Composition of Plant Membrane Lipids
Plant membranes predominantly consist of lipids, including phospholipids, glycolipids, and sterols such as cholesterol (CHO). The fatty acid composition is mainly characterized by 16 and 18 carbon chains with three double bonds. Different organelle membranes have specific lipid compositions. For example, mitochondrial membranes are rich in glycerophospholipids, particularly phosphatidylcholine (PC), phosphatidylethanolamine (PE), and phosphatidylinositol (PI), along with free sterols (FS) and sphingolipids. The lipid composition varies between the inner and outer layers of the plasma membrane, influencing membrane fluidity and permeability.
Biological Functions of Plant Membrane Lipids
- Membrane Structure and Fluidity: Even minor changes in lipid composition can significantly affect membrane properties, impacting membrane protein function and cell permeability.
- Stress Response: Lipid remodeling is a crucial strategy for plants to maintain growth and development under adverse environmental conditions. Lipids play roles in signaling pathways related to stress response.
- Photosynthesis: Certain glycolipids, such as monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), are essential for photosynthesis efficiency and chloroplast structure.
- Cell Division and Growth: Sterols, including cholesterol, brassicasterol (BR), and sitosterol, regulate cell division and growth. Abnormal sterol composition can lead to fertility issues and embryonic lethality.
- Signal Transduction: Lipids like phosphatidic acid (PA) and phosphatidylinositol phosphates (PIPs) are involved in signaling pathways that mediate cellular processes and stress responses.
Composition and Major Biological Functions of Extracellular Lipids
Extracellular lipids in plants encompass substances such as cutin and suberin, typically located on the plant surface, regulating and maintaining the normal structure of leaves and defending cells. They play vital roles in preventing water loss, protecting against pathogen invasion, preventing organ adhesion, and supporting pollen development processes. The composition of the cuticle mainly comprises cuticular wax and cutin, along with terpenes and flavonoids, found in various plant tissues such as leaves, seeds, and fruits. The synthesis of cuticle components is influenced by factors like water availability, salt concentration, and the plant hormone abscisic acid (ABA). The primary function of the cuticle is to act as a barrier against microbial pathogens and pests, regulate water loss while facilitating gas exchange. Increasing evidence suggests that the cuticle plays a crucial role in plant defense against pathogens, with studies showing enhanced immunity against pathogens like Pseudomonas syringae and Botrytis cinerea upon treatment with ABA. Alterations in the cuticle structure can lead to abnormal stomatal behavior, resulting in water loss and susceptibility to pathogen infection. Additionally, changes in temperature can affect cuticle strength. Under abiotic stress, such as heat and drought, the cuticle adapts by enhancing permeability. Cuticular wax has been proven to play a significant role in resisting various environmental stressors such as light, water, and temperature stresses.
Suberin, also known as cork, consists of monomers of C22 or longer chain fatty acids and their oxidized derivatives. It is localized in the cell walls near the plasma membrane, primarily found in plant tissues like seed coats, tubers, and root periderm. Suberin enhances the structural density of plant epidermis, preventing water loss and maintaining the integrity of seed coats and root epidermis. Its absence leads to increased permeability of seed coats, resulting in reduced germination rates and growth inhibition under salt stress conditions. For instance, in response to harmful concentrations of NaCl, the accumulation of suberin in castor bean roots significantly increases. Studies in maize have demonstrated the unique role of suberin in forming extracellular transport barriers. Under stress conditions such as salt and hypoxia, suberin deposition is significantly increased. Additionally, ABA not only correlates with wax synthesis but also serves as a hormone signal mediating suberin regulation in stress responses. Therefore, suberin accumulation serves as one of the stress responses in plant tissues.
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Signaling of Plant Lipids in Growth and Development and Stress Response
Lipid signaling plays a critical role in plant growth, development, and stress responses, encompassing a diverse array of lipid signaling molecules such as phosphatidic acid (PA), phosphoinositides, lysophospholipids, sphingolipids, and free fatty acids (FFAs). These signaling molecules are rapidly activated under abiotic stress conditions, undergoing strict regulation to trigger signaling cascades that significantly influence plant development and stress adaptation mechanisms.
- Phosphatidic Acid (PA): PA is implicated in responses to osmotic stress caused by dehydration and salinity, extreme temperature stresses, ABA signaling transduction, and pathogen attacks. For instance, PA promotes stomatal closure by binding to and inhibiting the protein phosphatase ABI1, a negative regulator in ABA response, highlighting its role in abiotic stress response and signaling.
