Impact of Bacterial Siderophores on Iron Status and Ionome in Pea

Lurthy, Tristan; Cantat, Cécile; Jeudy, Christian; Declerck, P; Gallardo, Karine; Barraud, Catherine; Leroy, Fanny; Ourry, Alain; Lemanceau, Philippe; Salon, Christophe; Mazurier, Sylvie

doi:10.3389/fpls.2020.00730

Cited by 62 publications

(51 citation statements)

References 59 publications

(69 reference statements)

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“…Beneficial Pseudomonas play key roles in soil nutrient cycles (N, P, K, C), soil health via the catabolism of several deleterious compounds (e.g., heavy metals and aromatic compounds) and the suppression of several pathogens by producing a wide range of antimicrobial compounds such as lipopeptides and antibiotics [24][25][26][27]. When associated with plants, Pseudomonas strains may potentiate its host's growth by facilitating nutrient acquisition (P, N, K, Fe) [28][29][30][31], or by the modulation of plant hormone concentrations (e.g., indoleacetic acid (IAA) biosynthesis and catabolism, biosynthesis of cytokinins, catabolism of ACC) [32][33][34][35]. Moreover, several Pseudomonas strains activate plant defense responses and induce systemic resistance through the activation of specific plant signaling mechanisms via their Microbe-Associated Molecular Patterns (MAMPs), effectors and other synthesized compounds [36].…”

Section: Pseudomonas: Common and Important Members Of The Plant Microbiomementioning

confidence: 99%

Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions

Glick

Nascimento

2021

Microorganisms

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The expression of the enzyme 1-aminocylopropane-1-carboxylate (ACC) deaminase, and the consequent modulation of plant ACC and ethylene concentrations, is one of the most important features of plant-associated bacteria. By decreasing plant ACC and ethylene concentrations, ACC deaminase-producing bacteria can overcome some of the deleterious effects of inhibitory levels of ACC and ethylene in various aspects of plant-microbe interactions, as well as plant growth and development (especially under stressful conditions). As a result, the acdS gene, encoding ACC deaminase, is often prevalent and positively selected in the microbiome of plants. Several members of the genus Pseudomonas are widely prevalent in the microbiome of plants worldwide. Due to its adaptation to a plant-associated lifestyle many Pseudomonas strains are of great interest for the development of novel sustainable agricultural and biotechnological solutions, especially those presenting ACC deaminase activity. This manuscript discusses several aspects of ACC deaminase and its role in the increased plant growth promotion, plant protection against abiotic and biotic stress and promotion of the rhizobial nodulation process by Pseudomonas. Knowledge regarding the properties and actions of ACC deaminase-producing Pseudomonas is key for a better understanding of plant-microbe interactions and the selection of highly effective strains for various applications in agriculture and biotechnology.

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Section: Pseudomonas: Common and Important Members Of The Plant Microbiomementioning

confidence: 99%

Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions

Glick

Nascimento

2021

Microorganisms

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“…In some cases, siderophores produced by rhizosphere bacteria may contribute to plant Fe nutrition. Amendment of bacterial siderophores, such as pyoverdine and ferrioxamine, have been found to promote Fe uptake by some plants (16)(17)(18). It remains unclear whether this effect is from direct assimilation of microbial siderophores by plants, ligand exchange, or reduction-based Fe uptake.…”

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confidence: 99%

Metabolic Interactions between Brachypodium and Pseudomonas fluorescens under Controlled Iron-Limited Conditions

