Abstract
The diversity of chemical structure of lipids present in the cell membranes, concerning both a hydrophilic (polarity and charge) and hydrophobic (chain length and unsaturation of fatty acids residues) parts, assists in providing suitable physical and chemical properties for the course of multiple reaction within the membrane. This review presents the results of the changes in the lipid composition of native membranes of plant cells under stress conditions and during developmental processes. It also discussed the use of lipids to create model systems which allow for interpretation of specificity of reactions taking place in the membrane fragments. The spontaneous formation by lipids closed spherical structures (bi-layers) in an aqueous medium, and monolayers at the water/air interface creates a convenient model system for the native membranes. The review focuses on the techniques of electrokinetic potential (zeta potential) measurements and Langmuir monolayers’ studies. The first gives the possibility to conclude about the modification of the polar part of the membranes, the second allows to determine their structural properties (fluidity, stiffness). The relatively rapid modification of the lipid composition under stress and during the course of developmental processes to ensure the optimal functions of membranes and organelles includes the changes of hydrophobic/hydrophilic character of lipid, as an important factor influencing the course of multiple reactions in cells. Understanding the physicochemical properties of lipids that accompany these processes may contribute to the correct description of the functionality of the cells under these conditions.
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Introduction
Plant membranes contain various lipid species of composition changing in response to both internal and external signals. Lipids constitute a group of specific amphiphilic biomolecules. The main lipid classes of cellular membranes are neutral lipids such as sterols and polar lipids like phospholipids, glycolipids and sphingolipids, all with unique biophysical properties. The majority of these lipids are the building material of the membrane but a few have also signal-transducing properties. The molecular composition of membrane lipids differs among cell types and subcellular membrane fractions. It was suggested that there are over 1000 lipid types in membranes (Brown 2011). Table 1 presents the distribution of the main polar lipids in individual plant organelles.
Phosphatidylcholine (PC) and phosphatidylethanolamine (PE) are the major phospholipids in plasmalemma. Polar groups of both have zwitterionic character. Phosphatidylglycerol (PG) and phosphatidylinositol (PI) as well as phosphatidylserine (PS) represent a smaller fraction of membrane lipids, all with negatively charged polar groups. Monogalactolipids (MGDG) and digalactolipids (DGDG) present in chloroplast membranes in high proportions are classified as polar lipids without exposed ionic charge.
Each of polar lipids is composed of fatty acid residues varying in chain length and degree of saturation (Table 2). The degree of saturation of lipid acyl residues determines the physicochemical properties of membranes (Chapman 1975; Quinn 1988; Quinn et al. 1989), in particular the mobility of the lipid molecules. It was suggested that different functions of membrane-bound proteins depend on fatty-acid saturation degree.
The presence of lipids with various polar groups determines specific electric properties of the membrane surface whereas different composition of hydrophobic fatty acids residues is responsible for “fluidity/stiffness” and permeability of membranes. The significance of membrane lipid composition and membrane lipid dynamics in stress conditions has been indicated in several reviews (Kültz 2005; Park et al. 2005; Vigh et al. 2005, 2007a, b; Horváth et al. 2008, 2012; Escribá et al. 2008; Mittler et al. 2012; Filek et al. 2012; Balogh et al. 2013; Crul et al. 2013). It was suggested that stress factors can activate lipid metabolic enzymes in the direction of such changes of polar groups and fatty acid composition which can prevent cell destruction (Balogh et al. 2013). A lot of evidence was collected indicating the role of lipids in such physiological processes such as photosynthesis, signal transduction, secretion, and cytoskeletal rearrangement, organ differentiation and pollination (Wang 2002; Farmer et al. 2003; Lindsey et al. 2003; Meijer and Munnik 2003; Sperling and Heinz 2003; Welti and Wang 2004). The explanation of the changes of membrane lipids composition in stressful and physiological conditions is important for understanding the membrane and cell functions (Welti et al. 2002).
Special attention was paid to the importance of the lipid composition of chloroplast membranes. However, despite numerous studies, the details of this structure/function relationship have remained elusive. Hawke et al. (1974) and Bolton and Harwood (1978) indicated that maturity of tissues was connected with defined proportions of galactosylglycerides in chloroplast membranes especially of that reach in linolenate acid residues. Likewise, degradation of protoplast lipids in etiolated crop seedlings and light-initiated development of chloroplast thylakoid membranes stimulated synthesis of glycosylglycerides (MGDG and DGDG) and PG while PC and PE pull decreased markedly. (Harwood 1998). Pick et al. (1987) reported that sulfoquinovosyl diacylglycerol was associated with the ATP synthase and that MGDG was bound to the reaction center of PSII (Murata et al. 1990; Gombos et al. 1994).
