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 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 Fitness Costs of Mutations Affecting the Systemic Acquired Resistance Pathway in Arabidopsis thaliana

Genetics ◽  
2004 ◽  
Vol 168 (4) ◽  
pp. 2197-2206 ◽  
Author(s):  
Andrew J. Heidel ◽  
Joseph D. Clarke ◽  
Janis Antonovics ◽  
Xinnian Dong
Keyword(s):  
Arabidopsis Thaliana ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Fitness Costs ◽  
Resistance Pathway

scholarly journals Antagonistic Interaction between Systemic Acquired Resistance and the Abscisic Acid–Mediated Abiotic Stress Response in Arabidopsis

2008 ◽  
Vol 20 (6) ◽  
pp. 1678-1692 ◽  
Author(s):  
Michiko Yasuda ◽  
Atsushi Ishikawa ◽  
Yusuke Jikumaru ◽  
Motoaki Seki ◽  
Taishi Umezawa ◽  
...  
Keyword(s):  
Abscisic Acid ◽  
Abiotic Stress ◽  
Stress Response ◽  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Abiotic Stress Response ◽  
Antagonistic Interaction

scholarly journals Overexpression of a Rice NPR1 Homolog Leads to Constitutive Activation of Defense Response and Hypersensitivity to Light

2005 ◽  
Vol 18 (6) ◽  
pp. 511-520 ◽  
Author(s):  
Mawsheng Chern ◽  
Heather A. Fitzgerald ◽  
Patrick E. Canlas ◽  
Duroy A. Navarre ◽  
Pamela C. Ronald
Keyword(s):  
Systemic Acquired Resistance ◽  
Environmental Changes ◽  
Acquired Resistance ◽  
Northern Analysis ◽  
Wild Type ◽  
Defense Genes ◽  
Isolation And Characterization ◽  
Broad Spectrum Resistance ◽  
Resistance Pathway

Arabidopsis NPR1/NIM1 is a key regulator of systemic acquired resistance (SAR), which confers lasting broad-spectrum resistance. Previous reports indicate that rice has a disease-resistance pathway similar to the Arabidopsis SAR pathway. Here we report the isolation and characterization of a rice NPR1 homologue (NH1). Transgenic rice plants overexpressing NH1 (NH1ox) acquire high levels of resistance to Xanthomonas oryzae pv. oryzae. The resistance phenotype is heritable and correlates with the presence of the transgene and reduced bacterial growth. Northern analysis shows that NH1ox rice spontaneously activates defense genes, contrasting with NPR1-overexpressing Arabidopsis, where defense genes are not activated until induction. Wild-type NH1, but not a point mutant corresponding to npr1-1, interacts strongly with the rice transcription factor rTGA2.2 in yeast two-hybrid. Greenhouse-grown NH1ox plants develop lesion-mimic spots on leaves at preflowering stage although no other developmental effects are observed. However, when grown in growth chambers (GCs) under low light, NH1ox plants are dwarfed, indicating elevated sensitivity to light. The GC-grown NH1ox plants show much higher salicylic acid (SA) levels than the wild type, whereas greenhouse-grown NH1ox plants contain lower SA. These results indicate that NH1 may be involved in the regulation of SA in response to environmental changes.

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 The glycosyltransferase UGT76B1 is critical for plant immunity as it governs the homeostasis of N-hydroxy-pipecolic acid

2020 ◽  
Author(s):  
Lennart Mohnike ◽  
Dmitrij Rekhter ◽  
Weijie Huang ◽  
Kirstin Feussner ◽  
Hainan Tian ◽  
...  
Keyword(s):  
Systemic Acquired Resistance ◽  
Plant Immunity ◽  
Acquired Resistance ◽  
Pipecolic Acid ◽  
Balance Growth ◽  
Loss Of Function ◽  
Long Distance ◽  
Knock Out ◽  
Endogenous Substrates ◽  
Mutant Lines

AbstractThe trade-off between growth and defense is a critical aspect of plant immunity. Therefore, plant immune response needs to be tightly regulated. The hormone regulating plant defense against biotrophic pathogens is salicylic acid (SA). Recently, N-hydroxy-pipecolic acid (NHP) was identified as second regulator for plant innate immunity and systemic acquired resistance. Although the biosynthetic pathway leading to NHP formation has already been identified, the route how NHP is further metabolized was unclear. Here, we present UGT76B1 as a UDP-dependent glycosyltransferase that modifies NHP by catalyzing the formation of 1-O-glucosyl-pipecolic acid (NHP-OGlc). Analysis of T-DNA and CRISPR knock-out mutant lines of UGT76B1 by targeted and non-targeted UHPLC-HRMS underlined NHP and SA as endogenous substrates of this enzyme in response to Pseudomonas infection and UV treatment. UGT76B1 shows similar KM for NHP and SA. ugt76b1 mutant plants have a dwarf phenotype and a constitutive defense response which can be suppressed by loss of function of the NHP biosynthetic enzyme FMO1. This suggests that elevated accumulation of NHP contributes to the enhanced disease resistance in ugt76b1. Externally applied NHP can move to distal tissue in ugt76b1 mutant plants. Although glycosylation is not required for the long distance movement of NHP during systemic acquired resistance, it is crucial to balance growth and defense.

scholarly journals Conservation of N-hydroxy-pipecolic acid-mediated systemic acquired resistance in crop plants

2019 ◽  
Author(s):  
Eric C. Holmes ◽  
Yun-Chu Chen ◽  
Elizabeth Sattely ◽  
Mary Beth Mudgett
Keyword(s):  
Systemic Acquired Resistance ◽  
Acquired Resistance ◽  
Signal Propagation ◽  
Crop Plants ◽  
Pipecolic Acid ◽  
List Type ◽  
In Planta ◽  
Long Distance ◽  
Plant Kingdom ◽  
Promising Strategy

SUMMARYSignal propagation and the coordination of whole-organism responses in plants rely heavily on small molecules. Systemic acquired resistance (SAR) is one such process in which long-distance signaling activates immune responses in uninfected tissue as a way to limit the spread of a primary, localized infection. Recently, N-hydroxy pipecolic acid (NHP) was discovered and shown to coordinate SAR in Arabidopsis. Here, we provide metabolic and biochemical evidence that NHP is conserved across the plant kingdom and demonstrate a role for NHP in mediating SAR responses in tomato and pepper. We reconstituted the NHP biosynthetic pathway in planta and show that transient expression of two NHP biosynthetic genes in tomato induces enhanced resistance to a bacterial pathogen in distal tissue. Our results suggest engineering strategies to induce NHP-mediated SAR are a promising route to improve broad-spectrum pathogen resistance in crops.IN BRIEFEngineering NHP production is a promising strategy to enhance disease resistance in crops.HIGHLIGHTSArabidopsis N-hydroxy-pipecolic acid (NHP) pathway is conserved across the plant kingdomApplication of NHP to tomato and pepper plants induces a robust SAR responseMetabolic engineering of the Arabidopsis NHP pathway in Solanum lycopersicum leads to enhanced NHP production and defense primingGenetic engineering for enhanced NHP production is a promising strategy to protect crop plants from multiple pathogens

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.

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