Variations in PA levels in SA-infiltrated wheat leaves compared to the water-infiltrated control
Plant disease resistance can be defined as the ability of the plant to prevent or restrict pathogen growth and multiplication. All plants, whether they are resistant or susceptible, respond to pathogen attack by the induction of a coordinated resistance strategy. Acceleration and/or amplification of the plant responses by the application of resistance inducers could provide a biologically, environmentally and commercially viable alternative to existing pathogen control methods .
Among pathogenic fungi, the obligate parasite
Induced partial resistance against
In the last fifteen years, SA itself has been described as playing a key role in the activation of defence systems against pathogens in plants. Despite several reports [11-14], works focusing on SA as a resistance inducer are far from being as extensive as those concerning BTH, a functional analogue of SA, and, as far as we know, a single one involved wheat .
Plant lipids and lipid metabolic pathways have been shown to be of crucial importance during a plant-pathogen interaction. Many changes in membrane lipids are known to occur in plants at the site of infection. Moreover, lipids and lipid metabolites, released from membranes, function and act as signal molecules in the activation of plant defence responses .
Over the past few years, it has become increasingly clear that phosphatidic acid (PA) is involved in stress signaling because it is rapidly and transiently formed in response to various environmental stimuli . PA could be generated by 2 distinct pathways as shown in figure 1: a first one involves phospholipase D (PLD) acting hydrolytically on membrane phospholipids, particularly phosphatidylcholine (PC) and phosphatidylethanolamine (PE); a second one involves phospholipase C (PLC) acting sequentially with diacylglycerol kinase (DGK)
Phospholipid-signaling pathways are complex, interrelated, and involve numerous enzymes and substrates . As an ubiquitous enzyme family, phospholipases play various roles in stress responses . Beside PLC and PLD, a main class of phospholipases A (PLA) hydrolyze phospholipids (such as PC) into the corresponding free fatty acid and lysophospholipid (such as lysoPC). Such a fatty acid can be a precursor for oxylipin biosynthesis, and lysoPC may be involved in multiple cellular processes . One important finding on functions of lysoPC is that it can activate H+-ATPase in the tonoplast and cause cytoplasmic acidification, which is shown to activate defense responses and phytoalexin production . The lipid messengers derived from hydrolysis of the plasma membrane are illustrated in figure 2.
Adaptation of higher plants to biotic and abiotic stress is often accompanied by the occurrence of lipid peroxidation and metabolites which derived therefrom are called oxylipins. Lipid peroxydation may be the result of a coordinated action of enzymes or the result of auto-oxidation (Figure 3). Oxylipins are potent signaling molecules in the defense response in plants . The synthesis of oxylipins is first catalyzed by lipoxygenases (LOXs), which add molecular oxygen to polyunsaturated fatty acids (PUFAs) to yield the corresponding fatty acid hydroperoxides that are substrates for other enzymes (figure 4) . Based on their regiospecificity, the dioxygenation occurs at C-9 or C-13 and LOXs have been thus classified as 9- and 13-LOX, which yield 9- or 13-hydroperoxides, respectively . In the case of linolenic acid C18:3 and 13-LOX, the resulting product is 13-HPOT (hydroperoxy octadectrienoic acid) . These LOX-derived hydroperoxides can be converted through different reactions of the LOX pathway, particularly by an allene oxide synthase (AOS) leading to jasmonic acid (JA). Most of the LOX-derived compounds are considered as acting in plant defense reactions: indeed, C6 volatiles induce defense-related genes expression , divinyl ethers are antifungal , and JA is an important signaling compound that is involved in plant response to biotic stress [28,29]. Jasmonates are primarily derived from the C18:3 FA, which is released from membrane lipids via the activity of phospholipase A1.
