Publications by authors named "Corné M J Pieterse"

125 Publications

Experimental-Evolution-Driven Identification of Rhizosphere Competence Genes in Pseudomonas protegens.

mBio 2021 Jun 8:e0092721. Epub 2021 Jun 8.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, The Netherlands.

Beneficial plant root-associated microorganisms carry out a range of functions that are essential for plant performance. Establishment of a bacterium on plant roots, however, requires overcoming several challenges, including competition with neighboring microorganisms and host immunity. Forward and reverse genetics have led to the identification of mechanisms that are used by beneficial microorganisms to overcome these challenges, such as the production of iron-chelating compounds, the formation of strong biofilms, or the concealment of characteristic microbial molecular patterns that trigger the host immune system. However, how such mechanisms arose from an evolutionary perspective is much less understood. To study bacterial adaptation in the rhizosphere, we employed experimental evolution to track the physiological and genetic dynamics of root-dwelling Pseudomonas protegens in the Arabidopsis thaliana rhizosphere under axenic conditions. This simplified binary one plant/one bacterium system allows for the amplification of key adaptive mechanisms for bacterial rhizosphere colonization. We identified 35 mutations, including single-nucleotide polymorphisms, insertions, and deletions, distributed over 28 genes. We found that mutations in genes encoding global regulators and in genes for siderophore production, cell surface decoration, attachment, and motility accumulated in parallel, underlining the finding that bacterial adaptation to the rhizosphere follows multiple strategies. Notably, we observed that motility increased in parallel across multiple independent evolutionary lines. All together, these results underscore the strength of experimental evolution in identifying key genes, pathways, and processes for bacterial rhizosphere colonization and a methodology for the development of elite beneficial microorganisms with enhanced root-colonizing capacities that can support sustainable agriculture in the future. Beneficial root-associated microorganisms carry out many functions that are essential for plant performance. Establishment of a bacterium on plant roots, however, requires overcoming many challenges. Previously, diverse mechanisms that are used by beneficial microorganisms to overcome these challenges were identified. However, how such mechanisms have developed from an evolutionary perspective is much less understood. Here, we employed experimental evolution to track the evolutionary dynamics of a root-dwelling pseudomonad on the root of . We found that mutations in global regulators, as well as in genes for siderophore production, cell surface decoration, attachment, and motility, accumulate in parallel, emphasizing these strategies for bacterial adaptation to the rhizosphere. We identified 35 mutations distributed over 28 genes. All together, our results demonstrate the power of experimental evolution in identifying key pathways for rhizosphere colonization and a methodology for the development of elite beneficial microorganisms that can support sustainable agriculture.
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http://dx.doi.org/10.1128/mBio.00927-21DOI Listing
June 2021

Evolutionary "hide and seek" between bacterial flagellin and the plant immune system.

Cell Host Microbe 2021 04;29(4):548-550

Plant-Microbe Interactions, Department of Biology, Science for Life, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands.

Bacterial flagellin is a potent host immune activator. Parys et al. (2021) and Colaianni et al. (2021) dissected effects of flagellin epitope variants on host immune detection and bacterial motility. They report in this issue of Cell Host & Microbe that Arabidopsis-associated bacterial microbiota differentially evolved flg22 variants that allow tunability between motility and defense activation.
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http://dx.doi.org/10.1016/j.chom.2021.03.010DOI Listing
April 2021

A family of pathogen-induced cysteine-rich transmembrane proteins is involved in plant disease resistance.

Planta 2021 Apr 15;253(5):102. Epub 2021 Apr 15.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, 800.56, 3508 TB, Utrecht, The Netherlands.

Main Conclusion: Overexpression of pathogen-induced cysteine-rich transmembrane proteins (PCMs) in Arabidopsis thaliana enhances resistance against biotrophic pathogens and stimulates hypocotyl growth, suggesting a potential role for PCMs in connecting both biological processes. Plants possess a sophisticated immune system to protect themselves against pathogen attack. The defense hormone salicylic acid (SA) is an important player in the plant immune gene regulatory network. Using RNA-seq time series data of Arabidopsis thaliana leaves treated with SA, we identified a largely uncharacterized SA-responsive gene family of eight members that are all activated in response to various pathogens or their immune elicitors and encode small proteins with cysteine-rich transmembrane domains. Based on their nucleotide similarity and chromosomal position, the designated Pathogen-induced Cysteine-rich transMembrane protein (PCM) genes were subdivided into three subgroups consisting of PCM1-3 (subgroup I), PCM4-6 (subgroup II), and PCM7-8 (subgroup III). Of the PCM genes, only PCM4 (also known as PCC1) has previously been implicated in plant immunity. Transient expression assays in Nicotiana benthamiana indicated that most PCM proteins localize to the plasma membrane. Ectopic overexpression of the PCMs in Arabidopsis thaliana resulted in all eight cases in enhanced resistance against the biotrophic oomycete pathogen Hyaloperonospora arabidopsidis Noco2. Additionally, overexpression of PCM subgroup I genes conferred enhanced resistance to the hemi-biotrophic bacterial pathogen Pseudomonas syringae pv. tomato DC3000. The PCM-overexpression lines were found to be also affected in the expression of genes related to light signaling and development, and accordingly, PCM-overexpressing seedlings displayed elongated hypocotyl growth. These results point to a function of PCMs in both disease resistance and photomorphogenesis, connecting both biological processes, possibly via effects on membrane structure or activity of interacting proteins at the plasma membrane.
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http://dx.doi.org/10.1007/s00425-021-03606-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8049917PMC
April 2021

A coumarin exudation pathway mitigates arbuscular mycorrhizal incompatibility in Arabidopsis thaliana.

