Lipidomics in Plants Under Abiotic Stress Conditions: An Overview

Abstract

Lipids are ubiquitous macromolecules that play essential roles in several metabolic processes in plants, such as primary and secondary metabolism, energy storage, and lipid signaling, also being major constituents of membranes. Considering their importance, lipid contents, proportion, and composition are widely modulated in response to environmental conditions, which is even more important under unfavorable conditions such as abiotic stresses. In recent years, technological advances have allowed for the analysis of the global lipid profile, also known as lipidomics, which has emerged as a powerful tool for the comprehensive analysis of the modulation and roles of lipids under different conditions. This review provides a current overview of plant lipidomics research, covering the different lipid classes found in plants, analytical techniques, and the main lipid-related responses under temperature, water, salt, alkali, heavy metal, nutrient deficiency, light, and oxidative stress.

1. Introduction

Cell membranes, including plasma and endomembranes, are the structures allowing for the compartmentalization that creates life. Membranes are composed of a variety of lipids that differ in their head group and fatty acid composition [1]. Membrane remodeling comprises the changes in the unsaturation degree and the proportion of different lipid classes, which alter membrane fluidity and permeability, and vesicle formation [2,3]. Among these lipids, the three main classes are glycerolipids, sphingolipids, and sterols [2].

Glycerolipids are the most abundant class of lipids, comprising phospholipids (PLs), galactolipids (GLs), triacylglycerols (TAGs), and sulfolipids (SLs) [4]. PLs, such as phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylserine (PS), and phosphatidylinositol (PI), are the main components of biological membranes [5,6]. They consist of a glycerol backbone connecting two hydrophobic fatty acid chains with a hydrophilic phosphate head group, which can also contain choline, ethanolamine, serine, or inositol [2,6]. Due to their amphipathic nature, phospholipids play an essential role in maintaining the structure and function of cell membranes and organelles [7,8]. On the other hand, GLs, such as monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), are the major components of thylakoid membranes [2,9]. MGDG and DGDG are also crucial for the assembly and function of the photosynthetic machinery [8,10]. Sphingolipids, in turn, comprise glycosyl inositolphosphoceramides (GIPCs), glucosylceramides (GCers), ceramides (Cers), and free long-chain bases (LCBs) [11]. This group of lipids contains a sphingosine backbone instead of a glycerol backbone and composes about 10% of total plant lipids [12,13]. Sphingolipids are components of the plasma membrane and endomembrane system, being crucial to the maintenance of membrane integrity [13,14]. The third group of membrane lipids are sterols, isoprenoid derivatives that are plant membrane components and precursors of hormones such as brassinosteroids [15,16]. The most abundant sterols in plants are β-sitosterol, campesterol, and stigmasterol [15]. Sterols are involved in maintaining membrane fluidity and permeability, cellular polarity, and they also play a role in signaling and stress response pathways [17].

Triacylglycerols (TAGs) are lipids composed of three fatty acids esterified to glycerol and are involved in energy storage, being the major component of vegetable oils [18,19]. Due to their high energy storage capacity, oils are widely used for food, feed, biodiesel, and industrial chemicals. In plants, TAGs are synthesized in the endoplasmic reticulum of most plant tissues, being stored in specialized organelles called lipid droplets (LDs) [20]; however, the major storage sites of TAGs in plants are seeds and fruits [21]. Under carbon and energy deficit conditions, TAGs are hydrolyzed into fatty acids and other metabolites to generate ATP and carbon skeletons by peroxisomal β-oxidation [20]. The breakdown of TAGs occurs primarily by lipases, also being reported to occur during autophagy in response to stresses [22]. Therefore, in addition to developmental processes such as seed germination, seedling establishment, stomatal opening, and flower development, TAGs are also important in stress responses [19,23,24]. For instance, TAG biosynthesis under stress conditions represents a strategy to store cytotoxic lipid intermediates generated by membrane lipid remodeling, such as free fatty acids, diacylglycerol (DAG), and other hydrolytic byproducts, which can lead to lipotoxicity [19,25]. In addition, LDs are required for the adequate function of LD-associated proteins such as caleosins, proteins involved in stress sensing and signaling, which are also involved in the biosynthesis of oxylipins [26]. As a result, biotic and abiotic stresses are often related to the increase in TAGs [19].