The phospholipase A (PLA) superfamily which catalyzes the hydrolysis of membrane phospholipids, acts up-stream the LOX to generate the corresponding PUFAs and lysophospholipids . PLA may be involved in the release of free fatty acids for the biosynthesis of JA during the activation of plant defence responses. Indeed, three tobacco genes that encode putative members of the patatin family of PLAs, were identified . Their expression is induced by microbial elicitors and upon exposure to pathogen. The high expression level of these PLA genes precedes the accumulation of JA in pathogen-inoculated or elicitor-treated tissues. Activation of PLA has also been reported in response to TMV infection in tobacco  and elicitor treatment of cultured parsley cells .
FAs not only serve as the major source of reserve energy but also consist of complex lipids, which are essential components of cellular membrane lipids. Increasing evidence also shows the involvement of FAs and their derivatives in signaling and altering normal and disease-related physiologies in microbes, insects, animals, and plants. In plants, FAs modulate a variety of responses to biotic and abiotic stresses. For instance, PUFAs levels in chloroplastic membranes affect membrane lipid fluidity and determine the plant’s ability to acclimatize to temperature stress . Linolenic acid (18:3) is involved in protein modifications in heat-stressed plants . FAs also regulate salt, drought, and heavy metal tolerance as well as wound-induced responses and defense against insect and herbivore feeding in plants . FA metabolic pathways play significant roles in defense against pathogens. Classically, only passive roles were assigned to FAs in plant defense such as providing biosynthetic precursors for cuticular components (studies of FA metabolic mutants also reveal an active signaling role for the cuticle in plant defense) or JA, well known for its role in wound responses and plant defense against insect pathogens. However, recent works demonstrate more direct roles for FAs and their breakdown products in inducing various modes of plant defenses. Both 16- and 18-carbon FAs participate in defense to modulate basal, effector-triggered, and systemic immunity in plants .
Furthermore, lipid transfer proteins (LTPs), located in the cell wall, participate in the
In this review, we will discuss further and extend the study conducted by Renard-Merlier
Moreover, the effect of one resistance inducer, namely SA, on lipid metabolism is evaluated by molecular and biochemical approaches.
Phospholipids being the major membrane components, we investigated PC, PE, DAG and PA content variation in wheat leaves infiltrated with salicylic acid (SA). SA can modulate the content variation of these compounds, reservoirs from which biologically active lipids and precursors of oxidized lipids are released.
At the transcriptional level, a PLC-encoding gene expression was investigated in an attempt to assign any participation of this pathway in the phospholipids equilibrium described above.
We also investigated free FAs and PLFAs content variations in SA-infiltrated wheat leaves; this pool of lipids is quite interesting since it ensures several functions, from being an energy source to acting as cellular messengers; the latter being highly related to resistance induction in plants. The lipoxygenase response to SA-infiltration, at the molecular and enzymatic level, was also evaluated; this enzyme activity is important for oxylipins biosynthesis in plants, because of its position upstream the cascade of enzymatic lipid peroxydation.
An LTP-encoding gene expression was also monitored, taking into account the possible antifungal activity of LTPs as well as their ability to bind and transport membrane lipids, thus participating in lipid-mediated signaling mechanisms.
2. Material and methods
2.1. Treatments application
Ten-day-old wheat seedlings were treated with solutions of Iodus 40® (1g/L), HSA (1g/L), Milsana® (0.3% v/v) and trehalose (15g/L) as described by Renard-Merlier
2.2. RNA extraction and quantification of gene expression by real-time PCR
SA and water-infiltrated wheat leaves were sampled at 3, 6, 9, 12, 15, 18, 21, 24, 48, 72 and 96 hours after infiltration (hai) and stored at -80oC until use. Total RNA was extracted from 100 mg plant tissue using RNeasy Plant Mini Kit (Quiagen, The Netherlands) with some modifications of the protocol. cDNA synthesis was carried out using High Capacity cDNA Reverse Transcription Kit (Applied Biosystems, USA) according to the manufacturer’s protocol. Real Time qPCR was performed using ABI Prism 7300 detection system (Applied Biosystems, USA). The
2.3. LOX assay
LOX was assayed as described in  according to  and  with slight modifications. The results are the mean of three biological repetitions.
