scholarly journals Pipecolic Acid Is Induced in Barley upon Infection and Triggers Immune Responses Associated with Elevated Nitric Oxide Accumulation

2019 ◽  
Vol 32 (10) ◽  
pp. 1303-1313 ◽  
Author(s):  
Miriam Lenk ◽  
Marion Wenig ◽  
Kornelia Bauer ◽  
Florian Hug ◽  
Claudia Knappe ◽  
...  
Keyword(s):  
Nitric Oxide ◽  
Immune Responses ◽  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
Systemic Immunity ◽  
Exogenous Application ◽  
Barley Leaves

Pipecolic acid (Pip) is an essential component of systemic acquired resistance, priming resistance in Arabidopsis thaliana against (hemi)biotrophic pathogens. Here, we studied the potential role of Pip in bacteria-induced systemic immunity in barley. Exudates of barley leaves infected with the systemic immunity–inducing pathogen Pseudomonas syringae pv. japonica induced immune responses in A. thaliana. The same leaf exudates contained elevated Pip levels compared with those of mock-treated barley leaves. Exogenous application of Pip induced resistance in barley against the hemibiotrophic bacterial pathogen Xanthomonas translucens pv. cerealis. Furthermore, both a systemic immunity–inducing infection and exogenous application of Pip enhanced the resistance of barley against the biotrophic powdery mildew pathogen Blumeria graminis f. sp. hordei. In contrast to a systemic immunity-inducing infection, Pip application did not influence lesion formation by a systemically applied inoculum of the necrotrophic fungus Pyrenophora teres. Nitric oxide (NO) levels in barley leaves increased after Pip application. Furthermore, X. translucens pv. cerealis induced the accumulation of superoxide anion radicals and this response was stronger in Pip-pretreated compared with mock-pretreated plants. Thus, the data suggest that Pip induces barley innate immune responses by triggering NO and priming reactive oxygen species accumulation.

scholarly journals Arabidopsis UGT76B1 glycosylates N-hydroxy-pipecolic acid and inactivates systemic acquired resistance in tomato

2020 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Mary Beth Mudgett ◽  
Elizabeth S. Sattely
Keyword(s):  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Defense Responses ◽  
Pipecolic Acid ◽  
Systemic Resistance ◽  
Biosynthetic Genes ◽  
Solanaceous Plants

AbstractSystemic acquired resistance (SAR) is a mechanism that plants utilize to connect a local pathogen infection to global defense responses. N-hydroxy-pipecolic acid (NHP) and a glycosylated derivative are produced during SAR, yet their individual roles in the response have not yet been elucidated. Here we report that Arabidopsis thaliana UGT76B1 can generate glycosylated NHP (NHP-Glc) in vitro and when transiently expressed alongside Arabidopsis NHP biosynthetic genes in two Solanaceous plants. During infection, Arabidopsis ugt76b1 mutants do not accumulate NHP-Glc and accumulate less glycosylated salicylic acid (SA-Glc) than wild type plants. The metabolic changes in ugt76b1 mutant plants are accompanied by enhanced defense to the bacterial pathogen Pseudomonas syringae, suggesting that glycosylation of SAR molecules NHP and SA by UGT76B1 plays an important role in defense modulation. Transient expression of Arabidopsis UGT76B1 with the Arabidopsis NHP biosynthesis genes ALD1 and FMO1 in tomato increases NHP-Glc production and reduces NHP accumulation in local tissue, and abolishes the systemic resistance seen when expressing NHP-biosynthetic genes alone. These findings reveal that the glycosylation of NHP by UGT76B1 alters defense priming in systemic tissue and provide further evidence for the role of the NHP aglycone as the active metabolite in SAR signaling.

scholarly journals N-hydroxy-pipecolic acid is a mobile signal that induces systemic disease resistance in Arabidopsis

2018 ◽  
Author(s):  
Yun Chu Chen ◽  
Eric C. Holmes ◽  
Jakub Rajniak ◽  
Jung-Gun Kim ◽  
Sandy Tang ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Systemic Acquired Resistance ◽  
Systemic Disease ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
In Planta ◽  
Global Response ◽  
Promising Target ◽  
Pathogenesis Related