Investigating the mutants of Arabidopsis, Millar et al. (1998) have found that plants with a high content of long-chain fatty acid (18–22 carbons) were characterized by a specific modification of the chloroplast membrane structure, altered morphology (connected with the failure of flowering shoots to elongate), modified spatial pattern of siliques and altered floral phenotype.
The differences in membrane lipid composition were also linked to embryogenesis in in vitro cultures. The higher content of PE in comparison to PC and the presence of more unsaturated fatty acids (linolec, 18:2 and linolenic, 18:3) was observed in embryogenic membranes of wheat calli (Laggner et al. 2003). Earlier, Reidiboym-Talleux and Grenier-De March (1999) in studies of Prunus savium found that embryogenic calli were characterized by a higher content of total phospholipids compared to non-embryogenic ones and that this may be explained by the differences between the lipid biosynthetic pathways in both types of tissues. In the induction/blocking of embryogenesis hormones play an important role, mainly auxins. Liu et al. (1995) suggested that 2,4-d (2,4-dichlorophenoxyacetic acid—synthetic auxin), usually added to media to induce non-embryogenic calli, affected the synthesis of membrane lipids resulting in the formation of more unsaturated ones. Auxins, as negatively charged substances (derivatives of indolilo acetic acid) can be adsorbed on membranes at the places of the specific lipid composition (“domains”). The heterogeneity of the membrane structure characterized by the formation of specific centers ensures the possibility of interactions with particles of various character, present in the environment.
Taking into account the importance of the specific composition of ionic organic compounds (auxins, other anionic, i.e., gibberellins and cationic—cytokines, substances) as well as inorganic ions (e.g., calcium cations) in stimulation of physiological process (Wilson and Crawford 1974; Rochester et al. 1987a, b) the induction of ions transport alongside plants (and tissues) by external application of electric field was investigated (Verma et al. 1988; Mamta et al. 1987; Zhang et al. 1997b, 2000; Sumorek and Pietrzyk 1999; Nechitailo and Gordeev 2001; Filek et al. 2005b). The special attention was directed to the activation of the flowering of both photo-periodic (Adamec 1989; Adamec and Krekule 1989; Adamec et al. 1989; Machácková et al. 1989) and thermo-periodic plants (Filek et al. 2002a, 2003a, 2006; Machačkova et al. 2004; Biesaga-Koscielniak et al. 2010) and to pollination process (Wędzony and Filek 1996, 1998; Mól et al. 2004).
Application of neuro-electrophysiological techniques for studying the electric properties of plant membranes allowed the description of not only differences in surface charge of the membranes of various genotypes and tissues (Kinraide et al. 1992) but also the changes caused by external chemical (Pawlikowska-Pawlega et al. 2000, 2007; Karcz and Burdach 2002; Karcz and Kurtyka 2007; Kurtyka et al. 2011) and physical factors, such as temperature (Hejnowicz et al. 1995; Filek and Kościelniak 1996, 1997; Piotrowska et al. 2000; Król et al. 2004; Karcz and Burdach 2007, Kupisz and Trebacz 2011) and light (Trębacz et al. 1989; Szarek and Trebacz 1999; Koselski et al. 2008). Electrical signals generated in plants under such conditions were classified as action potentials, similarly as was done for animal tissues. The long-distance propagation of these signals was associated with local changes of ion concentrations (mainly calcium and potassium) connected with activation of ion channels, whereas restoration of the resting potential, determined by the presence of polar and charged groups on the membrane surface (specific for each cell) was dependent on the activation of the electrogenic proton pump (Zawadzki and Trębacz 1982, 1985; Trębacz et al. 2006). It was suggested that activation/blocking of protein channels localized in membranes was also associated with the mechanical tension via changes in unsaturation of lipid fatty acids (Allakhverdiev et al. 2001, 2010; Moreno et al. 2012).
Gas chromatography and nuclear magnetic resonance (NMR) techniques (Shiao and Shiao 1989; Kirby et al. 2011) allowed for a precise analysis of changes in the quantitative and qualitative composition of membrane lipids. In the studies of heavy metals’ action it was found that their application influenced both polar and hydrophobic parts of plant membranes. High concentrations of such metals such as cadmium (Cd) (Hernandez and Cooke 1997; Quartacci et al. 2005; Nouairi et al. 2006, Filek et al. 2009, 2010), lead (Pb) (Przymusinski et al. 1991; Stefanov et al. 1993, 1995), aluminum (Al) (Lindberg et al. 1991; Papernik and Kochian 1997; Zhang et al. 1997a; Ishikawa and Wagatsuma 1998) and copper (Cu) (Quartacci et al. 2001; Ibrahim et al. 2012) induced changes in the proportions of phospholipids and galactolipids as well as in the degree of fatty acid saturation. However, this effect was strongly dependent on the composition of membrane lipids (characteristic for plant genotype) as well as on the dose of applied metals. Generally, the lipid peroxidation (an increase of fatty acid saturation) was observed due to the action of reactive oxygen species. It is assumed that excess of reactive oxygen species is generated during oxidative stress which is a consequence of the impact of environmental stress factors (Koca et al. 2007; Sharma et al. 2012).
