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. 2015 May 29;10(6):e1031938. doi: 10.1080/15592324.2015.1031938

Aluminum ions alter the function of non-specific phospholipase C through the changes in plasma membrane physical properties

Přemysl Pejchar *, Jan Martinec 1
PMCID: PMC4622580  PMID: 26024014

Abstract

The first indication of the aluminum (Al) toxicity in plants growing in acidic soils is the cessation of root growth, but the detailed mechanism of Al effect is unknown. Here we examined the impact of Al stress on the activity of non-specific phospholipase C (NPC) in the connection with the processes related to the plasma membrane using fluorescently labeled phosphatidylcholine. We observed a rapid and significant decrease of labeled diacylglycerol (DAG), product of NPC activity, in Arabidopsis seedlings treated with AlCl3. Interestingly, an application of the membrane fluidizer, benzyl alcohol, restored the level of DAG during Al treatment. Our observations suggest that the activity of NPC is affected by Al-induced changes in plasma membrane physical properties.

Keywords: aluminum toxicity, Arabidopsis thaliana, benzyl alcohol, BODIPY, diacylglycerol, membrane fluidity, non-specific phospholipase C

List of abbreviations

BA

benzyl alcohol

BODIPY

4, 4-difluoro-4-bora-3a, 4a-diaza-s-indacene

BY-2

Bright Yellow 2

DAG

diacylglycerol

HP-TLC

high-performance thin-layer chromatography

MS

Murashige-Skoog

NPC

non-specific phospholipase C

PA

phosphatidic acid

PC

phosphatidylcholine

PC-PLC

phosphatidylcholine-specific phospholipase C

PIP2

phosphatidylinositol 4, 5-bisphosphate

PI-PLC

phosphatidylinositol-specific phospholipase C

PLD

phospholipase D

PM

plasma membrane

Low pH of soil enables release of toxic aluminum (Al) ions from its insoluble forms fixed in soil minerals causing that Al is a major growth–limiting factor in the regions with acid soils. Prolonged exposure to Al ions leads to changes in root morphology, e.g. root thickening, bursting, changes in the cell wall architecture, and even cell death. However, the first indication of the Al toxicity in plants is rapid cessation of root growth. The root tip has been found to be the most Al-responsive part of roots.1 Although molecular mechanisms of the prompt Al-mediated root growth inhibition are largely unclear, it is known that a number of physiologically important processes connected with plasma membrane (PM) are affected by Al.2-9 The rapid response of root growth suggests that signaling pathways are a part of the mechanism participating in Al toxicity.

Phospholipid-signaling pathway is now considered to be one of the important plant signaling mechanisms involved in many different reactions of plants to environmental factors such as drought, cold, salinity or pathogen attack (for a review see refs.10,11). Al has been shown to affect the phospholipid-signaling pathway as well. Changes of phospholipase A2 activity in vitro,12 phospholipase D (PLD) activity13,14 and phosphatidylinositol-specific phospholipase C (PI-PLC) activity15-17 after Al treatment were demonstrated. In addition to PI-PLC, non-specific phospholipase C (NPC, PC-PLC in prokaryotes and animals), an enzyme that is able to hydrolyse phosphatidylcholine (PC) instead of phosphatidylinositol 4,5-bisphosphate (PIP2), was characterized in plants18 in relation with a number of different cell processes or stress condition18-26 including Al stress.27,28

Studies of the target of Al action in plants have demonstrated that Al binds to the apoplast29 and changes the properties of the PM.8,9 Recent study introduced by Krtková et al.30 revealed that Al treatment induced cessation of Arabidopsis root growth and loss of membrane fluidity. When a membrane fluidizer benzyl alcohol was applied in the presence of Al, membrane fluidity was restored. Moreover, partial restoration of root growth was observed. This suggests that the physical state of PM could play a role in morphological changes caused by Al toxicity. We previously described that the formation of diacylglycerol (DAG) generated by NPC is rapidly inhibited by Al in tobacco cell line BY-2 and in tobacco pollen tubes, that Al inhibits growth of tobacco pollen tubes and that this growth, arrested by Al, can be rescued by externally added DAG.27 This raises question: what is the role of the NPC/DAG in aluminum toxicity? Here we report that NPC activity in Arabidopsis seedlings is influenced by the physical state of PM.