2.4. Fatty acid extraction and analysis
Total cellular FAs extraction and purification were performed by the authors in  using adapted protocols from . The results are means of three independent repetitions.
Free FAs, PLFA and PL extraction was carried out according to the method described in . Data shown are the results of the first experiment, which need to be confirmed by a biological repetition.
3. Results and discussion
3.1. PA content increases after SA infiltration
Because of its central position in the pathways mentioned above, the first results presented here have been obtained for PA. Table 1 shows the variations in PA levels in SA-infiltrated leaves, compared to the control. No change in PA content was observed during the first 24 hours after infiltration (hai) of SA, compared to the water-infiltrated wheat leaves; even though a slight accumulation of PA was observed in water-infiltrated leaves in comparison to the untreated plants, probably due to the stress generated by the infiltration. However, SA induced increases in PA content from 24 h till 96 hai, with a maximum of 6.2-fold increase at 72 hai.
|Time after SA infiltration|
|PA content||2.2-fold increase||2.7-fold increase||6.2-fold increase||1.19-fold increase|
These results confirm some variations in PA content reported by several authors. Treatment of
PLC gene expression is up-regulated and DAG content increases in SA-infiltrated leaves
In order to corroborate the PA formation with the PLC-DGK pathway activation, the expression of the
PA formation through the phospholipase C pathway results from two enzymes acting sequentially: PLC hydrolyses phosphatidylinositol-4,5-bisphosphate [PtdIns(4,5)P2, also abbreviated as PIP2] into inositol-1,4,5-trisphosphate [Ins(1,4,5)P3] and DAG. DAG remains in the membrane and is rapidly phosphorylated to PA by DGK (Figure 1). The variation in DAG levels in SA-infiltrated wheat leaves is presented in table 2. During the first 24 h after SA infiltration, no clear variation pattern in DAG content was observed. However, SA induced the accumulation of DAG from 24 till 96 hai, with a maximum of 2.18-fold increase at 72hai. Interestingly, DAG accumulation, as well as
Twenty four hours after infiltration, SA induces the expression of PLC-encoding gene, simultaneously with an accumulation of DAG and PA. One could think that DAG content must decrease in order to fulfill PA formation; indeed, the contribution of DAG could only be confirmed by the investigation of DGK activity. Even if the subsequent enzymatic conversion of DAG doesn’t lead to PA formation, one must keep in mind that the hydrolysis of PtdIns(4,5)P2 into Ins(1,4,5)P3 is of a great interest since the latter diffuses into the cytosol where it possibly triggers calcium flux/release from intracellular stores .
In addition, the simultaneous increase of these compounds could be due to the durable
|Time after SA infiltration|
|DAG content||1.1-fold increase||1.1-fold decrease||Ø||1.26-fold increase||1.62-fold increase||2.18-fold increase||1.56-fold increase|
3.3. PE and PC contents vary in SA-infiltrated leaves
PA could also be generated by the phospholipase D pathway which hydrolyzes structural membrane phospholipids such as PE and PC (Figure 1). The variations of PE and PC levels in SA-infiltrated leaves compared to the control are presented in table 3. While accumulation of PC was observed during the whole time-course experiment (except for 24 and 96 hai), PE accumulated the first 18h after treatment. Afterward, SA induced a decrease in the PE content between 24 and 96 hai, with a maximum decrease at 48 and 72 hai. These results match the increased PA level in SA-infiltrated wheat leaves in the same period, suggesting that this pathway is involved in PA formation. Since PC level was maintained and even increased, this phospholipid doesn’t seem to be involved in PA production, under SA treatment. The PE/PC ratio is also reduced from 48 till 96 hai. Substantial alterations in the lipid composition of plasma membrane are a widely known process to stress adaptation, such as water deficit: the PC/PE ratio changed from 1.1 in plants non-acclimated to water stress to 0.69 in acclimated ones .