- Phosphoinositides: Among these, inositol trisphosphate (IP3) is one of the most abundant in plant cells, participating in both developmental processes and stress responses. IP3 mediates cellular responses by controlling Ca2+ levels, such as releasing Ca2+ in the cytosol of guard cells to facilitate stomatal closure. Additionally, inositol hexaphosphate (IP6) plays a role in mobilizing calcium in the ABA signaling pathway, further illustrating the importance of phosphoinositides in plant stress responses.
- Lysophospholipids: As minor membrane components and signaling mediators, lysophospholipids like lysophosphatidic acid and sphingosine-1-phosphate (S1P) partake in various biological reactions. They accumulate in response to cold damage or pathogen infection and have been shown to participate in phytochrome signaling pathways, underscoring their versatility in plant stress and developmental signaling.
- Sphingolipids: The synthesis of sphingolipids, a conserved mechanism across eukaryotes, involves the production of long-chain bases (LCBs) in the endoplasmic reticulum, further modified into ceramides (Cer). Sphingolipids and their metabolites are involved in numerous cellular processes and environmental responses. They play roles in plant defense-related programmed cell death (PCD), with various LCBs and Cer contributing to or inhibiting PCD, illustrating the complex regulatory functions of sphingolipids in plant stress responses.
In addition to the signaling lipids mentioned, ongoing research continues to explore the importance of other lipids like oxidized fatty acids (OFAs), N-acylethanolamines (NAEs), and fatty amides in plant-fungal interactions, signaling between animals and plants, and in mediating plant growth and pathogen defense mechanisms. This research underscores the complex and crucial roles that lipids play in plant biology, offering potential pathways for enhancing plant resilience to stress and improving crop productivity.
Changes in Lipids in the Study of Plant Growth and Development
Lipid metabolism plays a crucial role in various developmental processes in plants, including embryo development, sex determination, flowering and fruiting, induction of haploid and callus tissues, cytoplasmic male sterility, and secondary metabolism. Fatty acids and their derivatives are key components of the anther cuticle and pollen wall. Disruptions in lipid metabolism can therefore impact these structures, leading to cytoplasmic male sterility, which is characterized by abnormalities in the cell membranes of the anther and pollen wall during their development.
In studies comparing the anthers of male-sterile and fertile maize, significant differences were observed in the levels of glycerolipids, glycerophospholipids, and sphingomyelins. In the sterile variants, a substantial downregulation was noted in lipids such as LPA, PC, LPC, PS, PI, along with reductions in PG, DG, PA, PE, MGDG, and DGDG. Conversely, an upregulation was seen in ceramides and triglycerides. The ratio of PC to PE, which influences membrane fluidity and the formation of non-bilayer phases, was found to be lower in sterile plants, indicating altered membrane dynamics. PS, a lipid involved in cell death signaling and lipid metabolism, was also significantly reduced, highlighting the role of PC and PS in pollen sterility. These findings suggest that lipid metabolic blockages might be one of the causes of male sterility in maize.
Furthermore, the biosynthesis of Paclitaxel, a compound linked with apoptosis in Taxus wallichiana var. mairei, has been shown to correlate with changes in cell membrane and membrane phospholipids. Comparative lipidomics between different varieties of Taxus species revealed significant alterations in membrane phospholipids during apoptosis, with increases in PA and lyso-phosphatidylcholine and a decrease in PC. The increase in PA, a product of phospholipase D activity, suggests its activation as a key mediator of apoptosis.
Lipid Changes in Response to Non-Biological Stressors in Plants
Lipid changes play a crucial role in the response of plants to various abiotic stresses such as temperature and water deficits, which are key factors influencing plant growth. When exposed to different stress conditions, plants experience metabolic imbalances, leading to symptoms like wilting or cell death. To maintain normal physiological functions, plants activate their intrinsic defense mechanisms, which involve alterations in lipid, protein, or other molecular contents.
In studies focusing on plant responses to cold stress, it has been repeatedly shown that cold perception is closely linked to lipid content. High levels of phospholipids (PL) correlate positively with cold tolerance, with phosphatidylglycerol (PG) being a major factor. Additionally, the levels of monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG) dynamically change. It is inferred that membrane damage caused by cold stress may result from the accumulation of reactive oxygen species (ROS), leading to decreased photosynthetic rates and lipid peroxidation. Cold stress symptoms include dehydration and wilting, accelerating senescence. Changes in the levels of major unsaturated fatty acids in membrane lipids typically determine membrane fluidity. Under dehydrated conditions, plants increase the degree of unsaturation (DU) of membrane lipids to mitigate negative effects. Unsaturated fatty acids are vital for normal growth under low-temperature conditions. For instance, in Arabidopsis, a decrease in 18:2 fatty acids can lead to plant death, while high levels of trienoic fatty acids (16:3 and 18:3) in chloroplasts maintain photosynthesis. The unsaturation of PG in chloroplasts is a key factor in plant cold tolerance. Studies have also reported increases in polyunsaturated acyl groups and polyunsaturated lysophosphatidylcholines (LPCs) under cold stress.
