- Research article
- Open Access
Salicylic acid signaling inhibits apoplastic reactive oxygen species signaling
© Xu and Brosché; licensee BioMed Central Ltd. 2014
- Received: 13 March 2014
- Accepted: 29 May 2014
- Published: 4 June 2014
Reactive oxygen species (ROS) are used by plants as signaling molecules during stress and development. Given the amount of possible challenges a plant face from their environment, plants need to activate and prioritize between potentially conflicting defense signaling pathways. Until recently, most studies on signal interactions have focused on phytohormone interaction, such as the antagonistic relationship between salicylic acid (SA)-jasmonic acid and cytokinin-auxin.
In this study, we report an antagonistic interaction between SA signaling and apoplastic ROS signaling. Treatment with ozone (O3) leads to a ROS burst in the apoplast and induces extensive changes in gene expression and elevation of defense hormones. However, Arabidopsis thaliana dnd1 (defense no death1) exhibited an attenuated response to O3. In addition, the dnd1 mutant displayed constitutive expression of defense genes and spontaneous cell death. To determine the exact process which blocks the apoplastic ROS signaling, double and triple mutants involved in various signaling pathway were generated in dnd1 background. Simultaneous elimination of SA-dependent and SA-independent signaling components from dnd1 restored its responsiveness to O3. Conversely, pre-treatment of plants with SA or using mutants that constitutively activate SA signaling led to an attenuation of changes in gene expression elicited by O3.
Based upon these findings, we conclude that plants are able to prioritize the response between ROS and SA via an antagonistic action of SA and SA signaling on apoplastic ROS signaling.
- Cell death
- Gene expression
- Jasmonic acid
- Reactive oxygen species
- Salicylic acid
As sessile organisms, plants have evolved a highly sophisticated and elaborate signaling network to respond and adapt to various biotic and abiotic stresses. To precisely respond to diverse stimuli in different tissues or developmental stages, the defense signaling network must be orchestrated within a larger physiological and developmental context. Numerous data from large scale transcriptome profiling analysis strongly support the existence of regulatory interactions and coordination between signaling networks, rather than linear pathways [1, 2]. To some extent the signaling components of this intricate network to biotic and abiotic stresses are universal [3, 4]. Comparing multiple gene expression experiments performed on the Affymetrix ATH1 platform has identified a universal stress response transcriptome . In addition to a general stress response, there are also several studies that indicate that plants are able to prioritize between different stresses and that a combination of stresses leads to unique gene expression profiles [6–10]. Execution of an appropriate defense response is linked to multiple interacting components, including a rapid and transient Reactive Oxygen Species (ROS) burst, altered cytoplasmic and chloroplastic Ca2+ transients, plant hormones including salicylic acid (SA), jasmonic acid (JA), abscisic acid (ABA), ethylene, and transcriptional reprogramming [11–13].
Activation of a ROS burst is a common response to both biotic and abiotic stress [14, 15]. In addition, ROS are signaling molecules involved in control and regulation of other biological processes, such as aging, cell death, and development [16, 17]. Exposure of plants with the gaseous ROS ozone (O3) triggers an apoplastic ROS production, which is similar to the ROS burst observed after pathogen infection and activation of cell wall peroxidases and NADPH oxidases [14, 18, 19]. Extensive comparisons of altered gene expression profiles from Arabidopsis thaliana elicited by O3 and other abiotic and biotic stresses indicate a high degree of overlap between O3 and treatment with a bacterial microbe associated molecular pattern (MAMP) flg22 [13, 20–22]. One of the earliest responses elicited by flg22 treatment is an apoplastic ROS burst [23, 24], thus providing a mechanistic link for the similarity between gene expression changes elicited by O3 and flg22. Apoplastic ROS are also regulators of cell death through interplay with several other signaling pathways, including SA and JA/ethylene signaling pathways .
SA, JA, and ethylene are involved in many aspects of defense signaling and numerous studies have investigated the interaction between these hormones . It is generally believed that antagonism between SA and JA allows plants to prioritize the defense between biotrophic or necrotrophic pathogens and insects. SA antagonism of JA signaling is a robust response observed both when plants are infected with different pathogens ; and when plants are directly treated with hormones . Regulators of the SA-JA antagonism include the SA receptor/transcriptional co-activator NPR1 and the transcription factor ORA59 [29, 30]. Several additional signals directly or indirectly interplay with SA to promote defense response . Early in 1990s, SA level and ROS (e.g. H2O2) production were found to be closely connected . Both elevated endogenous SA and application of exogenous SA in Arabidopsis and tobacco are accompanied by increased ROS (H2O2 and O2-) production [33–36], indicating the existence of a positive feedback amplification loop with SA and ROS as central players. However, continuous defense signal amplification would waste energy and indicate that coordination of SA-dependent and independent signaling components with ROS signaling are of central importance to provide an appropriate defense response.
Lesion mimic mutants that display spontaneous cell death have been extensively used to study the regulation of cell death . In addition to misregulated cell death they often have other phenotypes including dwarfism, constitutively higher accumulation of SA and enhanced pathogen resistance [38, 39]. Some of them show accumulation of ROS (H2O2 and O2-) in or around the lesion area , which make lesion mimic mutants a powerful tool to investigate the relationship between ROS and SA. In genetic analysis, production of SA can be reduced by the mutation sid2, which is defective in the main biosynthesis pathway (ISOCHORISMATE SYNTHASE1, ICS1), or by expression of a bacterial SA degrading enzyme NahG. In several lesion mimic mutants, including acd6, acd11 and lht1 expression of NahG abolishes cell death [41–43]. Given the importance of SA in defense signaling it is not surprising that several other regulators working in parallel with SA signaling, or affecting SA accumulation, have been identified through various screens including suppression of lesion mimic phenotypes [44–46]. These regulators include ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1), AG2-LIKE DEFENSE RESPONSE PROTEIN1 (ALD1) and FLAVIN-DEPENDENT MONOXYGENASE1 (FMO1) which regulate cell death and defense responses [46–49]. Like SID2, ALD1 and FMO1 are necessary for systemic accumulation of SA and downstream signaling after pathogen infection [49, 50]. Furthermore, a chloroplastic derived O2- signal can be processed by EDS1 to control SA-dependent H2O2 accumulation as part of a mechanism limiting cell death .
