterial taxa carrying the nitrogenase gene (nifH) was larger in stem xylem than in other organs such as root and leaf endosphere. Of the 25 core bacterial taxa identified in xylem sap, several isolated strains were confirmed to be active nitrogen-fixers or to assist with biological nitrogen fixation. On this basis, we established synthetic communities (SynComs) consisting of two core diazotrophs and two helpers. GFP-tagged strains and ¹⁵N isotopic dilution method demonstrated that these SynComs do thrive and contribute, through biological nitrogen fixation, 11.8% of the total N accumulated in maize stems. These core taxa in xylem sap represent an untapped resource that can be exploited to increase crop productivity.

SUBMITTER: Zhang L

PROVIDER: S-EPMC9187771 | biostudies-literature | 2022 Jun

REPOSITORIES: biostudies-literature

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A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants.

Zhang Liyu L Zhang Meiling M Huang Shuyu S Li Lujun L Gao Qiang Q Wang Yin Y Zhang Shuiqing S Huang Shaomin S Yuan Liang L Wen Yanchen Y Liu Kailou K Yu Xichu X Li Dongchu D Zhang Lu L Xu Xinpeng X Wei Hailei H He Ping P Zhou Wei W Philippot Laurent L Ai Chao C

Nature communications 20220611 1

Microbiomes are important for crop performance. However, a deeper knowledge of crop-associated microbial communities is needed to harness beneficial host-microbe interactions. Here, by assessing the assembly and functions of maize microbiomes across soil types, climate zones, and genotypes, we found that the stem xylem selectively recruits highly conserved microbes dominated by Gammaproteobacteria. We showed that the proportion of bacterial taxa carrying the nitrogenase gene (nifH) was larger in ...[more]

PMID: 35688828

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Project description:Continuous light (CL) or a predominant nitrogen supply as ammonium (NH4+) can induce leaf chlorosis and inhibit plant growth. The similarity in injuries caused by CL and NH4+ suggests involvement of overlapping mechanisms in plant responses to these conditions; however, these mechanisms are poorly understood. We addressed this topic by conducting full factorial experiments with tomato plants to investigate the effects of NO3- or NH4+ supply under diurnal light (DL) or CL. We used plants at ages of 26 and 15 days after sowing to initiate the treatments, and we modulated the intensity of the stress induced by CL and an exclusive NH4+ supply from mild to strong. Under DL, we also studied the effect of nitrogen (N) deficiency and mixed application of NO3- and NH4+. Under strong stress, CL and exclusive NH4+ supply synergistically inhibited plant growth and reduced chlorophyll content. Under mild stress, when no synergetic effect between CL and NH4+ was apparent on plant growth and chlorophyll content, we found a synergetic effect of CL and NH4+ on the accumulation of several plant stress hormones, with an especially strong effect for jasmonic acid (JA) and 1-aminocyclopropane-1-carboxylic acid (ACC), the immediate precursor of ethylene, in xylem sap. This modulation of the hormonal composition suggests a potential role for these plant hormones in plant growth responses to the combined application of CL and NH4+. No synergetic effect was observed between CL and NH4+ for the accumulation of soluble carbohydrates or of mineral ions, indicating that these plant traits are less sensitive than the modulation of hormonal composition in xylem sap to the combined CL and NH4+ application. Under diurnal light, NH4+ did not affect the hormonal composition of xylem sap; however, N deficiency strongly increased the concentrations of phaseic acid (PA), JA, and salicylic acid (SA), indicating that decreased N concentration rather than the presence of NO3- or NH4+ in the nutrient solution drives the hormone composition of the xylem sap. In conclusion, N deficiency or a combined application of CL and NH4+ induced the accumulation of JA in xylem sap. This accumulation, in combination with other plant hormones, defines the specific plant response to stress conditions.

Project description:BackgroundSubstance transport in higher land plants is mediated by vascular bundles, consisting of phloem and xylem strands that interconnect all plant organs. While the phloem mainly allocates photoassimilates, the role of the xylem is the transport of water and inorganic nutrients from roots to all aerial plant parts. Only recently it was noticed that in addition to mineral salts, xylem sap contains organic nutrients and even proteins. Although these proteins might have important impact on the performance of above-ground organs, only a few of them have been identified so far and their physiological functions are still unclear.ResultsWe used root-pressure xylem exudate, collected from cut Brassica napus stems, to extract total proteins. These protein preparations were then separated by high-resolution two-dimensional gel electrophoresis (2-DE). After individual tryptic digests of the most abundant coomassie-stained protein spots, partial peptide sequence information was deduced from tandem mass spectrometric (MS/MS) fragmentation spectra and subsequently used for protein identifications by database searches. This approach resulted in the identification of 69 proteins. These identifications include different proteins potentially involved in defence-related reactions and cell wall metabolism.ConclusionThis study provides a comprehensive overview of the most abundant proteins present in xylem sap of Brassica napus. A number of 69 proteins could be identified from which many previously were not known to be localized to this compartment in any other plant species. Since Brassica napus, a close relative of the fully sequenced model plant Arabidopsis thaliana, was used as the experimental system, our results provide a large number of candidate proteins for directed molecular and biochemical analyses of the physiological functions of the xylem under different environmental and developmental conditions. This approach will allow exploiting many of the already established functional genomic resources, like i.e. the large mutant collections, that are available for Arabidopsis.

Project description:In Mexico, the center of maize origin (Zea mays ssp. mays), there are landraces from the highlands that develop extensive aerial root systems which secrete a carbohydrate-rich mucilage. This mucilage produces a favorable environment for nitrogenase activity by diazotrophs. This plant-microbial interaction enables the fixation of nitrogen (N) from the atmosphere, reducing the required N that otherwise must come from the soil and/or fertilizers. The objective of this research was to investigate the degree to which other landraces of maize and nutrient management affect aerial root growth and the ability of maize to perform and benefit from N2 fixation. In two replicated field experiments in Columbus, Ohio, USA in 2019 and 2020, we planted 21 maize landraces and three improved varieties with and without fertilizer to measure their growth, production of aerial roots, and rate of atmospheric N2 fixation using the 15N natural abundance method. Maize accessions varied in the growth rate and number of nodes with aerial roots. Up to 36% of plant N was derived from the atmosphere, with values varying by accession, the reference plant used, and the fertilizer level. Moreover, there was a positive relationship between early growth parameters and numbers of nodes with aerial roots, which, in turn, predicted the amount of N derived from the atmosphere. Thus, larger seedlings may experience enhanced root growth and thereby benefit more from N fixation. By phenotyping a diverse set of maize accessions with and without fertilizer, this study explores both environmental and quantitative genetic variation in the traits involved in N fixation capacity, clarifying that N fixation found in the Sierra Mixe landrace is more broadly distributed than previously thought. In sum, farmers stewarding genetic diversity in a crop center of origin have preserved traits essential for biological symbioses that contribute to maize's nutrient requirements. These traits may enable maize crops grown by Mexican farmers, and farmers globally, to benefit from N fixation from the atmosphere.

Dataset Information

A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants.

Publications

A highly conserved core bacterial microbiota with nitrogen-fixation capacity inhabits the xylem sap in maize plants.

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