Autophagy is a catabolic pathway that degrades and recycles cellular components, also participating in developmental processes, stress responses, and programmed cell death [22,27]. Studies have reported that organellar autophagy is essential for lipid homeostasis, functioning in the lipid turnover via TAG synthesis [28]. Moreover, under carbon starvation conditions, LDs are degraded via lipophagy into fatty acids to produce energy through β-oxidation [28,29].

In addition to the barriers imposed by membranes, lipids can also create physical barriers on the epidermis surface. For instance, cutin and suberin are mainly composed of fatty acid (FA) derivatives, epoxyacids, polyhydroxyacids, and saturated very long-chain FAs, being major barriers of the plant epidermal surface and root endodermis [30,31,32]. Lipids are also involved in plant–microbe interactions, modulating the signaling, perception, or defenses with either beneficial or phytopathogenic microorganisms, functioning like chemical barriers against infection [33,34]. These signals can be emitted from plants to microbes, microbes to plants, or microbes to microbes and include rhizodeposits of FAs, sterols, lipopolysaccharides, peptidoglycans, flagellin, and chitin [33]. Several lipid classes, such as fatty acids, phospholipids, lysophospholipids, phosphatidic acid, DAGs, inositol phosphate, oxylipins, sphingolipids, and N–acylethanolamine, are also known to participate in plant stress signaling by inducing the transcription of defense-related genes and by functioning in membrane perception and trafficking processes [3,35,36,37].

Plants are exposed to a wide range of environmental stresses, including drought, heat, cold, salt, and herbivore and pathogen attacks. These stresses can significantly affect plant growth, development, and productivity, as well as their lipid regulation, synthesis, degradation, relocalization, or restructuring [38,39]. For instance, stress through high or low temperatures directly impacts membrane fluidity by altering the interactions and composition of membrane lipids [40], while biotic stresses can induce the production of defense lipids such as oils and waxes [41]. Moreover, biotic and abiotic stresses commonly lead to oxidative stress due to the overproduction of unstable free radicals, such as reactive oxygen species (ROS), reactive nitrogen species, reactive carbonyl species, and reactive sulfur species [42,43]. The excess of these free radicals causes oxidative damage to biomolecules such as lipids, altering membrane permeability and stability, disrupting electron transport chains, and finally leading to cell death processes, including autophagy [44]. In this context, lipidomics has emerged as a powerful tool to investigate and comprehend the lipid metabolism, including the consequences of stresses and, thus, providing information on how to overcome the negative effects of these stresses. Although many specific studies on lipidomics in plants have been conducted, a comprehensive overview of plant lipidomics, particularly concerning abiotic stress responses, has not been extensively reported on in the literature. To better understand the potential of lipidomics in the study of plant stress responses, we begin with an overview of the current status of lipidomics research. We then provide a brief review of the main lipid classes and the biological processes affected by lipid composition. Finally, we discuss the effects of different stressors on these lipid-related responses.

2. Overview of Current Research on Plant Lipidomics

Lipids are a diverse group of biomolecules that play important roles in a variety of biological processes, and recent advances in analytical techniques have led to the emergence of lipidomics [45,46]. This technique provides insights into the complex biological processes underlying plant growth, development, and adaptation to stresses [41,47]. Considering that abiotic and biotic stresses are major limiting factors in agriculture, the use of lipidomics is an essential tool in studying the role of lipids in plant stress responses.

Searches on the Scopus and PubMed databases indicate a growing number of publications containing the term “plant lipidomics” in their title, abstract, or keywords (Figure 1a). From the 773 publications about “plant lipidomics” found on the Scopus database, 388 were related to the subject area “biochemistry, genetics and molecular biology”, 351 were related to “agricultural and biological sciences”, and 181 were related to “chemistry” (Figure 1c). When limiting the search to “plant stress lipidomics”, 390 publications were found in the Scopus database, with 123 publications on “biochemistry, genetics, and molecular biology” and 122 publications on “agricultural and biological sciences” (Figure 1b,d). China was the country with the highest number of publications about “plant lipidomics” (304) and “plant stress lipidomics” (98), followed by the United States and Germany (Figure 1e,f). These numbers highlight the growing potential of lipidomics in the study of plant stress biology.

Up to now, the majority of publications on lipidomics and plant stresses have focused on abiotic stresses, with temperature (heat and cold stress) being the most studied environmental factor (

Table 1. An overview of the main lipidomic studies approaching plant abiotic stress responses.