Elevation of cytosolic Ca2+ and production of ROS are among the earliest events after initiation of stress responses . Many studies have explored the role of CNGC2 (CYCLIC NUCLEOTIDE GATED CHANNEL2) in regulation of Ca2+ fluxes across the plasma membrane and its contribution to signaling in the context of immunity [53, 54], senescence , heat stress , and pollen growth . Null mutation of CNGC2 was first isolated as defense no death1 (dnd1), a mutant which exhibits a lesion mimic phenotype which is dependent on growth conditions , increased accumulation of SA and constitutive defense activation , and altered Ca2+ transport . Studies conducted in this mutant indicate that the influx of Ca2+ is associated with the pleiotropic phenotype; however, the precise mechanism with regards to Ca2+ signaling is still elusive. Furthermore, whereas in wildtype O3 strongly alters transcript levels for many defense genes, in dnd1 this response is blocked . Due to the pleiotropic phenotype of dnd1 it is far from straight forward to pinpoint the exact process which blocks the apoplastic ROS signal initiated by O3 treatment. In this study we investigate through genetic analysis the relationship between dnd1, the hormones SA, JA and ethylene, and apoplastic ROS signaling in the regulation of defense gene expression and cell death. In particular, we identify a novel antagonistic interplay between SA and apoplastic ROS signaling that may confer a high degree of responsiveness of plant responses to a fluctuating environment.
The dnd1mutant displays constitutive expression of defense genes
Mutants with constitutive defense activation are defective in ROS signaling
Consistent with previous characterization of these mutants as constitutive defense mutants, a majority of the marker genes, including PAD3, SAG21, WRKY40 and WRKY75, had increased expression in the mutants as compared to Col-0 in control conditions (Figure 2b; note the logarithmic scale). A two hour O3 treatment led to strong induction of the defense genes in Col-0, whereas the effect of O3 was attenuated in all of the constitutive defense mutants, which was more pronounced in dnd1 (Figure 2b). We conclude that constitutive activation of defense signaling in several different mutants interfere with the plants ability to properly respond to a ROS signal from the apoplast.
SA signaling inhibits apopastic ROS signaling
Elimination of SA in dnd1partially restores its response to apoplastic ROS
Morphology and amount of cell death in dnd1 single, double and triple mutants
Size of the rossette
Reference to single mutant
Slim and curled leaves
MAP kinase phosphatase
More curled leaves than dnd1
Note: Highly dwarfed, seedless
More curled leaves than dnd1
Note: No trichomes, male sterile
Wider leaves than dnd1
Wider leaves than dnd1
Note: Bleached leaves
Leaf is less curled than dnd1 single mutant
G protein subunits
Round leaf shape
Wider leaves than dnd1
Note: Slow growth, difficult to obtain seeds
R gene mediated proteins/Defense
Note: Few seeds
dnd1 sid2 ald1
Wider leaves than dnd1
dnd1 sid2 eds1
Wider leaves than dnd1
dnd1 aos sid2
Wider leaves than dnd1
Note: No trichomes, male sterile
dnd1 sid2 pad4
Wider leaves than dnd1
dnd1 ald1 pad4
Wider leaves than dnd1
The name given to dnd1, defense no death, was based on its lack of pathogen induced cell death . Numerous other mutants with spontaneous cell death and elevated levels of SA have been identified and includes accelerated cell death 5 (acd5) and CALMODULIN BINDING TRANSCRIPTION ACTIVATOR (CAMTA3/sr1) [90, 91]. To further explore if the cell death phenotype of dnd1 was due to activation of similar signaling pathway as in other lesion mimic mutants, we introduced the acd5 and sr1 mutations into the dnd1 background. The lesion and dwarfism phenotype in the resulting double mutants were severely enhanced, indicating that dnd1 activated cell death in parallel pathways to acd5 and sr1 (Figure 5 and Additional file 2).
Several SA dependent and independent regulators additively contribute to the attenuated apoplastic ROS response
JA signaling restricts lesion formation
Interplay between the hormones SA and JA optimizes the response to abiotic and biotic stresses [12, 92]. In addition, the JA insensitive mutants jar1 and coi1 have previously been shown to be sensitive to O3[14, 18, 21]. To gain further insight into the role of JA in the dnd1 pleiotropic phenotypes, a mutation that blocks JA biosynthesis , allene oxide synthase (aos) was introduced into dnd1 and dnd1sid2. The dnd1aos double mutants showed severe dwarfism compared to dnd1 single mutant (Figure 7 and Additional file 2). Similar to the dnd1 single mutant, the dnd1aos double mutant had an attenuated gene expression response after two hours O3 treatment (Figure 8). Simultaneous mutations of both SA and JA signaling in dnd1sid2aos relieved the growth retardance of the dnd1aos double mutant, but induced more visible chlorosis than either dnd1aos or dnd1sid2 double mutants (Figure 7). We conclude that JA has no major role in the attenuation of apoplastic ROS signaling, but is involved in regulation of plant development and cell death in the dnd1 background.
Constitutive activation of ethylene signaling does not impact on apoplastic ROS signaling
Treatment of Arabidopsis with flg22 rapidly activates an apoplastic RBOH-dependent ROS burst , and in turn induces SA related genes, including SID2, PR1 and NPR1 (NON-EXPRESSOR OF PR GENES1) [69, 96, 97]. Meta-analysis of microarray data shows that 4 hours flg22 treatment triggers similar changes in gene expression as elicited by an apoplastic ROS burst with O3, implying that flg22 and O3 induce similar apoplastic ROS signals. Consistent with our findings that dnd1 has an attenuated response to O3 (Figure 2b), flg22 triggered oxidative burst was significantly reduced in dnd1. Flg22 treatment can reduce SA induced changes in gene expression , the same type of interaction observed between apoplastic ROS and SA described in this study (Figure 3). This suggests that the effect of flg22 on SA mediated gene expression could be mediated via an apoplastic ROS burst.
If the flg22-SA and apoplastic ROS-SA antagonisms are two aspects of the same biological phenomenon, what benefit does this antagonism provide to the plant? Activating plant defenses is costly to the plant, and given the large number of potential biotic and abiotic challenges that a plant could face, it has a clear need to prioritize which challenge should be given the highest priority. This forms the basis for SA-JA antagonism where defense against insects and necrotrophic fungi rely on the JA branch and defense against biotrophic pathogens on the SA branch. The apoplastic ROS burst could have different sources, either locally from e.g. activation of RBOH or cell wall peroxidases by an invading pathogen or from systemic signaling, the so called ROS wave. The ROS wave is mediated by RBOHD generated ROS production and its ability to travel along the plant suggests that it could act as a systemic signal in response to various environmental stimuli . Thus, there could be a situation where one part of the plant has already initiated SA mediated defenses due to e.g. pathogen attack, would subsequently be the recipient of the ROS wave from another part of the plant. In this situation it might be preferable to execute the already initiated local defense program and put lower emphasis on the systemic ROS signal. This might reveal itself as the antagonism by SA on apoplastic ROS signaling observed in this study and could be a beneficial way for the plant to respond and prioritize between different environmental stimuli.