Changes in lipid composition of plant membranes were indicated also in other types of stresses such as drought, low/high temperature and air pollution (Sikorska and Kacperska 1980; Smolenska-Sym and Kacperska 1994, 1996). Osmotic stress induced by salinity and water deficit provokes a disturbance in the relation water-ions in cells which leads to the initiation of mechanical tensions in membranes (contraction, expansion). An increased fraction of phospholipids, especially PC and an increased degree of fatty acid unsaturation was detected under such conditions (Quartacci et al. 1995; Aziz and Larher 1998; Wu et al. 2005; Toumi et al. 2008; Filek et al. 2012). However, registered modifications of the lipids composition were dependent on the tolerance of plant genotypes (genetically engineered) to osmotic stress thus changes of fatty acid saturation in the opposite direction were also found (Martins et al. 2008; Filek et al. 2012). Similarly, alterations of lipid membranes induced by low temperature were correlated with genetically modified plant resistance and/or with their acclimation to cold and frost. In most of the articles the increase of phospholipid unsaturation was established after low and frost temperature application as well as under action of air pollution (Kacperska-Palacz 1978; Yoshida 1978; Sikorska and Kacperska 1982; Jouve et al. 1993; Alonso et al. 1997; Harwood 1997; Routaboul et al. 2000; Campos et al. 2003; Pukacki 2004; de Oliveira et al. 2010). Such raise of a pull of unsaturated lipids associated with the formation of a more fluid membrane was suggested as one of the steps of cell protection in these stress conditions.
The presence of the hydrophobic part and hydrophilic head group in lipids gives them the ability to a specific organization in aqueous media. This structure stimulates spontaneous formation of closed structures of bi- and multi-layers (liposomes). At the hydrophobic/hydrophilic interface lipid molecules position themselves with the fatty acid residues directed toward the air and with polar groups to water forming monolayers. These structures are used to precise characterization of the modification of membranes under the influence of both chemical and physical factors. The review presents the selected physicochemical techniques that enable to describe the effects of the chemical and physical signals onto electric and structural properties of individual and mixtures of lipids.
Liposomes
Most of the plant membrane phospholipids may form in aqueous medium bi- or multi-layer liposomes (mimicking cell membranes) by sonification. Also DGDG have a tendency to build bilayers, oppositely to MGDG, which form rather hexagonal structures (Bottier et al. 2007). For formation model liposomes both individual and mixtures of lipids were used. Liposomes have drawn considerable attention as structures that may have potential application as drug carriers for target delivery (Nag and Awasthi 2013). Phospholipid liposomes exhibit negative (PG, PI, PS) or zero (PC, PE, DGDG) charge in water solution; however, to mimic the presence of proteins in membranes, cationic molecules (trimethylammonium-propane TAP) were introduced to liposomes (Ma et al. 2010). Moreover, sterols—the natural components of membranes were also used for preparation of the mixed lipid–sterol bilayers (Hua and Song-Nian 1998; Magarkar et al. 2012).
Since, in liposomes polar part of lipid molecule is exposed to water environment, thus when charged such structures can migrate in electric field. The velocity of movement of such objects (similarly as of all other charged particles) in the direction of the respective electrodes is dependent on their charge and applied electric field ΔE and is mathematically described by Smoluchowski equation:
where u is the electrophoretic mobility equal to particle velocity U per unit electric field ΔE, ε and ε 0 are dielectric constants of medium and vacuum, ζ electrokinetic potential also known as zeta potential, η medium viscosity, κa particle radius normalized to the Debye length 1/κ, being a good representation of the range of electrostatic forces acting in polar media. This equation is valid for κa ≫ 1, i.e., for objects of sizes larger than Debye layer thickness.
For objects smaller than Debye length Hückel formula is valid: \(u = {\raise0.7ex\hbox{$U$} \!\mathord{\left/ {\vphantom {U {\varDelta E}}}\right.\kern-0pt} \!\lower0.7ex\hbox{${\varDelta E}$}} = {\raise0.7ex\hbox{${2\varepsilon \varepsilon_{0} \zeta }$} \!\mathord{\left/ {\vphantom {{2\varepsilon \varepsilon_{0} \zeta } {3\eta }}}\right.\kern-0pt} \!\lower0.7ex\hbox{${3\eta }$}}\). In case of objects of intermediate sizes Henry introduced correction function f(κa) depending on κa parameter \(u = {\raise0.7ex\hbox{$U$} \!\mathord{\left/ {\vphantom {U {\varDelta E}}}\right.\kern-0pt} \!\lower0.7ex\hbox{${\varDelta E}$}} = \left( {{\raise0.7ex\hbox{${\varepsilon \varepsilon_{0} \zeta }$} \!\mathord{\left/ {\vphantom {{\varepsilon \varepsilon_{0} \zeta } \eta }}\right.\kern-0pt} \!\lower0.7ex\hbox{$\eta $}}} \right)f\left( {\kappa {\kern 1pt} a} \right)\). All these three formulas represent approximate solutions valid when particle charge and thus its potential is relatively small.
