scholarly journals Multi-Omics Revealed Molecular Mechanisms Underlying Guard Cell Systemic Acquired Resistance

2020 ◽  
Vol 22 (1) ◽  
pp. 191
Author(s):  
Lisa David ◽  
Jianing Kang ◽  
Daniel Dufresne ◽  
Dan Zhu ◽  
Sixue Chen

Systemic Acquired Resistance (SAR) improves immunity of plant systemic tissue after local exposure to a pathogen. Guard cells that form stomatal pores on leaf surfaces recognize bacterial pathogens via pattern recognition receptors, such as Flagellin Sensitive 2 (FLS2). However, how SAR affects stomatal immunity is not known. In this study, we aim to reveal molecular mechanisms underlying the guard cell response to SAR using multi-omics of proteins, metabolites and lipids. Arabidopsis plants previously exposed to pathogenic bacteria Pseudomonas syringae pv. tomato DC3000 (Pst) exhibit an altered stomatal response compared to control plants when they are later exposed to the bacteria. Reduced stomatal apertures of SAR primed plants lead to decreased number of bacteria in leaves. Multi-omics has revealed molecular components of SAR response specific to guard cells functions, including potential roles of reactive oxygen species (ROS) and fatty acid signaling. Our results show an increase in palmitic acid and its derivative in the primed guard cells. Palmitic acid may play a role as an activator of FLS2, which initiates stomatal immune response. Improved understanding of how SAR signals affect stomatal immunity can aid biotechnology and marker-based breeding of crops for enhanced disease resistance.

2021 ◽  
Author(s):  
Lisa David ◽  
Jianing Kang ◽  
Joshua J Nicklay ◽  
Craig Dufresne ◽  
Sixue Chen

After localized invasion by bacterial pathogens, systemic acquired resistance (SAR) is induced in uninfected plant tissues, resulting in enhanced defense against a broad range of pathogens. Although SAR requires mobilization of signaling molecules via the plant vasculature, the specific molecular mechanisms remain elusive. The lipid transfer protein-defective in induced resistance 1-1 (DIR1-1) was identified in Arabidopsis thaliana by screening for mutants that were defective in SAR. Here we demonstrate that stomatal response to pathogens is altered in systemic leaves by SAR, and this guard cell SAR defense requires DIR1. Using a multi-omics approach, we have determined potential SAR signaling mechanisms specific for guard cells in systemic leaves by profiling metabolite, lipid, and protein differences between guard cells in wild type and dir1-1 mutant during SAR. We identified two 18C fatty acids and two 16C wax esters as putative SAR-related molecules dependent on DIR1. Proteins and metabolites related to amino acid biosynthesis and response to stimulus were also changed in guard cells of dir1-1 compared to wild type. Identification of guard cell-specific SAR-related molecules may lead to new avenues of genetic modification/molecular breeding for disease resistant plants.


2021 ◽  
Vol 8 ◽  
Author(s):  
Lisa David ◽  
Jianing Kang ◽  
Josh Nicklay ◽  
Craig Dufresne ◽  
Sixue Chen

After localized invasion by bacterial pathogens, systemic acquired resistance (SAR) is induced in uninfected plant tissues, resulting in enhanced defense against a broad range of pathogens. Although SAR requires mobilization of signaling molecules via the plant vasculature, the specific molecular mechanisms remain elusive. The lipid transfer protein defective in induced resistance 1 (DIR1) was identified in Arabidopsis thaliana by screening for mutants that were defective in SAR. Here, we demonstrate that stomatal response to pathogens is altered in systemic leaves by SAR, and this guard cell SAR defense requires DIR1. Using a multi-omics approach, we have determined potential SAR signaling mechanisms specific for guard cells in systemic leaves by profiling metabolite, lipid, and protein differences between guard cells in the wild type and dir1-1 mutant during SAR. We identified two long-chain 18 C and 22 C fatty acids and two 16 C wax esters as putative SAR-related molecules dependent on DIR1. Proteins and metabolites related to amino acid biosynthesis and response to stimulus were also changed in guard cells of dir1-1 compared to the wild type. Identification of guard cell-specific SAR-related molecules may lead to new avenues of genetic modification/molecular breeding for disease-resistant plants.