Lesion mimic mutants have been crucial to identify various regulators of cell death, including the role of hormones and ROS [37, 100]. As a lesion mimic mutant, dnd1 also contributes to the study of e.g. the potential role of Ca2+ in cell death regulation. The extensive double mutant collection generated in this work to study the role of apoplastic ROS signaling also allow the dissection of signaling pathways involved in regulation of cell death in dnd1. Of the 22 double mutants and seven triple mutants generated, many of them did not alter the extent of cell death, thus excluding a role for MAP kinases, G-proteins and several transcription factors in execution of cell death in dnd1 (Table 1). However there were several informative mutant combinations mainly related to ethylene, JA, SA and SA-related processes. The ethylene mutants (etr1-1, ein2) and JA biosynthesis mutant (aos) enhanced growth defects of dnd1, but did not alter the extent of cell death, implicating that these hormonal signal pathways in the dnd1 background are not strictly required for cell death execution. In contrast, ein2 enhances cell death in the lesion mimic double mutant syp121syp122 and the JA insensitive coi1 (coronatine insensitive1) enhances the lesions in hrl1 (hypersensitive response-like lesions1) [102, 103]. Thus, the requirements for ethylene and JA in cell death regulation appear to be context dependent.
SA is a crucial regulator of cell death shown by introducing the SA deficient mutant sid2 or a bacterial salicylate hydroxylase (NahG) into several lesion mimic mutants, including acd6, atg5, and dnd1[37, 46, 104]. These observations indicate that biosynthesis of SA via ICS1 acts as a central hub of a SA inducing cell death program. However, SA depletion by introducing sid2 could only partially relieve the cell death in dnd1. Several other mutations which are typically associated with or acting in parallel with SA also partially reduced cell death in dnd1 and included eds1, pad4, ald1 and fmo1 (Table 1; Additional file 2). Furthermore, substantially reduced cell death and improved growth was observed in triple mutants with ald1, eds1, fmo1 or pad4 in the dnd1sid2 background (Figure 5 and Additional file 2). FMO1 is a suggested positive regulator of cell death . ALD1 is associated with biosynthesis of Pip (a non-protein amino acid pipecolic acid, a product of lysine degradation). Endogenous Pip is a regulator of SAR (systemic acquired resistance) and contributes to defense and SA signal amplification . Since cell death was further reduced in dnd1ald1sid2 as compared to the double mutants dnd1sid2 and dnd1ald1, this indicates that SA and the lysine catabolite Pip function synergistically in regulating cell death (Figure 10b). EDS1 and PAD4 are interacting proteins that play multiple roles in plant defenses, including regulation of cell death and amplification of transcriptional responses . Expression of EDS1 is negatively regulated by CAMTA3/SR1 (a CaM binding transcription factor) . Mutation of CAMTA3/SR1 in dnd1 background resulted in enhanced cell death (Figure 5), possibly a result of increased EDS1 signaling and increased SA production in dnd1sr1.
Extensive double and triple mutant analysis to find regulators of cell death has been done in the background of acd6 and syp121syp122[46, 101]. ACD6 encodes a plasma membrane protein with a cytoplasmic ankyrin repeat motif, but how this protein migh activate cell death is unknown. The syp121syp122 double mutant lacks two syntaxin proteins which are part of the SNARE machinery, controlling vesicle traffic and bulk transport of cargo in cells. Despite the different biological processes impaired in dnd1, acd6 and syp121syp122, exactly the same regulators were found to be the crucial in all three lesion mimic mutants, and implicate SA biosynthesis (via SID2), in combination with EDS1, PAD4, ALD1 or FMO1 as the major pathway towards cell death. Furthermore, other double mutants between various lesion mimic mutants and i.e. sid2 or eds1 show the same suppression of cell death and include acd11, lsd1, ssi2 and lht1. Thus in contrast to the context dependence of JA or ethylene for cell death execution, the requirement for SA and EDS1 appears more universal.
Future research should focus on how EDS1, PAD4, ALD1 and FMO1 interact with SA to regulate cell death. It is unlikely that low SA accumulation on its own would be sufficient to fully prevent cell death [46, 48, 59]. EDS1 shuttles between the cytoplasm and nucleus, where nuclear EDS1 localization regulates defense gene expression  and cytosolic EDS1 regulates cell death . However, SA might be more likely to execute its function through changes in gene expression. Thus one potential explanation for the full suppression of cell death in lesion mimics when both sid2 and eds1 are mutated could be that both nuclear and cytosolic regulators of cell death are removed. ALD1-dependent Pip accumulation in systemic leaves during SAR is dependent on FMO1, indicating that there is possible signal amplification loop between Pip, ALD1, FMO1 and SA [49, 109]. All together, we propose a signaling network where ALD1, EDS1, and FMO1 work synergistically with SA to induce cell death in lesion mimic mutants (Figure 10b).
In summary, we have identified an antagonistic relationship between SA and apoplastic ROS signaling that regulate defense gene expression in plants. This mechanism is likely timing and context dependent. Furthermore, identification of regulatory components required for execution of cell death in dnd1 reinforces the crucial role of SA, ALD1 and EDS1 in cell death regulation. How the altered cytosolic Ca2+ transport in dnd1 connects to downstream signaling pathways will require more studies and may include a recently identified dnd1 suppressor mutant, repressor of defense no death1 (rdd1) .
Plant materials and growth conditions
Mutant seeds were obtained from the Nottingham Arabidopsis Stock Centre (NASC; http://arabidopsis.info/) or were gifts from Dr Günter Brader (wrky70), Dr Hans Thordal-Christensen (ald1, fmo1), Dr Heribert Hirt (mpk3, mpk6), Dr. Jeff Dangl (rar1-21), Dr. Alan Jones (gpa1, agb1), Dr. Bonnie Bartel (ibr5), Dr Miguel Torres (rbohD, rbohF) and Dr. Roberto Solano (jin1). Wild type Arabidopsis accession Columbia-0 (Col-0) was used as control plant for all experiments. Double and triple mutants were constructed using dnd1 as pollen acceptor. All mutants were in the Col-0 background, double and triple mutants were screened for the visible dnd1 mutant phenotype (dwarf, curly leaves, and early senescence) and subsequently genotyped using PCR-based CAPS, dCAPS and T-DNA markers (see Additional file 3). The homozygosity of all double and triple mutants was confirmed in F3 or F4 generations.