Plant Mol Biol 2021 Apr 6. Epub 2021 Apr 6.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.

Key Message: Overexpression of genes involved in coumarin production and secretion can mitigate mycorrhizal incompatibility in nonhost Arabidopsis plants. The coumarin scopoletin, in particular, stimulates pre-penetration development and metabolism in mycorrhizal fungi. Although most plants can benefit from mutualistic associations with arbuscular mycorrhizal (AM) fungi, nonhost plant species such as the model Arabidopsis thaliana have acquired incompatibility. The transcriptional response of Arabidopsis to colonization by host-supported AM fungi switches from initial AM recognition to defense activation and plant growth antagonism. However, detailed functional information on incompatibility in nonhost-AM fungus interactions is largely missing. We studied interactions between host-sustained AM fungal networks of Rhizophagus irregularis and 18 Arabidopsis genotypes affected in nonhost penetration resistance, coumarin production and secretion, and defense (salicylic acid, jasmonic acid, and ethylene) and growth hormones (auxin, brassinosteroid, cytokinin, and gibberellin). We demonstrated that root-secreted coumarins can mitigate incompatibility by stimulating fungal metabolism and promoting initial steps of AM colonization. Moreover, we provide evidence that major molecular defenses in Arabidopsis do not operate as primary mechanisms of AM incompatibility nor of growth antagonism. Our study reveals that, although incompatible, nonhost plants can harbor hidden tools that promote initial steps of AM colonization. Moreover, it uncovered the coumarin scopoletin as a novel signal in the pre-penetration dialogue, with possible implications for the chemical communication in plant-mycorrhizal fungi associations.
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http://dx.doi.org/10.1007/s11103-021-01143-xDOI Listing
April 2021

Transcriptome Signatures in WCS417 Shed Light on Role of Root-Secreted Coumarins in -Mutualist Communication.

Microorganisms 2021 Mar 11;9(3). Epub 2021 Mar 11.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands.

WCS417 is a root-colonizing bacterium with well-established plant-beneficial effects. Upon colonization of 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 -WCS417 interaction, we analyzed the transcriptome of WCS417 growing in root exudates of coumarin-producing Col-0 and the coumarin-biosynthesis mutant . 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.
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http://dx.doi.org/10.3390/microorganisms9030575DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8000642PMC
March 2021

The Induced Resistance Lexicon: Do's and Don'ts.

Trends Plant Sci 2021 Jul 30;26(7):685-691. Epub 2021 Jan 30.

Department of Biotechnology, Faculty of Bioscience Engineering, Ghent University, 9000 Ghent, Belgium. Electronic address:

To be protected from biological threats, plants have evolved an immune system comprising constitutive and inducible defenses. For example, upon perception of certain stimuli, plants can develop a conditioned state of enhanced defensive capacity against upcoming pathogens and pests, resulting in a phenotype called 'induced resistance' (IR). To tackle the confusing lexicon currently used in the IR field, we propose a widely applicable code of practice concerning the terminology and description of IR phenotypes using two main phenotypical aspects: local versus systemic resistance, and direct versus primed defense responses. Our general framework aims to improve uniformity and consistency in future scientific communication, which should help to avoid further misinterpretations and facilitate the accessibility and impact of this research field.
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http://dx.doi.org/10.1016/j.tplants.2021.01.001DOI Listing
July 2021

Aphid feeding induces the relaxation of epigenetic control and the associated regulation of the defense response in Arabidopsis.

New Phytol 2021 05 15;230(3):1185-1200. Epub 2021 Feb 15.

Department of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences and Linnean Center for Plant Biology, Uppsala, 75007, Sweden.

Environmentally induced changes in the epigenome help individuals to quickly adapt to fluctuations in the conditions of their habitats. We explored those changes in Arabidopsis thaliana plants subjected to multiple biotic and abiotic stresses, and identified transposable element (TE) activation in plants infested with the green peach aphid, Myzus persicae. We performed a genome-wide analysis mRNA expression, small RNA accumulation and DNA methylation Our results demonstrate that aphid feeding induces loss of methylation of hundreds of loci, mainly TEs. This loss of methylation has the potential to regulate gene expression and we found evidence that it is involved in the control of plant immunity genes. Accordingly, mutant plants deficient in DNA and H3K9 methylation (kyp) showed increased resistance to M. persicae infestation. Collectively, our results show that changes in DNA methylation play a significant role in the regulation of the plant transcriptional response and induction of defense response against aphid feeding.
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http://dx.doi.org/10.1111/nph.17226DOI Listing
May 2021

Mechanisms underlying iron deficiency-induced resistance against pathogens with different lifestyles.

J Exp Bot 2021 03;72(6):2231-2241

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Padualaan, CH Utrecht, The Netherlands.