Stress Condition	Plant Species	Tissue	Analytical Technique	Reference
Alkali	Maize	Roots	ESI-MS/MS	Xu et al. [55]
	Sunflower	Seeds	LC-MS	Lu et al. [56]
Cold	Arabidopsis thaliana	Leaves	LC-MS	Tarazona et al. [57]
	Arabidopsis thaliana	Leaves	GC-MS	Chen et al. [58]
	Banana	Fruits	LC-MS	Liu et al. [59]
	Barley	Leaves	LC-MS	Zhao et al. [60]
	Bell pepper	Fruits	ESI-MS/MS	Kong et al. [61]
	Bell pepper	Fruits	LC-MS	Xu et al. [62]
	Blueberry	Fruits	GC-MS	Wang et al. [63]
	Cabbage	Leaves	LC-MS	Zainal et al. [64]
	Cotton	Seeds	LC-MS	Dhaliwal et al. [65]
	Dendrobium	Leaves	UPLC-QTOF-MS	Zhan et al. [66]
	Maize	Roots	ESI-MS/MS	Zhao et al. [67]
	Maize	Leaves	LC-MS/MS	Gao et al. [68]
	Meconopsis racemosa	Leaves	ESI-MS/MS	Zheng et al. [69]
	Moss species	Leaves	UPLC-QTOF-MS	Lu et al. [70]
	Panax notoginseng	Leaves	ESI-MS/MS	Liu et al. [71]
	Peach	Fruits	GC-MS	Zhu et al. [72]
	Peach	Fruits	ESI-MS/MS	Chen et al. [14]
	Wheat	Leaves	LC-QqQ-MS	Cheong et al. [73]
	Wild tomato	Leaves	UPLC-QTOF-MS	Zhang et al. [74]
Drought	Arabidopsis thaliana	Leaves	LC-MS/MS	Tarazona et al. [57]
	Argan tree	Leaves	GC-MS	Rabeh et al. [75]
	Barley	Roots	LC-MS	Sarabia et al. [76]
	Camellia sinensis	Leaves	GC-MS and LC-MS	Shen et al. [77]
	Cotton	Seeds	LC-MS/MS	Liu et al. [78]
	Italian ryegrass × tall fescue	Leaves	UPLC-MS	Perlikowski et al. [79]
	Maize	Leaves	LC-MS	Kränzlein et al. [80]
	Sorghum	Leaf cuticle	GC-MS	Zhang et al. [49]
	Thyme	Leaves	DIFT-ICR-MS	Moradi et al. [81]
Waterlogging	Arabidopsis thaliana	Leaves	ESI-MS/MS	Wang et al. [82]
	Boehmeria nivea	Leaves	UPLC-QTOF/MS	Shao et al. [83]
	Rice	Grains	LC-MS	Xu et al. [84]
	Rice	Leaves	LC-MS	Basu et al. [85]
	Wheat	Leaves	ESI-MS/MS	Xu et al. [86]
Heat	Arabidopsis thaliana	Leaves	LC-MS	Higashi et al. [87]
	Arabidopsis thaliana	Leaves	LC-MS	Higashi et al. [88]
	Arabidopsis thaliana	Leaves	LC-MS	Shiva et al. [89]
	Arabidopsis thaliana	Leaves	LC-MS	Korte et al. [90]
	Arabidopsis thaliana	Seeds and seedlings	ESI/MS	Qian et al. [91]
	Begonia	Leaves	LC-MS	Sun et al. [92]
	Castor bean	Leaves	UPLC-QTOF/MS	Zhang et al. [93]
	Panax notoginseng	Leaves	ESI-MS/MS	Liu et al. [71]
	Peanut	Anthers	ESI-MS/MS	Lwe et al. [94]
	Soybean	Leaves	ESI-MS/MS	Narayanan et al. [48]
	Tall fescue	Leaves	ESI-MS/MS	Zhang et al. [95]
	Tall fescue	Leaves	ESI-MS/MS	Zhang et al. [54]
	Wheat	Leaves	LC-MS/MS	Hu et al. [96]
Heavy metals	Halimione portulacoides	Leaves, stems, and roots	LC-MS	Figueira et al. [97]
	Soybean	Leaves	LC-MS	Andresen et al. [98]
	Wheat	Roots	ESI-MS/MS	Wu et al. [99]
Light	Arabidopsis thaliana	Leaves	HPLC	Rastogi et al. [100]
	Arabidopsis thaliana	Leaves	UPLC-MS	Burgos et al. [101]
	Cotton	Leaves and roots	GC-MS	Kargiotidou et al. [102]
	Moss	Leaves	LC-MS	Callahan et al. [103]
	Tea plants	Leaves	UPLC-TOF-MS	Wang et al. [104]
	Tomato	Leaves	UHPLC-APCI-QTOF-MS	Spicher et al. [105]
Nutrient deficiency	Arabidopsis thaliana	Leaves	LC-MS	Okazaki et al. [106]
	Ettlia oleoabundans	Cells	LC–QTOF-MS	Matich et al. [107]
	Halimione portulacoides	Leaves	LC-MS	Custódio et al. [108]
	Haptophytes	Cells	HPLC–HRAM–MS	Lowenstein et al. [109]
	Lobosphaera incisa	Cells	LC-MS	Kokabi et al. [110]
	Rapeseed	Leaves	LC-MS/MS	Peng et al., 2023 [111]
	Rice	Leaves and roots	UPLC-QTOF-MS	Honda et al. [112]
	Soybean	Leaves and roots	ESI-MS/MS	Narasimhan et al. [113]
	Tea plant	Leaves	UPLC-MS	Liu et al. [114]
	Tomato	Leaves and roots	GC-MS	Pfaff et al. [115]
	Wheat	Leaves	GC-MS	Li et al. [116]
Salt	Barley	Roots	HPLC-ESI-QTOF-MS	Natera et al. [117]
	Barley	Roots	HPLC-ESI-QTOF-MS	Ho et al. [118]
	Barley	Roots	HPLC-ESI-QTOF-MS	Yu et al. [119]
	Carex rigescens	Leaves	ESI-MS/MS	Hu et al. [51]
	Cotton	Seeds	LC-MS/MS	Liu et al. [78]
	Cotton	Roots	LC-MS	Liu et al. [120]
	Kentucky bluegrass	Leaves	ESI-MS/MS	Zhang et al. [121]
	Mesembryanthemum crystallinum	Leaves	HPLC–ESI–MS/MS	Guo et al. [122]
	Sweet Potato	Leaves	UPLC-QTOF/MS	Yu et al. [123]
	Tomato	Leaves	UHPLC/QTOF-MS	Buffagni et al. [52]

