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

2020 ◽  
Author(s):  
Pauline L Trapet ◽  
Eline H Verbon ◽  
Renda R Bosma ◽  
Kirsten Voordendag ◽  
Johan A Van Pelt ◽  
...  
Keyword(s):  
Induced Resistance ◽  
Pseudomonas Syringae ◽  
Sufficient Conditions ◽  
Fe Deficiency ◽  
Systemic Resistance ◽  
Mineral Nutrient ◽  
Wild Type ◽  
Starvation Stress ◽  
Fe Homeostasis ◽  
Hyaloperonospora Arabidopsidis

Abstract 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.

scholarly journals Induced Systemic Resistance in Arabidopsis thaliana Against Pseudomonas syringae pv. tomato by 2,4-Diacetylphloroglucinol-Producing Pseudomonas fluorescens

2012 ◽  
Vol 102 (4) ◽  
pp. 403-412 ◽  
Author(s):  
David M. Weller ◽  
Dmitri V. Mavrodi ◽  
Johan A. van Pelt ◽  
Corné M. J. Pieterse ◽  
Leendert C. van Loon ◽  
...  
Keyword(s):  
Arabidopsis Thaliana ◽  
Pseudomonas Fluorescens ◽  
Induced Resistance ◽  
Pseudomonas Syringae ◽  
Induced Systemic Resistance ◽  
Signal Transduction Pathway ◽  
Systemic Resistance ◽  
Wild Type ◽  
Challenge Inoculation ◽  
Dependent Signal

Pseudomonas fluorescens strains that produce the polyketide antibiotic 2,4-diacetylphloroglucinol (2,4-DAPG) are among the most effective rhizobacteria that suppress root and crown rots, wilts, and damping-off diseases of a variety of crops, and they play a key role in the natural suppressiveness of some soils to certain soilborne pathogens. Root colonization by 2,4-DAPG-producing P. fluorescens strains Pf-5 (genotype A), Q2-87 (genotype B), Q8r1-96 (genotype D), and HT5-1 (genotype N) produced induced systemic resistance (ISR) in Arabidopsis thaliana accession Col-0 against bacterial speck caused by P. syringae pv. tomato. The ISR-eliciting activity of the four bacterial genotypes was similar, and all genotypes were equivalent in activity to the well-characterized strain P. fluorescens WCS417r. The 2,4-DAPG biosynthetic locus consists of the genes phlHGF and phlACBDE. phlD or phlBC mutants of Q2-87 (2,4-DAPG minus) were significantly reduced in ISR activity, and genetic complementation of the mutants restored ISR activity back to wild-type levels. A phlF regulatory mutant (overproducer of 2,4-DAPG) had ISR activity equivalent to the wild-type Q2-87. Introduction of DAPG into soil at concentrations of 10 to 250 μM 4 days before challenge inoculation induced resistance equivalent to or better than the bacteria. Strain Q2-87 induced resistance on transgenic NahG plants but not on npr1-1, jar1, and etr1 Arabidopsis mutants. These results indicate that the antibiotic 2,4-DAPG is a major determinant of ISR in 2,4-DAPG-producing P. fluorescens, that the genotype of the strain does not affect its ISR activity, and that the activity induced by these bacteria operates through the ethylene- and jasmonic acid-dependent signal transduction pathway.

scholarly journals Effects of Jasmonic Acid, Ethylene, and Salicylic Acid Signaling on the Rhizosphere Bacterial Community of Arabidopsis thaliana

2011 ◽  
Vol 24 (4) ◽  
pp. 395-407 ◽  
Author(s):  
Rogier F. Doornbos ◽  
Bart P. J. Geraats ◽  
Eiko E. Kuramae ◽  
L. C. Van Loon ◽  
Peter A. H. M. Bakker
Keyword(s):  
Salicylic Acid ◽  
Bacterial Community ◽  
Induced Resistance ◽  
Plant Pathogens ◽  
Plant Diseases ◽  
Systemic Resistance ◽  
Culturable Bacteria ◽  
Wild Type ◽  
Defense Signaling ◽  
Rhizosphere Bacterial Community