1997 ◽  
Vol 10 (6) ◽  
pp. 716-724 ◽  
Author(s):  
Saskia C. M. Van Wees ◽  
Corné M. J. Pieterse ◽  
Annemiek Trijssenaar ◽  
Yvonne A. M. Van 't Westende ◽  
Femke Hartog ◽  
...  

Selected nonpathogenic, root-colonizing bacteria are able to elicit induced systemic resistance (ISR) in plants. To elucidate the molecular mechanisms underlying this type of systemic resistance, an Arabidopsis-based model system was developed in which Pseudomonas syringae pv. tomato and Fusarium oxysporum f. sp. raphani were used as challenging pathogens. In Arabidopsis thaliana ecotypes Columbia and Landsberg erecta, colonization of the rhizosphere by P. fluorescens strain WCS417r induced systemic resistance against both pathogens. In contrast, ecotype RLD did not respond to WCS417r treatment, whereas all three ecotypes expressed systemic acquired resistance upon treatment with salicylic acid (SA). P. fluorescens strain WCS374r, previously shown to induce ISR in radish, did not elicit ISR in Arabidopsis. The opposite was found for P. putida strain WCS358r, which induced ISR in Arabidopsis but not in radish. These results demonstrate that rhizosphere pseudomonads are differentially active in eliciting ISR in related plant species. The outer membrane lipopolysaccharide (LPS) of WCS417r is the main ISR-inducing determinant in radish and carnation, and LPS-containing cell walls also elicit ISR in Arabidopsis. However, mutant WCS417rOA¯, lacking the O-antigenic side chain of the LPS, induced levels of protection similar to those induced by wild-type WCS417r. This indicates that ISR-inducing bacteria produce more than a single factor that trigger ISR in Arabidopsis. Furthermore, WCS417r and WCS358r induced protection in both wildtype Arabidopsis and SA-nonaccumulating NahG plants without activating pathogenesis-related gene expression. This suggests that elicitation of an SA-independent signaling pathway is a characteristic feature of ISR-inducing biocontrol bacteria.


2007 ◽  
Vol 20 (10) ◽  
pp. 1192-1200 ◽  
Author(s):  
Min Woo Lee ◽  
Hua Lu ◽  
Ho Won Jung ◽  
Jean T. Greenberg

Effector proteins injected by the pathogenic bacteria Pseudomonas syringae into plants can have profound effects on the pathogen–host interaction due to their efficient recognition by plants and the subsequent triggering of defenses. The AvrRpt2 effector triggers strong local and systemic defense (called systemic acquired resistance [SAR]) responses in Arabidopsis thaliana plants that harbor a functional RPS2 gene that encodes an R protein in the coiled-coil, nucleotide-binding domain, leucine-rich repeat class. The newly identified win3-T mutant shows greatly reduced resistance to P. syringae carrying avrRpt2. In win3-T plants, RIN4 cleavage, an early AvrRpt2-induced event, is normal. However, salicylic acid accumulation is compromised, as is SAR induction and the local hypersensitive cell death response after infection by P. syringae carrying avrRpt2. WIN3 encodes a member of the firefly luciferase protein superfamily. Expression of WIN3 at an infection site partially requires PAD4, a protein known to play a quantitative role in RPS2-mediated signaling. WIN3 expression in tissue distal to an infection site requires multiple salicylic acid regulatory genes. Finally, win3-T plants show modestly increased susceptibility to virulent P. syringae and modestly reduced SAR in response to P. syringae carrying avrRpm1. Thus, WIN3 is a key element of the RPS2 defense response pathway and a basal and systemic defense component.


