Root-Secreted Coumarins and the Microbiota Interact to Improve Iron Nutrition in Arabidopsis.
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ABSTRACT:
SUBMITTER: Harbort CJ
PROVIDER: S-EPMC7738756 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Pseudomonas simiae WCS417 is a root-colonizing bacterium with well-established plant-beneficial effects. Upon colonization of Arabidopsis roots, WCS417 evades local root immune responses while triggering an induced systemic resistance (ISR) in the leaves. The early onset of ISR in roots shows similarities with the iron deficiency response, as both responses are associated with the production and secretion of coumarins. Coumarins can mobilize iron from the soil environment and have a selective antimicrobial activity that impacts microbiome assembly in the rhizosphere. Being highly coumarin-tolerant, WCS417 induces the secretion of these phenolic compounds, likely to improve its own niche establishment, while providing growth and immunity benefits for the host in return. To investigate the possible signaling function of coumarins in the mutualistic Arabidopsis-WCS417 interaction, we analyzed the transcriptome of WCS417 growing in root exudates of coumarin-producing Arabidopsis Col-0 and the coumarin-biosynthesis mutant f6'h1. We found that coumarins in F6'H1-dependent root exudates significantly affected the expression of 439 bacterial genes (8% of the bacterial genome). Of those, genes with functions related to transport and metabolism of carbohydrates, amino acids, and nucleotides were induced, whereas genes with functions related to cell motility, the bacterial mobilome, and energy production and conversion were repressed. Strikingly, most genes related to flagellar biosynthesis were down-regulated by F6'H1-dependent root exudates and we found that application of selected coumarins reduces bacterial motility. These findings suggest that coumarins' function in the rhizosphere as semiochemicals in the communication between the roots and WCS417. Collectively, our results provide important novel leads for future functional analysis of molecular processes in the establishment of plant-mutualist interactions.
| S-EPMC8000642 | biostudies-literature
Project description:The factors that contribute to the composition of the root microbiome and, in turn, affect plant fitness are not well understood. Recent work has highlighted a major contribution of the soil inoculum in determining the composition of the root microbiome. However, plants are known to conditionally exude a diverse array of unique secondary metabolites, that vary among species and environmental conditions and can interact with the surrounding biota. Here, we explore the role of specialized metabolites in dictating which bacteria reside in the rhizosphere. We employed a reduced synthetic community (SynCom) of Arabidopsis thaliana root-isolated bacteria to detect community shifts that occur in the absence of the secreted small-molecule phytoalexins, flavonoids, and coumarins. We find that lack of coumarin biosynthesis in f6'h1 mutant plant lines causes a shift in the root microbial community specifically under iron deficiency. We demonstrate a potential role for iron-mobilizing coumarins in sculpting the A. thaliana root bacterial community by inhibiting the proliferation of a relatively abundant Pseudomonas species via a redox-mediated mechanism. This work establishes a systematic approach enabling elucidation of specific mechanisms by which plant-derived molecules mediate microbial community composition. Our findings expand on the function of conditionally exuded specialized metabolites and suggest avenues to effectively engineer the rhizosphere with the aim of improving crop growth in iron-limited alkaline soils, which make up a third of the world's arable soils.
| S-EPMC6589675 | biostudies-literature
Project description:The chemical composition of root exudates strongly impacts the interactions of plants with microorganisms in the rhizosphere and the efficiency of nutrient acquisition. Exudation of metabolites is in part mediated by ATP-binding cassette (ABC) transporters. In order to assess the contribution of individual ABC transporters to root exudation, we performed an LC-MS based non-targeted metabolite profiling of semi-polar metabolites accumulating in root exudates of Arabidopsis thaliana plants and mutants deficient in the expression of ABCG36 (PDR8/PEN3), ABCG37 (PDR9) or both transporters. Comparison of the metabolite profiles indicated distinct roles for each ABC transporter in root exudation. Thymidine exudation could be attributed to ABCG36 function, whereas coumarin exudation was strongly reduced only in ABCG37 deficient plants. However, coumarin exudation was compromised in abcg37 mutants only with respect to certain metabolites of this substance class. The specificity of ABCG37 for individual coumarins was further verified by a targeted LC-MS based coumarin profiling method. The response to iron deficiency, which is known to strongly induce coumarin exudation, was also investigated. In either treatment, the distribution of individual coumarins between roots and exudates in the investigated genotypes suggested the involvement of ABCG37 in the exudation specifically of highly oxygenated rather than monohydroxylated coumarins.