Systemically induced resistance is a promising strategy to control plant diseases, as it affects numerous pathogens. However, since induced resistance reduces one or both growth and activity of plant pathogens, the indigenous microflora may also be affected by an enhanced defensive state of the plant. The aim of this study was to elucidate how much the bacterial rhizosphere microflora of Arabidopsis is affected by induced systemic resistance (ISR) or systemic acquired resistance (SAR). Therefore, the bacterial microflora of wild-type plants and plants affected in their defense signaling was compared. Additionally, ISR was induced by application of methyl jasmonate and SAR by treatment with salicylic acid or benzothiadiazole. As a comparative model, we also used wild type and ethylene-insensitive tobacco. Some of the Arabidopsis genotypes affected in defense signaling showed altered numbers of culturable bacteria in their rhizospheres; however, effects were dependent on soil type. Effects of plant genotype on rhizosphere bacterial community structure could not be related to plant defense because chemical activation of ISR or SAR had no significant effects on density and structure of the rhizosphere bacterial community. These findings support the notion that control of plant diseases by elicitation of systemic resistance will not significantly affect the resident soil bacterial microflora.

scholarly journals Induction of Systemic Resistance to Botrytis cinerea in Tomato by Pseudomonas aeruginosa 7NSK2: Role of Salicylic Acid, Pyochelin, and Pyocyanin

2002 ◽  
Vol 15 (11) ◽  
pp. 1147-1156 ◽  
Author(s):  
Kris Audenaert ◽  
Theresa Pattery ◽  
Pierre Cornelis ◽  
Monica Höfte
Keyword(s):  
Pseudomonas Aeruginosa ◽  
Salicylic Acid ◽  
Botrytis Cinerea ◽  
Induced Resistance ◽  
Mammalian Cells ◽  
Cell Damage ◽  
Systemic Resistance ◽  
Wild Type ◽  
Induce Resistance

The rhizobacterium Pseudomonas aeruginosa 7NSK2 produces secondary metabolites such as pyochelin (Pch), its precursor salicylic acid (SA), and the phenazine compound pyocyanin. Both 7NSK2 and mutant KMPCH (Pch-negative, SA-positive) induced resistance to Botrytis cinerea in wild-type but not in transgenic NahG tomato. SA-negative mutants of both strains lost the capacity to induce resistance. On tomato roots, KMPCH produced SA and induced phenylalanine ammonia lyase activity, while this was not the case for 7NSK2. In 7NSK2, SA is probably very efficiently converted to Pch. However, Pch alone appeared not to be sufficient to induce resistance. In mammalian cells, Fe-Pch and pyocyanin can act synergistically to generate highly reactive hydroxyl radicals that cause cell damage. Reactive oxygen species are known to play an important role in plant defense. To study the role of pyocyanin in induced resistance, a pyocyanin-negative mutant of 7NSK2, PHZ1, was generated. PHZ1 is mutated in the phzM gene encoding an O-methyltransferase. PHZ1 was unable to induce resistance to B. cinerea, whereas complementation for pyocyanin production or co-inoculation with mutant 7NSK2-562 (Pch-negative, SA-negative, pyocyanin-positive) restored induced resistance. These results suggest that pyocyanin and Pch, rather than SA, are the determinants for induced resistance in wild-type P. aeruginosa 7NSK2.

scholarly journals Induction of systemic resistance in tomato by the autochthonous phylloplane resident Bacillus cereus

2006 ◽  
Vol 41 (8) ◽  
pp. 1247-1252 ◽  
Author(s):  
Bernardo de Almeida Halfeld-Vieira ◽  
José Roberto Vieira Júnior ◽  
Reginaldo da Silva Romeiro ◽  
Harllen Sandro Alves Silva ◽  
Maria Cristina Baracat-Pereira
Keyword(s):  
Bacillus Cereus ◽  
Induced Resistance ◽  
Pseudomonas Syringae ◽  
Induced Systemic Resistance ◽  
Resistance Mechanism ◽  
Systemic Resistance ◽  
Tomato Plants

