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Lipids of Halophyte Species Growing in Lake Elton Region (South East of the European Part of Russia)

  • Olga A. Rozentsvet
  • Viktor N. Nesterov
  • Elena S. Bogdanova
Living reference work entry
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Abstract

The chapter describes the specificity of lipid composition of halophytes growing in Prieltonie, one of the saline regions of the northern part of the Caspian lowland of Russia. In addition to salinization, the plants growing in this region experience the effects of intense insolation and high temperature – throughout most of their vegetative season. Soil salinization is one of the main factors affecting on the dominance of halophytes in the region. The adaptation of plants to salt stress is based on the ability of cells to control the transport of salt across membranes. The structural basis for cell membranes is provided by amphiphilic lipids with a polar hydrophilic group and nonpolar hydrophobic fatty acids, as well as steroid compounds. The halophyte groups (eu-, cryno-, and glycohalophytes) differ in their lipid composition: the contents of different groups and classes of lipids – as well as in the fatty acid composition. Lipids are specifically allocated in the plant cell. Glyceroglycolipids are predominantly concentrated in the cell plastids. Glycerophospholipids form the matrix of extra-chloroplastic membranes. The content of glycerolipids in the chloroplast membranes positively correlates with the size of the chloroplast and the content of photosynthetic pigments. The chloroplast and mitochondrial membranes of halophytes contain detergent-resistant regions enriched in sterols, ceramides, and saturated lipids. The differences in the lipid composition in membranes of cells, organelles, and microdomenes are associated with the specifics of salt metabolism of the halophyte species and indicate involvement of lipids in the adaptation of plants to the abiotic environmental factors.

Keywords

Halophyte Lipids Membranes Photosynthetic apparatus Rafts 

Abbreviations

Car

Carotenoids

Cer

Cerebrosides

Chl (a, b)

Chlorophylls (a, b)

DGDG

Digalactosyldiacylglycerol

DPG

Diphosphatidylglycerol

DRM

Detergent-resistant microdomenes

ES

Esterified sterols

FA

Fatty acids

GL

Glyceroglycolipids

LHC

Light-harvesting complexes

MDA

Malonic dialdehyde

MGDG

Monogalactosyldiacylglycerol

ML

Membrane lipids

NL

Neutral lipids

PA

Phosphatidic acid

PA

Photosynthetic apparatus

PC

Phosphatidylcholine

PE

Phosphatidylethanolamine

PG

Phosphatidylglycerol

PI

Phosphatidylinositol

PL

Phospholipids

ROS

Reactive oxygen species

SE

Standard error

SQDG

Sulfoquinovosyldiacylglycerol

ST

Sterols

1 Introduction

Accumulation of salts in the soil is one of the main environmental factors limiting the growth and productivity of plants (Flowers and Colmer 2015). The expansion of the area of saline soils on the planet is associated with the global climate change, spread of irrigation, and population growth, and it poses threats to the human health, to the ecosystems, and to the national economies (Shabala et al. 2014). Halophyte plants are capable to survive on highly salinized soils throughout their entire life cycle. This is a heterogeneous group in respect to their ecological, physiological, biochemical, morphological, and anatomical features. On the basis of the types of salt tolerance, halophytes can be divided into salt-accumulating, salt-excreting, and salt-impermeable. The morphological and anatomical differences include the presence or absence of salt glands in leaves, the types of leaf structure (xeromorphic or succulent), and Kranz anatomy of chlorenchyma in some species (Voznesenskaya et al. 2007; Grigore et al. 2014). The specifics of anatomical and morphological features underlie differences in the organization of ion transport, water metabolism, and photosynthesis – and, as a consequence, in the strategy of salt tolerance (Balnokin et al. 2005).

The damage of plants under the conditions of salinization comes from disorders in the ion homeostasis, which lead to osmotic stress; from the toxic effects of salts on the synthesis and functions of proteins; and from the oxidative stress caused by the excessive production of reactive oxygen species (ROS) (Bose et al. 2013). The mechanisms that counteract the adverse effects of salts include (1) control of the absorption of ions by roots and their transport into leaves – the processes mediated by transport proteins, channels, and aquaporins; (2) synthesis of compatible osmolytes; (3) alterations in the photosynthetic pathways; (4) changes in the structure of membranes; (5) induction of antioxidant synthesis; and (6) activation of the hormonal system (Flowers and Colmer 2015; Reginato et al. 2014). Not all halophytes possess the full spectrum of the adaptive biochemical mechanisms. Salt-excreting and salt-impermeable halophytes, for example, protect their rhizosphere by limiting the influx of ions into the root cells. In salt-accumulating plants, on the other hand, removal of salts from the cytosol occurs in the aboveground organs: these plants compartmentalize ions in the apoplast or vacuoles using the ion pumps of the cellular membranes. The osmoregulatory role in salt-accumulating halophytes is played by Na+ ions; salt-excreting and salt-impermeable halophytes regulate their osmotic balance using low-molecular organic substances, such as proline, betaine, sugars, etc. (Mansour et al. 2002).

Many of the mechanisms of plant adaptation to salinization are associated with the processes occurring in biological membranes (Shabala and Mackay 2011). The very basic functions of membranes – the barrier function and the function of selective transport (mediated by lipids and transport proteins, respectively) – gave major adaptive advantages to biological cells at the early stages of their evolution, which included the ability of those cells to sustain high salinity of their natural habitats (Dowhan et al. 2016). The structural basis for cell membranes is provided by amphiphilic lipids with a polar hydrophilic group and nonpolar hydrophobic acyl chains, as well as steroid compounds. The lipid composition of membranes of a plant cell supports their specific functions (Drin 2014). In addition to their structural role in membranes, lipids act as secondary messengers and modulators of enzymes and receptors. Lipids of plant membranes are also initial components of various phospholipase-dependent signaling systems (Munnik and Testerink 2009).

In the last decades, our knowledge about the structural-functional organization of cell membranes has undergone a significant transformation. The biological membrane is no longer considered a homogeneous lipid bilayer with proteins embedded. There is a growing body of evidence that membranes are a mosaic of discrete microdomains (Nickels et al. 2017). These microdomains have a specific lipid composition, different from the rest of the membrane – and, hence, they are characterized by high stability and packing density (Laloi et al. 2007; Simons and Sampaio 2011).

Although the term “lipid” has not been accurately defined, lipids are commonly regarded as a group of natural compounds extracted from the biological tissues by a mixture of polar and nonpolar solvents. In the mechanisms of plant adaptation to salinity, lipids play a key role in the regulation of membrane fluidity, which is a major factor modulating the functions of proteins, including the proteins of transport systems. Membrane fluidity is determined by the lipid composition of the membrane, the degree of lipid unsaturation, and the length of lipid hydrocarbon chains (Los and Murata 2004).