Iron (Fe) is a poorly available mineral nutrient which affects the outcome of many cross-kingdom interactions. In Arabidopsis thaliana, Fe starvation limits infection by necrotrophic pathogens. Here, we report that Fe deficiency also reduces disease caused by the hemi-biotrophic bacterium Pseudomonas syringae and the biotrophic oomycete Hyaloperonospora arabidopsidis, indicating that Fe deficiency-induced resistance is effective against pathogens with different lifestyles. Furthermore, we show that Fe deficiency-induced resistance is not caused by withholding Fe from the pathogen but is a plant-mediated defense response that requires activity of ethylene and salicylic acid. Because rhizobacteria-induced systemic resistance (ISR) is associated with a transient up-regulation of the Fe deficiency response, we tested whether Fe deficiency-induced resistance and ISR are similarly regulated. However, Fe deficiency-induced resistance functions independently of the ISR regulators MYB72 and BGLU42, indicating that both types of induced resistance are regulated in a different manner. Mutants opt3 and frd1, which display misregulated Fe homeostasis under Fe-sufficient conditions, show disease resistance levels comparable with those of Fe-starved wild-type plants. Our results suggest that disturbance of Fe homeostasis, through Fe starvation stress or other non-homeostatic conditions, is sufficient to prime the plant immune system for enhanced defense.
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http://dx.doi.org/10.1093/jxb/eraa535DOI Listing
March 2021

Collection of Sterile Root Exudates from Foliar Pathogen-Inoculated Plants.

Methods Mol Biol 2021 ;2232:305-317

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, The Netherlands.

In nature and agriculture, plants interact with an astonishing number of microbes, collectively referred to as the "plant microbiome." Roots are a microbial hotspot where beneficial plant-microbe interactions are established that support plant growth and provide protection against pathogens and insects. Recently, we discovered that in response to foliar pathogen attack, plant roots can recruit specific protective microbes into the rhizosphere. Root exudates play an essential role in the interaction between plant roots and rhizosphere microbiota. In order to study the chemical communication between plant roots and the rhizosphere microbiome, it is essential to study the metabolite profile of root exudates. Here, we describe a detailed protocol for the collection of sterile root exudates that are secreted by Arabidopsis thaliana roots in response to inoculation of the leaves with the biotrophic pathogen Hyaloperonospora arabidopsidis.
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http://dx.doi.org/10.1007/978-1-0716-1040-4_23DOI Listing
March 2021

Soil-Borne Legacies of Disease in Arabidopsis thaliana.

Methods Mol Biol 2021 ;2232:209-218

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, The Netherlands.

The rhizosphere microbiome of plants is essential for plant growth and health. Recent studies have shown that upon infection of leaves with a foliar pathogen, the composition of the root microbiome is altered and enriched with bacteria that in turn can systemically protect the plant against the foliar pathogen. This protective effect is extended to successive populations of plants that are grown on soil that was first conditioned by pathogen-infected plants, a phenomenon that was coined "the soil-borne legacy." Here we provide a detailed protocol for soil-borne legacy experiments with the model plant Arabidopsis thaliana after infection with the obligate biotrophic pathogen Hyaloperonospora arabidopsidis. This protocol can easily be extended to infection with other pathogens or even infestation with herbivorous insects and can function as a blueprint for soil-borne legacy experiments with crop species.
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http://dx.doi.org/10.1007/978-1-0716-1040-4_17DOI Listing
March 2021

Coumarin Communication Along the Microbiome-Root-Shoot Axis.

Trends Plant Sci 2021 02 3;26(2):169-183. Epub 2020 Oct 3.

Plant-Microbe Interactions, Department of Biology, Science for Life, Utrecht University, Padualaan 8, 3584, CH, Utrecht, The Netherlands. Electronic address:

Plants shape their rhizosphere microbiome by secreting root exudates into the soil environment. Recently, root-exuded coumarins were identified as novel players in plant-microbiome communication. Beneficial members of the root-associated microbiome stimulate coumarin biosynthesis in roots and their excretion into the rhizosphere. The iron-mobilizing activity of coumarins facilitates iron uptake from the soil environment, while their selective antimicrobial activity shapes the root microbiome, resulting in promotion of plant growth and health. Evidence is accumulating that, in analogy to strigolactones and flavonoids, coumarins may act in microbiome-to-root-to-shoot signaling events. Here, we review this multifaceted role of coumarins in bidirectional chemical communication along the microbiome-root-shoot axis.
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http://dx.doi.org/10.1016/j.tplants.2020.09.008DOI Listing
February 2021

The Soil-Borne Identity and Microbiome-Assisted Agriculture: Looking Back to the Future.

Mol Plant 2020 10 29;13(10):1394-1401. Epub 2020 Sep 29.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Padualaan 8, 3584 CH Utrecht, the Netherlands.

Looking forward includes looking back every now and then. In 2007, David Weller looked back at 30 years of biocontrol of soil-borne pathogens by Pseudomonas and signified that the progress made over decades of research has provided a firm foundation to formulate current and future research questions. It has been recognized for more than a century that soil-borne microbes play a significant role in plant growth and health. The recent application of high-throughput omics technologies has enabled detailed dissection of the microbial players and molecular mechanisms involved in the complex interactions in plant-associated microbiomes. Here, we highlight old and emerging plant microbiome concepts related to plant disease control, and address perspectives that modern and emerging microbiomics technologies can bring to functionally characterize and exploit plant-associated microbiomes for the benefit of plant health in future microbiome-assisted agriculture.
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http://dx.doi.org/10.1016/j.molp.2020.09.017DOI Listing
October 2020

Editorial: New Horizons in Food Science via Agricultural Immunity.