| S-EPMC5473935 | biostudies-literature
Project description:We present a gnotobiotic system for microbiota reconstitution on Arabidopsis thaliana under contrasting iron availability. This system induces iron starvation in plants by providing an unavailable form, mimicking conditions in alkaline soils. Inoculation of taxonomically diverse bacteria reconstitutes plants with a synthetic microbiota, allowing observation of nutrient-dependent interactions with commensals. Experimental optimization, including media composition and preparation of seedlings and bacteria, is discussed. This system provides a framework that can be adapted to study plant-microbiota interactions in further nutritional contexts. For complete details on the use and execution of this protocol, please refer to Harbort et al. (2020).
| S-EPMC7757726 | biostudies-literature
Project description:Both nitric oxide (NO) and strigolactone (SL) are growth regulating signal components in plants; however, regarding their possible interplay our knowledge is limited. Therefore, this study aims to provide new evidence for the signal interplay between NO and SL in the formation of root system architecture using complementary pharmacological and molecular biological approaches in the model Arabidopsis thaliana grown under stress-free conditions. Deficiency of SL synthesis or signaling (max1-1 and max2-1) resulted in elevated NO and S-nitrosothiol (SNO) levels due to decreased S-nitrosoglutathione (GSNO) reductase (GSNOR) protein abundance and activity indicating that there is a signal interaction between SLs and GSNOR-regulated levels of NO/SNO. This was further supported by the down-regulation of SL biosynthetic genes (CCD7, CCD8 and MAX1) in GSNOR-deficient gsnor1-3. Based on the more pronounced sensitivity of gsnor1-3 to exogenous SL (rac-GR24, 2 µM), we suspected that functional GSNOR is needed to control NO/SNO levels during SL-induced primary root (PR) elongation. Additionally, SLs may be involved in GSNO-regulated PR shortening as suggested by the relative insensitivity of max1-1 and max2-1 mutants to exogenous GSNO (250 µM). Collectively, our results indicate a connection between SL and GSNOR-regulated NO/SNO signals in roots of A. thaliana grown in stress-free environment. As this work used max2-1 mutant and rac-GR24 exerting unspecific effects to both SL and karrikin signaling, it cannot be ruled out that karrikins are partly responsible for the observed effects, and this issue needs further clarification in the future.
| S-EPMC7350899 | biostudies-literature
Project description:Plants host at the contact zone with soil a distinctive root-associated bacterial microbiota believed to function in plant nutrition and health. We investigated the diversity of the root microbiota within a phylogenetic framework of hosts: three Arabidopsis thaliana ecotypes along with its sister species Arabidopsis halleri and Arabidopsis lyrata, as well as Cardamine hirsuta, which diverged from the former ? 35 Mya. We surveyed their microbiota under controlled environmental conditions and of A. thaliana and C. hirsuta in two natural habitats. Deep 16S rRNA gene profiling of root and corresponding soil samples identified a total of 237 quantifiable bacterial ribotypes, of which an average of 73 community members were enriched in roots. The composition of this root microbiota depends more on interactions with the environment than with host species. Interhost species microbiota diversity is largely quantitative and is greater between the three Arabidopsis species than the three A. thaliana ecotypes. Host species-specific microbiota were identified at the levels of individual community members, taxonomic groups, and whole root communities. Most of these signatures were observed in the phylogenetically distant C. hirsuta. However, the branching order of host phylogeny is incongruent with interspecies root microbiota diversity, indicating that host phylogenetic distance alone cannot explain root microbiota diversification. Our work reveals within 35 My of host divergence a largely conserved and taxonomically narrow root microbiota, which comprises stable community members belonging to the Actinomycetales, Burkholderiales, and Flavobacteriales.