Seeds were sown on germination medium containing ½ Murashige and Skoog (MS) and 0.4% phyto gel, stratified for three days, the plates were placed at 22°C/19°C under a 12-h light/12-h dark cycle for one week. Subsequently, one week old plants were transplanted into 1:1 peat: vermiculite mixture, five seedlings per pot (8 × 8 cm), grown at 22°C/19°C, and relative humidity of 70%/90%, under a 12-h light/12-h dark cycle for two weeks. All plants were grown in controlled environment growth chambers (Weiss Bio1300; Weiss Gallenkamp). Three weeks old plants were used for all experiments. Plants for O3 treatment and clean air control were randomized and grown side by side in identical environment.
Ozone and SA treatment
O3 treatment was started at 9 am. Three weeks old plants were exposed with 350 nL L-1 ozone for two hours. To study the role of SA, Col-0 was treated with 0.3mM and 1 mM SA for 24-hr before ozone exposure. All samples were harvested in parallel from ozone treated and clean air control after the onset of ozone treatment, and immediately shock-frozen in liquid nitrogen.
Determination of cell death
Three and five week old plants grown in clean air were used for trypan blue staining. From three rosettes per genotype and staining, one fully expanded and representative leaf (not the oldest leaf) was used for figures. The experiment was repeated at least three times per genotype. Trypan blue stain was performed as previously described in .
5-15 plants per genotype from control or O3 treatment were pooled, frozen in liquid nitrogen and stored at -80°C. Total RNA was extracted using GeneJet Plant RNA purification Mini Kit (Fermentas, now part of Thermo Scientific).
RNA was isolated from three to four week old Col-0 and dnd1 plants. RNA samples from six biological replicates were used for cDNA synthesis, labeling with Cy3 and Cy5, and array hybridization was done as previously described . Full experimental details and raw data are available from ArrayExpress, accession number E-MEXP-3768. The dnd1 raw data and Affymetrix raw data were processed with robust multiarray average normalization using Bioconductor limma and affy packages in R [112, 113]. Gene expression for each experiment was computed by log2-base fold changes between treatment and control, or between wild type and mutants. The processed data was discretized and clustered using Bayesian Hierarchical Clustering method, as implemented in the R package BHC . Bootstrap analysis was done as previously described in .
Raw data from the Affymetrix ATH1-121501 platform was obtained from several data sources: NASC Arrays http://affymetrix.arabidopsis.info/link_to_iplant.shtml (BTH, NASCARRAYS-392; Senescence experiment 1, NASCARRAYS-52; Senescence experiment 2, NASCARRAYS-150; SA, NASCARRAYS-192). (ArrayExpress http://www.ebi.ac.uk/arrayexpress/ (MeJA, EATMX-13) Gene Expression Omnibus http://www.ncbi.nlm.nih.gov/geo/ (H2O2, GSE5530; Syringolin, E-MEXP-739; csn3, csn4 and csn5, GSE9728; lht1, GSE19109; mkk1mkk2, GSE10646; sni1, GSE6827; siz1, GSE6583; SA 24 h, GSE14961; Ethylene, GSE14247; Flg22, GSE5615; Botrytis cinerea infection, GSE5684; Pseudomonas syringae ES4326, GSE18978;). Raw data for acd11 were obtained from John Munday.
Real-time quantitative PCR analysis
Two ug of RNA was DNAseI treated and used for cDNA synthesis with RevertAid Premium Reverse Transcriptase according to the manufactures’ instructions (Fermentas, now part of Thermo Scientific). The reverse transcription reaction was diluted to a final volume of 100 ul, and 1 ul was used per PCR reaction. Quantitative PCR was performed in triplicate with EvaGreen Supermix (Solis Biodyne) on a CFX384 thermal cycler 1000 (Bio-Rad). The cycle condition was performed as previously described . Three reference genes (SAND, TIP41, YLS8) were used for normalization. Amplification efficiency of all primer pairs were calculated through amplification of serially diluted cDNA. Primer sequences and amplification efficiency are listed in Additional file 4. Gene expression analysis was performed using qBaseplus2 (Biogazelle). At least three biological repeats per experiment were used for analysis. Statistical analysis was calculated by two-way ANOVA with Tukey-test using SigmaPlot 11.0.
We thank Leena Grönholm for plant care, Tuomas Puukko for excellent technical assistance and photography, Johanna Leppälä and Lauri Vaahtera for comments on the manuscript and Jarkko Salojärvi for help with clustering. We acknowledge the Finnish DNA Microarray Center (Turku Centre for Biotechnology) for manufacturing the microarrays used in this study. This research was supported by the Academy of Finland (grants: 135751, 140981 and 273132 to M.B). E.X. is a member of the Finnish Doctoral Program in Plant Science.
- Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM: Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci U S A. 2000, 97 (21): 11655-11660. 10.1073/pnas.97.21.11655.PubMed CentralPubMedGoogle Scholar
- Cheong YH, Chang H-S, Gupta R, Wang X, Zhu T, Luan S: Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002, 129 (2): 661-677. 10.1104/pp.002857.PubMed CentralPubMedGoogle Scholar
- Bowler C, Fluhr R: The role of calcium and activated oxygens as signals for controlling cross-tolerance. Trends Plant Sci. 2000, 5 (6): 241-246. 10.1016/S1360-1385(00)01628-9.PubMedGoogle Scholar
- Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K: Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol. 2006, 9 (4): 436-442. 10.1016/j.pbi.2006.05.014.PubMedGoogle Scholar
- Ma S, Bohnert HJ: Integration of Arabidopsis thaliana stress-related transcript profiles, promoter structures, and cell-specific expression. Genome Biol. 2007, 8 (4): R49-10.1186/gb-2007-8-4-r49.PubMed CentralPubMedGoogle Scholar
- Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R: When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 2004, 134 (4): 1683-1696. 10.1104/pp.103.033431.PubMed CentralPubMedGoogle Scholar
- Vaahtera L, Brosché M: More than the sum of its parts–how to achieve a specific transcriptional response to abiotic stress. Plant Sci. 2011, 180 (3): 421-430. 10.1016/j.plantsci.2010.11.009.PubMedGoogle Scholar
- Tognetti VB, Mühlenbock P, Van Breusegem F: Stress homeostasis–the redox and auxin perspective. Plant Cell Environ. 2012, 35 (2): 321-333. 10.1111/j.1365-3040.2011.02324.x.PubMedGoogle Scholar
- Atkinson NJ, Lilley CJ, Urwin PE: Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol. 2013, 162 (4): 2028-2041. 10.1104/pp.113.222372.PubMed CentralPubMedGoogle Scholar
- Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Bones AM, Nielsen HB, Mundy J: Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol. 2013, 161 (4): 1783-1794. 10.1104/pp.112.210773.PubMed CentralPubMedGoogle Scholar
- Bari R, Jones JD: Role of plant hormones in plant defence responses. Plant Mol Biol. 2009, 69 (4): 473-488. 10.1007/s11103-008-9435-0.PubMedGoogle Scholar
- Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC: Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol. 2012, 28: 489-521. 10.1146/annurev-cellbio-092910-154055.PubMedGoogle Scholar
- Sierla M, Rahikainen M, Salojärvi J, Kangasjärvi J, Kangasjärvi S: Apoplastic and chloroplastic redox signaling networks in plant stress responses. Antioxid Redox Signal. 2013, 18 (16): 2220-2239. 10.1089/ars.2012.5016.PubMedGoogle Scholar
- Overmyer K, Brosché M, Pellinen R, Kuittinen T, Tuominen H, Ahlfors R, Keinänen M, Saarma M, Scheel D, Kangasjärvi J: Ozone-induced programmed cell death in the Arabidopsis radical-induced cell death1 mutant. Plant Physiol. 2005, 137 (3): 1092-1104. 10.1104/pp.104.055681.PubMed CentralPubMedGoogle Scholar
- Nanda AK, Andrio E, Marino D, Pauly N, Dunand C: Reactive Oxygen Species during Plant‒microorganism Early Interactions. J Integr Plant Biol. 2010, 52 (2): 195-204. 10.1111/j.1744-7909.2010.00933.x.PubMedGoogle Scholar
- Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R: Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol. 2011, 14 (6): 691-699. 10.1016/j.pbi.2011.07.014.PubMedGoogle Scholar
- Wrzaczek M, Brosché M, Kangasjärvi J: ROS signaling loops-production, perception, regulation. Curr Opin Plant Biol. 2013, 16 (5): 575-582. 10.1016/j.pbi.2013.07.002.PubMedGoogle Scholar
- Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjärvi J: Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell. 2000, 12 (10): 1849-1862. 10.1105/tpc.12.10.1849.PubMed CentralPubMedGoogle Scholar
- Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel HJ, Overmyer K, Kangasjärvi J, Sandermann H, Langebartels C: Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell Environ. 2002, 25 (6): 717-726. 10.1046/j.1365-3040.2002.00859.x.Google Scholar
- Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjärvi J: Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol. 2010, 10 (1): 95-10.1186/1471-2229-10-95.PubMed CentralPubMedGoogle Scholar
- Blomster T, Salojärvi J, Sipari N, Brosché M, Ahlfors R, Keinänen M, Overmyer K, Kangasjärvi J: Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol. 2011, 157 (4): 1866-1883. 10.1104/pp.111.181883.PubMed CentralPubMedGoogle Scholar
- Vaahtera L, Brosché M, Wrzaczek M, Kangasjärvi J: Specificity in ROS signaling and transcript signatures. Antioxid Redox Signal. 2013, http://dx.doi.org/10.1089/ars.2013.5662,Google Scholar
- Mersmann S, Bourdais G, Rietz S, Robatzek S: Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 2010, 154 (1): 391-400. 10.1104/pp.110.154567.PubMed CentralPubMedGoogle Scholar
- Dubiella U, Seybold H, Durian G, Komander E, Lassig R, Witte C-P, Schulze WX, Romeis T: Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A. 2013, 110 (21): 8744-8749. 10.1073/pnas.1221294110.PubMed CentralPubMedGoogle Scholar
- Overmyer K, Brosché M, Kangasjärvi J: Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 2003, 8 (7): 335-342. 10.1016/S1360-1385(03)00135-3.PubMedGoogle Scholar
- Robert-Seilaniantz A, Grant M, Jones JD: Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol. 2011, 49: 317-343. 10.1146/annurev-phyto-073009-114447.PubMedGoogle Scholar
- Spoel SH, Johnson JS, Dong X: Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc Natl Acad Sci U S A. 2007, 104 (47): 18842-18847. 10.1073/pnas.0708139104.PubMed CentralPubMedGoogle Scholar
- Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon L, Pieterse CM: Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 2008, 147 (3): 1358-1368. 10.1104/pp.108.121392.PubMed CentralPubMedGoogle Scholar
- Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux J-P, Brown R, Kazan K: NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell. 2003, 15 (3): 760-770. 10.1105/tpc.009159.PubMed CentralPubMedGoogle Scholar
- Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, Pauwels L, Goossens A, Körbes AP, Memelink J, Ritsema T: Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell. 2013, 25 (2): 744-761. 10.1105/tpc.112.108548.PubMed CentralPubMedGoogle Scholar
- Vlot AC, Dempsey DMA, Klessig DF: Salicylic acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol. 2009, 47: 177-206. 10.1146/annurev.phyto.050908.135202.PubMedGoogle Scholar