|Time after SA infiltration|
|PE content||1.4-fold increase||1.3-fold increase||Ø||1.3-fold decrease||6.6-fold decrease||6.2-fold decrease||2.3-fold decrease|
|PC content||1.4-fold increase||2.9-fold increase||3.8-fold increase||Ø||1.8-fold increase||1.4-fold increase||Ø|
In conclusion, SA seems to induce the formation of PA through the activation of phospholipases C and/or D pathways. In
Treatment of tomato cell cultures with the fungal elicitor xylanase resulted in a rapid and dose-dependent nitric oxide (NO) accumulation, required for PA production via the activation of PLC-DGK pathway. PA and, correspondingly, xylanase were shown to induce ROS production .
The PLD pathway is involved in every mentioned stress signaling, except cold-induced stress. Several
Moreover, signaling lipids can affect the activity of target enzymes. In , the authors showed an activation of a calcium-dependent protein kinase DcCPK1 by PA in
All together, these results are the first evidence for SA as an inducer of PA formation in wheat leaves. Increases in PA levels in SA-treated wheat leaves seem to be highly related to the induction of plant genes encoding phospholipases that are involved in the synthesis or release of PA.
LOX gene expression and LOX activity are enhanced upon SA-infiltration
In the present experiments, the
In grapevine plantlets, rhamnolipids induced for
Figure 7 shows the LOX activity in leaf extracts at 6, 12, 18, 24, 48, 72 and 96 h after SA infiltration in comparison to water-infiltrated leaves. During the first 48h, the LOX activity was decreased in SA-infiltrated leaves. However, SA induced significant 1.7 and 3.8-fold increases in LOX activity at 72h and 96hai, compared to the control.
When compared together, profiles of
In non-infectious context, the induction of a LOX activity was also assessed in wheat by Renard-Merlier
LOX-derived products such as hydroperoxy, hydroxyl and keto fatty acids accumulate in plants in response to attack by pathogens and treatment with inducers of plant defence responses . For example, in
3.5. FAs content varies in resistance inducers-treated wheat plants
3.5.1. Total FAs content vary in trehalose, Iodus40, Milsana and HSA-treated wheat leaves
In wheat, Renard-Merlier
Table 4 presents a summary of the observed variations of several FAs content at the quantitative and qualitative levels induced by the four tested resistance inducers and these results are now discussed on the basis of the most recent literature as well as our results presented above.
|i||4.0-fold increase||2.4-fold increase||Ø||Ø||Ø||Ø||Ø||1.3-fold decrease|
|ni||Ø||Ø||1.2-fold increase||2.2-fold increase||Ø||Ø||1.5-fold decrease||1.33-fold decrease|
|i||2.8-fold increase||1.5-fold increase||Ø||Ø||Ø||Ø||Ø||Ø|
|i||4.8-fold increase||1.5-fold increase||Ø||Ø||Ø||Ø||1.8-fold decrease||2.0-fold decrease|
|i||Ø||Ø||Ø||Ø||1.6-fold increase||1.15-fold increase||Ø||Ø|
Lauric acid (C12:0) content quantitatively increased after Iodus 40® (2.8-fold), Milsana® (4.8-fold) and trehalose (4-fold) treatment in (i) plants (2 days after inoculation). In , the authors showed that
Contents of C20:2 (eicosadienoic acid) decreased in Iodus 40®- and Milsana®-treated (ni) plants compared to the corresponding controls (4 days after treatment). The decrease was confirmed at the qualitative level only for Iodus 40®. In (i) conditions, only Milsana® induced a significant decrease in C20:2 content at both levels whereas TR induced a decrease perceptible at the qualitative level only. In (i) plants, C20:2 increased (data not shown). C20:2 content seemed to be affected by fungal infection of the plant to a greater extent than by any of the resistance inducing treatments, since similar quantities were found in water-control (i) plants as well as in resistance inducers-treated plants. The link between C20:2 and infection was also reported in .Transgenic