For very high ζ values, the \(u = f\left( \zeta \right)\) relation can be obtained numerically only. For liposomes of defined size the Henry equation is suggested for obtaining zeta potential values as f(κa) function can easily be obtained knowing liposome radius a and medium ionic strength necessary for κ calculation.
From measurements of electrophoretic mobility electrokinetic (zeta) potential calculated from appropriate equation can be used for obtaining the values of so called electrokinetic charge according to the formula (Gouy–Chappmann approximation):
where k is the Boltzman constant, T temperature and e is the elementary charge.
Electrokinetic (zeta) potential can be measured in zetameter apparatus, where the electrophoretic mobility values are directly converted to zeta using the Henry equation. Although zeta potential is not equal to surface potential, it is often used for the characterization of electric properties of liposomes, as an analogue of resting potential of cell membrane (Kutschera et al. 2010; Honary and Zahir 2013). The electric properties of some organelles (as plastids/chloroplasts) and protoplasts, with exposed lipid layers, can also be measured (Nagata and Melchers 1978; Abe and Takeda 1988; Obi et al. 1989a, b, 1990; Gimmler et al. 1991).
Knowing the changes of electric parameters of plant cell membranes induced by the interaction with various molecules (with ionic and polar groups) some physiological properties of the membranes may be described. Based on these results, one can conclude about the density and distribution of charges localized on membrane, possible surface shielding due to adsorption of organic and inorganic polar molecules (Rabinovich-Guilatt et al. 2004; Patila et al. 2007; Huynh et al. 2009). Many physiological reactions at membranes depend on local ion concentration. Thus, information about electric properties of bilayer as a function of the composition of the aqueous solution and of the lipid structure may be helpful in explanation of bio-processes.
The changes of the electrokinetic potential of plant membranes caused by various ions, which may be present inside or outside the cells, can provide information about their effect on membrane properties (Wagatsuma and Akiba 1989; Richter and Dainty 1990; Gringon and Sentenac 1991; Marschner 1995; Franco et al. 2002). The response of plant cell membranes to H+, Na+, Ni2+, Ca2+, Al3+, La3+, SeO4 2− at toxic concentrations were analyzed in detail (McLaughlin and Whitaker 1988; Suhayda et al. 1990; Kinraide 1994, 1998a, 2003; Kinraide et al. 1998; Zhang et al. 2001). It was indicated that electric potential of model membranes was dependent on both the amount and valency of ionic groups in adsorbed molecules, (Rudolphi-Skórska et al. 2014b), and their dimensions (Filek et al. 1982).
The biological interpretation of electric properties of lipid bilayers (surface charge, electric potential) was enriched by measurements of ion adsorption (Yermiyahu et al. 1997a, b) and ion distribution at cell membranes (Kirchner 1996). Experimental results of electrokinetic potentials and ion adsorption allowed us to use theoretical models for the description of the possibility of ion binding at various sites (“domains”) of cell membranes. These models were subsequently verified by experiments leading to an estimation of the interaction of ions with various surface groups (Kinraide et al. 1998). It was found that theoretically calculated values of the electric potential of mixed lipid layers correlated very well with the published zeta potentials of native protoplasts of various plants. For protoplast membranes, isolated from root system, it was shown that adsorption of inorganic ions on the surface of increased negative charge density correlated with ion charge and size. This information can be used to predict the possibility of growth and development of some genotypes (characteristic electric potential of root membranes) in a particular environment (of characteristic ion composition). Comparison of electrokinetic potential with resting potential measured using microelectrodes (surface potential of membranes) proved the very good agreement between results obtained by both techniques (Shomer et al. 2003).
Liposomes, prepared from individual lipids were also used in studies of interactions with organic substances such as peptides and antibodies (McLaughlin and Whitaker 1988; Beschiaschvili and Seelig 1992), hormones and polar organic substances (Filek et al. 2002b; Gzyl-Malcher et al. 2007; Pawlikowska-Pawlega et al. 2014). It was indicated that hormones of ionic character (as negatively charged auxins and gibberellins or positively charged cytokines) as well as molecules with polar groups (toxin–zearalenone) may modify the electric properties of liposomes composed of both negatively charged phospholipids (PG) and zwitterionic PC and PE. On the basis of changes of electrokinetic potential, the possibility of their adsorption on membranes containing these lipids was suggested. Detailed studies of lipids with defined amounts of saturated and/or unsaturated fatty acids allowed us to discuss the possibility of incorporation of some substances of more hydrophobic character (sterols, tocopherols) into lipid layer. Biological interpretation of electric properties of lipid membranes may be useful in explanation of some physiological and stress induced processes.