Under high-temperature conditions, lipid peroxidation and ROS accumulation can impair photosynthetic rates. Unlike cold stress, high-temperature stress typically leads to a decrease in lipid unsaturation, with increases in phosphatidic acid (PA) and inositol trisphosphate (IP3) concentrations. This change is influenced by fatty acid desaturases and affects cellular compartments such as the chloroplast stroma and thylakoid membranes, as well as other organelles like vacuoles and mitochondria. Tomato lipidomics analysis under high-temperature stress revealed significant reductions in highly unsaturated MGDG and DGDG. Wheat leaf lipid levels decreased universally under high-temperature stress, leading to decreased levels of polyunsaturated lipids and increased levels of saturated lipids.
High-temperature stress often accompanies drought stress. Under water deficit conditions, plants undergo significant morphological changes, such as leaf wilting and shedding, accompanied by changes in lipid composition. These changes include a decrease in total lipid content, the formation of PA, phosphatidylinositol (PI), sphingolipids, and oxidized fatty acids, along with decreases in phosphatidylethanolamine (PE), phosphatidylserine (PS), phosphatidylcholine (PC), and PG. MGDG and DGDG levels decrease significantly, while ceramide (Cers) concentrations decrease and sterol levels increase. The most notable feature is the decrease in lipid unsaturation. PA is involved in stomatal regulation, and IP3 and IP6 affect stomatal closure, indicating a close relationship between drought stress response and ABA and lipid signaling pathways. For example, birch seedlings under drought stress exhibit accumulation of reactive oxygen species (ROS). Drought-tolerant plants accumulate polyunsaturated fatty acids and antioxidants to inhibit fatty acid oxidation. Changes in lipids have been reported in passion fruit, wheat, and Arabidopsis under drought stress, while lipid composition in sorghum grown in drought conditions showed decreases in DGDG, MGDG, PG, PE, and significant increases in PA levels.
Under salt stress conditions, plants respond by limiting membrane absorption of Na+ and Cl-, preventing leakage of compatible solutes like glycerol and diffusion of harmful ions. Salt-tolerant plants reduce unsaturation to prevent gel phase formation and reduce oxidative damage. Lipid changes include increases in PA, PI, PS, and oxidized fatty acids, along with an increase in unsaturation levels. Changes in lipid composition indicate partial degradation of chloroplast membranes. Accumulation of PA leads to loss of cell vitality and activates the mitogen-activated protein kinase (MAPK) cascade, coupling with the activity of the Na+ channel transporter protein SOS1, resulting in membrane phosphorylation. Salt-tolerant plant types also accumulate diphosphatidylglycerol (DPG), which plays a crucial regulatory role in stabilizing mitochondrial membrane integrity. Studies comparing lipid composition in salt-tolerant and salt-sensitive roots and leaves of yam and barley showed significant decreases in PI and PG levels in leaves, with a more pronounced decrease in salt tolerance. Meanwhile, TG levels increased, with more significant accumulation in salt-sensitive varieties. PC and PE levels significantly decreased in salt-sensitive rice varieties, while the salt-tolerant varieties remained unaffected. This was accompanied by symptoms of leaf wilting, reduced chlorophyll levels, increased membrane permeability, and accumulation of peroxidation and ROS.
Lipid changes have also been reported under other stress conditions such as phosphorus deficiency and heavy metal stress. Phosphorus deficiency affects normal growth in plants and leads to changes in lipid composition, with decreases in glycerophospholipids (GPL) and increases in glyceroglycolipids (GGL). Similar phenomena have been observed in rice seedlings and soybeans. DGDG levels decrease under drought, low temperature, and other stress conditions but increase significantly under phosphorus deficiency, suggesting a special role for DGDG in plants responding to phosphorus deficiency. Phosphorus-deficient Arabidopsis cells maintain mitochondrial membrane integrity by replacing phospholipids with DGDG. Under low phosphorus conditions, maize leaf tissues transport PA and diacylglycerol (DAG) synthesized in the endoplasmic reticulum to chloroplasts as substrates for sugar lipid synthesis to ensure membrane lipid stability. In rice roots exposed to arsenic, lipidomics analysis showed increases in DG, MGDG, DGDG, and PA, while PC, PG, and PS concentrations decreased. Under cadmium stress, pepper seedlings show decreased levels of PC, MGDG, and DGDG in roots, while leaves exhibit accumulation of different phospholipids (PC, PG, PE) and decreased levels of MGDG and polyunsaturated fatty acids (linolenic acid, hexadecatrienoic acid), leading to decreased unsaturation.