In this chapter, we consider specifics of the lipid composition of halophytes, which are a part of the natural flora of Prieltonie, one of the salinized regions of the northern area of the Caspian lowlands (Russia). In addition, the chapter discusses the involvement of lipids in the functioning of the photosynthetic apparatus (PA) and their role in the organization of raft structures of endoplasmic membranes.

2 Halophytes of Prieltonie

Prieltonie is an area around Lake Elton (the largest salt lake in Europe), representing natural landscapes of the desert steppe. Lake Elton is located 18 m below the sea level, and salinity of its water reaches 400 g/L in the summer season. The halophytic vegetation of Prieltonie is very diverse and characterized by a zonal distribution of the communities, which is typical of lake basins (Sukhorukov 2014). Plants, growing under these conditions, tolerate intense environmental pressures: apart from salinization, they are subjected to high insolation and temperature – throughout most of their vegetative season. Soil salinization is, however, a major factor determining growth and development of Prieltonie plants, most of which are halophytes. Plant samples were collected during 2012–2015, usually in mid June in the first half of the day.

Table 1 shows the Prieltonie halophytes of different taxonomic and ecological groups. The halophytes belong to three families (Chenopodiaceae, Plumbaginaceae, and Asteraceae) and are represented by eight genera (Anabasis, Artemisia, Halocnemum, Halimione, Limonium, Petrosimonia, Salicornia, and Suaeda). Most of the species are obligate halophytes found exclusively in saline habitats. Species of the genus Artemisia can grow on both salinized and nonsaline soils, i.e., they are facultative halophytes. Depending on their ability to accumulate salts, these plants represent three ecological groups: salt-accumulating halophytes (euhalophytes); halophytes excreting excessive salt on the surface of their leaves (crynohalophytes); and halophytes preventing the uptake of salts through the root system (glycohalophytes).
Table 1

The systematic and environmental classification of halophytes

Taxon

Life form

Ecological group

The water content in overground part, %

Asterales

    

 Asteraceae

    

  Artemisia

    

   Artemisia santonica

Semishrub

Glycohalophyte

Xeromesophyte

60

   Artemisia pauciflora

Semishrub

Glycohalophyte

Xeromesophyte

54

   Artemisia lercheana

Semishrub

Glycohalophyte

Xeromesophyte

55

Caryophyllales

    

 Chenopodiaceae

    

  Anabasis

    

   Anabasis salsa

Semishrub

Euhalophyte

Xeromesophyte

55

  Halocnemum

    

   Halocnemum strobilaceum

Semishrub

Euhalophyte

Xeromesophyte

77

Halimone

    

   Halimone verrucifera

Annual herbs

Crynohalophyte

Xeromesophyte

76

  Petrosimonia

    

   Petrosimonia brachiata

Annual herbs

Euhalophyte

Xeromesophyte

75

  Salicornia

    

   Salicornia perennans

Annual herbs

Euhalophyte

Mesoxerophyte

85

  Suaeda

    

   Suaeda acuminate

Annual herbs

Euhalophyte

Mesoxerophyte

80

   Suaeda eltonica

Annual herbs

Euhalophyte

Mesoxerophyte

91

   Suaeda linifolia

Annual herbs

Euhalophyte

Mesoxerophyte

84

   Suaeda salsa

Annual herbs

Euhalophyte

Mesoxerophyte

86

Plumbaginales

    

 Plumbaginaceae

    

  Limonium

    

   Limonium caspium

Perennial herbs

Crynohalophyte

Xeromesophyte

57

   Limonium gmelinii

Perennial herbs

Crynohalophyte

Xeromesophyte

76

The content of water in the leaves/overground part of the plants studied depended on the strategy of their salt tolerance. In the euhalophyte group, it varied from 75% to 91%; in the group of crynohalophytes, the range of variation was from 57% to 76%; in glycohalophytes, water content did not exceed 60%. The specific value of water content in the leaves of a halophyte was determined by both its salt tolerance strategy and the life form of the plant. For example, the leaves of the half-shrubs H. strobilaceum (euhalophyte) and H. verrucifera (glycohalophyte) had the same water content as the leaves of the herbaceous euhalophyte P. brachiata (Rozentsvet et al. 2014). The euhalophyte group was also heterogeneous in regard to their ability to retain moisture. The leaves of P. brachiata, for example, had the lowest water content as compared to the leaves of Suaeda species – despite the fact that they belong to the same family. In general, euhalophytes were characterized by a higher content of water in their tissues comparatively to glyco- and crynohalophytes. The differences in water content are associated with the anatomical and morphological features of halophytes: euhalophytes are characterized by leaf halosucculence, whereas glyco- and crynohalophytes are haloxerophytic (Grigore et al. 2014).

In Prieltonie, euhalophytes grow on the most mineralized and moistened soils, in which salinity can reach 8% of the soil air-dry weight and moisture can be up to 38% (Table 2). Crynohalophytes grow at a level of soil salinity of 0.6–3.1%, but can adapt to different levels of soil moisture: L. gmelinii colonizes soils with a moisture of 25%, whereas L. caspium grows on soils with a moisture of 12%. Glycohalophytes grow under milder conditions as compared to other halophytes: soil salinity does not exceed 1.6%, and the moisture level is more than 25%.
Table 2

Physico-chemical characteristics of the soil in the basal zone of halophytes, differing in the type of salt accumulation

Species

Mineralized soils, % of the soil air-dry weight

Moistened soils, % of the soil air-dry weight

pH

Euhalophytes

0.7–8.0

4–38

7.9–9.7

Crynohalophytes

0.6–3.1

8–27

7.6–9.9

Glycohalophytes

0.4–1.6

13–27

8.2–9.4

Note. The minimum and maximum values are shown

The phytocenoses of the surroundings of Lake Elton form four belts, starting from the center of the basin. The most mineralized belt is mainly represented by two species: S. perennans and H. strobilaceum. More common in the second belt are annual species of the genus Suaeda, and herbaceous perennials from the genus Limonium can be found occasionally. In the third belt, the annuals Petrosimonia oppositifolia and S. linifolia are abundant, and the half shrub H. verrucifera can be found. The shrubs A. pauciflora, A. santonica, A. salsa, Atriplex cana, Suaeda physophora, and others form phytocenoses of the fourth belt (Sukhorukov 2014).