2021 ◽  
Vol 12 ◽  
Author(s):  
Qingfeng Zhou ◽  
Qi Meng ◽  
Xiaomin Tan ◽  
Wei Ding ◽  
Kang Ma ◽  
...  

Systemic acquired resistance (SAR) in plants is a defense response that provides resistance against a wide range of pathogens at the whole-plant level following primary infection. Although the molecular mechanisms of SAR have been extensively studied in recent years, the role of phosphorylation that occurs in systemic leaves of SAR-induced plants is poorly understood. We used a data-independent acquisition (DIA) phosphoproteomics platform based on high-resolution mass spectrometry in an Arabidopsis thaliana model to identify phosphoproteins related to SAR establishment. A total of 8011 phosphorylation sites from 3234 proteins were identified in systemic leaves of Pseudomonas syringae pv. maculicola ES4326 (Psm ES4326) and mock locally inoculated plants. A total of 859 significantly changed phosphoproteins from 1119 significantly changed phosphopeptides were detected in systemic leaves of Psm ES4326 locally inoculated plants, including numerous transcription factors and kinases. A variety of defense response-related proteins were found to be differentially phosphorylated in systemic leaves of Psm ES4326 locally inoculated leaves, suggesting that these proteins may be functionally involved in SAR through phosphorylation or dephosphorylation. Significantly changed phosphoproteins were enriched mainly in categories related to response to abscisic acid, regulation of stomatal movement, plant–pathogen interaction, MAPK signaling pathway, purine metabolism, photosynthesis-antenna proteins, and flavonoid biosynthesis. A total of 28 proteins were regulated at both protein and phosphorylation levels during SAR. RT-qPCR analysis revealed that changes in phosphorylation levels of proteins during SAR did not result from changes in transcript abundance. This study provides comprehensive details of key phosphoproteins associated with SAR, which will facilitate further research on the molecular mechanisms of SAR.


Genetics ◽  
2002 ◽  
Vol 160 (4) ◽  
pp. 1661-1671
Author(s):  
Klaus Maleck ◽  
Urs Neuenschwander ◽  
Rebecca M Cade ◽  
Robert A Dietrich ◽  
Jeffery L Dangl ◽  
...  

Abstract To identify Arabidopsis mutants that constitutively express systemic acquired resistance (SAR), we constructed reporter lines expressing the firefly luciferase gene under the control of the SAR-inducible PR-1 promoter (PR-1/luc). After EMS mutagenesis of a well-characterized transgenic line, we screened 250,000 M2 plants for constitutive expression of the reporter gene in vivo. From a mutant collection containing several hundred putative mutants, we concentrated on 16 mutants lacking spontaneous hypersensitive response (HR) cell death. We mapped 4 of these constitutive immunity (cim) mutants to chromosome arms. Constitutive expression of disease resistance was established by analyzing responses to virulent Peronospora parasitica and Pseudomonas syringae strains, by RNA blot analysis for endogenous marker genes, and by determination of salicylic acid levels in the mutants. The variety of the cim phenotypes allowed us to define distinct steps in both the canonical SAR signaling pathway and a separate pathway for resistance to Erysiphe cichoracearum, active in only a subset of the mutants.


2007 ◽  
Vol 97 (7) ◽  
pp. 794-802 ◽  
Author(s):  
Shobha D. Potlakayala ◽  
Darwin W. Reed ◽  
Patrick S. Covello ◽  
Pierre R. Fobert