). Most of these studies describe the overall changes in the lipid profile, linking them either to membrane- or signaling-related responses. The lipid profiles of genotypes with varying stress tolerance are often used to identify the underlying mechanism involved in stress responses [48,49,50]. Similarly, the lipidomics of plants treated with stress mitigators are also used to investigate those responses [51,52,53,54].

Mass spectrometry (MS), liquid chromatography (LC), and gas chromatography (GC) are the most commonly used techniques in plant lipidomics (Table 1). In addition, multiomic and integrated approaches, such as the combination of lipidomics, transcriptomics, and metabolomics, allow researchers to draw more comprehensive conclusions about the observed responses [52,53,77,124]. By combining these diverse datasets, multiomic analyses can reveal how stress conditions affect gene expression (genomics and transcriptomics), protein abundance and activity (proteomics), and metabolic profiles (metabolomics and lipidomics) simultaneously. This integrative approach allows for the identification of key regulatory networks, novel biomarkers, and stress-responsive pathways that might be overlooked when studying each omics layer in isolation.

3. Abiotic Stress Responses

In addition to their direct detrimental effects on plants, abiotic stresses also lead to secondary oxidative stress, with the overproduction of unstable molecules that oxidize unsaturated fatty acids, reducing membrane stability and increasing its fluidity and permeability [40]. As a result, plants change the levels of several PLs such as PC and PE to maintain membrane stability [3,40,125,126]. Considering the ubiquitous presence of oxidative stress during plant exposition to other stresses, its effects will be further discussed along with each stress.

