Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience

Etesami, Hassan; Glick, Bernard R.

doi:10.1016/j.micres.2024.127602

Cited by 42 publications

(6 citation statements)

References 307 publications

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“…Next to its pivotal role in plant growth and development ( 23 – 25 ), it regulates fungal physiology ( 67 ), microalgal growth ( 68 ), inflammatory and carcinogenic processes in animals and humans ( 69 , 70 ), and, as shown here, bacterial metabolism and physiology. Among the signals that play a major role in plant environments, IAA is emerging as a key compound, allowing plant-associated microbes to adapt efficiently to their hosts and to establish interactions with other (micro)organisms in plant niches ( 18 – 20 , 29 , 33 ). However, we are currently only at the beginning of understanding the mechanisms by which IAA regulates bacterial physiology, metabolism and social behavior.…”

Section: Discussionmentioning

confidence: 99%

“…The upregulation of the efflux pump AaeXAB in response to IAA as well as that of genes involved in capsule synthesis and with implications for antibiotic resistance may be indicative of stress. Previous studies have shown that IAA modulates different physiological and metabolic bacterial processes of importance during interaction with plants ( 19 , 20 , 33 ). For example, during plant colonization, bacteria face multiple stresses such as oxidative stress, presence of antimicrobial compounds, and adaptation to specific nutrients ( 95 – 98 ), and IAA has been shown to play a role in adapting to these and other environmental stresses ( 19 , 33 ).…”

Section: Discussionmentioning

confidence: 99%

“…In addition to its role as an inter-kingdom signal, IAA is an important bacterial signal molecule that regulates biofilm formation, primary and secondary metabolism, auxin catabolism, virulence factor production, chemotactic responses, and plant host colonization, among other processes ( 19 , 20 , 28 – 33 ). However, the molecular mechanisms underlying these regulatory processes have been identified in only a few cases, such as the IAA-mediated virulence suppression through the inhibition of phytotoxin biosynthesis ( 28 ).…”

Section: Introductionmentioning

confidence: 99%

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Auxin-mediated regulation of susceptibility to toxic metabolites, c-di-GMP levels, and phage infection in the rhizobacterium Serratia plymuthica

Rico-Jiménez,

Udaondo,

Krell

et al. 2024

mSystems

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The communication between plants and their microbiota is highly dynamic and involves a complex network of signal molecules. Among them, the auxin indole-3-acetic acid (IAA) is a critical phytohormone that not only regulates plant growth and development, but is emerging as an important inter- and intra-kingdom signal that modulates many bacterial processes that are important during interaction with their plant hosts. However, the corresponding signaling cascades remain largely unknown. Here, we advance our understanding of the largely unknown mechanisms by which IAA carries out its regulatory functions in plant-associated bacteria. We showed that IAA caused important changes in the global transcriptome of the rhizobacterium Serratia plymuthica and multidisciplinary approaches revealed that IAA sensing interferes with the signaling mediated by other pivotal plant-derived signals such as amino acids and 4-hydroxybenzoic acid. Exposure to IAA caused large alterations in the transcript levels of genes involved in amino acid metabolism, resulting in significant metabolic alterations. IAA treatment also increased resistance to toxic aromatic compounds through the induction of the AaeXAB pump, which also confers resistance to IAA. Furthermore, IAA promoted motility and severely inhibited biofilm formation; phenotypes that were associated with decreased c-di-GMP levels and capsule production. IAA increased capsule gene expression and enhanced bacterial sensitivity to a capsule-dependent phage. Additionally, IAA induced the expression of several genes involved in antibiotic resistance and led to changes in the susceptibility and responses to antibiotics with different mechanisms of action. Collectively, our study illustrates the complexity of IAA-mediated signaling in plant-associated bacteria. IMPORTANCE Signal sensing plays an important role in bacterial adaptation to ecological niches and hosts. This communication appears to be particularly important in plant-associated bacteria since they possess a large number of signal transduction systems that respond to a wide diversity of chemical, physical, and biological stimuli. IAA is emerging as a key inter- and intra-kingdom signal molecule that regulates a variety of bacterial processes. However, despite the extensive knowledge of the IAA-mediated regulatory mechanisms in plants, IAA signaling in bacteria remains largely unknown. Here, we provide insight into the diversity of mechanisms by which IAA regulates primary and secondary metabolism, biofilm formation, motility, antibiotic susceptibility, and phage sensitivity in a biocontrol rhizobacterium. This work has important implications for our understanding of bacterial ecology in plant environments and for the biotechnological and clinical applications of IAA, as well as related molecules.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Auxin-mediated regulation of susceptibility to toxic metabolites, c-di-GMP levels, and phage infection in the rhizobacterium Serratia plymuthica

Rico-Jiménez,

Udaondo,

Krell

et al. 2024

mSystems

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“…Bacteria can improve overall plant health by producing IAA that can induce root architecture alterations that enhance water and nutrient uptake ( Glick, 2012 ; Pii et al., 2015 ; Etesami et al., 2015b ). In addition, bacterial IAA helps plants mitigate abiotic stresses such as drought, salinity, and heavy metal toxicity ( Etesami and Glick, 2024 ). Besides, IAA PGPR has shown the ability for nutrient uptake, such as the ability to solubilize phosphate, nitrogen fixation, and siderophore, protease, and catalase production ( Kumar et al., 2022 ).…”

Section: Introductionmentioning

confidence: 99%

IAA-producing plant growth promoting rhizobacteria from Ceanothus velutinus enhance cutting propagation efficiency and Arabidopsis biomass

Ganesh,

Hewitt,

Devkota

et al. 2024

Front. Plant Sci.