Front Nutr 2020 28;7:19. Epub 2020 Feb 28.

Department of Veterinary Medicine, Utrecht University, Utrecht, Netherlands.

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http://dx.doi.org/10.3389/fnut.2020.00019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7093008PMC
February 2020

Carbonic anhydrases CA1 and CA4 function in atmospheric CO-modulated disease resistance.

Planta 2020 Mar 7;251(4):75. Epub 2020 Mar 7.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Padualaan 8, 3584 CH, Utrecht, the Netherlands.

Main Conclusion: Carbonic anhydrases CA1 and CA4 attenuate plant immunity and can contribute to altered disease resistance levels in response to changing atmospheric CO conditions. β-Carbonic anhydrases (CAs) play an important role in CO metabolism and plant development, but have also been implicated in plant immunity. Here we show that the bacterial pathogen Pseudomonas syringae and application of the microbe-associated molecular pattern (MAMP) flg22 repress CA1 and CA4 gene expression in Arabidopsis thaliana. Using the CA double-mutant ca1ca4, we provide evidence that CA1 and CA4 play an attenuating role in pathogen- and flg22-triggered immune responses. In line with this, ca1ca4 plants exhibited enhanced resistance against P. syringae, which was accompanied by an increased expression of the defense-related genes FRK1 and ICS1. Under low atmospheric CO conditions (150 ppm), when CA activity is typically low, the levels of CA1 transcription and resistance to P. syringae in wild-type Col-0 were similar to those observed in ca1ca4. However, under ambient (400 ppm) and elevated (800 ppm) atmospheric CO conditions, CA1 transcription was enhanced and resistance to P. syringae reduced. Together, these results suggest that CA1 and CA4 attenuate plant immunity and that differential CA gene expression in response to changing atmospheric CO conditions contribute to altered disease resistance levels.
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http://dx.doi.org/10.1007/s00425-020-03370-wDOI Listing
March 2020

Bioassays to Evaluate the Resistance of Whole Plants to the Herbivorous Insect Thrips.

Methods Mol Biol 2020 ;2085:93-108

Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University, Utrecht, The Netherlands.

Thrips are tiny, cell-content-feeding insects that are a major pest on crops and ornamentals. Besides causing direct feeding damage, thrips may also cause indirect damage by vectoring tospoviruses. Novel resistance mechanisms to thrips need to be discovered and validated. Induction of jasmonic acid-dependent defenses has been demonstrated to be essential for resistance to thrips, but underlying mechanisms still need to be discovered. For this, it is vital to use robust plant-thrips assays to analyze plant defense responses and thrips performance. In recently developed high-throughput phenotyping platforms, the feeding damage that is visible as silver spots, and the preference of thrips in a two-choice setup is assessed, using leaf discs. Here, we describe whole-plant thrips assays that are essential for (1) validation of findings obtained by the leaf disc assays, (2) assessment of longer-term effects on thrips feeding success and fecundity, (3) determination of spatial-temporal effects induced by primary thrips infestation on a secondary attack by thrips or other insects or pathogens, and (4) assessment of gene expression and metabolite changes. We present detailed methods and tips and tricks for (a) rearing and selection of thrips at different developmental stages, (b) treatment of the whole plant or an individual leaf with thrips, and (c) determination of feeding damage and visualization of thrips oviposition success in leaves.
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http://dx.doi.org/10.1007/978-1-0716-0142-6_7DOI Listing
December 2020

Rhizosphere-Associated Pseudomonas Suppress Local Root Immune Responses by Gluconic Acid-Mediated Lowering of Environmental pH.

Curr Biol 2019 11 24;29(22):3913-3920.e4. Epub 2019 Oct 24.

Plant-Microbe Interactions, Institute of Environmental Biology, Department of Biology, Science4Life, Utrecht University, 3508 CH Utrecht, the Netherlands. Electronic address:

The root microbiome consists of commensal, pathogenic, and plant-beneficial microbes [1]. Most members of the root microbiome possess microbe-associated molecular patterns (MAMPs) similar to those of plant pathogens [2]. Their recognition can lead to the activation of host immunity and suppression of plant growth due to growth-defense tradeoffs [3, 4]. We found that 42% of the tested root microbiota, including the plant growth-promoting rhizobacteria Pseudomonas capeferrum WCS358 [5, 6] and Pseudomonas simiae WCS417 [6, 7], are able to quench local Arabidopsis thaliana root immune responses that are triggered by flg22 [8], an immunogenic epitope of the MAMP flagellin [9], suggesting that this is an important function of the root microbiome. In a screen for WCS358 mutants that lost their capacity to suppress flg22-induced CYP71A12:GUS MAMP-reporter gene expression, we identified the bacterial genes pqqF and cyoB in WCS358, which are required for the production of gluconic acid and its derivative 2-keto gluconic acid. Both WCS358 mutants are impaired in the production of these organic acids and consequently lowered their extracellular pH to a lesser extent than wild-type WCS358. Acidification of the plant growth medium similarly suppressed flg22-induced CYP71A12:GUS and MYB51:GUS expression, and the flg22-mediated oxidative burst, suggesting a role for rhizobacterial gluconic acid-mediated modulation of the extracellular pH in the suppression of root immunity. Rhizosphere population densities of the mutants were significantly reduced compared to wild-type. Collectively, these findings show that suppression of immune responses is an important function of the root microbiome, as it facilitates colonization by beneficial root microbiota.
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http://dx.doi.org/10.1016/j.cub.2019.09.015DOI Listing
November 2019

Editorial: Harnessing Useful Rhizosphere Microorganisms for Pathogen and Pest Biocontrol - Second Edition.