Given that aluminum toxicity is associated with the unsaturation of long-chain bases (LCB), aluminum-tolerant rice varieties exhibit increased fatty acid unsaturation under aluminum stress, while sensitive varieties show decreased PL, such as PC, and changes in SL levels.
These findings illustrate the intricate role of lipid metabolism in plant responses to various abiotic stresses, providing insights into potential strategies for enhancing plant stress tolerance and productivity.
Lipid Changes in Plant Biotic Stress Response Studies
In response to biotic stress, plants undergo changes in lipid composition. For instance, there is an increase in glyceroglycolipids (GGL) and phosphatidylethanolamine (PE). Additionally, lipids play specific roles in biotic stress responses. Ergosterol (ERG) can recognize pathogens, while free fatty acids (FFAs), phosphatidylglycerol (PG), ceramides (Cer), and sphingosine-1-phosphate (S1P) mediate signal transduction in infected cells, activating the jasmonic acid (JA) signaling pathway and programmed cell death (PCD) pathways. Pathogen-induced accumulation of nitric oxide and reactive oxygen species promotes the production of azelaic acid (AzA), which acts as a signal for infection and transmits it to distant plant organs, providing salicylic acid (SA)-dependent defense. Phospholipases and ω-hydroxy fatty acids are involved in the regulation of plant-microbe interactions.
The behavior of microorganisms such as bacteria, fungi, and protists affects the root system of plants, leading to either symbiotic relationships promoting plant growth or causing death. This phenomenon is attributed to root exudates, including fatty acids, jasmonic acid (JA), and its derivatives, which act in defense against pathogens. Highly hydroxylated sphingolipids can enhance membrane stability and reduce membrane permeability during pathogen-induced PCD, thus increasing tolerance to fungal pathogens. Application of sphingolipids can protect tomato leaf cells from fungal toxins. Phosphatidic acid (PA) induces reactive oxygen species (ROS) production and activates the PCD pathway in plant defense against pathogens. Phosphoinositols and monogalactosyldiacylglycerols (MGDG) also play roles in defense against pathogens.
Abiotic stresses signal integration and adaptive responses in plants (Paes et al., 2022)
Unsaturated Fatty Acid Derivatives in Stress Response
Unsaturated fatty acid (UFA) derivatives play crucial roles in plant development, stress defense, and interactions with microorganisms. Their synthesis is regulated by compounds like abscisic acid, auxin, and jasmonic acid. UFA derivatives are integral to plant defense systems against stressors, including oxidative stress and microbial interactions. For example, jasmonic acid (JA) inhibits the growth of roots, shoots, and leaves, regulates plant-microbe interactions, and modulates the production of alkaloids, terpenoids, and phenolic secondary metabolites. It also influences hydrogen peroxide production and clearance and regulates the activity of antioxidant enzymes. JA induces senescence in barley and enhances soybean drought tolerance. Its derivative, 12-oxo-phytodienoic acid (OPDA), acts synergistically with JA, activating genes beyond those activated by JA alone.
Furthermore, compounds like hexenal and hexanal, along with their alcohol counterparts, are volatile and can initiate repair in injured tissues, reducing plant susceptibility to diseases and insect infestations. For instance, 12-oxo-dodecenoic acid promotes cell division and growth in injured tissues, participates in tissue healing, and inhibits bacterial proliferation. Additionally, epoxy fatty acids and hydroxylated fatty acids serve as endogenous signaling molecules and precursors for cutin and suberin molecules, reinforcing cell walls and protecting plant tissues from external damage. They induce the expression of defense-related proteins in barley and protect plant tissues from oxidative stress and cell death.
Moreover, fatty acid derivatives like divinyl ethers may have phytoalexin functions and are speculated to be associated with cell death. They are involved in the production of antimicrobial compounds by enzymes like divinyl ether synthase and peroxygenase. Studies have shown their accumulation in potato plants resistant to late blight and in tobacco plants infected with Tobacco mosaic virus.
Reference
- Paes de Melo, Bruno, et al. "Abiotic stresses in plants and their markers: a practice view of plant stress responses and programmed cell death mechanisms." Plants 11.9 (2022): 1100.