In Table 3 some examples of zeta potential data of liposomes and organelles isolated from plant cells are collected.
For chloroplasts, isolated from plants, it was found that after application of hormones electrokinetic potential of their membranes was changed in the same direction as that of liposomes, prepared from lipids extracted from chloroplasts (Filek et al. 2007). These dependencies were observed independently on tissue (vegetative and generative apexes of rape) from which lipids and chloroplasts were extracted. It was shown that gibberellic acid—hormone important for stimulation of generative development of winter plants—had stronger influence on physicochemical properties of membranes of apexes of vegetative plants, whereas, auxins—hormones which usually block the generative development of apexes—showed relatively weak action.
Some differences in values of electrokinetic potential obtained for model liposomes and native membranes were assigned to the presence of proteins containing charged groups. Comparison of electric charges calculated from electrokinetic potential of protoplasts and liposomes (prepared from protoplast’ lipids) allowed to separate the effects associated only with the presence of lipids originating from proteins (Filek et al. 2002b).
Monolayers
Lipid monolayers formed spontaneously at the water–air interface provide a model for studying the two-dimensional structure of this system (McConnell 1991; Knobler and Desai 1992; Möhwald 1993), to elucidate the interactions with polar substances (adsorbed from water solution—to mimic the polar side of cell membrane), as well as the effect of non-polar molecules incorporated into layer. Lipid monolayers are prepared using the Langmuir technique. In this technique, the dependence of surface pressure (π) on the layer compression degree (expressed by the value of the area accessible for dispersed molecule A) is measured to obtain so called surface pressure isotherm. Surface pressure is defined as the difference of surface tensions of the air–water interface (γ 0) minus that of the interface covered by the monolayer (γ). For some systems compression of the monolayer causes a series of two-dimensional phase transitions (Andelman et al. 1994). At some two-dimensional density of molecules (at defined compression degree), the hydrophobic parts of the molecules come into, but a layer remains disordered and fluid. Further compression can lead to layer transition to more condensed state, marked by a plateau in the isotherm or different slope of the isotherm. At further increase of molecular density highly ordered state, similar to that found in liquid crystals is formed (Figure 1).
At some stage corresponding to the highest molecular packing layer cannot be further compressed without destabilizing its two-dimensional structure (Gopal and Lee 2001). The surface pressure in such condition is defined as collapse pressure (π coll) is equivalent to the minimum surface tension of a monolayer. For fully compressed monolayers, the area per molecule (A lim, limiting area) is the smallest and characteristic for lipids building the layer. These two parameters, i.e., collapse pressure and limiting area can be easily determined being very important parameters characterizing a layer interacting with aqueous subphase of defined composition. Kundu et al. (2005) described two characteristic types of layer collapse: (1) when abrupt decrease of surface pressure appears after reaching its maximal value—so-called constant area collapse or (2) when the pressure remains almost constant despite the further compression—so-called constant pressure collapse.
The surface parameters (π coll and A lim) of Langmuir monolayers are used to detect subtle changes of mechanical properties related to the presence of various polar head groups in lipids and varying degrees of saturation of fatty acid residues. Their values allow to conclude about formation of “domains” which may interact with water soluble substances (Vollhardt 1993; Hu and Granek 1996) as well as to speculate about monolayer thicknesses (Saint-Jalmes and Gallet 1998). Application of Brewster angle microscopy or scanning probe microscopy makes possible the monitoring of the microdomains at a layer surface resulting from the interactions with molecules adsorbed from a subphase (Dynarowicz-Łątka et al. 2002; Miñones et al. 2002; Gzyl-Malcher et al. 2011; Sakamoto et al. 2013).
Stearic acid (SA), as a component of lipids in the membranes of plants and animals (Greń et al. 2012), was often used as reference substance for the study of the structural properties using Langmuir monolayers as model system. The presence of the polar carboxyl group and a long saturated hydrocarbon chain of the acid molecule allowed a spontaneous organization at the water/air interface (of hydrophilic/hydrophobic character).
Studying stearic acid monolayers, Kundu and Langevin (2008) showed the changes in the values of collapse pressure in the presence of both: monovalent (Na+) and divalent (Mg2+, Ca2+, Ba2+, Zn2+, and Cd2+) ions. The authors found that the degree of dissociation of the carboxyl group (pH dependent) affects isotherm shape and π coll value. This process was observed in the presence of both: mono- and bi-valent ions, being also dependent on the size of particular cation present in aqueous solution. Yazdanian et al. (1990) showed that under pH conditions in the range 5.5–6.0, i.e., as frequently occur in plant cells, appear the interaction of ions with monolayers.