Front Microbiol 2019 28;10:1935. Epub 2019 Aug 28.

Instituto de Agricultura Sostenible, Agencia Estatal Consejo Superior de Investigaciones Científicas, Córdoba, Spain.

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http://dx.doi.org/10.3389/fmicb.2019.01935DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6724568PMC
August 2019

Type III Secretion System of Beneficial Rhizobacteria WCS417 and WCS374.

Front Microbiol 2019 16;10:1631. Epub 2019 Jul 16.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, Netherlands.

Plants roots host myriads of microbes, some of which enhance the defense potential of plants by activating a broad-spectrum immune response in leaves, known as induced systemic resistance (ISR). Nevertheless, establishment of this mutualistic interaction requires active suppression of local root immune responses to allow successful colonization. To facilitate host colonization, phytopathogenic bacteria secrete immune-suppressive effectors into host cells via the type III secretion system (T3SS). Previously, we searched the genomes of the ISR-inducing rhizobacteria WCS417 and WCS374 for the presence of a T3SS and identified the components for a T3SS in the genomes of WCS417 and WCS374. By performing a phylogenetic and gene cluster alignment analysis we show that the T3SS of WCS417 and WCS374 are grouped in a clade that is enriched for beneficial rhizobacteria. We also found sequences of putative novel effectors in their genomes, which may facilitate future research on the role of T3SS effectors in plant-beneficial microbe interactions in the rhizosphere.
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http://dx.doi.org/10.3389/fmicb.2019.01631DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6647874PMC
July 2019

Rhizobacteria-Mediated Activation of the Fe Deficiency Response in Arabidopsis Roots: Impact on Fe Status and Signaling.

Front Plant Sci 2019 12;10:909. Epub 2019 Jul 12.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, Netherlands.

The beneficial root-colonizing rhizobacterium WCS417 stimulates plant growth and induces systemic resistance against a broad spectrum of plant diseases. In (Arabidopsis), the root transcriptional response to WCS417 shows significant overlap with the root response to iron (Fe) starvation, including activation of the marker genes and . Here, we investigated how colonization of Arabidopsis roots by WCS417 impacts Fe homeostasis in roots and shoots. Under Fe-sufficient conditions, root colonization by WCS417 induced a transient Fe deficiency response in the root and elevated both the total amount of Fe in the shoot and the shoot fresh weight. When plants were grown under Fe-starvation conditions, WCS417 still promoted plant growth, but did not increase the total amount of Fe, resulting in chlorosis. Thus, increased Fe uptake in response to WCS417 is essential to maintain Fe homeostasis in the more rapidly growing plant. As the WCS417-induced Fe deficiency response is known to require a shoot-derived signal, we tested whether the Fe deficiency response is activated in response to an increased Fe demand in the more rapidly growing shoot. Exogenous application of Fe to the leaves to reduce a potential shoot Fe shortage did not prevent WCS417-mediated induction of the Fe deficiency response in the roots. Moreover, the leaf Fe status-dependent shoot-to-root signaling mutant , which is impaired in the phloem-specific Fe transporter OPT3, still up-regulated the Fe deficiency response genes and in response to WCS417. Collectively, our results suggest that the WCS417-induced Fe deficiency response in the root is controlled by a shoot-to-root signaling system that functions independently of both leaf Fe status and OPT3.
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http://dx.doi.org/10.3389/fpls.2019.00909DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6639660PMC
July 2019

Beneficial microbes going underground of root immunity.

Plant Cell Environ 2019 10 5;42(10):2860-2870. Epub 2019 Aug 5.

Plant-Microbe Interactions, Institute of Environmental Biology, Department of Biology, Science4Life, Utrecht University, Utrecht, 3508, TB, The Netherlands.

Plant roots interact with an enormous diversity of commensal, mutualistic, and pathogenic microbes, which poses a big challenge to roots to distinguish beneficial microbes from harmful ones. Plants can effectively ward off pathogens following immune recognition of conserved microbe-associated molecular patterns (MAMPs). However, such immune elicitors are essentially not different from those of neutral and beneficial microbes that are abundantly present in the root microbiome. Recent studies indicate that the plant immune system plays an active role in influencing rhizosphere microbiome composition. Moreover, it has become increasingly clear that root-invading beneficial microbes, including rhizobia and arbuscular mycorrhiza, evade or suppress host immunity to establish a mutualistic relationship with their host. Evidence is accumulating that many free-living rhizosphere microbiota members can suppress root immune responses, highlighting root immune suppression as an important function of the root microbiome. Thus, the gate keeping functions of the plant immune system are not restricted to warding off root-invading pathogens but also extend to rhizosphere microbiota, likely to promote colonization by beneficial microbes and prevent growth-defense tradeoffs triggered by the MAMP-rich rhizosphere environment.
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http://dx.doi.org/10.1111/pce.13632DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6851990PMC
October 2019

Molecular dialogue between arbuscular mycorrhizal fungi and the nonhost plant Arabidopsis thaliana switches from initial detection to antagonism.