The objective of this work was to verify if the induced resistance mechanism is responsible for the capacity of a phylloplane resident bacteria (Bacillus cereus), isolated from healthy tomato plants, to control several diseases of this crop. A strain of Pseudomonas syringae pv. tomato was used as the challenging pathogen. The absence of direct antibiosis of the antagonist against the pathogen, the significant increase in peroxidases activity in tomato plants exposed to the antagonist and then inoculated with the challenging pathogen, as well as the character of the protection, are evidences wich suggest that biocontrol efficiency presented by the antagonist in previous works might be due to induced systemic resistance (ISR).

scholarly journals Iron deficiency induced changes in Fe homeostasis and 14-3-3 interactomics of Arabidopsis thaliana

2021 ◽  
Author(s):  
Jing Gao ◽  
Paula J. M. Kleeff ◽  
Ka Wan Li ◽  
Albertus H. Boer
Keyword(s):  
Arabidopsis Thaliana ◽  
Sufficient Conditions ◽  
Tca Cycle ◽  
Fe Deficiency ◽  
Functional Aspects ◽  
Clear Explanation ◽  
Fe Uptake ◽  
Physiological Analysis ◽  
Fe Homeostasis ◽  
Induced Changes

Abstract Members of 14-3-3 protein family are involved in the proper operation of Fe acquisition mechanisms at physiological and gene expression levels in Arabidopsis thaliana. To more directly and effectively observe whether members of 14-3-3 non-epsilon group have a function in Fe-deficiency adaptation, three higher order quadruple KOs, kappa/lambda/phi/chi (klpc), kappa/lambda/upsilon/nu(klun), and upsilon/nu/phi/chi (unpc) were generated and applied for physiological analysis in this study. The mutant plants that combine kl with un (klun) or kl with pc (klpc) mutations showed a better Fe uptake than Wt plants at low medium Fe, while this phenotype was absent in unpc mutant. The higher Fe uptake by klun correlated with a higher Fe-deficiency induced expression of selected Fe-related genes. The dynamics of 14-3-3-client interactions analysis showed that a subset of 27 proteins differentially interacted with 14-3-3 in roots caused by Fe deficiency. Many of these Fe responsive proteins have a role in glycolysis and TCA cycle, the FoF1-synthase and in the cysteine/methionine synthesis. Also, the 14-3-3 interactome of the klun roots showed significant differences with that of Wt roots under Fe sufficient conditions, where most of these differential binding proteins showed enhanced binding in the klun mutant. Nevertheless, a clear explanation for the observed phenotypes awaits a more detailed analysis of the functional aspects of 14-3-3 binding to the target proteins identified in this study.

scholarly journals OsIRO3 Plays an Essential Role in Iron Deficiency Responses and Regulates Iron Homeostasis in Rice

Plants ◽  
2020 ◽  
Vol 9 (9) ◽  
pp. 1095
Author(s):  
Wujian Wang ◽  
Jun Ye ◽  
Yanran Ma ◽  
Ting Wang ◽  
Huixia Shou ◽  
...  
Keyword(s):  
Iron Homeostasis ◽  
Molecular Mechanisms ◽  
Sufficient Conditions ◽  
Negative Regulator ◽  
Fe Deficiency ◽  
Plant Growth And Development ◽  
E Box ◽  
Young Leaves ◽  
Related Transcription Factor ◽  
Fe Homeostasis