The impact of ions on the “stability” of the monolayers was also studied. Avila et al. (1999) analyzed the change (decrease) of the A value at the set π levels. They found that this parameter is also dependent on the pH of the aqueous medium. The measurements of surface potential of Langmuir monolayers have shown that more stable layers are formed in the presence of cations (Yazdanian et al. 1990). This was explained as due to the compensation of negative charge of fatty acid monolayers by cations. Effect of trivalent ions so far has not been intensively studied. Only for the so-called rare elements, Silva et al. (1998) showed that in the presence of europium (Eu) and terbium (Tb) ions “loosening” of the surface structure occurs, while the opposite effect was observed after introduction of yttrium (Y) ions to the aqueous phase (Zotova et al. 1998). The differences between the impact of these ions on fatty acid monolayers can be related to sizes of ions and their sorption capacity.
Another important structural feature of the monolayers, which can be determined from π-A dependencies is so-called “elasticity”. Modification of the Langmuir technique by the introduction of dynamic oscillation function enabled He et al. (2002) to determine “dynamic elasticity” of stearic acid monolayer on water and on aqueous solutions containing bi- (CdCl2) and tri-valent (TbCl3) ions. They showed differences in monolayers’ “elasticity” dependent on the presence of both types of ions. In the presence of Cd ions elasticity of stearic acid layer was discontinuous function of molecular packing while in the presence of the Tb ions such “discontinuity” did not exist.
Abousalham et al. (2000) compared the properties of the monolayers prepared from stearic acid (saturated) with those obtained for the unsaturated fatty acids (oleic, linoleic, ricinoleic acids) and their oxidized forms: 13 (S)-hydroperoxyoctadeca-9Z, 11E-dienoic (13-HPODE) and 13 (S)-hydroxyoctadeca-9Z, 11 Edienoic (13 Hode) acids. They showed that the monolayers formed from acids containing unsaturated bonds and from oxidized fatty acids are more expanded. Measurements of surface potentials of the monolayers (using vibrating sensor electrode) allowed to conclude that orientation of molecules in layers formed from oxidized fatty acids was changed. With increasing compression degree molecules of these oxidized fatty acids underwent spontaneous desorption from monolayer to the aqueous subphase. This is an important observation that can be used to elucidate the mechanisms of physiological processes associated with stress, particularly with oxidative stress associated with oxidation by reactive oxygen species.
The fatty acids were also used as model substances in the preparation of two-component monolayers, mainly with cholesterol (an important component of cell membranes). The presence of OH group in the ring structure of cholesterol allows spontaneous organization of mixtures of this compound with long-chain fatty acids. Sparr et al. (1999) showed that, depending on the concentration of cholesterol in mixture with saturated fatty acid (palmitic acid, 16:0) either homogeneous monolayer with a uniform surface structure (at low cholesterol concentration) or heterogeneous ones (at higher ratios of cholesterol:fatty acid), rougher, comprising local folding, are formed. This effect can be explained by the presence in the native membranes “domains” of different sizes and shapes favorable specific adsorption of organic and inorganic substances from the aqueous medium.
Studies of monolayers of membrane lipids
Studies of phospholipid monolayers
The simplest phospholipid, in terms of chemical structure is a phosphatidic acid containing a negatively charged, phosphoric acid residue. Although, as shown previously (Table 1) in cell membranes it is present only in relatively small concentrations, it plays an important role in physiological processes as a significant signal substance (Testerink and Munnik 2005). Studies of phosphatidic acid monolayers, containing a saturated (myristic, 14:0) fatty acid as hydrophobic part (1,2-dimyristoyl-sn-glycero-3-phosphate, DMPA), provided information on the changes of monolayer “stiffness” depending on the ordering of the acyl chains. Schalke et al. (2000) suggest that the presence of saturated fatty acid residues causes a bent of hydrophilic part of the lipid (to “adapt” to the shrinking area available for molecules) which results in the formation of structures of a higher density of negative charge. This indicates that the increase in saturation of fatty acids in lipids of native membranes not only reduces the “permeability” of their hydrophobic part but also favors the formation surface “domains” exhibiting higher density of negative charge, which in turn may affect the possibility of adsorption of the compounds from cytosol (or inter-cellular space).
Effect of organic and inorganic ions on the structural properties of phosphatidic acid monolayers was examined inter alia by Vaknin et al. 2003; Faraudo and Travesset 2007a, b. The presence of polyamines, polycationic compounds responsible for the developmental processes of plants and their resistance to stress conditions, significantly modify both the surface pressure isotherms of monolayers and the electrokinetic potential of liposomes (Rudolphi-Skórska et al. 2014b). It was found that putrescine (polyamine of two positive charges) had a similar effect on physico-chemical parameters of the monolayers to that which was recorded for calcium ions. This may indicate that for modification of the structural and electrical properties of the cell membrane more important is the electric charge than the chemical structure of the adsorbed compound (organic and non-organic counter-ion).