3.1. Temperature Stress

In addition to oxidative stress, abiotic stresses also induce specific effects on plant membranes. For instance, heat stress induces the hyper-fluidity of membranes, protein denaturation, organelle swelling, and the separation of bilayer-forming lipids, dismantling membranes and producing cytotoxic carbonyl groups [40]. In response to these negative effects, plants adjust their membrane lipid composition by increasing the total phosphatidylglycerol, phosphatidylinositol, and saturated phosphatidylcholine and phosphatidylethanolamine [125]. Moreover, studies reported increases in galactolipids (linoleate), phospholipids (palmitate, stearate, and oleate), and triacylglycerols (α-linolenate and hexadecatrienoic acid) in chloroplasts, the endoplasmic reticulum, and the plasma membrane [40]. This increase in saturated and monounsaturated fatty acids (16:0, 18:0, and 18:1) results in higher membrane stiffness, counteracting the effects of heat stress, while the polyunsaturation of fatty acids is often related to lower heat tolerance [125]. In addition to membrane remodeling, lipids are essential for triggering signaling pathways and providing energy during stress responses. For instance, the catabolism of fatty acids is required for efficient stomatal opening during heat stress in Arabidopsis [90]. Regarding stress signaling, heat stress induces the accumulation of phosphatidylinositol through the activation of phosphatidylinositol phosphate kinase (PIPK), also inducing the accumulation of Ca²⁺, which activates calmodulin-binding kinases that, in turn, induce the expression of heat shock proteins [127].

Unlike heat stress, cold stress reduces membrane fluidity, and thus, tolerance responses comprise the increase in the contents of unsaturated lipids in relation to saturated lipids, increasing the fluidity of cell and plastid membranes [58,65,67,127]. Under cold stress, the influx of Ca²⁺ induces the accumulation of the signaling lipid phosphatidic acid, while increased MGDG is pointed to function in the synthesis of jasmonate, a phytohormone involved in cold stress tolerance [128]. In maize, cold stress tolerance is dependent on lipid remodeling by the modulation of the levels of several lipids, such as mono- and di-unsaturated lysophosphatidic acid, lysophosphatidylcholine, PC, and phosphatidylinositol, as well as polyunsaturated phosphatidic acid, MGDG, DAG, and TAG [68]. In cold-stressed maize roots, the major lipid classes are PC, phosphatidylethanolamine, phosphatidic acid, and phosphatidylinositol [67]. In barley, high levels of phosphatidic acid, lysophosphatidic acid, and MGDG are also reported to induce cold tolerance [60]. The cold-tolerant wild tomato Solanum habrochaites also shows higher contents of MGDG, DGDG, and phosphoinositide compared to cold-sensitive S. lycopersicum species, also showing the increased β-oxidation of fatty acids in mitochondria to produce energy under stress conditions [74]. Bryophytes living under low temperatures survive by producing very long-chain polyunsaturated fatty acids, accumulating phospholipids and glycolipids, and decreasing storage lipids [70]. Low temperatures are often used to increase the post-harvest life of several fruits; however, they can also cause chilling injuries and lipid remodeling [63]. In peach fruits, cold stress tolerance is associated with increased phosphatidylcholine and phosphatidylethanolamine (and DAGs and TAGS) and reduced phosphatidic acid accumulation, which reduces chilling injuries [129]. Blueberry, in turn, undergoes pitting during cold storage, which is followed by increases in DGDG, phosphatidic acid, phosphatidylserine, phosphatidylglycerol, phosphatidylinositol, lysophosphatidylcholine, and lysophosphatidylethanolamine and decreases in phosphatidylcholine [63].

3.2. Water Stress

Drought stress occurs when the water supply is below the plant requirements; it is a major stress impacting crop yield worldwide, mainly considering global climate changes [130,131]. The primary effect of drought in plants is cell dehydration, which triggers stomatal closure, oxidative stress, membrane and protein structure destabilization, and photosynthesis inhibition, ultimately leading to cell damage and death [131,132]. As a result, phospholipids such as phosphatidylcholine, phosphatidylethanolamine, and phosphatidylglycerol are the first to be degraded, dismantling membranes [127]. The production of signaling lipids, as well as lipid byproducts, is increased under drought, while essential oil production can be increased or decreased depending on the species [35,133,134,135]. The membrane’s peroxidation results in the increase in malondialdehyde, which is an important stress indicator [49,50]. Thus, to better resist drought, plants can modulate the synthesis and composition of several lipid classes. For instance, the increase in the cuticle deposition of cutin and waxes, as well as the composition of cuticle-associated very long-chain lipids, may seal the leaf surface, reducing transpiration, being an important tolerance response to drought stress [49,136]. For example, drought-tolerant wheat plants were found to increase the content of cutin, alkanoic acids, and 2-hydroxyacids while decreasing aldehydes, which was not observed in drought-sensitive plants [49]. The alkane pathway comprises the synthesis of aldehydes, secondary alcohols, and ketones, while the primary alcohol pathway results in the production of esters and primary alcohols present in waxes [137].