C18:1 (oleic acid) in Iodus 40®-treated (ni) plants showed a quantitative 1.2 fold-increase. C18:1, as well as other C18 and C16 FAs, are well known substrates for cutin monomer synthesis . One could suggest that Iodus 40®, by stimulating the accumulation of this FA, contributes to the reinforcement of the plant cuticule prior to fungal contamination. In cultured parsley cells, a biphasic time-course for C18:1 increase was obtained upon treatment with peptidic or fungal elicitors . In , the authors suggested that chloroplastic C18:1 level is critical for normal pathogen defense responses in
The amount of C18:2 increased (1.6-fold) 4 days after HSA treatment in (i) plants. For C18:2, the accumulation in sorbitol-treated barley leaves was reported from 12 h till 72h after treatment . Cold acclimating potato was found to accumulate linoleic acid (18:2) in the membrane glycerolipids of the leaves . C18:2 is also a substrate for cutin monomer synthesis and can therefore contribute to cuticle reinforcement.
Among the four inducers tested, Iodus40® had the largest effects on FA levels, since it increased C12:0 and C18:1 and decreased C20:2. This product, which active ingredient is laminarin (polysaccharide), induced decreases in lipid peroxydation level all over the time-course experiment .
Trehalose and Milsana® had similar effects on FAs profile with induced increases in C12:0 and decreases in C20:2 contents. However, TR and Milsana® modes of action are quite different in the wheat-powdery mildew interaction. TR activates phenylalanine ammonia-lyase (PAL) and peroxydase activity and enhances papilla autofluorescence and H2O2 accumulation. However, it does not affect catalase (CAT), cinnamyl alcohol dehydrogenase (CAD), LOX or oxalate oxidase (OXO) activities, and does not alter lipid peroxide levels . According to the authors in , treatments of wheat with Milsana® enhance H2O2 accumulation at the fungal penetration site without any possible correlation with the activation of enzymes involved in ROS metabolism. Only LOX, involved in both ROS regulation and lipid peroxidation, showed a 26 to 32% increase 48h postreatment in Milsana-infiltrated leaves. This weak effect of Milsana® on wheat lipid metabolism was confirmed at the lipid peroxydation level, which was shown to decrease in treated plants.
While HSA sprayings enhanced an increase in C18:2 levels only, HSA exhibited the most numerous and the highest effects in the wheat-powdery mildew interaction. HSA induced H2O2 accumulation, increases LOX activity in (i) conditions and decreases CAT activity in (ni) context .
While barley leaves treated with salicylate , sorbitol  or JA  accumulated C18:3, none of the 4 compounds tested induced any increase in C18:3 in wheat leaves according to our results.
3.5.2. Free FAs and PLFAs content vary in SA-infiltrated wheat leaves
The profile of free FAs and phospholipids FAs (PLFAs) in SA-infiltrated wheat leaves were also investigated and are presented in Table 5 and Table 6.
|μg/mg dry weight||2.38-fold|
|μg/mg dry weight||1.5-fold increase|
Upon treatment with SA, free palmitic acid (C16:0) accumulation was observed from 48 till 96 hai with an average of 2.38 fold-increase over this period and 1.4-fold increase at the qualitative level over the whole time-course experiment. Similar results were observed for the PLFAs C16:0, essentially the last 3 days of the experiment. Since monomers of cutin are synthesized C16:0, SA seems to induce the reinforcement of the plant cuticule. In
Increases in both classes of stearic acid C18:0 content and percentage were observed in SA-infiltrated leaves. In soybean, increased levels of C18:0 likely inhibit soybean seed colonization by the seed-borne pathogen
A transient 2-fold increase in free FAs C18:1 content was recorded. A sharp and rapid increase in C18:1 level was observed in parsley cells treated with a fungal elicitor . Recent studies suggest that free oleic acid (18:1) levels in the chloroplast regulate the defense response of plants to pathogens including programmed cell death and SAR .