3 Lipid Composition of Leaves of Prieltonie Halophytes

Lipids are one of the four classes of biomolecules that are essential components of cells of all living organisms (Dowhan 2016). Plant lipids and FA also play a key role in the regulation of plant interactions with their environments, since plants have a sedentary lifestyle (Nakamura and Li-Beisson 2016; Rozentsvet et al. 2017). Depending on their chemical structure, lipids are divided into polar and neutral (NL). Polar lipids are the main building material of membranes. They include glycolipids (GL), phospholipids (PL), and sphingolipids. GL and PL are derivatives of the triatomic alcohol glycerol, and sphingolipids are derivatives of the amino alcohol sphingosine. NL are a more diverse and multifunctional group of lipids. Some NL are deposited as the energy reserve of the cell; others are incorporated in the cell membranes and participate – along with glycero- and sphingolipids – in the regulation of cell metabolism. There are also NL that are involved in signal transduction and NL that create a protective layer on the surface of stems and leaves, preserving them from drying out and from infections (Moreaua et al. 2018).

Lipids are specifically allocated in the plant cell in accordance with their functions. GL are predominantly concentrated in the cell plastids (Nakamura and Li-Beisson 2016). However, they are also found in other cell membranes – in the highly curved regions of EPR and mitochondria, where membranes form bends, folds, and protrusions. Ample experimental data indicate the involvement of GL in the process of photosynthesis (Allakhverdiev et al. 2002; Deme et al. 2014). PL, for the most part, form the matrix of cell membranes, including plasmalemma, tonoplast, and the membranes of mitochondria and chloroplasts; they provide for compartmentalization of biochemical processes in the cell (Drin 2014).

Total lipids are usually extracted from biological samples with a mixture of polar and nonpolar solvents. In the case of plant tissues, a mixture of chloroform and methanol is commonly used. The quantitative analysis showed that euhalophytes contain less amount of total lipids than other types of halophytes (on average, 1.5–2.0 times as less, accounting for all extractable lipid substances; Fig. 1). The content of total lipids varies a lot in individual plants, yet the difference between halophytes with different strategies of salt tolerance is obvious and statistically significant.
Fig. 1

The content of total lipids in the leaves of halophytes, mg/g dry weight (F = 12.4, p = 0.005). Box plot of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes

The separation of cells’ total lipids by thin-layer and column chromatography (Rozentsvet et al. 2014, 2018) shows that the content of GL in the pool of total lipids varies from 10 to 45 mg/g of dry weight (Fig. 2a). Most diverse in regard to GL content are euhalophytes, and, at the same time, the content of GL in plants of this group is about two thirds of what is found in cryno- and glycohalophytes (F = 4.8, p = 0.01). The content of PL in plants of the three halophyte groups is almost the same (9–13 mg/g of dry weight; Fig. 2b). The NL content, on the other hand, shows a significant difference between the three groups. In the leaves of crynohalophytes, the content of NL is maximal and twice as high as in the leaves of eu- and glycohalophytes (F = 8.5, p = 0.02) (Fig. 2c).
Fig. 2

The content of in the leaves of halophytes, mg/g dry weight. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; glyco- (a), phospho- (b), and neutral lipids (c)

The analysis of FA composition of total lipids reveals predominance of FA with a chain length of 16–18 carbon atoms (more than 85% of total FA; Table 3). The relative content of FA with a chain shorter than 16 carbon atoms does not exceed 5% of total FA, whereas the content of long-chain FA (> C20) can reach 13% (e.g., in the euhalophyte S. perennans). The main saturated FA is palmitic (C16:0); it is especially abundant in the lipids of euhalophytes (24–28% of total FA), followed by crynohalophytes and glycohalophytes (Table 3). Unsaturated FA are represented by oleic (C18:1n-9), linoleic (C18:2n-6), and α-linolenic (C18:3n-3) acids. Their contents in total lipid extracts are ranged as follows: C18:1 < C18:2 < C18:3. The specific values, however, largely depend on the characteristics of the species. In the euhalophytes S. perennans and P. brachiata, for example, the contents of C18:1 are 7 and 24% of total FA, respectively. The content of C18:3 in eu-, cryno-, and glycohalophytes varies in the ranges of 25–41, 32–54, and 39–46% of total FA, respectively. The highest С18:3 content (54%) and, on the whole, the highest unsaturations of FA (77%) are characteristic of the crynohalophyte L. gmelinii.
Table 3