Membrane stability under drought, in turn, is increased through the synthesis of linolenic acid and the reduction in MGDG and fatty acid desaturation [75]. Photosynthetic capacity and membrane fluidity under drought are associated with higher total contents of DGDG and MGDG, and the DGDG/MGDG ratio, as they are the main components of photosynthetic membranes [50,79,127]. Other lipids modulated under drought stress include phosphatidylglycerol, phosphatidic acid, sulfoquinovosyldiacylglycerol, phosphatidylcholine, lyso-phosphatidylcholine, and phosphatidylinositol, pointing mainly to their function in membrane fluidity and lipid signaling [77]. Lipid signaling through phosphatidic acid, phosphatidyl serine, phosphatidyl glycerol, and phosphatidyl choline may also involve their interaction with dehydrins, which improve drought tolerance by increasing water retention capacity, chlorophyll content, antioxidant defense, and osmoregulation [138]. Moreover, these lipids, as well as sphingolipids and oxylipins, are known to interact with abscisic acid and nitric oxide, regulating stomatal closure [127,135]. In the opposite way, abscisic acid is also known to induce fatty acid biosynthesis [134]. In drought-tolerant thyme plants, the level of signaling lipids increases, while the level of oxylipins, which are induced by ROS, dramatically decreases [81]. The fact that the exogenous application of phosphatidylcholine increases drought tolerance in peach trees, increasing membrane stability, osmoprotection, and photosynthetic capacity, further supports the importance of these lipids under drought conditions [139].

Waterlogging or submergence stress is caused by the excess of water in the root zone in land plants, which leads to poor soil aeration and oxygen depletion to roots (hypoxia or anoxia), reducing aerobic respiration and energy production, inducing anaerobic fermentation, and ultimately impairing plant growth, development, and yield [140,141]. This stress induces the accumulation of ROS, leading to membrane peroxidation and electrolyte leakage, also reducing photosynthetic capacity due to damages to chloroplast membranes [85]. Hypoxia is reported to reduce the global contents of lipids, inhibiting their biosynthesis and inducing degradation, which culminates in free fatty acid accumulation [140]. Tolerance against waterlogging stress has been associated with lipid remodeling, with the changes being species- and stress duration-dependent. In ramie (Boehmeria nivea), for example, lipid droplet formation is increased in the inter-chloroplast cytoplasm, while fatty acid and 18:3 (n3) Coenzyme A (C18:3-CoA) contents are gradually increased [83]. Similarly, the unsaturation of very long-chain ceramides and acyl-CoAs is reported to reduce damages caused by hypoxia by interacting with ethylene pathways, while the modulation of wax deposition is also related to waterlogging adaptation [140,141,142]. Signaling lipids, such as phosphatidic acid, have been reported to increase under hypoxia [140]. In turn, lipids such as oxylipin jasmonate are important modulators of plant responses to reoxygenation, improving antioxidant capacity [141].

3.3. Salt and Alkali Stress

Salt stress is characterized as the accumulation of ions on the root zone, mostly sodium and chloride, which reduces the osmotic potential, impairing the uptake of water and nutrients [143,144,145]. Moreover, salt stress causes the overaccumulation of sodium on cells, disrupting electrochemical gradients and causing protein denaturation [146]. Alkali stress, also called saline–alkali stress, occurs when neutral or alkali salts accumulate in soils, increasing pH and causing chemical destruction, osmotic stress, ion toxicity, and nutrient and oxygen deficiency [147,148].

Membrane integrity and permeability are essential for the modulation of sodium uptake and compartmentalization [149]. Salt stress induces lipolysis and lipid peroxidation and reduces lipid biosynthesis, reducing total membrane lipid contents in salt-sensitive species; however, salt-tolerant species increase lipid homeostasis, also increasing total lipid content [150,151]. Salt stress also increases the saturation of fatty acids in sensitive species, resulting in more rigid membranes; however, halophytes show a high proportion of unsaturated fatty acids, maintaining membrane fluidity [151]. In addition, salt-tolerant species increase the contents and proportion of specific lipid groups, such as phospholipids [126]. For instance, the content of phosphatidylcholine, phosphatidylethanolamine, phosphatidylinositol, and phosphatidylserine are increased in these species, with high phosphatidylcholine-to-phosphatidylethanolamine (PC/PE) ratios also being related to increased salt tolerance [126,150,152,153]. The accumulation of glycerophosphocholine has shown osmolyte properties, also being a substrate for PC synthesis in barley roots [76]. Moreover, the increase in PLs is also observed in the membrane of vacuoles, highlighting the role of these lipids in increasing membrane stability [122]. Increases in phosphatidylinositol and phosphatidylserine were also observed under salt stress, being implicated in signaling responses through Ca²⁺ that trigger Na⁺ efflux [122,123,154,155]. In chloroplast membranes, the increase in phosphatidylglycerol is related to higher membrane stability, maintaining the function of light-harvesting complexes and photosystem II [156,157].