AbstractSystemic acquired resistance (SAR) is a global response in plants induced at the site of infection that leads to long-lasting and broad-spectrum disease resistance at distal, uninfected tissues. Despite the importance of this priming mechanism, the identity of the mobile defense signal that moves systemically throughout plants to initiate SAR has remained elusive. In this paper, we describe a new metabolite, N-hydroxy-pipecolic acid (N-OH-Pip), and provide evidence that this molecule is a mobile signal that plays a central role in initiating SAR signal transduction in Arabidopsis thaliana. We demonstrate that FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1), a key regulator of SAR-associated defense priming, can synthesize N-OH-Pip from pipecolic acid in planta, and exogenously applied N-OH-PIP moves systemically in Arabidopsis and can rescue the SAR-deficiency of fmo1 mutants. We also demonstrate that N-OH-Pip treatment causes systemic changes in the expression of pathogenesis-related genes and metabolic pathways throughout the plant, and enhances resistance to a bacterial pathogen. This work provides new insight into the chemical nature of a mobile signal for SAR and also suggests that the N-OH-Pip pathway is a promising target for metabolic engineering to enhance disease resistance.

scholarly journals Isolation of New Arabidopsis Mutants With Enhanced Disease Susceptibility to Pseudomonas syringae by Direct Screening

Genetics ◽  
1998 ◽  
Vol 149 (2) ◽  
pp. 537-548
Author(s):  
Sigrid M Volko ◽  
Thomas Boller ◽  
Frederick M Ausubel
Keyword(s):  
Pseudomonas Syringae ◽  
Fungal Pathogen ◽  
Systemic Acquired Resistance ◽  
Disease Susceptibility ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Avirulent Strain ◽  
Resistance Response ◽  
Arabidopsis Mutants ◽  
Pathogen Response

Abstract To identify plant defense components that are important in restricting the growth of virulent pathogens, we screened for Arabidopsis mutants in the accession Columbia (carrying the transgene BGL2-GUS) that display enhanced disease susceptibility to the virulent bacterial pathogen Pseudomonas syringae pv. maculicola (Psm) ES4326. Among six (out of a total of 11 isolated) enhanced disease susceptibility (eds) mutants that were studied in detail, we identified one allele of the previously described npr1/nim1/sai1 mutation, which is affected in mounting a systemic acquired resistance response, one allele of the previously identified EDS5 gene, and four EDS genes that have not been previously described. The six eds mutants studied in detail (npr1-4, eds5-2, eds10-1, eds11-1, eds12-1, and eds13-1) displayed different patterns of enhanced susceptibility to a variety of phytopathogenic bacteria and to the obligate biotrophic fungal pathogen Erysiphe orontii, suggesting that particular EDS genes have pathogen-specific roles in conferring resistance. All six eds mutants retained the ability to mount a hypersensitive response and to restrict the growth of the avirulent strain Psm ES4326/avrRpt2. With the exception of npr1-4, the mutants were able to initiate a systemic acquired resistance (SAR) response, although enhanced growth of Psm ES4326 was still detectable in leaves of SAR-induced plants. The data presented here indicate that eds genes define a variety of components involved in limiting pathogen growth, that many additional EDS genes remain to be discovered, and that direct screens for mutants with altered susceptibility to pathogens are helpful in the dissection of complex pathogen response pathways in plants.

scholarly journals Drought shifts sorghum root metabolite and microbiome profiles and enriches the stress response factor pipecolic acid

2020 ◽  
Author(s):  
Daniel F. Caddell ◽  
Katherine Louie ◽  
Benjamin Bowen ◽  
Julie A. Sievert ◽  
Joy Hollingsworth ◽  
...  
Keyword(s):  
Stress Response ◽  
Root Growth ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Pipecolic Acid ◽  
Bacterial Composition ◽  
Host Fitness ◽  
Exogenous Application ◽  
Resistance Pathway ◽  
Host Metabolism