Fatty acid composition of total lipids in the leaves of halophyte, % of sum

FA

S. perennans

S. acuminata

S. linifolia

S. salsa

S. eltonica

A. salsa

H. strobilaceum

P. oppositifolia

H. verrucifera

L. caspium

L. gmelinii

A. santonica

A. lercheana

A. pauciflora

C14:0

0.8 ± 0.1

1.5 ± 0.2

1.8 ± 0.6

2.5 ± 0.1

1.1 ± 0.1

1.4 ± 0.1

4.6 ± 1.0

1.3 ± 0

1.9 ± 0.5

4.3 ± 0.1

0.7 ± 0.1

3.0 ± 0.5

3.7 ± 0.1

1.9 ± 0.2

C16:0

24.4 ± 2.0

24.3 ± 0.3

24.1 ± 2.0

23.5 ± 1.0

23.7 ± 0.3

22.3 ± 1.5

27.6 ± 2.1

23.9 ± 0.7

23.1 ± 0.7

20.5 ± 1.5

20.7 ± 2.0

18.0 ± 1.0

14.6 ± 1.3

16.9 ± 1.5

C17:0

0.6 ± 0

0.7 ± 0.1

0.2 ± 0

0.2 ± 0

0.4 ± 0.1

C16:1n7

2.0 ± 0.5

1.6 ± 0.3

2.5 ± 1.5

2.3 ± 0.3

2.0 ± 0.2

1.2 ± 0.1

1.4 ± 0.3

2.6 ± 1.0

1.9 ± 1.0

1.6 ± 0.3

1.4 ± 0.5

1.2 ± 0.1

0.9 ± 0.1

0.8 ± 0.1

C18:0

2.6 ± 1.6

3.6 ± 1.0

3.3 ± 1.0

4.0 ± 1.2

3.0 ± 0.3

2.8 ± 0.3

2.6 ± 0.6

3.8 ± 2.0

3.0 ± 1.2

2.5 ± 0.2

1.5 ± 0.5

3.5 ± 0.5

2.2 ± 0.1

1.5 ± 0.1

C18:1n9

7.1 ± 0.4

8.0 ± 1.0

11.9 ± 2.0

8.7 ± 0.1

4.3 ± 0.4

19.2 ± 1.1

13.3 ± 1.5

23.9 ± 2.3

12.1 ± 0.2

12.2 ± 1.0

6.3 ± 1.3

8.1 ± 2.0

5.6 ± 0.5

6.2 ± 0.5

C18:2n6

20.0 ± 1.2

24.6 ± 0.3

14.3 ± 1.4

12.6 ± 0.2

21.6 ± 1.6

20.3 ± 1.7

15.8 ± 1.3

14.7 ± 2.0

13.7 ± 0.6

23.5 ± 2.0

14.9 ± 0.9

17.8 ± 0.8

20.4 ± 1.9

26.3 ± 2.5

C18:3n3

29.1 ± 0.3

26.9 ± 2.1

37.6 ± 1.5

40.8 ± 2.4

40.2 ± 1.8

29.0 ± 0.8

29.6 ± 3.0

25.3 ± 0.3

40.3 ± 2.0

32.2 ± 1.6

54.5 ± 0.4

38.7 ± 3.0

45.9 ± 3.7

40.8 ± 3.8

C20:0

1.3 ± 0.2

1.0 ± 0.1

1.4 ± 0

0.8 ± 0

0.8 ± 0.1

1.6 ± 0.4

1.5 ± 0.3

1.5 ± 0.5

1.1 ± 0.1

3.2 ± 1.2

1.5 ± 0

C22:0

7.8 ± 3.0

1.4 ± 0

0.8 ± 0.2

0.8 ± 0

1.5 ± 0.1

1.0 ± 0.5

1.8 ± 0.4

1.7 ± 0.1

0.6 ± 0.1

1.6 ± 0.8

0.6 ± 0

2.5 ± 0.1

C22:1n9

1.1 ± 0.2

0.7 ± 0.1

0.4 ± 0.1

0.3

C24:0

2.0 ± 0.2

2.3 ± 0.3

0.6 ± 0.3

2.4 ± 0.4

0.5 ± 0

0.5 ± 0

1.0 ± 0

1.2 ± 0.2

0.8 ± 0.2

1.1 ± 0

2.7 ± 1.7

0.5 ± 0

1.2 ± 0

Other>C20

1.2 ± 0.2

4.1 ± 0.4

1.0 ± 0.2

3.2 ± 0.9

2.1 ± 0.2

0.8 ± 0

1.1 ± 0.1

2.2 ± 1.0

3.8 ± 1.2

1.9 ± 0.5

UFA

59.3

61.8

66.3

64.4

68.1

69.7

60.1

66.5

68.0

69.9

77.1

65.8

73.1

74.1

LCFA

13.4

9.5

3.8

5.6

3.4

3.6

4.7

4.5

4.0

3.2

0

9.7

6.7

5.6

Notes. Data are mean ± SE

Thus, all these indicators – the content of total lipids, the ratio of individual lipid groups, and the FA composition of total lipid extracts – characterize different types of halotolerance in plants of natural flora.

4 Membrane-Forming Lipids of Halophytes

The adaptation of plants to salt stress is based on the ability of cells to control the transport of salt across membranes. The system of cell membranes is a well-organized branched network, which provides the necessary “microclimate” inside the cell, plays an active role in maintaining its vital functions, and controls the fluxes of metabolites and ions into and out of the cell. The main components of non-plastid membranes are PL, among which phosphatidylcholine (PC) and phosphatidylethanolamine (PE) are predominant. Diphosphatidylglycerol (DPG, cardiolipin) is a mitochondria-specific lipid (Horvath and Daum 2013). Plastid membranes are formed by galactoglycerolipids, monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), as well as sulfoquinovosyldiacylglycerol (SQDG) and phosphatidylglycerol (PG). They are synthesized in plastids and are the main plastidic lipids under normal conditions of plant growth (Wang and Benning 2012). Plant sterols (ST) are diverse, which is a characteristic feature of plants (Valitova et al. 2016).

4.1 Glycolipids

Among GL of higher plants, MGDG is usually dominant, followed by DGDG and SQDG (Kobayashi et al. 2016). The content of SQDG does not exceed 10–12% of total GL. The proportion of MGDG in the total pool of GL is comparable in eu- and crynohalophytes of Prieltonie flora and amounts to 44–45% (Fig. 3a). In the group of glycohalophytes, this indicator is a bit lower: 40%. At the same time, glycohalophytes have a higher proportion of another galactolipid, DGDG (Fig. 3b). The differences in the structure of MGDG and DGDG determine their ability to form lamellar (bilayer) and non-lamellar structures. Since DGDG molecules tend to form a bilayer and MGDG molecules are better accommodated in a monolayer, a change in the MGDG/DGDG ratio can affect the structure and microviscosity of membranes (Kobayashi et al. 2016). The MGDG/DGDG ratio is, therefore, used to evaluate salt tolerance and heat resistance of plants (Chen et al. 2006). Halophytic plants usually have low values of the ratio (1–1.5), whereas glycophytes are generally characterized by a two-fold predominance of MGDG over DGDG (Rozentsvet et al. 2014). In the examined plants, this indicator ranges, on average, from 0.9 to 1.0 in all the halophyte groups, which seems to be determined by the particular conditions of plant growth in this region. The proportion of SQDG in the total GL pool in eugalophytes is 12%, which is lower than in glycogalophytes (more than 15%; Fig. 3c).
Fig. 3

The relative content of individual glycolipids in the leaves of halophytes, % of sum. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) monogalactosyldiacylglycerol (MGDG), (b) digalactosyldiacylglycerol (DGDG), (c) sulfoquinovosyldiacylglycerol (SQDG)

The ratio between individual GL in halophytes is quite adaptable; it varies depending on the halophyte type and salinity of the environment. Hirayama and Mihara (1987) found that the higher was the halophilicity of a plant, the lower was the MGDG/DGDG ratio in the plant tissues. In the halophytes Aster tripolium and Sesuvium portulacastrum, the content of SQDG was shown to grow as the salinity of the environment increased (Ramani et al. 2004). Variability of GL composition turned out to be characteristic of the halophytes of natural flora as well.