The influence of calcium ions on the monolayers’ structure was also tested in systems formed from other than phosphatidic acid lipids, containing more complex polar part with the exposed negative charge. Garidel et al. (2000) showed that these ions may partially penetrate phosphatidylglycerol (PG) monolayers containing saturated fatty acid residues DMPG (1,2-dimyristoyl-sn-glycero-3-phospho-1-glycerol), which polar region, compared to monolayers of phosphatidic acid, is significantly larger. It was found that while the Ca2+ ions induce condensation of PG monolayer other bivalent ions (Mg2+ and Sr2+) act inversely. These different effects can be explained by two counter-acting processes: for calcium—by formation of ionic bonds with negative groups of phosphatidylglycerol (thus promoting formation of a more compact structure), while for Mg2+ and Sr2+—by ionization of lipid polar groups (leading to the layer expansion) (Garidel and Blume 2005). Infrared reflection absorption spectroscopy (IRAS), X-ray diffraction and reflectivity measurements confirmed that the ordering degree (condensation) of DPPG monolayers (1,2-dipalmitoyl-sn-glycero-3-phospho-glycerol) is dependent on the chemical nature of the interacting ion (Maltseva et al. 2006). In simultaneous presence of mono- and di-valent cations competition between layer condensing action of Ca2+ cations, and a condensation preventing influence of Na+ may lead to formation of “domains” of irregular shape and various sizes (Grigoriev et al. 2003). It has been postulated that the ionization of polar groups of PG caused an increase of hydration degree, which may result in local “deeper dipping” of the layer in the aqueous phase (Miñones et al. 2003). Experiments in which protein components (photosystem PSI) were introduced into PG monolayers (model of chloroplasts membranes) allowed to conclude about the changes in photosynthetic activity in the presence of cation excess. Wu et al. (2005) demonstrated that calcium ions modify the interaction between PSI and PG, mainly by neutralizing the phosphate group of PG, which resulted in a reorganization of the molecules in the PSI complex. Testing temperature dependence of the structural properties of DPPG monolayers showed the probability of formation of the lipid aggregates at lower temperatures, close to phase transition temperature (Vollhardt et al. 2000). This observation may be important for understanding the mechanisms of membrane changes in physiological processes occurring at low temperatures (stress, vernalization).
By studying mixed monolayers, formed from lipids containing the same polar groups differing in saturation degree of fatty acid residues Sanchez and Badia (2003) characterized the changes in the structure of the dialkylphosphatidylcholines (DPPC/DLPC; phosphatidylcholines with palmitic—16:0 and lauric 12:0 acids) mixed monolayers as a function of the ratio of the lipids. The authors showed that in such systems “domains” rich in lipid with longer fatty acid residues (DPPC) “floating” in the matrix of shorter lipid (DLPC arise) are formed. The existence of domains was also confirmed in the AFM (atomic force microscopy) images for mixtures of phosphatidylcholines with saturated (16:0) and unsaturated (18:1) acids (DPPC/DOPC) (Jurak and Chibowski 2010). The results of these studies lead to the conclusion that the presence of acids of fewer CH2 groups and higher unsaturation degree promotes the formation of the matrix for “domains” containing lipids of longer and saturated hydrocarbon chains. In mixed monolayers composed of the lipids of the same composition of hydrophobic part (16:0) and different polar groups (PC and PG) Saad et al. (2009) showed that mixed layers with greater fraction of DPPG exhibit higher elasticity. This physico-chemical property may be important in explaining physiological role of changes in lipid composition of native membranes during adaptation of cells to the action of low/high temperatures.
The effect of α-tocopherol (which increased concentration in natural membranes) is related to the adaptation of cells to stress conditions (Munné-Bosch et al. 1999) introduced to model lipid layers was examined inter alia by Jurak and Minones-Conde (2013) and Rudolphi-Skórska et al. (2014a). It has been shown (Jurak and Minones-Conde 2013) that α-tocopherol causes a destabilization of the layers of lipids containing saturated fatty acids (DPPC) by decreasing the ordering of the acyl chains, whereas it increases the stability of monolayers composed of unsaturated lipids (POPC/DOPC). These observations may help to clarify the cause-and-effect between changes in lipid unsaturation and tocopherol synthesis in cells exposed to stress factors.
Introduction of TAP—synthetic lipid with cationic polar group, to the phospholipid layer was a model for reasoning about the properties of monolayers containing the positively charged protein structures (model of natural membrane). In Gzyl-Malcher et al. (2011) studies it was found that the positive net charge of mixed DPPC/DTAP layers can be neutralized by introducing inorganic anions (SeO4 2−) to water solution, whereas organic anions (hormone—auxin) may penetrate the lipid monolayer causing its expansion/fluidization. Inorganic ions and charged hormones simultaneously present in aqueous phase interact in competitive way with oppositely charged polar groups of mixed layers formed from negatively charged DMPS (1,2-dimyristoyl-sn-glycero-3-phospho-l-serine) and DPTAP (Gzyl-Malcher et al. 2009).