et al. 2021

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Iron (Fe) availability has well-known effects on plant and microbial metabolism, but its effects on interspecies interactions are poorly understood. The purpose of this study was to investigate metabolite exchange between the grass Brachypodium distachyon strain Bd21 and the soil bacterium Pseudomonas fluorescens SBW25::gfp/lux (SBW25) during Fe limitation under axenic conditions. We compared the transcriptional profiles and root exudate metabolites of B. distachyon plants grown semihydroponically with and without SBW25 inoculation and Fe amendment. Liquid chromatography-mass spectrometry analysis of the hydroponic solution revealed an increase in the abundance of the phytosiderophores mugineic acid and deoxymugineic acid under Fe-limited conditions compared to Fe-replete conditions, indicating greater secretion by roots presumably to facilitate Fe uptake. In SBW25-inoculated roots, expression of genes encoding phytosiderophore biosynthesis and uptake proteins increased compared to that in sterile roots, but external phytosiderophore abundances decreased. P. fluorescens siderophores were not detected in treatments without Fe. Rather, expression of SBW25 genes encoding a porin, a transporter, and a monooxygenase was significantly upregulated in response to Fe deprivation. Collectively, these results suggest that SBW25 consumed root-exuded phytosiderophores in response to Fe deficiency, and we propose target genes that may be involved. SBW25 also altered the expression of root genes encoding defense-related enzymes and regulators, including thionin and cyanogenic glycoside production, chitinase, and peroxidase activity, and transcription factors. Our findings provide insights into the molecular bases for the stress response and metabolite exchange of interacting plants and bacteria under Fe-deficient conditions. IMPORTANCE Rhizosphere bacteria influence the growth of their host plant by consuming and producing metabolites, nutrients, and antibiotic compounds within the root system that affect plant metabolism. Under Fe-limited growth conditions, different plant and microbial species have distinct Fe acquisition strategies, often involving the secretion of strong Fe-binding chelators that scavenge Fe and facilitate uptake. Here, we studied interactions between P. fluorescens SBW25, a plant-colonizing bacterium that produces siderophores with antifungal properties, and B. distachyon, a genetic model for cereal grain and biofuel grasses. Under controlled growth conditions, bacterial siderophore production was inhibited in the root system of Fe-deficient plants, bacterial inoculation altered transcription of genes involved in defense and stress response in the roots of B. distachyon, and SBW25 degraded phytosiderophores secreted by the host plant. These findings provide mechanistic insight into interactions that may play a role in rhizosphere dynamics and plant health in soils with low Fe solubility.

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“…Specific microbial populations are counter-selected by iron competition (←Fe→), by FPC toxicity ( ), or microbial antagonism; these populations represent a source of iron (and of other nutriments) when metabolized (i). A siderophore produced by a pseudomonad strain recruited in the rhizosphere of an iron-stressed plant can also favor plant iron nutrition (j) ( Jin et al, 2010 ), and distinct pvds of different strains of Pseudomonas differently favor plant iron nutrition (k) ( Lurthy et al, 2020 ), suggesting that plant iron nutrition is impacted differently depending on the pseudomonads recruited in the rhizosphere.…”

Section: Biological Levers To Promote Plant Iron Uptake and Regulate Iron Homeostasismentioning

confidence: 99%

“…Thus, plant iron nutrition was promoted by siderophores synthesized by a Pseudomonas strain originating from the rhizosphere of Fe-deficient clover ( Jin et al, 2010 ). Also, a siderophore from a pseudomonad strain highly represented in the rhizosphere of a pea cultivar tolerant to IDC significantly improved iron nutrition of this plant ( Lurthy et al, 2020 ). Similarly, two strains ( P. simiae WCS417 and P. capeferrum WCS358) highly tolerant to the antimicrobial effect of root phenolics promoted Arabidopsis growth via siderophore production ( Figure 2 ; Berendsen et al, 2015 ; Stringlis et al, 2018 ).…”

Section: Consequences For the Development Of Iron Biofortification Strategiesmentioning

confidence: 99%

Importance of the Rhizosphere Microbiota in Iron Biofortification of Plants

et al. 2021

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Increasing the iron content of plant products and iron assimilability represents a major issue for human nutrition and health. This is also a major challenge because iron is not readily available for plants in most cultivated soils despite its abundance in the Earth’s crust. Iron biofortification is defined as the enhancement of the iron content in edible parts of plants. This biofortification aims to reach the objectives defined by world organizations for human nutrition and health while being environment friendly. A series of options has been proposed to enhance plant iron uptake and fight against hidden hunger, but they all show limitations. The present review addresses the potential of soil microorganisms to promote plant iron nutrition. Increasing knowledge on the plant microbiota and plant-microbe interactions related to the iron dynamics has highlighted a considerable contribution of microorganisms to plant iron uptake and homeostasis. The present overview of the state of the art sheds light on plant iron uptake and homeostasis, and on the contribution of plant-microorganism (plant-microbe and plant-plant-microbe) interactions to plant nutritition. It highlights the effects of microorganisms on the plant iron status and on the co-occurring mechanisms, and shows how this knowledge may be valued through genetic and agronomic approaches. We propose a change of paradigm based on a more holistic approach gathering plant and microbial traits mediating iron uptake. Then, we present the possible applications in plant breeding, based on plant traits mediating plant-microbe interactions involved in plant iron uptake and physiology.

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Impact of Bacterial Siderophores on Iron Status and Ionome in Pea

Cited by 62 publications

References 59 publications

Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions

Pseudomonas 1-Aminocyclopropane-1-carboxylate (ACC) Deaminase and Its Role in Beneficial Plant-Microbe Interactions

Metabolic Interactions between Brachypodium and Pseudomonas fluorescens under Controlled Iron-Limited Conditions

Importance of the Rhizosphere Microbiota in Iron Biofortification of Plants

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