4.2 Phospholipids

In most non-plastid membranes, PC and PE are the dominant PL (Nakamura and Li-Beisson 2016). Apart from PC and PE, plants also contain PG, DPG, phosphatidylinositol (PI), and phosphatidic acid (PA). In all the studied halophytes of Prieltonie, the total content of the first three PL exceeds 85%, which gives one a reason to consider them the main PL. The analysis of PL contents in Prieltonie halophytes revealed a correlation of this parameter with the salt-accumulating strategy of plants: eugalophytes contained ~20% more PC than glyco- and crynohalophytes (Fig. 4a).
Fig. 4

The relative content of major phospholipids in halophyte leaves, % of sum. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) phosphatidylcholine (PC), (b) phosphatidylethanolamine (PE), (c) phosphatidylglycerol (PG)

In regard to PE, no significant differences between halophytes of the three groups were revealed (Fig. 4b). Taking into account that PC and PE are localized on the outer and inner sides of cell membranes, respectively, a high content of PC may indicate a greater transmembrane asymmetry and curvature of the membranes, as well as a higher lateral pressure applied to membrane proteins. The ratio of PC/PE can also be associated with the resistance of cells to salinity. In euhalophytes, for example, the relative content of PC is 1.5–2-fold of that in cryno- and glycohalophytes. PC and PE are known to differ by the size of their polar heads and the configuration of their lamellar (favored by PC) and hexagonal (characteristic of PE) phases (Wu et al. 2005). In addition to breaking the bilayer structure of biological membranes, hexagonal phase can facilitate the formation of membrane pores and water channels and, correspondingly, increase the passive diffusion of water through the membrane. In the examined halophytes, the average content of PE does not exceed 10% of total PL.

The third major type of PL in halophytes is PG. This is the only subclass of PL that is contained in the thylakoid membranes. Prieltonie crynohalophytes have an especially high content of PG in their leaves: 17% of total PL on average (F = 5.7, p = 0.04; Fig. 4c). In other halophyte groups, the relative content of PG in plant leaves is about 10% of total PL. The examined halophytes also differ by the total content of minor lipids in their leaves. In euhalophytes, it does not exceed 10%; in the plants of other halophyte groups, it is 17–20%.

4.3 Sterols

Sterols (ST) are important components of eukaryotic membranes (Moreaua et al. 2018). Free ST integrate well into phospholipid layers forming cell membranes (Valitova et al. 2016). Intermolecular interactions between ST and membrane glycero- and sphingolipids modulate the physical state of membranes, limiting the mobility of lipid acyl chains and regulating the membrane fluidity and permeability (Schaller 2004). Normally, ST regulate the aggregate state of lipid ensembles of biological membranes: on the one hand, they make highly viscous membranes more fluid; on the other, they keep fluidity of membranes in check by limiting the mobility of phospholipid hydrophobic tails (Moreaua et al. 2018).

To date, the most studied ST are ST of the plasma membrane. Interesting results, for example, were obtained in the study of plasmalemma lipids of callus cells of the halophyte Spartina patens (Wu et al. 2005). In those cells, ST turned out to be the dominant class of lipids, followed by GL and PL. There are also data on the involvement of ST in the formation of endomembranes, including membranes of EPR, mitochondria, and chloroplasts (Nesterov et al. 2017). In response to the action of NaCl, the content of free ST was shown to grow, and the ST/PL ratio increased as well (Wu et al. 2005). The content of free ST in the leaves of Prieltonie euhalophytes amounts to 15% of total NL (F = 23.8, p = 0.001). In the halophytes of other groups, it is lower (~8%; Fig. 5a). Esterified ST (ES) carry out reserve and transport functions. In the cells of halophytes, the relationships between them are reciprocal: their content was found to be minimal in euhalophytes and maximal in glycohalophytes (F = 5.6, p = 0.05) (Fig. 5b). An important indicator of salt tolerance is the PL/ST ratio, which is used to assess the sensitivity of plants to salt exposure. In salt-tolerant tomatoes, for example, the PL/ST ratio in the plasma membranes of callus cells was lower than in salt-sensitive species (Kerkeb et al. 2001). As the concentration of NaCl in the medium increased, the content of ST in the plasmalemma of callus cells of S. patens was shown to grow (Wu et al. 2005), whereas the PL/ST ratio in the plasma membrane of wheat roots was found to diminish. It is believed that the high content of ST in the plasma membrane preserves the integrity and structure of lipid bilayer but decrease permeability of the membrane. Our tests have shown that the PL/ST ratio in the halophytes of different groups varies as follows: euhalophytes, 3.8; crynohalophytes, 4.9; and glycohalophytes, 8.1 (Fig. 5c) – meaning that euhalophyte membranes contain more ST in relation to PL.
Fig. 5

The relative content sterols in halophyte leaves, % of sum neutral lipids. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) free sterols (ST), (b) esterified sterols (ES), (c) the ratio of phospholipids to sterols (PL/ST)

It should be pointed out that it is not only the content of ST but their composition as well that is important. In contrast to the animal membranes, the membranes of higher plants contain several ST: 24-methylcholesterol, β-sitosterol, stigmasterol, campesterol, and others (Schaller 2004). In the experiments with S. patens, Wu et al. found that the ratios of ST/PL and ST/GL did not change much when the concentration of NaCl in the medium was raised (Wu et al. 2005). The composition of ST, on the other hand, changed significantly: the proportion of sitosterol decreased and that of campesterol increased. The molecules of sitosterol and campesterol have a side hydrocarbon chain attached to a tetracyclic carbon structure. The substituents in the side chains of sitosterol and campesterol are ethyl and methyl groups, respectively. The shorter methyl group has a lower degree of rotation – and this makes interactions of campesterol with PL stronger, providing for a tighter packing of lipids in the bilayer.

4.4 Sphingolipids

Sphingolipids amount to 10% of total plant lipids (Michaelson et al. 2016). In the chemical structure of sphingolipids, sphingosine is attached to FA by an amide bond. There are four main types of plant sphingolipids: ceramides, glycosylceramides, free sphingoid bases, and glycosyl inositol phosphoceramides. The latter are dominant in plants (Markham et al. 2006; Michaelson et al. 2016). Sphingolipids are involved in cell signaling, apoptosis, and plant responses to hypothermia, hypoxia, etc. In addition to maintaining the structural integrity of membranes, plant sphingolipids are involved in the formation of special clusters or microdomains (rafts) in the lipid bilayer. In rafts, free ST and sphingolipids were estimated to amount to 30 and 20–40% of total lipids, respectively (Laloi et al. 2007; Simons and Sampaio 2011). It should be noted that sphingolipids are wax-like substances; they can fill holes and gaps in the membrane, reducing water loss and restoring membrane integrity – yet, at the same time, impairing membrane permeability. Sphingolipids are mainly localized in the compartments that are not photosynthetically active, but their biosynthesis is directly linked to the metabolic reactions in chloroplasts (Chen et al. 2010). Impairment of sphingolipid synthesis can, therefore, lead to the disruption of the chloroplast envelope, disorganization of thylakoid membranes and degradation of photosynthetic pigments. The content of sphingolipids in the chloroplast membranes of eu- and glycohalophytes is only 2–3%, and it does not depend on the strategy of salt accumulation (Nesterov et al. 2017). In halophyte mitochondria, on the other hand – the organelles supplying the cell with energy – the content of sphingolipids reaches 11% of total membrane lipids (Rozentsvet et al. 2019). The relative content of sphingolipids in euhalophytes is three-fold of that in glycohalophytes. Thus, sphingolipids, along with other lipids, participate in the formation of the strategy of salt tolerance in plants.