Studies using Langmuir technique were performed also for mixtures of phospholipids extracted from the plants for detecting the changes of structural properties of membranes associated with the differentiation (embryogenesis) (Filek et al. 2003a, b, 2005a; Gzyl et al. 2004; Gzyl-Malcher et al. 2007). Lipids obtained from non-embryogenic calli formed more “condensed” monolayers than that from embryogenic calli. In the presence of hormones, the larger changes of monolayer properties were detected for lipids of non-embrogenic in comparison to that of embryogenic calli. This may suggest that the presence of hormones in media of non-embryogenic calli is necessary to induce changes in membrane structure needed for differentiation processes in the direction of embryogenesis.
Studies of glycolipid monolayers
In comparison to experiments carried out for model phospholipid systems, physicochemical properties of layers of galactolipids, (compounds typical for plant cell membranes) were tested to a lesser extent. Glycolipids: digalactosyldiacylglycerol (DGDG) and the mono-galactosyldiacylglycerol (MGDG) constitute a major class (approx. 75 %) of lipids of chloroplasts membranes (Dormann and Benning 2002; Hincha 2003; Bruno et al. 2005). Compared to the layers formed from individual galactolipids, an equimolar mixture of MGDG and DGDG exhibits different physico-chemical properties, indicating interactions between the polar groups at the water/air interface. Studies of Bottier et al. (2007) using Raman and Fourier Transform Infrared (FTIR) spectroscopies confirmed the existence of such interactions, as evidenced by higher ordering of the acyl chains in the mixture, than in layers formed from the individual components. The work of Gzyl-Malcher et al. (2008), based on the analysis of structural parameters of monolayers formed from galactolipids extracted from callus cells (obtained from a variety of plant tissues) demonstrated that layers of galactolipids extracted from inflorescences are more expanded and less stable than those formed from galactolipids extracted from immature embryos. Since the calli derived from immature embryos exhibit greater regenerative abilities than those obtained from the inflorescences, the differences in the structure of the membranes of the two tissues may be important in describing the mechanism of plant regeneration.
The balance between the amount of DGDG and MGDG is essential for the functioning of proteins that form antenna complexes of photosystems in chloroplasts (Pali et al. 2003). As shown by Dynarowicz-Łątka et al. (2005), the presence of glycolipids in mixed monolayers containing also phospholipids plays an important role in the organization of the monolayer. Depending on the amount of the sugar groups a partial segregation of the monolayer arises.
This may explain the possibility of the specific inclusion of photosystem complexes PSII and PSI by the lipid membranes of chloroplasts.
The role of tocopherol in protection of chloroplast membrane against reactive oxygen species generated during photosynthesis and under environmental stress conditions was studied by Rudolphi-Skórska et al. (2014b). It was found that the presence of tocopherol in ozonized monolayer of MGDG or DGDG partially inhibits lipid oxidation by reducing the amount of lipid undergoing oxidation. The protective action of tocopherol was greater for lipid with single sugar group.
The physicochemical properties of galactolipid layers were also tested in terms of interaction with metal ions. In view of the importance of the stress induced by cadmium ions for physiological processes occurring in chloroplasts the changes of structural parameters of mixed monolayers of MGDG and DGDG caused by the interaction with the metal ions were determined. Gzyl-Malcher et al. (2008) showed that cadmium ions to a greater extent influence structural properties of glycolipid containing one sugar group. Introduction of tocopherol to MGDG/DGDG mixtures affected the interaction of Cd ions with monolayers, independently of proportions between galactolipid species (Gzyl-Malcher et al. 2010). This observation can be used to conclude about the physiological modification of the glycolipid composition in chloroplast membranes in processes of plant adaptation to the stress caused by heavy metals.
Conclusion
Examples of use of the results of the measurements of physicochemical properties of lipids for interpretation of the structural and functional changes in the native membranes were presented. The continuation of this type of research may contribute to the detailed description of the mechanism of physiological reactions occurring under stress and during the course of developmental processes in plants.
Author contribution statement
Study conception and design: Rudolphi-Skórska E., Sieprawska A.; acquisition of data: Rudolphi-Skórska E.; analysis and interpretation of data: none; drafting of manuscript: Rudolphi-Skórska E., Sieprawska A.; critical revision: Rudolphi-Skórska E., Sieprawska A. Author’s percent contribution: Rudolphi-Skórska E.—60 %; Sieprawska A.—40%
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Rudolphi-Skórska, E., Sieprawska, A. Physicochemical techniques in description of interactions in model and native plant membranes under stressful conditions and in physiological processes. Acta Physiol Plant 38, 22 (2016). https://doi.org/10.1007/s11738-015-2034-1
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DOI: https://doi.org/10.1007/s11738-015-2034-1