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Climate-induced drought impacts plant growth and development. Recurring droughts increase the demand for water for food production and landscaping. Native plants in the Intermountain West region of the US are of keen interest in low water use landscaping as they are acclimatized to dry and cold environments. These native plants do very well at their native locations but are difficult to propagate in landscape. One of the possible reasons is the lack of associated microbiome in the landscaping. Microbiome in the soil contributes to soil health and impacts plant growth and development. Here, we used the bulk soil from the native plant Ceanothus velutinus (snowbrush ceanothus) as inoculant to enhance its propagation. Snowbrush ceanothus is an ornamental plant for low-water landscaping that is hard to propagate asexually. Using 50% native bulk soil as inoculant in the potting mix significantly improved the survival rate of the cuttings compared to no-treated cuttings. Twenty-four plant growth-promoting rhizobacteria (PGPR) producing indole acetic acid (IAA) were isolated from the rhizosphere and roots of the survived snowbrush. Seventeen isolates had more than 10µg/mL of IAA were shortlisted and tested for seven different plant growth-promoting (PGP) traits; 76% showed nitrogen-fixing ability on Norris Glucose Nitrogen free media,70% showed phosphate solubilization activity, 76% showed siderophore production, 36% showed protease activity, 94% showed ACC deaminase activity on DF-ACC media, 76% produced catalase and all of isolates produced ammonia. Eight of seventeen isolates, CK-6, CK-22, CK-41, CK-44, CK-47, CK-50, CK-53, and CK-55, showed an increase in shoot biomass in Arabidopsis thaliana. Seven out of eight isolates were identified as Pseudomonas, except CK-55, identified as Sphingobium based on 16S rRNA gene sequencing. The shortlisted isolates are being tested on different grain and vegetable crops to mitigate drought stress and promote plant growth.

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“…The impact of these metabolites on microbial community dynamics and plant interactions in aquatic systems has also been explored in recent research. For example, a study by Etesami & Glick [14] in coastal marshlands showed that secondary metabolites from rhizosphere bacteria significantly affect the growth patterns of both plant hosts and neighboring microbial populations, potentially influencing the overall ecosystem stability and resilience to environmental stressors.…”

Section: Introductionmentioning

confidence: 99%

Antibiosis and GC-MS of secondary metabolites of rhizosphere bacteria from Manatee foodplants in the humic freshwater ecosystem of Eniong river, Nigeria

Fatunla,

Essien,

Ita

et al. 2024

Recent Adv. Nat. Sci

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Microorganisms are able to synthesize secondary metabolites of various structures and bioactivities. These metabolites are produced to help the organism compete successfully with other organisms in their natural habitat and adapt with changing environmental milieu. The ability of rhizosphere bacteria (Bacillus subtilis NC_000964.3 and Pseu-domonas aeruginosa NC_002516.2) isolated from the rhizospheric soil of Manatee food plants Mimosa pygra, Ipomeoa aquatica and Pistia stratoites to inhibit the growth of human pathogens (P. aeruginosa, E. coli, S. aureus and B. subtilis) was evaluated using standard methods. It was observed that the growth extracts of B. subtilis strains M5, M8 and P7 and P. aeruginosa strains I3 and M9 contained useful bioactive compound. GC-MS analysis of the cell -free methanol extract of the antibiotic producing bacterial strains was also evaluated and the results showed that their inhibitory potentials against bacterial pathogens are due to the presence of phenylethyl alcohol, 2-ethyl-4-methyl-1,3-dioxolane, bicyclo [4.2.0] octa-1,3,5-triene and 4-amino-2-methyl-5,6-dimethyl pyrimidine for B. subtilis and 3,4-dimethyl tetrahydrofuran, 4,6-dimethyl-4-hydroxy-5- heptenoic acid and 2,4-dimethyl-4-heptanol for Pseudomonas aeruginosa. These strains of rhizosphere bacteria may be exploited to produce new antibiotics.

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Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience

Cited by 42 publications

References 307 publications

Auxin-mediated regulation of susceptibility to toxic metabolites, c-di-GMP levels, and phage infection in the rhizobacterium Serratia plymuthica

Auxin-mediated regulation of susceptibility to toxic metabolites, c-di-GMP levels, and phage infection in the rhizobacterium Serratia plymuthica

IAA-producing plant growth promoting rhizobacteria from Ceanothus velutinus enhance cutting propagation efficiency and Arabidopsis biomass

Antibiosis and GC-MS of secondary metabolites of rhizosphere bacteria from Manatee foodplants in the humic freshwater ecosystem of Eniong river, Nigeria

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