Systemic acquired resistance (SAR) is an induced defense response that confers long-lasting protection against a broad range of microbial pathogens. Here we show that treatment of Brassica napus plants with the SAR-inducing chemical benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) significantly enhanced resistance against virulent strains of the bacterial pathogen Pseudomonas syringae pv. maculicola and the fungal pathogen Leptosphaeria maculans. Localized preinoculation of plants with an avirulent strain of P. syringae pv. maculicola also enhanced resistance to these pathogens but was not as effective as BTH treatment. Single applications of either SAR-inducing pretreatment were effective against P. syringae pv. maculicola, even when given more than 3 weeks prior to the secondary challenge. The pretreatments also led to the accumulation of pathogenesis-related (PR) genes, including BnPR-1 and BnPR-2, with higher levels of transcripts observed in the BTH-treatment material. B. napus plants expressing a bacterial salicylate hydroxylase transgene (NahG) that metabolizes salicylic acid to catechol were substantially compromised in SAR and accumulated reduced levels of PR gene transcripts when compared with untransformed controls. Thus, SAR in B. napus displays many of the hallmarks of classical SAR including long lasting and broad host range resistance, association with PR gene activation, and a requirement for salicylic acid.


2019 ◽  
Vol 86 (1) ◽  
pp. 39-47 ◽  
Author(s):  
Hiroyuki Hagiwara ◽  
Rieko Ogura ◽  
Takeshi Fukumoto ◽  
Toshiaki Ohara ◽  
Mikio Tsuda ◽  
...  

Abstract The fungicide tolprocarb (TPC) is a melanin biosynthesis inhibitor, but it may also have another mode of action. Here in tests of TPC for inducing plant systemic acquired resistance (SAR), TPC induced promoter activity of the tobacco pathogenesis-related gene PR-1a in Arabidopsis thaliana and genes for PBZ1, β-1,3-glucanase, and chitinase 1 in the defense-related salicylic acid (SA) signaling pathway in rice, but not genes for the jasmonate signaling pathway. Probenazole (PBZ), a commercially used plant defense activator, induced genes in both signaling pathways. The antibacterial activity of TPC was equivalent to that of PBZ. Irrigation with 200 μM TPC prevented growth by Pseudomonas syringae pv. maculicola in A. thaliana, and 30 μM TPC inhibited Xanthomonas oryzae pv. oryzae growth in rice. The results of this study suggest that TPC functions not only as a melanin biosynthesis inhibitor but also as an SAR inducer and is applicable as a novel bacterial control agent that induces SAR activity in both A. thaliana and rice.


Plant Disease ◽  
2001 ◽  
Vol 85 (5) ◽  
pp. 481-488 ◽  
Author(s):  
F. J. Louws ◽  
M. Wilson ◽  
H. L. Campbell ◽  
D. A. Cuppels ◽  
J. B. Jones ◽  
...  

Acibenzolar-S-methyl (CGA 245704 or Actigard 50WG) is a plant activator that induces systemic acquired resistance (SAR) in many different crops to a number of pathogens. Acibenzolar-S-methyl was evaluated for management of bacterial spot (Xanthomonas axonopodis pv. vesicatoria) and bacterial speck (Pseudomonas syringae pv. tomato) of tomato in 15 and 7 field experiments, respectively. Experiments were conducted over a 4-year period in Florida, Alabama, North Carolina, Ohio, and Ontario using local production systems. Applied at 35 g a.i. ha-1, acibenzolar-S-methyl reduced foliar disease severity in 14 of the 15 bacterial spot and all 7 bacterial speck experiments. Disease control was similar or superior to that obtained using a standard copper bactericide program. Acibenzolar-S-methyl also reduced bacterial fruit spot and speck incidence. Tomato yield was not affected by using the plant activator in the field when complemented with fungicides to manage foliar fungal diseases, but tomato transplant dry weight was negatively impacted. X. axonopodis pv. vesicatoria population densities on greenhouse-grown tomato transplants were reduced by acibenzolar-S-methyl treatment. Bacterial speck and spot population densities on leaves of field-grown plants were not dramatically affected. Acibenzolar-S-methyl can be integrated as a viable alternative to copper-based bactericides for field management of bacterial spot and speck, particularly where copper-resistant populations predominate.


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