ABSTRACTInteractions between plants and their root-associated microbiome are important for determining host fitness during periods of stress. During drought, monoderm bacteria are more abundant in sorghum roots than in those of watered controls. Additionally, a reversion from monoderm to diderm dominance occurs in drought-stressed roots one week after rewatering. However, the mechanisms driving this rapid microbiome composition shift is currently unknown. To understand if changes in host metabolism are correlated with this shift, we employed 16S amplicon sequencing and metabolomics of root, rhizosphere, and soil at the peak of a preflowering drought and 24 hours after rewatering. The microbiomes of droughted roots, rhizospheres, and soils differed from watered controls, and shifts in bacterial composition were observed in root and rhizosphere 24 hours after rewatering, highlighting the rapid response of microbes to the cessation of drought. Next, we performed metabolomic profiling to identify putative drivers of this process. During drought, we observed a high abundance of abiotic stress response factors, including antioxidants, osmolytes, amino acids, and plant hormones. After rewatering, large shifts in metabolite abundances were observed in rhizosphere, whereas shifts in root and soil were subtle. In addition, pipecolic acid, a well-characterized systemic acquired resistance signalling compound, was enriched in roots and rhizosphere during drought. We found that exogenous application of pipecolic acid suppresses root growth via a systemic acquired resistance-independent mechanism. Collectively, these data provide a comprehensive characterization of metabolite shifts across three compartments during drought, and elucidate a potential role of pipecolic acid in the sorghum drought response.IMPORTANCEPlant-associated microbial communities shift in composition and contribute to host fitness during drought. In particular, Actinobacteria are enriched in plant roots and rhizosphere during drought. However, the mechanisms plants use to drive this shift are poorly understood. Here we apply a combination of bacterial and metabolite profiling in root, rhizosphere, and soil during drought and drought-recovery to investigate potential contributions of host metabolism towards shifts in bacterial composition. Our results demonstrate that drought alters metabolic profiles and that the response to rewatering differs between compartments; we identify drought-responsive metabolites that are highly correlated with Actinobacteria abundance. Furthermore, our study reports for the first time that pipecolic acid is a drought-enriched metabolite in sorghum roots. We demonstrate that exogenous application of pipecolic acid is able to provoke one of the classic drought responses in roots, root growth suppression, and that this activity functions independently from the systemic acquired resistance pathway.

scholarly journals An engineered pathway for N-hydroxy-pipecolic acid synthesis enhances systemic acquired resistance in tomato

2019 ◽  
Vol 12 (604) ◽  
pp. eaay3066 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Elizabeth S. Sattely ◽  
Mary Beth Mudgett
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Acid Synthesis ◽  
Crop Plants ◽  
Pipecolic Acid ◽  
External Control ◽  
Long Distance ◽  
Engineering Strategy ◽  
Molecular Machinery

Systemic acquired resistance (SAR) is a powerful immune response that triggers broad-spectrum disease resistance throughout a plant. In the model plant Arabidopsis thaliana, long-distance signaling and SAR activation in uninfected tissues occur without circulating immune cells and instead rely on the metabolite N-hydroxy-pipecolic acid (NHP). Engineering SAR in crop plants would enable external control of a plant’s ability to mount a global defense response upon sudden changes in the environment. Such a metabolite-engineering approach would require the molecular machinery for producing and responding to NHP in the crop plant. Here, we used heterologous expression in Nicotiana benthamiana leaves to identify a minimal set of Arabidopsis genes necessary for the biosynthesis of NHP. Local expression of these genes in tomato leaves triggered SAR in distal tissues in the absence of a pathogen, suggesting that the SAR trait can be engineered to enhance a plant’s endogenous ability to respond to pathogens. We also showed tomato produces endogenous NHP in response to a bacterial pathogen and that NHP is present across the plant kingdom, raising the possibility that an engineering strategy to enhance NHP-induced defenses could be possible in many crop plants.

scholarly journals Pseudomonas syringae Elicits Emission of the Terpenoid (E,E)-4,8,12-Trimethyl-1,3,7,11-Tridecatetraene in Arabidopsis Leaves Via Jasmonate Signaling and Expression of the Terpene Synthase TPS4