4.5 Lipid Peroxidation

Unsaturated FA of polar lipids are the main targets for ROS generated under oxidative stress, which intensifies oxidative processes, including lipid peroxidation. When lipid peroxidation is stimulated, the lipid content decreases, and membrane parameters, such as microviscosity and electrostatic charge, change. Under severe oxidative stress, the structure of lipid bilayer is disturbed and defective zones appear in the cell membranes, this violating not only the barrier function of membranes but also the functional activity of membrane-bound proteins. Malonic dialdehyde (MDA) is one of the end products of lipid peroxidation, and its content is an integral characteristic of the ratio between anabolism and catabolism of biopolymers (Labudda 2013). The changes induced by ROS products in the cell can be considered as the basis for subsequent recovery processes. In plant cells, FA of both polar and neutral lipids undergo oxidative transformations.

The lipid/MDA ratios calculated for different types of membrane lipids (PL/MDA and GL/MDA) show that these lipids are equally susceptible to peroxidation. However, the values of PL/MDA and GL/MDA in euhalophytes and GL/MDA in crynohalophytes are 1.5–2 times higher than those in glycohalophytes. This indicates that glycohalophyte cell membranes experience greater oxidative stress under salinization (Fig. 6a and b). One can, therefore, conclude that cell membranes of eu- and crynohalophytes are more stable and less prone to oxidative processes.
Fig. 6

The lipid peroxidation in halophyte leaves, μmol/g fresh weight. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) the content of malonic dialdehyde (MDA), (b) the ratio phospholipids to MDA (PL/MDA), (c) the ratio glycolipids to MDA (GL/MDA)

Thus, reorganization and specificity of lipid composition in the halophytes of natural flora are essential factors in the formation of their salt tolerance strategy.

5 The Role of Lipids in the Organization of Photosynthetic Apparatus of Halophytes

The photosynthetic apparatus of plants is a complex multilevel system, which performs the functions of light absorption and conversion of the light energy into the energy of chemical bonds. The structure of photosynthetic apparatus reflects functional characteristics of plant species; it can differ in the parameters of leaf assimilation apparatus (Ivanova and Pyankov 2002), the number and size of chloroplasts in the photosynthetic cells, and the molecular organization of photosynthetic membranes (Ivanova 2014).

Leaf architectonics is defined by the number of cells per unit of leaf area, as well as their size and shape. These parameters optimize the leaf structure for the passage of light and diffusion of carbon dioxide from the intra-leaf space into the chloroplasts (Mokronosov and Gavrilenko 1992). The parameters of leaf architectonics are not purely anatomical; they characterize the surface area for CO2 exchange and the CO2 path from the intercellular space to the chloroplast stroma and are also associated with the conductivity of mesophyll.

Glycogalophyte plants showed the highest photosynthetic activity estimated by the average parameters of the CO2 gas exchange rate in the leaves of the studied species in the period 2012–2015 (Fig. 7).
Fig. 7

Gas exchange rate in halophyte leaves, μmol m−2 s−1. Box plot of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes

PA structural organization was assessed at the leaf and chloroplast levels by observing the number and volume of palisade and spongy tissue cells, and the number, and volume of the chloroplasts within the palisade and spongy parenchyma cells (Fig. 8).
Fig. 8

Quantitative characteristic of assimilating tissues in halophyte leaves. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) the number of palisade and sponge tissue cells (Ncell), pieces, (b) the number of chloroplasts in the palisade tissue (Nchl), pieces, (c) the volume cells (Vcell), 103 μm3, (d) the volume of chloroplasts (Vchl), μm3

The mesostructural analysis of leaves of Prieltonie halophytes, representing different ecological groups, shows that leaves of cryno- and glycohalophytes are characterized by a much larger number of cells, which are much smaller in volume (Fig. 8c). In general, the number of chlorenchyma cells per leaf area varies from 41 to 1060 thousand per cm2 (Fig. 8a). It is known that chloroplasts are mainly concentrated in cells of palisade tissue (Rozentsvet et al. 2018). The highest number of chloroplasts in the palisade cells of the investigated halophytes was found in euhalophytes (Fig. 8b), which is twice as high as the average values for this parameter in most plants (60–80 chloroplasts per cell) (Mokronosov and Gavrilenko 1992). In cryno- and glycohalophytes, the number of chloroplasts in the palisade tissue was lower than that in euhalophytes. In halophytes, the structure of chloroplasts was typical for plants; the plastids were a proper lenticular shape, and there was a well-developed thylakoid system and a fine-grained stroma. However, the chloroplast volume was 2–3 times higher in euhalophytes as compared with cryno- and glycohalophytes (Fig. 8d).

Photosynthetic pigments – chlorophylls (Chl) and carotenoids (Car) – are responsible for light absorption and photochemical reactions in chloroplasts. The content of Chl in the examined halophytes varies on the average from 2.5 to 4.0, and Car varies from 0.5 to 1.3 mg/g of dry weight (Fig. 9a and b). The Chl a/b ratio in these species is 2.4–2.6, and the Chl/Car – ~5.0. In the leaves of cryno- and glycohalophytes, the contents of both green and yellow pigments are, at least, twice as high as those in euhalophytes – despite the fact that the latter are characterized by larger chloroplasts. The amount of Chl is not related to the size of chloroplasts; the Chl a/b ratio, however, is inversely proportional to the volume and surface area of the organelles (r = −0. 97 at p < 0.05 for both parameters). The fraction of Chl in light-harvesting complexes (LHC) is lower in euhalophytes as compared to other halophyte groups. In other words, large chloroplasts are characterized by a lower Chl a/b ratio and LHC content, which indicates a different balance between photosystem (PS) I and II in different types of halophytes.
Fig. 9

The content of pigments in halophyte leaves. Box plots of 14 species grouped according to ecological group: Eh, euhalophytes; Ch, crynohalophytes; Gh, glycohalophytes; (a) total chlorophyll (Chl a + b), (b) carotenoids (Car)