New Phytol 2019 07 13;223(2):867-881. Epub 2019 Apr 13.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, 3508 TB, Utrecht, the Netherlands.

Approximately 29% of all vascular plant species are unable to establish an arbuscular mycorrhizal (AM) symbiosis. Despite this, AM fungi (Rhizophagus spp.) are enriched in the root microbiome of the nonhost Arabidopsis thaliana, and Arabidopsis roots become colonized when AM networks nurtured by host plants are available. Here, we investigated the nonhost-AM fungus interaction by analyzing transcriptional changes in Rhizophagus, Arabidopsis and the host plant Medicago truncatula while growing in the same mycorrhizal network. In early interaction stages, Rhizophagus activated the Arabidopsis strigolactone biosynthesis genes CCD7 and CCD8, suggesting that detection of AM fungi is not completely impaired. However, in colonized Arabidopsis roots, fungal nutrient transporter genes GintPT, GintAMT2, GintMST2 and GintMST4, essential for AM symbiosis, were not activated. RNA-seq transcriptome analysis pointed to activation of costly defenses in colonized Arabidopsis roots. Moreover, Rhizophagus colonization caused a 50% reduction in shoot biomass, but also led to enhanced systemic immunity against Botrytis cinerea. This suggests that early signaling between AM fungi and Arabidopsis is not completely impaired and that incompatibility appears at later interaction stages. Moreover, Rhizophagus-mediated defenses coincide with reduced Arabidopsis growth, but also with systemic disease resistance, highlighting the multifunctional role of AM fungi in host and nonhost interactions.
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http://dx.doi.org/10.1111/nph.15798DOI Listing
July 2019

Mining the natural genetic variation in Arabidopsis thaliana for adaptation to sequential abiotic and biotic stresses.

Planta 2019 Apr 14;249(4):1087-1105. Epub 2018 Dec 14.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, PO Box 80056, 3508 TB, Utrecht, The Netherlands.

Main Conclusion: In this genome-wide association study, we obtained novel insights into the genetic basis of the effect of herbivory or drought stress on the level of resistance against the fungus Botrytis cinerea. In nature, plants function in complex environments where they encounter different biotic and abiotic stresses individually, sequentially or simultaneously. The adaptive response to a single stress does not always reflect how plants respond to such a stress in combination with other stresses. To identify genetic factors that contribute to the plant's ability to swiftly adapt to different stresses, we investigated the response of Arabidopsis thaliana to infection by the necrotrophic fungus B. cinerea when preceded by Pieris rapae herbivory or drought stress. Using 346 natural A. thaliana accessions, we found natural genetic variation in the level of resistance against single B. cinerea infection. When preceded by herbivory or drought stress, the level of B. cinerea resistance was differentially influenced in the 346 accessions. To study the genetic factors contributing to the differential adaptation of A. thaliana to B. cinerea infection under multi-stress conditions, we performed a genome-wide association study supported by quantitative trait loci mapping and fine mapping with full genome sequences of 164 accessions. This yielded several genes previously associated with defense to B. cinerea and additional candidate genes with putative roles in the plant's adaptive response to a combination of herbivory, drought and B. cinerea infection.
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http://dx.doi.org/10.1007/s00425-018-3065-9DOI Listing
April 2019

Corrigendum: How Can We Define "Optimal Microbiota?": A Comparative Review of Structure and Functions of Microbiota of Animals, Fish, and Plants in Agriculture.

Front Nutr 2018 28;5:113. Epub 2018 Nov 28.

Plant-Microbe Interactions, Department of Biology, Science4Life Utrecht University, Utrecht, Netherlands.

[This corrects the article DOI: 10.3389/fnut.2018.00090.].
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http://dx.doi.org/10.3389/fnut.2018.00113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6279912PMC
November 2018

Combining QTL mapping with transcriptome and metabolome profiling reveals a possible role for ABA signaling in resistance against the cabbage whitefly in cabbage.

PLoS One 2018 6;13(11):e0206103. Epub 2018 Nov 6.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, the Netherlands.

Whiteflies are among the world's most significant agricultural pests and chemical insecticides are extensively used to reduce crop damage to acceptable levels. However, nearly all insecticides pose a threat to the environment and alternative control methods, such as breeding of crop varieties that are inherently insect-resistant, are needed. Previously, a strong source of plant-age dependent resistance to the cabbage whitefly (Aleyrodes proletella) has been identified in the modern white cabbage (Brassica oleracea var. capitata) variety Rivera. However, nothing is known about the molecular mechanisms or the genes involved in this resistance. In the present study, a multidisciplinary approach combining transcriptome and metabolome profiling with genetic mapping was used to identify the molecular players of whitefly resistance in cabbage. Transcriptome profiles of young (susceptible) and older (resistant) Rivera plants were analyzed using RNA sequencing. While many genes involved in general processes were differentially expressed between both ages, several defense-related processes were overrepresented in the transcriptome profile of older plants. Hormone measurements revealed that jasmonic acid (JA) levels decreased upon whitefly infestation at both plant ages. Interestingly, abscisic acid (ABA) levels showed contrasting effects in response to whitefly infestation: ABA levels were reduced in young plants but induced in older plants upon whitefly feeding. Auxin levels were significantly lower in older plants compared with young plants, independent of whitefly presence, while glucosinolate levels were higher. Additionally, whitefly performance was monitored in an F2 population derived from a cross between Rivera and the susceptible white cabbage variety Christmas Drumhead. Significant QTL intervals were mapped on chromosome 2 and 9 for oviposition rate and whitefly adult survival, respectively. Several genes that were higher expressed in older plants and located in the identified QTL intervals were orthologous to Arabidopsis genes that have been related to ABA signaling, suggesting a role for ABA in the regulation of resistance towards whiteflies. Our results show that combining different omics approaches is a useful strategy to identify candidate genes underlying insect resistance.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0206103PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6219772PMC
April 2019

How Can We Define "Optimal Microbiota?": A Comparative Review of Structure and Functions of Microbiota of Animals, Fish, and Plants in Agriculture.