2008 ◽  
Vol 21 (11) ◽  
pp. 1482-1497 ◽  
Author(s):  
Elham Attaran ◽  
Michael Rostás ◽  
Jürgen Zeier
Keyword(s):  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Induced Defense ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Microbial Pathogens ◽  
Terpene Synthase ◽  
Knockout Mutant ◽  
Direct Role ◽  
Ja Signaling

Volatile, low–molecular weight terpenoids have been implicated in plant defenses, but their direct role in resistance against microbial pathogens is not clearly defined. We have examined a possible role of terpenoid metabolism in the induced defense of Arabidopsis thaliana plants against leaf infection with the bacterial pathogen Pseudomonas syringae. Inoculation of plants with virulent or avirulent P. syringae strains induces the emission of the terpenoids (E,E)-4,8,12-trimethyl-1,3,7,11-tridecatetraene (TMTT), β-ionone and α-farnesene. While the most abundant volatile, the C16-homoterpene TMTT, is produced relatively early in compatible and incompatible interactions, emission of both β-ionone and α-farnesene only increases in later stages of the compatible interaction. Pathogen-induced synthesis of TMTT is controlled through jasmonic acid (JA)-dependent signaling but is independent of a functional salicylic acid (SA) pathway. We have identified Arabidopsis T-DNA insertion lines with defects in the terpene synthase gene TPS4, which is expressed in response to P. syringae inoculation. The tps4 knockout mutant completely lacks induced emission of TMTT but is capable of β-ionone and α-farnesene production, demonstrating that TPS4 is specifically involved in TMTT formation. The tps4 plants display at least wild type–like resistance against P. syringae, indicating that TMTT per se does not protect against the bacterial pathogen in Arabidopsis leaves. Similarly, the ability to mount SA-dependent defenses and systemic acquired resistance (SAR) is barely affected in tps4, which excludes a signaling function of TMTT during SAR. Besides P. syringae challenge, intoxication of Arabidopsis leaves with copper sulfate, a treatment that strongly activates JA biosynthesis, triggers production of TMTT, β-ionone, and α-farnesene. Taken together, our data suggest that induced TMTT production in Arabidopsis is a by-product of activated JA signaling, rather than an effective defense response that contributes to resistance against P. syringae.

scholarly journals GmRAR1 and GmSGT1 Are Required for Basal, R Gene–Mediated and Systemic Acquired Resistance in Soybean

2009 ◽  
Vol 22 (1) ◽  
pp. 86-95 ◽  
Author(s):  
Da-Qi Fu ◽  
Said Ghabrial ◽  
Aardra Kachroo
Keyword(s):  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Soybean Mosaic Virus ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
R Gene ◽  
Extreme Resistance ◽  
Basal Resistance ◽  
Effector Triggered Immunity ◽  
Specific Proteins

RAR1, SGT1, and HSP90 are important components of effector-triggered immunity (ETI) in diverse plants, where RAR1 and SGT1 are thought to serve as HSP90 co-chaperones. We show that ETI in soybean requires RAR1 and SGT1 but not HSP90. Rsv1-mediated extreme resistance to Soybean mosaic virus (SMV) and Rpg-1b-mediated resistance to Pseudomonas syringae were compromised in plants silenced for GmRAR1 and GmSGT1-2 but not GmHSP90. This suggests that RAR1- or SGT1-dependant signaling is not always associated with a dependence on HSP90. Unlike in Arabidopsis, SGT1 in soybean also mediates ETI against the bacterial pathogen P. syringae. Similar to Arabidopsis, soybean RAR1 and SGT1 proteins interact with each other and two related HSP90 proteins. Plants silenced for GmHSP90 genes or GmRAR1 exhibited altered morphology, suggesting that these proteins also contribute to developmental processes. Silencing GmRAR1 and GmSGT1-2 impaired resistance to virulent bacteria and systemic acquired resistance (SAR) in soybean as well. Because the Arabidopsis rar1 mutant also showed a defect in SAR, we conclude that RAR1 and SGT1 serve as a point of convergence for basal resistance, ETI, and SAR. We demonstrate that, although soybean defense signaling pathways recruit structurally conserved components, they have distinct requirements for specific proteins.