The decrease in glycolipid content, such as MGDG and DGDG, is related to the negative effects of salinity in sensitive species [158], while its increase is related to the higher stability of the photosynthetic apparatus [152]. The proportion between these two glycolipids is essential to confer tolerance against salt stress, as the increase in the DGDG/MGDG ratio stabilizes the membrane by increasing the ratio of bilayer-forming to non-bilayer-forming, while salinity often reduces the DGDG/MGDG ratio in sensitive plants [156,159,160]. The breakdown of DGDG and MGDG during salt stress generates polyunsaturated fatty acids that are involved in jasmonate biosynthesis, increasing the levels of this hormone [159]. Sulfoquinovosyl diacylglycerol (SQDG) is another glycolipid associated with the lipid–protein interactions of the photosynthetic apparatus, whose increase is often related to salt tolerance [161]. Sphingolipids, such as PhytoSph, PhytoCer, PhytoCer-OHFA, Phyto-GluCer, and phosphatidyl ceramide, are also reported to alter the tolerance against salt stress in Arabidopsis, with their proportion to other lipid groups being essential for tolerance [120].

Similar to the other lipid groups, increased sterol contents are related to higher salt tolerance, while the proportion between sterol groups in response to salinity varies according to the tissue [162]. Moreover, the proportion between sterols and phospholipids is often increased in salt-tolerant species, resulting in lower membrane permeability to Na⁺ and Cl⁻ [163]. LD accumulation is also known to improve recovery after salt stress, probably by providing fatty acids used in membrane reconstruction [164].

In addition to salinity, alkali stress is also known to induce deep lipid remodeling. In sunflower, for example, alkali stress increases the contents of saccharolipids and glycerolipids and reduces the contents of glycerophospholipids in sunflower seeds, also affecting seed oil quality [56]. Maize roots also show extensive lipid remodeling under alkali stress, with reductions in the contents of phosphatidylcholine and inductions in the synthesis of phospholipids and galactolipids in plastids and the production of C34:6 galactolipids, pointing to the induction of the prokaryotic pathway [55]. The modulation of root exudates is also an important defense response against alkali stress. In wheat, alkali stress was reported to increase glycolysis, fatty acid synthesis, and phenolic acid synthesis [165]. In the halophyte Leymus chinensis, the accumulation and secretion of organic acids, amino acids, and fatty acids are involved in alkali tolerance [166].

3.4. Heavy Metals

Heavy metal stress induces significant changes in plant metabolism as a means of coping with stress or even eliminating heavy metals. One of the primary changes observed is lipid peroxidation, which can compromise the integrity of the plasma membrane [167,168]. Additionally, heavy metal stress can lead to both qualitative and quantitative changes in membrane lipids, altering the membrane’s permeability and function [169]. For instance, the presence of mercury (Hg) in the environment alters the lipid pattern in the leaves of the saltmarsh halophyte Halimione portulacoides. This alteration affects the level of unsaturation, fluidity, and stability of the membrane, which in turn influences the plant’s tolerance to Hg [97].

Cadmium (Cd) is another heavy metal that significantly impacts the composition of lipophilic compounds in both leaves and roots. Changes in lipid composition under sublethal Cd toxicity likely serve as adjustment mechanisms to maintain membrane fluidity [98]. In wheat roots, Cd stress results in decreased concentrations of several key lipids, including digalactosyldiacylglycerol, monogalactosyldiacylglycerol, phosphatidylcholine, phosphatidylethanolamine, phosphatidylglycerol, phosphatidylserine, and lysophosphatidylcholine. Additionally, the concentrations of specific glycerolipids such as C36:4, C34:2, C34:3, and C36:6 are also reduced under Cd stress [99].