Iron (Fe) homeostasis is essential for plant growth and development, and it is strictly regulated by a group of transcriptional factors. Iron-related transcription factor 3 (OsIRO3) was previously identified as a negative regulator for Fe deficiency response in rice. However, the molecular mechanisms by which OsIRO3 regulate Fe homeostasis is unclear. Here, we report that OsIRO3 is essential for responding to Fe deficiency and maintaining Fe homeostasis in rice. OsIRO3 is expressed in the roots, leaves, and base nodes, with a higher level in leaf blades at the vegetative growth stage. Knockout of OsIRO3 resulted in a hypersensitivity to Fe deficiency, with severe necrosis on young leaves and defective root development. The iro3 mutants accumulated higher levels of Fe in the shoot under Fe-deficient conditions, associated with upregulating the expression of OsNAS3, which lead to increased accumulation of nicotianamine (NA) in the roots. Further analysis indicated that OsIRO3 can directly bind to the E-box in the promoter of OsNAS3. Moreover, the expression of typical Fe-related genes was significantly up-regulated in iro3 mutants under Fe-sufficient conditions. Thus, we conclude that OsIRO3 plays a key role in responding to Fe deficiency and regulates NA levels by directly, negatively regulating the OsNAS3 expression.

The Tonoplast-Localized Transporter OsNRAMP2 is involved in Fe Homeostasis and affects Seed Germination in rice

2021 ◽  
Author(s):  
Yun Li ◽  
Jingjun Li ◽  
Yihong Yu ◽  
Xia Dai ◽  
Changyi Gong ◽  
...  
Keyword(s):  
Seed Germination ◽  
Natural Resistance ◽  
Fe Deficiency ◽  
Shoot Biomass ◽  
Wild Type ◽  
Crop Development ◽  
In The Wild ◽  
Macrophage Protein ◽  
Fe Homeostasis ◽  
Fe Toxicity

Abstract Vacuolar storage of iron (Fe) is important for Fe homeostasis in plants. When sufficient, the excess Fe could be stored in vacuoles for remobilization in case of Fe deficiency. Although the mechanism of Fe remobilization from vacuoles is critical for crop development under low Fe stress, the transporters that mediate vacuolar Fe translocation into the cytosol in rice remains unknown. Here, we showed that under higher Fe 2+ concentrations, the Δccc1 yeast mutant transformed with rice natural resistance-associated macrophage protein 2 (OsNRAMP2) became more sensitive to Fe toxicity. In rice protoplasts and transgenic plants expressing Pro35S: OsNRAMP2-GFP, OsNRAMP2 was localized to tonoplast. Vacuolar Fe contents in osnramp2 knockdown lines were higher than in the wild-type, while the growth of osnramp2 knockdown plants was significantly influenced by Fe deficiency. Furthermore, the germination of osnramp2 knockdown plants was arrested. Inversely, the vacuolar Fe contents of Pro35S: OsNRAMP2-GFP lines were significantly lower than in the wild-type, and overexpression of OsNRAMP2 increased shoot biomass under Fe deficiency. Taken together, we propose that OsNRAMP2 transports Fe from the vacuole to the cytosol and plays a pivotal role in seed germination.

scholarly journals Riboflavin Induces Disease Resistance in Plants by Activating a Novel Signal Transduction Pathway

2000 ◽  
Vol 90 (8) ◽  
pp. 801-811 ◽  
Author(s):  
H. Dong ◽  
S. V. Beer
Keyword(s):  
Signal Transduction ◽  
Protein Kinase ◽  
Induced Resistance ◽  
Pseudomonas Syringae ◽  
Kinase Inhibitor ◽  
Signal Transduction Pathway ◽  
Systemic Resistance ◽  
Transduction Pathway ◽  
Pr Genes ◽  
Npr1 Gene

The role of riboflavin as an elicitor of systemic resistance and an activator of a novel signaling process in plants was demonstrated. Following treatment with riboflavin, Arabidopsis thaliana developed systemic resistance to Peronospora parasitica and Pseudomonas syringae pv. Tomato, and tobacco developed systemic resistance to Tobacco mosaic virus (TMV) and Alternaria alternata. Riboflavin, at concentrations necessary for resistance induction, did not cause cell death in plants or directly affect growth of the culturable pathogens. Riboflavin induced expression of pathogenesis-related (PR) genes in the plants, suggesting its ability to trigger a signal transduction pathway that leads to systemic resistance. Both the protein kinase inhibitor K252a and mutation in the NIM1/NPR1 gene which controls transcription of defense genes, impaired responsiveness to riboflavin. In contrast, riboflavin induced resistance and PR gene expression in NahG plants, which fail to accumulate salicylic acid (SA). Thus, riboflavin-induced resistance requires protein kinase signaling mechanisms and a functional NIM1/NPR1 gene, but not accumulation of SA. Riboflavin is an elicitor of systemic resistance, and it triggers resistance signal transduction in a distinct manner.