Front Nutr 2018 2;5:90. Epub 2018 Oct 2.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, Netherlands.

All multicellular organisms benefit from their own microbiota, which play important roles in maintaining the host nutritional health and immunity. Recently, the number of studies on the microbiota of animals, fish, and plants of economic importance is rapidly expanding and there are increasing expectations that productivity and sustainability in agricultural management can be improved by microbiota manipulation. However, optimizing microbiota is still a challenging task because of the lack of knowledge on the dominant microorganisms or significant variations between microbiota, reflecting sampling biases, different agricultural management as well as breeding backgrounds. To offer a more generalized view on microbiota in agriculture, which can be used for defining criteria of "optimal microbiota" as the goal of manipulation, we summarize here current knowledge on microbiota on animals, fish, and plants with emphasis on bacterial community structure and metabolic functions, and how microbiota can be affected by domestication, conventional agricultural practices, and use of antimicrobial agents. Finally, we discuss future tasks for defining "optimal microbiota," which can improve host growth, nutrition, and immunity and reduce the use of antimicrobial agents in agriculture.
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http://dx.doi.org/10.3389/fnut.2018.00090DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6176000PMC
October 2018

Receptors and Signaling Pathways for Recognition of Bacteria in Livestock and Crops: Prospects for Beneficial Microbes in Healthy Growth Strategies.

Front Immunol 2018 27;9:2223. Epub 2018 Sep 27.

Laboratory of Plant Pathology, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.

Modern animal and crop production practices are associated with the regular use of antimicrobials, potentially increasing selection pressure on bacteria to become resistant. Alternative approaches are needed in order to satisfy the demands of the growing human population without the indiscriminate use of antimicrobials. Researchers have brought a different perspective to solve this problem and have emphasized the exploitation of animal- and plant-associated microorganisms that are beneficial to their hosts through the modulation of the innate immune system. There is increasing evidence that plants and animals employ microbial perception and defense pathways that closely resemble each other. Formation of pattern recognition receptor (PRR) complexes involving leucine-rich repeat (LRR)-containing proteins, mitogen-activated protein kinase (MAPK)-mediated activation of immune response genes, and subsequent production of antimicrobial products and reactive oxygen species (ROS) and nitric oxide (NO) to improve defenses against pathogens, add to the list of similarities between both systems. Recent pioneering work has identified that animal and plant cells use similar receptors for sensing beneficial commensal microbes that are important for the maintenance of the host's health. Here, we reviewed the current knowledge about the molecular mechanisms involved in the recognition of pathogenic and commensal microbes by the innate immune systems of animal and plants highlighting their differences and similarities. In addition, we discuss the idea of using beneficial microbes to modulate animal and plant immune systems in order to improve the resistance to infections and reduce the use of antimicrobial compounds.
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http://dx.doi.org/10.3389/fimmu.2018.02223DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6170637PMC
October 2019

Abundantly Present miRNAs in Milk-Derived Extracellular Vesicles Are Conserved Between Mammals.

Front Nutr 2018 18;5:81. Epub 2018 Sep 18.

Department of Biochemistry and Cell Biology, Faculty of Veterinary Medicine Utrecht University, Utrecht, Netherlands.

Mammalian milk is not only a source of nutrition for the newborn, but also contains various components that regulate further development. For instance, milk is an abundant source of microRNAs (miRNAs), which are evolutionary conserved small non-coding RNAs that are involved in post-transcriptional regulation of target mRNA. MiRNAs present in milk can occur in extracellular vesicles (EVs), which are nanosized membrane vesicles released by many cell types as a means of intercellular communication. The membrane of EVs protects enclosed miRNAs from degradation and harbors molecules that allow specific targeting to recipient cells. Although several studies have investigated the miRNA content in milk EVs from individual species, little is known about the evolutionary conserved nature of EV-associated miRNAs among different species. In this study, we profiled the miRNA content of purified EVs from human and porcine milk. These data were compared to published studies on EVs from human, cow, porcine, and panda milk to assess the overlap in the top 20 most abundant miRNAs. Interestingly, several abundant miRNAs were shared between species (e.g., let-7 family members let-7a, let-7b, let-7f, and miR-148a). Moreover, these miRNAs have been implicated in immune-related functions and regulation of cell growth and signal transduction. The conservation of these miRNA among species, not only in their sequence homology, but also in their incorporation in milk EVs of several species, suggests that they are evolutionarily selected to regulate cell function in the newborn.
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http://dx.doi.org/10.3389/fnut.2018.00081DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6153340PMC
September 2018

A Comparative Review on Microbiota Manipulation: Lessons From Fish, Plants, Livestock, and Human Research.