Light reactions of photosynthesis are performed by pigment-peptide complexes, which are incorporated in the inner membranes of chloroplasts (Kobayashi et al. 2016). The chloroplast inner membranes are divided into two morphological domains: granal and stromal thylakoids – and these domains are characterized by a certain specificity of lipid and protein composition. PS II and its LHC are localized in the regions of close contact between thylakoids in grana, whereas PS I and a fraction of LHC and the coupling factor are concentrated in the agranal areas of thylakoids exposed to stroma. The cytochrome b6/f complex is spread all over the thylakoid membranes (Andersson and Anderson 1980; Deme et al. 2014). In these membranes, uncharged galactolipids (MGDG and DGDG) amount to 60–80% of total lipids (Kobayashi et al. 2016). The rest of lipids are represented by anionic species (SQDG and PG). It has been shown that a partial MGDG deficiency increases the ion conductivity of thylakoid membranes at high light intensities, which makes PS II more susceptible to photoinhibition and can reduce the efficiency of light absorption. DGDG promotes membrane stacking, owing to its ability to form hydrogen bonds between the polar heads of its molecules incorporated in the adjacent membrane layers (Yamamoto et al. 2014). A higher content of DGDG in the thylakoid membranes leads to a more compact packing of grana and stabilizes the structural organization of the PS II complex. SQDG is a lipid, which is unique for plants. Along with another anionic lipid, PG, it determines the surface charge of thylakoid membranes, affecting the functional activity of their protein membrane complexes (Nakamura and Li-Beisson 2016). PG is also necessary for the organization of photosynthetic reaction centers and antenna complexes (Wang and Benning 2012). Changes in the lipid composition of thylakoid membranes contribute to the development of adaptive processes in plants and other photosynthetic organisms.

As it turned out, the content of glycerolipids in the chloroplast membranes positively correlates with the size of the chloroplast and the content of photosynthetic pigments. In the examined halophytes, the total content of glycerolipids decreases in the same sequence as the number of chloroplasts in the cells of palisade and spongy parenchyma. Larger chloroplasts are characterized by a higher content of glycerolipids – especially DGDG, which is responsible for the granal packing of thylakoids, and MGDG, which is localized in the marginal thylakoid regions.

The proportion of unsaturated FA in the chloroplast lipids is more than 60%. There is a clear tendency in the changes of individual esterified unsaturated FA in chloroplasts depending of the plant halophilicity: eu- > cryno- > glycohalophytes. The more halophilic a plant is, the higher is the relative content of linolenic acid (C18:3n3), and the lower are the contents of linoleic (C18:2n6) and oleic (C18:1n9) acids. This confirms the data on the participation of desaturases in the specific organization of thylakoid membranes in different halophyte groups (Los and Murata 2004).

So, the greater efficiency of photosynthesis in euhalophytes is ensured by the large size of their cells and chloroplasts, a large number of chloroplasts per cell. A positive correlation between the contents of MGDG and DGDG on the one hand and the gas exchange rate on the other (r = 0.94 at p < 0.050) is also related to a greater photosynthesis efficiency.

6 Lipid Rafts in the Membranes of Chloroplasts and Mitochondria

For a long time, the lateral organization of biological membranes has been considered to be based on a uniform distribution of lipids and proteins responsible for the functions performed by cellular organelles. The studies of last decades, however, have shown the presence of discrete micro-domains in the biological membranes, which have a specific composition, structure, and functions (Nickels et al. 2017). Different terms are used to describe these domains: lipid or membrane rafts, detergent-resistant membrane areas (DRM), micro- or nanodomains, etc. Despite some variation in terminology and classification, it is generally accepted that these membrane areas are small (10–200 nm), heterogeneous, and highly dynamic – i.e., they can be defined as microdomains. Under certain conditions, microdomains can aggregate to form macrodomains.

Lipid rafts take part in such processes as intercellular interactions, endocytosis, intracellular signal transduction, lipid sorting, protein trafficking from the Golgi apparatus to the plasma membrane, regulation of ion channels, etc. (Simons and Sampaio 2011). Not all of their functions are known, yet the existing experimental data allow one to argue that microdomains regulate the biological activity of cellular and subcellular membranes and, hence, the activity of the cell as a whole (Cacas et al. 2012).

Initially, lipid rafts were discovered and thoroughly studied in the plasmalemma of animal and yeast cells. As for plant cells, their lipid rafts have been believed to include all the structural and signal lipids found in animal cells (Mongrand et al. 2010). In the plant cell, rafts were found in plasmalemma, vacuole membranes, and membranes of the Golgi apparatus (Laloi et al. 2007; Ozolina et al. 2013). In the euhalophyte S. perennans and glycohalophyte A. santonica, raft structures were also found in the membranes of chloroplasts and mitochondria (Nesterov et al. 2017; Rozentsvet et al. 2019). An observation supporting the existence of rafts in plant membranes is the appearance of an opalescence zone in the sucrose gradient after high-speed centrifugation of detergent-treated plant material. In the case of halophytes, such a zone was found in the region of 15% sucrose – and this is what distinguishes DRM isolated from the chloroplasts and mitochondria of halophytes from DRM of other plant objects. For example, when DRM were isolated from mitochondria by a similar technique, the opalescence band was in the zone of 16% sucrose; from plasmalemma, at 30% sucrose; and from tonoplast, at 25% sucrose (Ozolina et al. 2013). These differences are due to both the functional characteristics of the membranes and the properties of the species.

The packing density of DRM is believed to be higher than usual, due to their specific lipid composition in comparison with other membrane regions (Laloi et al. 2007). The specific lipid composition of DRM also depends on their origin: the membranes that DRM are isolated from. According to some authors, prevailing in lipid rafts are ST, sphingolipids (cerebrosides, Cer), and glycerolipids with saturated FA (Simons and Sampaio 2011). In halophytes S. perennans and A. santonica, the most abundant components of DRM (and of membranes not treated with a detergent as well) are GL: 46 and 53%, respectively (Fig. 10a and b). Their relative content in chloroplast DRM lipid extracts, though, is lowered from 60–70% to 20% as compared to total chloroplast lipids. The second most abundant components of chloroplast DRM are lipids responsible for the formation of rafts: ST and Cer, with the contribution of PL becoming less than 20% – whereas in total chloroplast lipids, the proportion of PL amounts to 25–30%. In plants with different strategies of salt tolerance, the lipid composition of chloroplast DRM differs substantially. The main raft-specific lipids of S. perennans are ST; in A. santonica, Cer are the most abundant ones.
Fig. 10

The content of raft-forming lipids in the membranes of chloroplasts: (a) S. perennans. (b) A. santonica; ML, membrane lipids