- Chen Z, Silva H, Klessig DF: Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science. 1993, 262 (5141): 1883-1886. 10.1126/science.8266079.PubMedGoogle Scholar
- Kawano T, Sahashi N, Takahashi K, Uozumi N, Muto S: Salicylic acid induces extracellular superoxide generation followed by an increase in cytosolic calcium ion in tobacco suspension culture: the earliest events in salicylic acid signal transduction. Plant Cell Physiol. 1998, 39 (7): 721-730. 10.1093/oxfordjournals.pcp.a029426.Google Scholar
- Kawano T, Muto S: Mechanism of peroxidase actions for salicylic acid‒induced generation of active oxygen species and an increase in cytosolic calcium in tobacco cell suspension culture. J Exp Bot. 2000, 51 (345): 685-693. 10.1093/jexbot/51.345.685.PubMedGoogle Scholar
- Khokon M, Okuma E, Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y: Involvement of extracellular oxidative burst in salicylic acid‒induced stomatal closure in Arabidopsis. Plant Cell Environ. 2011, 34 (3): 434-443. 10.1111/j.1365-3040.2010.02253.x.PubMedGoogle Scholar
- Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y: SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid‒induced accumulation of reactive oxygen species in Arabidopsis. Plant J. 2013, 73 (1): 91-104. 10.1111/tpj.12014.PubMedGoogle Scholar
- Lorrain S, Vailleau F, Balagué C, Roby D: Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?. Trends Plant Sci. 2003, 8 (6): 263-271. 10.1016/S1360-1385(03)00108-0.PubMedGoogle Scholar
- Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X: Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol. 2007, 17 (20): 1784-1790. 10.1016/j.cub.2007.09.025.PubMedGoogle Scholar
- Monaghan J, Germain H, Weihmann T, Li X: Dissecting plant defence signal transduction: modifiers of snc1 in Arabidopsis. Can J Plant Pathol. 2010, 32 (1): 35-42. 10.1080/07060661003621001.Google Scholar
- Jabs T, Dietrich RA, Dangl JL: Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide. Science. 1996, 273 (5283): 1853-1856. 10.1126/science.273.5283.1853.PubMedGoogle Scholar
- Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT: The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell. 1999, 11 (9): 1695-1708. 10.1105/tpc.11.9.1695.PubMed CentralPubMedGoogle Scholar
- Brodersen P, Malinovsky FG, Hématy K, Newman M-A, Mundy J: The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol. 2005, 138 (2): 1037-1045. 10.1104/pp.105.059303.PubMed CentralPubMedGoogle Scholar
- Liu G, Ji Y, Bhuiyan NH, Pilot G, Selvaraj G, Zou J, Wei Y: Amino acid homeostasis modulates salicylic acid–associated redox status and defense responses in Arabidopsis. Plant Cell. 2010, 22 (11): 3845-3863. 10.1105/tpc.110.079392.PubMed CentralPubMedGoogle Scholar
- Yoshioka K, Kachroo P, Tsui F, Sharma SB, Shah J, Klessig DF: Environmentally sensitive, SA‒dependent defense responses in the cpr22 mutant of Arabidopsis. Plant J. 2001, 26 (4): 447-459.PubMedGoogle Scholar
- Jurkowski GI, Smith RK, Yu IC, Ham JH, Sharma SB, Klessig DF, Fengler KA, Bent AF: Arabidopsis DND2, a second cyclic nucleotide-gated ion channel gene for which mutation causes the “defense, no death” phenotype. Mol Plant Microbe Interact. 2004, 17 (5): 511-520. 10.1094/MPMI.2004.17.5.511.PubMedGoogle Scholar
- Ng G, Seabolt S, Zhang C, Salimian S, Watkins TA, Lu H: Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis. Genetics. 2011, 189 (3): 851-859. 10.1534/genetics.111.132332.PubMed CentralPubMedGoogle Scholar
- Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, Parker JE: Salicylic acid–independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the nudix hydrolase NUDT7. Plant Cell. 2006, 18 (4): 1038-1051. 10.1105/tpc.105.039982.PubMed CentralPubMedGoogle Scholar
- Venugopal SC, Jeong R-D, Mandal MK, Zhu S, Chandra-Shekara A, Xia Y, Hersh M, Stromberg AJ, Navarre D, Kachroo A: Enhanced disease susceptibility 1 and salicylic acid act redundantly to regulate resistance gene-mediated signaling. PLoS Genet. 2009, 5 (7): e1000545-10.1371/journal.pgen.1000545.PubMed CentralPubMedGoogle Scholar
- Návarová H, Bernsdorff F, Döring A-C, Zeier J: Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. Plant Cell. 2012, 24 (12): 5123-5141. 10.1105/tpc.112.103564.PubMed CentralPubMedGoogle Scholar
- Song JT, Lu H, McDowell JM, Greenberg JT: A key role for ALD1 in activation of local and systemic defenses in Arabidopsis. Plant J. 2004, 40 (2): 200-212. 10.1111/j.1365-313X.2004.02200.x.PubMedGoogle Scholar
- Straus MR, Rietz S, Ver Loren Van Themaat E, Bartsch M, Parker JE: Salicylic acid antagonism of EDS1‒driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J. 2010, 62 (4): 628-640. 10.1111/j.1365-313X.2010.04178.x.PubMedGoogle Scholar
- Steinhorst L, Kudla J: Calcium and Reactive Oxygen Species Rule the Waves of Signaling. Plant Physiol. 2013, 163 (2): 471-485. 10.1104/pp.113.222950.PubMed CentralPubMedGoogle Scholar
- Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao Y, Ryan CA, Berkowitz GA: Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proc Natl Acad Sci U S A. 2010, 107 (49): 21193-21198. 10.1073/pnas.1000191107.PubMed CentralPubMedGoogle Scholar
- Ma W, Berkowitz GA: Leaf senescence signaling: Ca2+ conduction by plant cyclic nucleotide gated channels and associated signaling components in pathogen defense signal transduction cascades. New Phytol. 2010, 190 (3): 566-572.PubMedGoogle Scholar
- Ma W, Smigel A, Walker RK, Moeder W, Yoshioka K, Berkowitz GA: The Ca2+-conducting Arabidopsis cyclic nucleotide gated channel2 acts through nitric oxide to repress senescence programming. Plant Physiol. 2010, 154 (2): 733-743. 10.1104/pp.110.161356.PubMed CentralPubMedGoogle Scholar
- Finka A, Cuendet AFH, Maathuis FJ, Saidi Y, Goloubinoff P: Plasma membrane cyclic nucleotide gated calcium channels control land plant thermal sensing and acquired thermotolerance. Plant Cell. 2012, 24 (8): 3333-3348. 10.1105/tpc.112.095844.PubMed CentralPubMedGoogle Scholar
- Chaiwongsar S, Strohm AK, Roe JR, Godiwalla RY, Chan CW: A cyclic nucleotide‒gated channel is necessary for optimum fertility in high‒calcium environments. New Phytol. 2009, 183 (1): 76-87. 10.1111/j.1469-8137.2009.02833.x.PubMedGoogle Scholar