Because we worked with different plant model organism than in our previous work,27 first we tested the reaction of Arabidopsis seedlings to Al stress in the view of NPC activity. We utilized the fluorescent derivative of PC (BODIPY-PC) as a phospholipase substrate. For NPC activity measurements, 7-day-old seedlings were treated with different concentrations of AlCl3 in the presence of BODIPY-PC for 2 h. HP-TLC analysis of the labeled products showed significantly lower production of BODIPY-DAG in the seedlings treated with AlCl3 (Fig. 1). The effect of Al on DAG formation was concentration-dependent. Lower DAG production (74% of control, non-treated seedlings) was detected already for 1 µM AlCl3 and was more pronounced for 10 µM and 100 µM AlCl3 (Fig. 1). Based on these results, 10 µM AlCl3 was chosen as a working concentration for in situ measurements of NPC activity in following experiments. In contrast to NPC activity in situ in Arabidopsis seedlings under salt stress,25 here we observed negative effect of Al on DAG production. Thus, the possible influence of Al ions on BODIPY-PC incorporation into the roots of Arabidopsis seedlings exposed to Al treatment was examined by laser scanning confocal microscopy. Rapid incorporation for both Al-treated and non-treated seedlings with no effect of Al on this process was observed (Fig. 2). This makes in situ method usable also for Al-treated Arabidopsis seedlings.

Figure 1.

Figure 1.

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Concentration dependence of BODIPY-DAG production in Arabidopsis seedlings treated with Al. NPC activity in Arabidopsis seedlings was measured according to Kocourková et al.25 Seven-day-old Arabidopsis seedlings (5 seedlings for each sample) were grown in MS medium, transferred into 1/8 MS medium (pH 4) containing different concentrations in the range 0–100 µM AlCl3 and 0.66 µg ml−1 of fluorescent phosphatidylcholine (BODIPY-PC, D-3771, Invitrogen, USA) and were incubated on an orbital shaker at 23°C for 2 h. Lipids were extracted, separated by high-performance thin layer chromatography and quantified. Identification of the BODIPY-DAG corresponding spot was based on comparison with the BODIPY-DAG standard prepared as described earlier.31 Each value is related to the control non-treated cells (100%). The plotted values are the means + SD from 3 independent experiments run in duplicates. DAG; diacylglycerol, NPC; non-specific phospholipase C, PC; phosphatidylcholine.

Figure 2.

Figure 2.

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Incorporation of BODIPY-PC into the Arabidopsis roots is not affected by Al. A) Seven-day-old Arabidopsis seedlings were grown, fluorescently labeled and treated with 10 µM AlCl3 for 15 min as described in Figure 1. Incorporation of BODIPY-PC was observed by Zeiss LSM 5 DUO confocal laser scanning microscope. Bar = 20 µm. B) Quantification of BODIPY-PC incorporation. Mean pixel intensity in the meristematic zone of root tip was measured using ImageJ software. The plotted values are the means + SD. PC; phosphatidylcholine.

Based on observations concerning Al-induced changes of membrane fluidity30 and as we detected the most NPC activity in the PM-enriched fraction,27 we examined the possible connection between PM physical state and NPC activity during Al stress. We utilized benzyl alcohol to change PM fluidity and we measured DAG formation in Arabidopsis wt seedlings. Seven-day-old seedlings were treated with 20 mM benzyl alcohol with or without 10 µM AlCl3 in the presence of BODIPY-PC for 2 h. HP-TLC analysis of the labeled products showed that BODIPY-DAG production is decreased in seedlings treated with AlCl3. In contrast, higher production of BODIPY-DAG was observed when seedlings were treated with benzyl alcohol alone compared to non-treated seedlings. Intriguingly, strong effect on DAG formation was observed when the seedlings were treated with benzyl alcohol and AlCl3 together. In that case, benzyl alcohol was able to restore the inhibition of BODIPY-DAG formation induced by Al-treatment alone (Fig. 3) and thus to prevent inhibiting effect of Al on NPC activity. Similar results were observed for the tobacco cell line BY-2 and pollen tubes (data not shown). These results indicate that the physical state of PM influences NPC activity that leads to decrease in the DAG level during Al stress.