scholarly journals Uncoupling Salicylic Acid-Dependent Cell Death and Defense-Related Responses From Disease Resistance in the Arabidopsis Mutant acd5

Genetics ◽  
2000 ◽  
Vol 156 (1) ◽  
pp. 341-350
Author(s):  
Jean T Greenberg ◽  
F Paul Silverman ◽  
Hua Liang
Keyword(s):  
Cell Death ◽  
Salicylic Acid ◽  
Disease Resistance ◽  
Pseudomonas Syringae ◽  
Higher Plants ◽  
Ethylene Signaling ◽  
Symptom Development ◽  
Wild Type ◽  
Dependent Cell ◽  
Arabidopsis Mutant

Abstract Salicylic acid (SA) is required for resistance to many diseases in higher plants. SA-dependent cell death and defense-related responses have been correlated with disease resistance. The accelerated cell death 5 mutant of Arabidopsis provides additional genetic evidence that SA regulates cell death and defense-related responses. However, in acd5, these events are uncoupled from disease resistance. acd5 plants are more susceptible to Pseudomonas syringae early in development and show spontaneous SA accumulation, cell death, and defense-related markers later in development. In acd5 plants, cell death and defense-related responses are SA dependent but they do not confer disease resistance. Double mutants with acd5 and nonexpressor of PR1, in which SA signaling is partially blocked, show greatly attenuated cell death, indicating a role for NPR1 in controlling cell death. The hormone ethylene potentiates the effects of SA and is important for disease symptom development in Arabidopsis. Double mutants of acd5 and ethylene insensitive 2, in which ethylene signaling is blocked, show decreased cell death, supporting a role for ethylene in cell death control. We propose that acd5 plants mimic P. syringae-infected wild-type plants and that both SA and ethylene are normally involved in regulating cell death during some susceptible pathogen infections.

scholarly journals Bacterial effector targeting of a plant iron sensor facilitates iron acquisition and pathogen colonization

2021 ◽  
Author(s):  
Yingying Xing ◽  
Ning Xu ◽  
Deepak D Bhandari ◽  
Dmitry Lapin ◽  
Xinhua Sun ◽  
...  
Keyword(s):  
Pseudomonas Syringae ◽  
Iron Uptake ◽  
Iron Acquisition ◽  
Iron Accumulation ◽  
Regulatory Proteins ◽  
Mineral Nutrient ◽  
Effector Protein ◽  
Iron Regulatory Proteins ◽  
Protein Levels ◽  
Pathogen Colonization

Abstract Acquisition of nutrients from different species is necessary for pathogen colonization. Iron is an essential mineral nutrient for nearly all organisms, but little is known about how pathogens manipulate plant hosts to acquire iron. Here, we report that AvrRps4, an effector protein delivered by Pseudomonas syringae bacteria to plants, interacts with and targets the plant iron sensor protein BRUTUS (BTS) to facilitate iron uptake and pathogen proliferation in Arabidopsis thaliana. Infection of rps4 and eds1 by P. syringae pv. tomato (Pst) DC3000 expressing AvrRps4 resulted in iron accumulation, especially in the plant apoplast. AvrRps4 alleviates BTS-mediated degradation of bHLH115 and ILR3(IAA-Leucine resistant 3), two iron regulatory proteins. In addition, BTS is important for accumulating immune proteins Enhanced Disease Susceptibility1 (EDS1) at both the transcriptional and protein levels upon Pst (avrRps4) infections. Our findings suggest that AvrRps4 targets BTS to facilitate iron accumulation and BTS contributes to RPS4/EDS1-mediated immune responses.

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