| S-EPMC3896156 | biostudies-literature
Project description:Root secretion of coumarin-phenolic type compounds has been recently shown to be related to Arabidopsis thaliana tolerance to Fe deficiency at high pH. Previous studies revealed the identity of a few simple coumarins occurring in roots and exudates of Fe-deficient A. thaliana plants, and left open the possible existence of other unknown phenolics. We used HPLC-UV/VIS/ESI-MS(TOF), HPLC/ESI-MS(ion trap) and HPLC/ESI-MS(Q-TOF) to characterize (identify and quantify) phenolic-type compounds accumulated in roots or secreted into the nutrient solution of A. thaliana plants in response to Fe deficiency. Plants grown with or without Fe and using nutrient solutions buffered at pH 5.5 or 7.5 enabled to identify an array of phenolics. These include several coumarinolignans not previously reported in A. thaliana (cleomiscosins A, B, C, and D and the 5'-hydroxycleomiscosins A and/or B), as well as some coumarin precursors (ferulic acid and coniferyl and sinapyl aldehydes), and previously reported cathecol (fraxetin) and non-cathecol coumarins (scopoletin, isofraxidin and fraxinol), some of them in hexoside forms not previously characterized. The production and secretion of phenolics were more intense when the plant accessibility to Fe was diminished and the plant Fe status deteriorated, as it occurs when plants are grown in the absence of Fe at pH 7.5. Aglycones and hexosides of the four coumarins were abundant in roots, whereas only the aglycone forms could be quantified in the nutrient solution. A comprehensive quantification of coumarins, first carried out in this study, revealed that the catechol coumarin fraxetin was predominant in exudates (but not in roots) of Fe-deficient A. thaliana plants grown at pH 7.5. Also, fraxetin was able to mobilize efficiently Fe from a Fe(III)-oxide at pH 5.5 and pH 7.5. On the other hand, non-catechol coumarins were much less efficient in mobilizing Fe and were present in much lower concentrations, making unlikely that they could play a role in Fe mobilization. The structural features of the array of coumarin type-compounds produced suggest some can mobilize Fe from the soil and others can be more efficient as allelochemicals.
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Project description:Low availability of Fe significantly limits crop yields in many parts of the world. However, it is largely unknown which genes and alleles adjust plant growth in Fe limited environments. Using natural variation of a geographically restricted panel of Arabidopsis thaliana accessions, we identify allelic variation at the FRO2 locus associated with root length under iron deficiency. We show that non-coding sequence variation at the FRO2 locus leads to variation of FRO2 transcript levels, as well as ferric chelate reductase activity, and is causal for a portion of the observed root length variation. These FRO2 allele dependent differences are coupled with altered seedling phenotypes grown on iron-limited soil. Overall, we show that these natural genetic variants of FRO2 tune its expression. These variants might be useful for improvement of agronomically relevant species under specific environmental conditions, such as in podzols or calcareous soils.
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Project description:Though central to our understanding of how roots perform their vital function of scavenging water and solutes from the soil, no direct genetic evidence currently exists to support the foundational model that suberin acts to form a chemical barrier limiting the extracellular, or apoplastic, transport of water and solutes in plant roots. Using the newly characterized enhanced suberin1 (esb1) mutant, we established a connection in Arabidopsis thaliana between suberin in the root and both water movement through the plant and solute accumulation in the shoot. Esb1 mutants, characterized by increased root suberin, were found to have reduced day time transpiration rates and increased water-use efficiency during their vegetative growth period. Furthermore, these changes in suberin and water transport were associated with decreases in the accumulation of Ca, Mn, and Zn and increases in the accumulation of Na, S, K, As, Se, and Mo in the shoot. Here, we present direct genetic evidence establishing that suberin in the roots plays a critical role in controlling both water and mineral ion uptake and transport to the leaves. The changes observed in the elemental accumulation in leaves are also interpreted as evidence that a significant component of the radial root transport of Ca, Mn, and Zn occurs in the apoplast.
| S-EPMC2679201 | biostudies-literature
Project description:Most land plants live in association with arbuscular mycorrhizal (AM) fungi and rely on this symbiosis to scavenge phosphorus (P) from soil. The ability to establish this partnership has been lost in some plant lineages like the Brassicaceae, which raises the question of what alternative nutrition strategies such plants have to grow in P-impoverished soils. To understand the contribution of plant-microbiota interactions, we studied the root-associated fungal microbiome of Arabis alpina (Brassicaceae) with the hypothesis that some of its components can promote plant P acquisition. Using amplicon sequencing of the fungal internal transcribed spacer 2, we studied the root and rhizosphere fungal communities of A. alpina growing under natural and controlled conditions including low-P soils and identified a set of 15 fungal taxa consistently detected in its roots. This cohort included a Helotiales taxon exhibiting high abundance in roots of wild A. alpina growing in an extremely P-limited soil. Consequently, we isolated and subsequently reintroduced a specimen from this taxon into its native P-poor soil in which it improved plant growth and P uptake. The fungus exhibited mycorrhiza-like traits including colonization of the root endosphere and P transfer to the plant. Genome analysis revealed a link between its endophytic lifestyle and the expansion of its repertoire of carbohydrate-active enzymes. We report the discovery of a plant-fungus interaction facilitating the growth of a nonmycorrhizal plant under native P-limited conditions, thus uncovering a previously underestimated role of root fungal microbiota in P cycling.
| S-EPMC5676915 | biostudies-literature