Figure 3.

Figure 3.

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Effect of benzyl alcohol on BODIPY-diacylglycerol formation in Al-treated Arabidopsis seedlings. Seven-day-old Arabidopsis seedlings were grown, fluorescently labeled, treated with 20 mM benzyl alcohol and 10 µM AlCl3 for 2 h and processed as described in Figure 1. Each value is related to the control non-treated cells (100%). The plotted values are the means + SD from 5 independent experiments run in duplicates. BA; benzyl alcohol, C; non-treated control, DAG; diacylglycerol.

Interestingly, some components of prokaryotic (gram-positive bacteria Clostridium perfringens and Bacillus cereus) phospholipid-signaling pathway have been shown to be affected by Al-induced changes in membrane properties.32,33 Al3+-mediated changes on membrane fluidity did not affect PC-PLC-mediated hydrolysis of PC while PI-PLC-mediated hydrolysis of PIP2 was decreased in liposomes. Authors suggest that it could be partially due to a higher lipid packing induced by Al3+, which could affect the interaction between the enzyme and its substrate.32 However, we showed previously that the activity of NPC, an enzyme that is able to hydrolyse PC, is affected by Al in tobacco27 and we confirmed such finding in this study also for Arabidopsis. The possible explanation of this difference is that plant NPCs, a gene family that consist of 6 members denoted NPC1-NPC6 in Arabidopsis, are similar to gram-negative bacterial PC-PLCs, not to gram-positive ones.34 This could result in a slightly different mechanism of response to the Al-induced changes in membrane properties. However, both affected enzymatic activities produce DAG. This may suggest that DAG is an important molecule in Al3+-mediated changes on membrane fluidity rather than the type of DAG-producing enzyme.

DAG is known as a key intermediate of glycerolipid metabolism in plants.35 Additionally, NPC family in plants was first characterized in relation to phospholipid-to-galactosyl diacylglycerol exchange.18 In contrast, the signaling role of DAG in plants is under debate but a number of studies imply that DAG is likely to act as a signaling molecule in some systems36 including Al stress.27,28 However, DAG seems to be important also for the structure and dynamics of biological membranes. DAG can modify membrane curvature and can induce unstable asymmetric regions in membrane bilayers.37,38 Moreover, molecular dynamics simulations revealed that DAG decreases lateral diffusion of molecules, produces a strong “condensing effect” in PC bilayers and increases the spacing between PC headgroups with the largest spacing usually occurring between the first and the second nearest-neighbor PC headgroups from a DAG, due to the umbrella effect.39 Compared to other lipids, DAG has also increased translocation across membrane leaflets (flip-flop).40 These instabilities are important in many physiological processes, such as exocytosis, endocytosis, membrane biogenesis and cell division. Moreover, it has been found that mechanism of the rapid Al-mediated inhibition of the root growth is related to the inhibition of endocytosis9,30 and the root growth was described to be controlled through the local auxin biosynthesis and signaling.41,42 Intriguingly, the overexpression of auxin transporter gene OsPIN2 alleviated Al-mediated membrane rigidity43 and NPC3 and NPC4, members of the Arabidopsis NPC gene family, were shown to be affected by auxin.24 Here we show for the first time that plant NPC activity is altered by physical state of plasma membrane. We hypothesize that Al-mediated membrane rigidity decreases NPC activity. This leads to the decrease of DAG production and to the modification of plasma membrane that could result in the inhibition of the processes mentioned above.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.

Acknowledgments

The authors thank Daniela Kocourková and Kateřina Raková for their excellent technical assistance.

Funding

This work was supported by the Czech Science Foundation grants no. P501/12/P950, P501/12/1942 and 13–19073S.

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