- Clough SJ, Fengler KA, Yu LC, Lippok B, Smith RK, Bent AF: The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A. 2000, 97 (16): 9323-9328. 10.1073/pnas.150005697.PubMed CentralPubMedGoogle Scholar
- Genger RK, Jurkowski GI, McDowell JM, Lu H, Jung HW, Greenberg JT, Bent AF: Signaling pathways that regulate the enhanced disease resistance of Arabidopsis “defense, no death” mutants. Mol Plant Microbe Interact. 2008, 21 (10): 1285-1296. 10.1094/MPMI-21-10-1285.PubMed CentralPubMedGoogle Scholar
- Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA: Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell. 2007, 19 (3): 1081-1095. 10.1105/tpc.106.045096.PubMed CentralPubMedGoogle Scholar
- Yu LC, Parker J, Bent AF: Gene-for-gene disease resistance without the hypersensitive response in Arabidopsis dnd1 mutant. Proc Natl Acad Sci U S A. 1998, 95 (13): 7819-7824. 10.1073/pnas.95.13.7819.PubMed CentralPubMedGoogle Scholar
- Chan CW, Wohlbach DJ, Rodesch MJ, Sussman MR: Transcriptional changes in response to growth of Arabidopsis in high external calcium. FEBS Lett. 2008, 582 (6): 967-976. 10.1016/j.febslet.2008.02.043.PubMedGoogle Scholar
- Dohmann EM, Levesque MP, De Veylder L, Reichardt I, Jürgens G, Schmid M, Schwechheimer C: The Arabidopsis COP9 signalosome is essential for G2 phase progression and genomic stability. Development. 2008, 135 (11): 2013-2022. 10.1242/dev.020743.PubMedGoogle Scholar
- Simanshu DK, Zhai X, Munch D, Hofius D, Markham JE, Bielawski J, Bielawska A, Malinina L, Molotkovsky JG, Mundy JW, Patel DJ, Brown RE: Arabidopsis Accelerated Cell Death 11, ACD11, Is a Ceramide-1-Phosphate Transfer Protein and Intermediary Regulator of Phytoceramide Levels. Cell Rep. 2014, 6 (2): 388-399. 10.1016/j.celrep.2013.12.023.PubMed CentralPubMedGoogle Scholar
- Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, MacKinlay J, Loake GJ, Mundy J, Morris PC: Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol. 2008, 148 (1): 212-222. 10.1104/pp.108.120006.PubMed CentralPubMedGoogle Scholar
- Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC: Salicylic acid‒mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J. 2007, 49 (1): 79-90.PubMedGoogle Scholar
- Maleck K, Neuenschwander U, Cade RM, Dietrich RA, Dangl JL, Ryals JA: Isolation and characterization of broad-spectrum disease-resistant Arabidopsis mutants. Genetics. 2002, 160 (4): 1661-1671.PubMed CentralPubMedGoogle Scholar
- Ahlfors R, Brosché M, Kollist H, Kangasjärvi J: Nitric oxide modulates ozone‒induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J. 2009, 58 (1): 1-12. 10.1111/j.1365-313X.2008.03756.x.PubMedGoogle Scholar
- Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F: Interplay between MAMP‒triggered and SA‒mediated defense responses. Plant J. 2008, 53 (5): 763-775. 10.1111/j.1365-313X.2007.03369.x.PubMedGoogle Scholar
- Shah J, Zeier J: Long-distance communication and signal amplification in systemic acquired resistance. Front Plant Sci. 2013, 4: 30-PubMed CentralPubMedGoogle Scholar
- Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F: ROS signaling: the new wave?. Trends Plant Sci. 2011, 16 (6): 300-309. 10.1016/j.tplants.2011.03.007.PubMedGoogle Scholar
- Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR: EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science. 1999, 284 (5423): 2148-2152. 10.1126/science.284.5423.2148.PubMedGoogle Scholar
- Chang C, Kwok SF, Bleecker AB, Meyerowitz EM: Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science. 1993, 262 (5133): 539-544. 10.1126/science.8211181.PubMedGoogle Scholar
- Nakagami H, Soukupová H, Schikora A, Zárský V, Hirt H: A mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J Biol Chem. 2006, 281 (50): 38697-38704. 10.1074/jbc.M605293200.PubMedGoogle Scholar
- Monroe-Augustus M, Zolman BK, Bartel B: IBR5, a dual-specificity phosphatase-like protein modulating auxin and abscisic acid responsiveness in Arabidopsis. Plant Cell. 2003, 15 (12): 2979-2991. 10.1105/tpc.017046.PubMed CentralPubMedGoogle Scholar
- Torres MA, Dangl JL, Jones JD: Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A. 2002, 99 (1): 517-522. 10.1073/pnas.012452499.PubMed CentralPubMedGoogle Scholar
- Li J, Brader G, Palva ET: The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell. 2004, 16 (2): 319-331. 10.1105/tpc.016980.PubMed CentralPubMedGoogle Scholar
- Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R: JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell. 2004, 16 (7): 1938-1950. 10.1105/tpc.022319.PubMed CentralPubMedGoogle Scholar
- Zheng Z, Mosher SL, Fan B, Klessig DF, Chen Z: Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol. 2007, 7 (1): 2-10.1186/1471-2229-7-2.PubMed CentralPubMedGoogle Scholar
- Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R: A knock‒out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J. 2002, 31 (1): 1-12. 10.1046/j.1365-313X.2002.01328.x.PubMedGoogle Scholar
- Wildermuth MC, Dewdney J, Wu G, Ausubel FM: Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001, 414 (6863): 562-565. 10.1038/35107108.PubMedGoogle Scholar
- Cao H, Glazebrook J, Clarke JD, Volko S, Dong X: The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats. Cell. 1997, 88 (1): 57-63. 10.1016/S0092-8674(00)81858-9.PubMedGoogle Scholar
- Falk A, Feys BJ, Frost LN, Jones JD, Daniels MJ, Parker JE: EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc Natl Acad Sci U S A. 1999, 96 (6): 3292-3297. 10.1073/pnas.96.6.3292.PubMed CentralPubMedGoogle Scholar
- Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J: Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci U S A. 1999, 96 (23): 13583-13588. 10.1073/pnas.96.23.13583.PubMed CentralPubMedGoogle Scholar
- Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F, Glazebrook J: Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog. 2009, 5 (2): e1000301-10.1371/journal.ppat.1000301.PubMed CentralPubMedGoogle Scholar
- Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy A, Poovaiah B: Ca2+/calmodulin regulates salicylic-acid-mediated plant immunity. Nature. 2009, 457 (7233): 1154-1158. 10.1038/nature07612.PubMedGoogle Scholar
- Chen J-G, Gao Y, Jones AM: Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol. 2006, 141 (3): 887-897. 10.1104/pp.106.079202.PubMed CentralPubMedGoogle Scholar