3.5. Nutrient Deficiency

When the availability of any of the 14 essential mineral nutrients is below the plant requirements, it is called nutritional deficiency, which results in reduced growth, production, and even death [170]. As these nutrients have unique functions in plants, the effects of their deficiencies will vary according to the nutrient, its levels, source, and plant species [170,171]. For instance, nitrogen is a major component of proteins and macromolecules, such as RuBisCo and chlorophylls, and thus, its deficiency affects overall plant metabolism, also harming photosynthetic machinery and capacity [171,172]. Phosphorus, in turn, is involved in energy metabolism, nucleic acids, and phospholipids, the main components of membranes, while potassium is an important osmolyte regulating cell turgor and stomatal opening [172,173].

Nitrogen depletion is related to decreases in total lipid contents, while higher tolerance is associated with higher fatty acid unsaturation and chloroplast membrane stability [113,116]. Moreover, nitrogen deficiency is related to lower contents of phosphatidylglycerol and glucuronosyl diacylglycerol, as well as a lower MGDG/DGDG ratio [111]. In oleaginous microalga species, nitrogen and phosphorus starvation differentially affect the production and composition of storage lipids, with nutrient deficiency resulting in a higher production of triacylglycerols enriched in important commercial biochemicals, such as the long-chain polyunsaturated fatty acid arachidonic acid [107,110]. Similarly, the accumulation of triacylglycerols is also affected by nitrogen depletion in tea plants [114]. In soybean, nitrogen deficiency mainly affects the content of galactolipids, compared to phospholipids, with nodulated roots accumulating more phospholipids and showing a higher MGDG/DGDG ratio [113].

Phosphorus deficiency causes extensive membrane lipid remodeling, including the change of phospholipids to non-phospholipids, with the ability to maintain the content of phospholipids being an important tolerance response [112,174]. As a consequence of lower phospholipid contents, plants increase the contents of membrane galactolipids, also increasing triacylglycerol contents in leaves and roots [115]. In Arabidopsis and rice, in addition to membrane remodeling, the presence of glucuronosyldiacylglycerol is related to higher tolerance to phosphorus depletion [106].

3.6. Light

Light quantity, quality, and photoperiod are shown to affect lipid dynamics and composition in plants [175,176]. High irradiances induce higher photosynthetic rates and consequently, a greater accumulation of lipids. Additionally, there are changes in lipid composition under high light conditions [175]. Blue light, in particular, stimulates lipid biosynthesis in plants. This has been demonstrated in tea plants, where high levels of blue light (200 μmol m^–2 s^–1) upregulated 15 genes involved in lipid synthesis [104]. Blue light increases lipid biosynthesis by inducing the flux of fatty acid biosynthesis, the Calvin cycle, and the Krebs cycle [177]. In contrast, Arabidopsis thaliana plants grown under amber light (595 nm) also show a greater accumulation of lipids, likely linked to oxidative stress. The most pronounced increases were in tocopherols, which play a crucial role in eliminating singlet oxygen [100,175]. Tocopherols are also responsible for initiating stress responses caused by high light irradiance in tomatoes [105].

Increased solar radiation can lead to higher levels of fatty acids stored in seeds and alter their composition, resulting in a greater proportion of C18:1 fatty acids and lower amounts of C18:2 fatty acids [102,175]. Analyzing the response of membrane lipid composition in plants under different light intensities reveals that light significantly affects lipid levels. Darkness induces a decrease in glycerolipids, whereas high light conditions lead to an increase in these lipids [101].

4. Concluding Remarks

Great variation in the lipidomic results was observed among species and abiotic stresses, with most conclusions pointing to membrane remodeling and lipid signaling. Few studies, however, report on the mechanisms involved in energy metabolism and lipid catabolism and anabolism. Also, studies about crosstalk among abiotic stressors or that relate the role of lipids and plant hormones in the response to abiotic stressors are missing. In this context, most efforts in plant lipidomics have been directed towards exploratory changes in the contents, proportions, and compositions of lipids. However, deeper conclusions can be drawn by using integrative approaches, which allow for a comprehensive analysis not only of lipid composition but also of the underlying mechanisms involved in the responses. Another promising field is the identification of new lipids with abiotic stress mitigation functions. This could enable the development of new products and tolerant genotypes, as well as the manipulation of environmental conditions to produce specific lipids with commercial appeal. Moreover, as a currently evolving field, omics approaches, including lipidomics, have great potential to help researchers elucidate plant responses to abiotic stresses, which is paramount under the current climate change scenario.