Front Nutr 2018 5;5:80. Epub 2018 Sep 5.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, Netherlands.

During recent years the impact of microbial communities on the health of their host (being plants, fish, and terrestrial animals including humans) has received increasing attention. The microbiota provides the host with nutrients, induces host immune development and metabolism, and protects the host against invading pathogens (1-6). Through millions of years of co-evolution bacteria and hosts have developed intimate relationships. Microbial colonization shapes the host immune system that in turn can shape the microbial composition (7-9). However, with the large scale use of antibiotics in agriculture and human medicine over the last decades an increase of diseases associated with so-called dysbiosis has emerged. Dysbiosis refers to either a disturbed microbial composition (outgrowth of possible pathogenic species) or a disturbed interaction between bacteria and the host (10). Instead of using more antibiotics to treat dysbiosis there is a need to develop alternative strategies to combat disturbed microbial control. To this end, we can learn from nature itself. For example, the plant root (or "rhizosphere") microbiome of sugar beet contains several bacterial species that suppress the fungal root pathogen , an economically important fungal pathogen of this crop (11). Likewise, commensal bacteria present on healthy human skin produce antimicrobial molecules that selectively kill skin pathogen . Interestingly, patients with atopic dermatitis (inflammation of the skin) lacked antimicrobial peptide secreting commensal skin bacteria (12). In this review, we will give an overview of microbial manipulation in fish, plants, and terrestrial animals including humans to uncover conserved mechanisms and learn how we might restore microbial balance increasing the resilience of the host species.
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http://dx.doi.org/10.3389/fnut.2018.00080DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6134018PMC
September 2018

Genome-wide association study reveals novel players in defense hormone crosstalk in Arabidopsis.

Plant Cell Environ 2018 10 3;41(10):2342-2356. Epub 2018 Jul 3.

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, The Netherlands.

Jasmonic acid (JA) regulates plant defenses against necrotrophic pathogens and insect herbivores. Salicylic acid (SA) and abscisic acid (ABA) can antagonize JA-regulated defenses, thereby modulating pathogen or insect resistance. We performed a genome-wide association (GWA) study on natural genetic variation in Arabidopsis thaliana for the effect of SA and ABA on the JA pathway. We treated 349 Arabidopsis accessions with methyl JA (MeJA), or a combination of MeJA and either SA or ABA, after which expression of the JA-responsive marker gene PLANT DEFENSIN1.2 (PDF1.2) was quantified as a readout for GWA analysis. Both hormones antagonized MeJA-induced PDF1.2 in the majority of the accessions but with a large variation in magnitude. GWA mapping of the SA- and ABA-affected PDF1.2 expression data revealed loci associated with crosstalk. GLYI4 (encoding a glyoxalase) and ARR11 (encoding an Arabidopsis response regulator involved in cytokinin signalling) were confirmed by T-DNA insertion mutant analysis to affect SA-JA crosstalk and resistance against the necrotroph Botrytis cinerea. In addition, At1g16310 (encoding a cation efflux family protein) was confirmed to affect ABA-JA crosstalk and susceptibility to Mamestra brassicae herbivory. Collectively, this GWA study identified novel players in JA hormone crosstalk with potential roles in the regulation of pathogen or insect resistance.
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http://dx.doi.org/10.1111/pce.13357DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6175328PMC
October 2018

Microbial small molecules - weapons of plant subversion.

Nat Prod Rep 2018 05;35(5):410-433

Plant-Microbe Interactions, Department of Biology, Science4Life, Utrecht University, Utrecht, The Netherlands.

Covering: up to 2018 Plants live in close association with a myriad of microbes that are generally harmless. However, the minority of microbes that are pathogens can severely impact crop quality and yield, thereby endangering food security. By contrast, beneficial microbes provide plants with important services, such as enhanced nutrient uptake and protection against pests and diseases. Like pathogens, beneficial microbes can modulate host immunity to efficiently colonize the nutrient-rich niches within and around the roots and aerial tissues of a plant, a phenomenon mirroring the establishment of commensal microbes in the human gut. Numerous ingenious mechanisms have been described by which pathogenic and beneficial microbes in the plant microbiome communicate with their host, including the delivery of immune-suppressive effector proteins and the production of phytohormones, toxins and other bioactive molecules. Plants signal to their associated microbes via exudation of photosynthetically fixed carbon sources, quorum-sensing mimicry molecules and selective secondary metabolites such as strigolactones and flavonoids. Molecular communication thus forms an integral part of the establishment of both beneficial and pathogenic plant-microbe relations. Here, we review the current knowledge on microbe-derived small molecules that can act as signalling compounds to stimulate plant growth and health by beneficial microbes on the one hand, but also as weapons for plant invasion by pathogens on the other. As an exemplary case, we used comparative genomics to assess the small molecule biosynthetic capabilities of the Pseudomonas genus; a genus rich in both plant pathogenic and beneficial microbes. We highlight the biosynthetic potential of individual microbial genomes and the population at large, providing evidence for the hypothesis that the distinction between detrimental and beneficial microbes is increasingly fading. Knowledge on the biosynthesis and molecular activity of microbial small molecules will aid in the development of successful biological agents boosting crop resiliency in a sustainable manner and could also provide scientific routes to pathogen inhibition or eradication.
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http://dx.doi.org/10.1039/c7np00062fDOI Listing
May 2018