scholarly journals N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis

2018 ◽  
Vol 115 (21) ◽  
pp. E4920-E4929 ◽  
Author(s):  
Yun-Chu Chen ◽  
Eric C. Holmes ◽  
Jakub Rajniak ◽  
Jung-Gun Kim ◽  
Sandy Tang ◽  
...  
Keyword(s):  
Disease Resistance ◽  
Systemic Acquired Resistance ◽  
Systemic Disease ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Pipecolic Acid ◽  
In Planta ◽  
Global Response ◽  
Promising Target ◽  
Pathogenesis Related

Systemic acquired resistance (SAR) is a global response in plants induced at the site of infection that leads to long-lasting and broad-spectrum disease resistance at distal, uninfected tissues. Despite the importance of this priming mechanism, the identity and complexity of defense signals that are required to initiate SAR signaling is not well understood. In this paper, we describe a metabolite, N-hydroxy-pipecolic acid (N-OH-Pip) and provide evidence that this mobile molecule plays a role in initiating SAR signal transduction in Arabidopsis thaliana. We demonstrate that FLAVIN-DEPENDENT MONOOXYGENASE 1 (FMO1), a key regulator of SAR-associated defense priming, can synthesize N-OH-Pip from pipecolic acid in planta, and exogenously applied N-OH-Pip moves systemically in Arabidopsis and can rescue the SAR-deficiency of fmo1 mutants. We also demonstrate that N-OH-Pip treatment causes systemic changes in the expression of pathogenesis-related genes and metabolic pathways throughout the plant and enhances resistance to a bacterial pathogen. This work provides insight into the chemical nature of a signal for SAR and also suggests that the N-OH-Pip pathway is a promising target for metabolic engineering to enhance disease resistance.

scholarly journals Arabidopsismlo3mutant plants exhibit spontaneous callose deposition and signs of early leaf senescence

2019 ◽  
Author(s):  
Stefan Kusch ◽  
Susanne Thiery ◽  
Anja Reinstädler ◽  
Katrin Gruner ◽  
Krzysztof Zienkiewicz ◽  
...  
Keyword(s):  
Salicylic Acid ◽  
Powdery Mildew ◽  
Pseudomonas Syringae ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Bacterial Pathogen ◽  
Resistance Locus ◽  
Callose Deposition ◽  
Powdery Mildew Fungi ◽  
Hyaloperonospora Arabidopsidis

The family of Mildew resistance Locus O (MLO) proteins is best known for its profound effect on the outcome of powdery mildew infections: when the appropriate MLO protein is absent, the plant is fully resistant to otherwise virulent powdery mildew fungi. However, most members of the MLO protein family remain functionally unexplored. Here, we investigateArabidopsis thaliana MLO3, the closest relative ofAtMLO2, AtMLO6andAtMLO12, which are the ArabidopsisMLOgenes implicated in the powdery mildew interaction. The co-expression network ofAtMLO3suggests association of the gene with plant defense-related processes such as salicylic acid homeostasis. Our extensive analysis shows thatmlo3mutants are unaffected regarding their infection phenotype upon challenge with the powdery mildew fungiGolovinomyces orontiiandErysiphe pisi, the oomyceteHyaloperonospora arabidopsidis, and the bacterial pathogenPseudomonas syringae(the latter both in terms of basal and systemic acquired resistance), indicating that the protein does not play a major role in the response to any of these pathogens. However,mlo3genotypes display spontaneous callose deposition as well as signs of early senescence in six-or seven-week-old rosette leaves in the absence of any pathogen challenge, a phenotype that is reminiscent ofmlo2mutant plants. We hypothesize that de-regulated callose deposition inmlo3genotypes is the result of a subtle transient aberration of salicylic acid-jasmonic acid homeostasis during development.

Sign in / Sign up

Export Citation Format

Share Document