In the mitochondria, the differences between the composition of DRM lipids and that of total lipids turned out to be even greater in the studied halophytes. In contrast to chloroplasts, about 60% of mitochondrial lipids are PL; GL amount to less than a third of the total, and the rest of lipids (~13%) are Cer and ST. In mitochondrial DRM, more than 80% of lipids are raft-specific lipids (ST + Cer), followed by PL and then by GL. Similarly, the composition of mitochondrial DRM of human T cells was different from the composition of DRM isolated from plasmalemma: the former had a high content of gangliosides and ST and a relatively low content of PL (Garofalo et al. 2015). In both halophyte species examined in this work, the most abundant components of mitochondrial DRM are ST, amounting to ~70% of total. ST play an important structural role in DRM: they contribute to the tight packing of lipids in the liquid ordered domains by filling in the spaces between lipid molecules (Michaelson et al. 2016). The relative content of Cer is lower than the content of ST and varies depending on the species (23% in S. perennans and 11% in A. santonica). Some differences between the two species are also found in the PL composition of their mitochondrial DRM. In A. santonica, the predominant PL of mitochondrial DRM is PC; in S. perennans, it is DPG. The content of each of these components, however, does not exceed 5% of total membrane lipids (Rozentsvet et al. 2019).

A characteristic feature of DRM lipids is a relatively high degree of their saturation (Mongrand et al. 2010). In chloroplast and mitochondrial lipids, saturated FA amounts only to 35% – yet in lipids of chloroplast DRM, more than 50% of FA are saturated (Fig. 11a and b).
Fig. 11

The content of raft-forming lipids in the membranes of mitochondria: (a) S. perennans, (b) A. santonica, ML, membrane lipids

In DRM, the content of the main unsaturated FA (C18:3n3) is reduced to trace amounts (Rozentsvet et al. 2019). The relative content of С18:2 in the lipids of chloroplast and mitochondrial DRM is also low and does not exceed 7%. On the other hand, lipids of chloroplast and mitochondrial DRM have a high content of monoene FA: 30–35% of total FA. Monoene FA can be used as markers for chloroplast and mitochondrial DRM, since they are synthesized in plastids and then utilized both in FA biosynthesis and as oxidative substrates (Los and Murata 2004).

The concept of membrane rafts or DRM implies that lipids, along with proteins, are essential structural and functional components of membrane microdomains. Now it is generally accepted that dynamic lateral heterogeneity is crucial for membrane transport, namely, for concentrating transport proteins in certain regions of the membrane. Particular attention is given to DRM as platforms for signaling molecules.

In respect to membrane transport in halophytes, of special importance is the ability of their cells, chloroplasts, and vacuole to accumulate Na+ (Bassil et al. 2011). Na+ can enter the plant cell via ion channels (Shabala and Mackay 2011) or transporters (Khan 2011). Ion channels can selectively open or close for certain ions (K+, Na+, Ca2+, Cl) in response to hormonal, mechanical, and osmotic stimuli that affect membrane potential. In contrast to ion channels, the systems defined as Na+/H+ antiporters (NHX) transfer ions against their concentration gradients, utilizing the proton-motive force generated by H+-ATPase (Bassil et al. 2011). These energy-dependent systems, which include vacuolar transporters NHX1-4, plasma-membrane transporters (NHX7-8), and transporters that transfer Na+ into chloroplasts (NhaD), maintain low concentrations of Na+ in the cytoplasmic compartment (Bassil et al. 2011).

Other important H+-pump systems that increase salt tolerance of plants are vacuolar H+-ATPase and H+-pyrophosphatase. It has been shown that V-H+-ATPase is clustered in the rafts of vacuolar membranes, confirming the importance of rafts for the organization of transport processes (Ozolina et al. 2013).

It is quite possible that one of the functions of raft structures in halophytes is providing a platform for the structural organization of transport systems. It is clear, however, that DRM endomembranes can perform other functions as well: they can stabilize membranes and/or regulate sequestration of Na+ when the salt is accumulated in the plant cell. This supposition is confirmed by the fact that in the salt-accumulating S. perennans, the content of ST in the chloroplast DRM is about 23% of total membrane lipids, whereas in the salt-impermeable A. santonica, it is only 3%. However, the relative contents of total raft-specific lipids in S. perennans and A. santonica are 37 and 27% of total membrane lipids, respectively.

7 Conclusion

The chapter describes the specificity of lipid composition of halophytes growing in Prieltonie, one of the saline regions of the northern part of the Caspian lowland of Russia. In addition to salinization, the plants growing in this region experience the effects of intense insolation and high temperature – throughout most of their vegetative season. Soil salinization is one of the main factors affecting the growth and development of plants there, which determines the dominance of halophytes in the region. The differences in the contents of water and ions in the photosynthetic organs of halophytic plants correspond to the differences in their strategy of salt tolerance.

The halophyte groups (eu-, cryno-, and glycohalophytes) differ in their lipid composition: the contents of different groups and classes of lipids – as well as in the FA composition of their lipids. As the content of salts in the soil grows, the ratio of ST/PL in plant membranes increases, and other parameters (the ratios of MGDG/DGDG, PC/PE and PL/ST; the degree of FA unsaturation) change as well. The changes are aimed at maintaining the structure and orderliness of lipid bilayer, necessary to control the permeability and functional activity of cellular membranes. Therefore, adjustment of the lipid composition of plant membranes is an essential factor, contributing to the strategy of salt tolerance of the halophytes of natural flora.

The examination of meso- and ultrastructural parameters of halophyte leaves and the analysis of their correlation dependencies allow us to make the following conclusions. In halophytes, the rate of gas exchange is determined by such parameters as the cell volume, the number of chloroplasts, content and the ratio of pigments, as well as the contents of lipids in photosynthetic membranes.

The chloroplast and mitochondrial membranes of halophytes contain detergent-resistant regions (DRM) enriched in ST, Cer, and saturated lipids. The differences in the lipid composition of DRM are associated with the specifics of salt metabolism of the studied plant species and indicate involvement of DRM in the adaptation of plants to the abiotic environmental factors.

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Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Olga A. Rozentsvet
    • 1
  • Viktor N. Nesterov
    • 1
  • Elena S. Bogdanova
    • 1
  1. 1.Samara Federal Research Scientific Center RAS, Institute of Ecology of Volga River Basin RASTogliattiRussia

Section editors and affiliations

  • Oscar Vicente
    • 1
  1. 1.Instituto de Conservación y Mejora de la Agrodiversidad Valenciana (COMAV)Universitat Politècnica de ValènciaValenciaSpain

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