- Cutler S, Ghassemian M, Bonetta D, Cooney S, McCourt P: A protein farnesyl transferase involved in abscisic acid signal transduction in Arabidopsis. Science. 1996, 273 (5279): 1239-1241. 10.1126/science.273.5279.1239.PubMedGoogle Scholar
- Azevedo C, Sadanandom A, Kitagawa K, Freialdenhoven A, Shirasu K, Schulze-Lefert P: The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science. 2002, 295 (5562): 2073-2076. 10.1126/science.1067554.PubMedGoogle Scholar
- Greenberg JT, Silverman FP, Liang H: Uncoupling salicylic acid-dependent cell death and defense-related responses from disease resistance in the Arabidopsis mutant acd5. Genetics. 2000, 156 (1): 341-350.PubMed CentralPubMedGoogle Scholar
- Kim Y, Park S, Gilmour SJ, Thomashow MF: Roles of CAMTA transcription factors and salicylic acid in configuring the low‒temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 2013, 75 (3): 364-376. 10.1111/tpj.12205.PubMedGoogle Scholar
- Thaler JS, Humphrey PT, Whiteman NK: Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 2012, 17 (5): 260-270. 10.1016/j.tplants.2012.02.010.PubMedGoogle Scholar
- Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR: CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases. Cell. 1993, 72 (3): 427-441. 10.1016/0092-8674(93)90119-B.PubMedGoogle Scholar
- Moubayidin L, Di Mambro R, Sabatini S: Cytokinin–auxin crosstalk. Trends Plant Sci. 2009, 14 (10): 557-562. 10.1016/j.tplants.2009.06.010.PubMedGoogle Scholar
- Zeng W, He SY: A prominent role of the flagellin receptor FLAGELLIN-SENSING2 in mediating stomatal response to Pseudomonas syringae pv tomato DC3000 in Arabidopsis. Plant Physiol. 2010, 153 (3): 1188-1198. 10.1104/pp.110.157016.PubMed CentralPubMedGoogle Scholar
- Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J: Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant. 2008, 1 (3): 423-445. 10.1093/mp/ssn019.PubMed CentralPubMedGoogle Scholar
- Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS: Tell me more: roles of NPRs in plant immunity. Trends Plant Sci. 2013, 18 (7): 402-411. 10.1016/j.tplants.2013.04.004.PubMedGoogle Scholar
- Sato M, Tsuda K, Wang L, Coller J, Watanabe Y, Glazebrook J, Katagiri F: Network modeling reveals prevalent negative regulatory relationships between signaling sectors in Arabidopsis immune signaling. PLoS Pathog. 2010, 6 (7): e1001011-10.1371/journal.ppat.1001011.PubMed CentralPubMedGoogle Scholar
- Miller G, Schlauch K, Tam R, Cortes D, Torres MA, Shulaev V, Dangl JL, Mittler R: The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci Signal. 2009, 2 (84): ra45-PubMedGoogle Scholar
- Jones A: Does the plant mitochondrion integrate cellular stress and regulate programmed cell death?. Trends Plant Sci. 2000, 5 (5): 225-230. 10.1016/S1360-1385(00)01605-8.PubMedGoogle Scholar
- Zhang Z, Lenk A, Andersson MX, Gjetting T, Pedersen C, Nielsen ME, Newman M-A, Hou B-H, Somerville SC, Thordal-Christensen H: A lesion-mimic syntaxin double mutant in Arabidopsis reveals novel complexity of pathogen defense signaling. Mol Plant. 2008, 1 (3): 510-527. 10.1093/mp/ssn011.PubMedGoogle Scholar
- Xie D-X, Feys BF, James S, Nieto-Rostro M, Turner JG: COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science. 1998, 280 (5366): 1091-1094. 10.1126/science.280.5366.1091.PubMedGoogle Scholar
- Devadas SK, Enyedi A, Raina R: The Arabidopsis hrl1 mutation reveals novel overlapping roles for salicylic acid, jasmonic acid and ethylene signalling in cell death and defence against pathogens. Plant J. 2002, 30 (4): 467-480. 10.1046/j.1365-313X.2002.01300.x.PubMedGoogle Scholar
- Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K: Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell. 2009, 21 (9): 2914-2927. 10.1105/tpc.109.068635.PubMed CentralPubMedGoogle Scholar
- Olszak B, Malinovsky FG, Brodersen P, Grell M, Giese H, Petersen M, Mundy J: A putative flavin-containing mono-oxygenase as a marker for certain defense and cell death pathways. Plant Sci. 2006, 170 (3): 614-623. 10.1016/j.plantsci.2005.10.016.Google Scholar
- Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE: Arabidopsis EDS1 connects pathogen effector recognition to cell compartment–specific immune responses. Science. 2011, 334 (6061): 1401-1404. 10.1126/science.1211641.PubMedGoogle Scholar
- Rustérucci C, Aviv DH, Holt BF, Dangl JL, Parker JE: The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. Plant Cell. 2001, 13 (10): 2211-2224. 10.1105/tpc.13.10.2211.PubMed CentralPubMedGoogle Scholar
- García AV, Blanvillain-Baufumé S, Huibers RP, Wiermer M, Li G, Gobbato E, Rietz S, Parker JE: Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog. 2010, 6 (7): e1000970-10.1371/journal.ppat.1000970.PubMed CentralPubMedGoogle Scholar
- Dempsey D, Klessig DF: SOS–too many signals for systemic acquired resistance?. Trends Plant Sci. 2012, 17 (9): 538-545. 10.1016/j.tplants.2012.05.011.PubMedGoogle Scholar
- Chin K, DeFalco TA, Moeder W, Yoshioka K: The Arabidopsis Cyclic Nucleotide-Gated Ion Channels AtCNGC2 and AtCNGC4 Work in the Same Signaling Pathway to Regulate Pathogen Defense and Floral Transition. Plant Physiol. 2013, 163 (2): 611-624. 10.1104/pp.113.225680.PubMed CentralPubMedGoogle Scholar
- Cui F, Brosché M, Sipari N, Tang S, Overmyer K: Regulation of ABA dependent wound induced spreading cell death by MYB108. New Phytol. 2013, 200 (3): 634-640. 10.1111/nph.12456.PubMedGoogle Scholar
- Gautier L, Cope L, Bolstad BM, Irizarry RA: affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004, 20 (3): 307-315. 10.1093/bioinformatics/btg405.PubMedGoogle Scholar
- Smyth GK: Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and Bioconductor. 2005, New York: Springer, 397-420.Google Scholar
- Rich S, Emma C, Robert D, Yang X: BHC: Bayesian Hierarchical Clustering. 2011, R package version 1.16.0Google Scholar
- Palma K, Thorgrimsen S, Malinovsky FG, Fiil BK, Nielsen HB, Brodersen P, Hofius D, Petersen M, Mundy J: Autoimmunity in Arabidopsis acd11 is mediated by epigenetic regulation of an immune receptor. PLoS Pathog. 2010, 6 (10): e1001137-10.1371/journal.ppat.1001137.PubMed CentralPubMedGoogle Scholar
- Brosché M, Kangasjärvi J: Low antioxidant concentrations impact on multiple signalling pathways in Arabidopsis thaliana partly through NPR1. J Exp Bot. 2012, 63 (5): 1849-1861. 10.1093/jxb/err358.PubMed CentralPubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.