A 2,7-fold decrease in C18:2 PLFAs was observed 72 till 96 hai of SA. In sorbitol-treated barley leaves, the accumulation of C18:2 occurred from 12 h till 72h after treatment . The development of asexual spores, and the formation of cleistothecia and sclerotia of
One of the most interesting results is the general decrease of C18:3 level after SA-infiltration. Most of the studies report increases in 18:3 levels such in suspension cells of California poppy (
In barley leaves, 13-LOX are induced by SA and jasmonates. Upon SA treatment, free C18:3 and C18:2 accumulate in a 10:1 ratio reflecting their relative occurrence in leaf tissues . The release of 18:3 from plant membrane lipids by stress-activated lipases is thought to provide the substrate for lipoxygenase and subsequent octadecanoid (oxylipin) pathway synthesis of JA and methyl jasmonate [101,102]. JA and methyl jasmonate participate in the signal regulation of a number of plant processes including wound and pathogen defense responses. Efforts have been successful to identify and characterize fatty acids esterifying lipases that are activated by pathogen attack and/or environmental stress. Results suggest that both A1 and A2 phospholipases are involved in 18:3 mobilization form membrane lipids . In the C4 monocotyledon sorghum (
However, in tobacco tissues expressing a hypersensitive response to TMV, an increase in the saturation of fatty acids contained in the microsomal phospholipids was observed while C18:3 content decreased by 9% . Interestingly, the authors credited the change of FAs composition to a four-fold increase in LOX activity of the infected tobacco tissues.
The decreases in free FAs observed with our model could be explained by a rapid dioxygenation
ltp gene expression is induced by SA infiltration
The effect of SA on the expression of a lipid transfer protein-encoding gene
The LTPs extracellular distribution in the exposed surfaces in vascular tissue systems, high abundance and corresponding genes expression in response to infection by pathogens suggest that they are active plant-defense proteins . A combined expression of chitinase and LTP-encoding genes in transgenic carrot plants enhances resistance to
Moreover, LTPs are known to be differentially expressed during a pathogenic interaction because they are potentially good ligands to oleic C18:1, linoleic C18:2 and eicosadienoic acids C20:2 . Among 28 identified wheat nsLTP, eight nsLTP expressed in yeast exhibited lipid binding activity . These proteins could be involved in the intracellular traffic of phospholipids and in the transport of cutin monomers. Interestingly, SA induces the expression of the
The present chapter provides evidences for the effect of resistance inducers on wheat lipid metabolism and presents the strategy we used in order to characterize their mode of action at different levels: total FA content and relative proportion, PA, PE and DAG contents, expression of genes such as PLC and LTP-encoding ones. Lipid metabolism is therefore a marker of induced resistance in wheat. To our knowledge, such findings have never been presented before on
Salicylic acid is very likely to induce the formation of PA through the activation of phospholipases C and/or D pathways: induction of
The tested resistance inducers had some similarities in their mode of action, relatively to total FAs profiles. Trehalose and Milsana® seem to share similar modes of action via the increase of C12:0 and decrease of C20:2 contents. Iodus® exhibited the largest effects on FAs profiles, inducing increases in C12:0 and C18:1 and decreases in C20:2. HSA, however, was the only resistance inducer that modulated positively the content of C18:2.
Future investigations have to be extended to other genes expression and corresponding enzymatic activities acting downstream of lipoxygenase in order to figure out whether the LOX-derived hydroperoxides are metabolized during the JA synthesis. Furthermore, a global approach using microarrays based on wheat cDNA chips would be a useful tool for increasing our knowledge of the plant lipidome in our wheat-powdery pathosystem.
Christine TAYEH is supported by the French Ministry of National Education and Research.
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