Plant Central Metabolism to Abiotic Stress: Comparison
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Please note this is a comparison between Version 2 by Jessie Wu and Version 1 by Yuan Xu.

Plants are constantly exposed to a plethora of stresses under natural conditions. Stress in plants can be described as anything that can cause a change from ideal growth and developmental conditions. Stresses can be classified as abiotic or biotic, where abiotic stresses are caused by nonliving factors in the surrounding environment, such as extremes in temperature, drought, flooding, and high salinity. Abiotic stresses are unavoidable to plants due to their inability to move. 

  • abiotic stresses
  • drought
  • plant
  • heat
  • salinity
  • cold
  • flooding
  • metabolism

3.1. Flooding Stress

1. Flooding Stress

The major damage to plants from soil flooding is oxygen deprivation, which negatively affects mitochondrial respiration [14][1]. When the oxidative phosphorylation of the mitochondrial respiration is impaired under anaerobic conditions, respiratory adenosine triphosphate (ATP) production drops substantially [60][2]. To cope with the energy crisis, plants increase the glycolytic flux to produce more ATP via a faster depletion of sugar reservoirs [14][1]. In such stress conditions, plants must generate sufficient ATP to maintain cellular functions and regenerate oxidized NAD+ to maintain the glycolytic flux. Pyruvate accumulated from glycolysis can be channeled through fermentation pathways to restore the pool of NAD+ required for glycolysis [60][2].
Ethanol fermentation and lactate fermentation are the two fermentation pathways in plants that use pyruvate as the substrate. In ethanol fermentation, pyruvate is decarboxylated to acetaldehyde via pyruvate decarboxylase (PDC) and then reduced to ethanol via alcohol dehydrogenase (ADH) with concomitant oxidation of NADH to NAD+ [61][3]. Due to the substantially lower energy yield of ethanol fermentation (2 mol ATP per mol glucose consumed), as compared to mitochondrial respiration (36–38 mol ATP per mol glucose consumed), ethanol fermentation must proceed at higher rates to meet the energy demand of cellular functions [62][4]. Accumulation of the volatile and phytotoxic ethanol and acetaldehyde has been measured in various tree and grass species exposed to flooding [63,64,65][5][6][7]. In flooding tolerant trees, a large amount of ethanol produced from ethanol fermentation in flooded roots could be transported to leaves via the transpiration stream, where it is sequentially oxidized to acetaldehyde and acetate via ADH and aldehyde dehydrogenase in leaves [65,66][7][8]. Acetate is converted into acetyl-CoA via acetate-activating enzymes and re-enters central metabolism, which recovers carbon that would otherwise be lost as ethanol in hypoxic tissues [67][9]. In lactate fermentation, pyruvate is reduced to lactate by lactate dehydrogenase with concomitant oxidation of NADH [68][10]. Because lactate is a weak acid, its accumulation could cause cellular acidification, potentially leading to the inactivation of enzymes and cell damage [69][11].
In addition to the adjustment in carbon metabolism via ethanol and lactate fermentation, oxygen deprivation also greatly affects nitrogen metabolism in plant cells [70][12]. Alanine is one of the most dramatically accumulated amino acids upon oxygen deficiency [71][13]. The major route for anaerobic accumulation of alanine is via alanine aminotransferase (AlaAT), which favors the conversion of pyruvate and glutamate to alanine and 2-oxoglutarate under hypoxia [72][14]. How do plants regenerate glutamate as the substrate for AlaAT under hypoxia? The reductive amination of 2-oxoglutarate via the NADH-dependent glutamate synthase (NADH-GOGAT) may be responsible for the newly synthesized glutamate under hypoxia [73][15]. The increased NADH-GOGAT activity also regenerates NAD+ needed for maintaining the glycolytic flux upon oxygen deficiency [70][12]. Another route for anaerobic accumulation of alanine is via a process known as γ-aminobutyric acid (GABA) shunt, where glutamate-derived GABA is converted to succinic semialdehyde, concomitantly converting pyruvate to alanine [74][16]. The accumulation of alanine and GABA has been proposed as an adaptive mechanism under hypoxia to safeguard the carbon that would be otherwise lost during ethanol fermentation and save the ATP that would be used otherwise for assimilating glutamine and asparagine via ATP-consuming enzymes [74][16]. Changes in many other amino acids, such as aspartate, glutamate, and tyrosine, have been observed in several species under flooding stress [75,76,77,78,79][17][18][19][20][21]. In addition, photorespiratory intermediates, such as serine, glycine, glycolate, and glycerate, increased in roots of Medicago truncatula under waterlogging, suggesting a higher photorespiration rate, probably due to the lower stomatal conductance [76][18].
The TCA cycle operates in noncyclic mode upon oxygen deficiency [73][15]. Anaerobic accumulation of alanine is accompanied by the production of 2-oxoglutarate, which can enter mitochondria to form succinate via 2-oxoglutarate dehydrogenase and succinate CoA ligase, generating additional ATP to alleviate the energy shortage due to the oxygen limitation. The mitochondrial NAD+ required to oxidize 2-oxoglutarate is generated by reducing oxaloacetate to malate via malate dehydrogenase [75][17]. Because the TCA cycle enzyme succinate dehydrogenase (SDH) requires oxygen, the accumulation of succinate is typical during hypoxia conditions induced by flooding [73][15]. Changes in other TCA cycle intermediates, such as citrate, malate, and fumarate, have occurred in several species under flooding stress [75,76,77,78,79][17][18][19][20][21].

3.2. Drought Stress

2. Drought Stress

The low water availability in drought-stressed plants limits photosynthesis and restricts plant growth and development [80][22]. The decline in net CO2 assimilation under a water limitation is due to the decreased CO2 diffusion from the atmosphere to the sites of carboxylation within chloroplasts, which is caused by stomatal closure and probably also the increased mesophyll diffusional resistance [80][22]. The diffusional resistances of CO2 under water deficits are thought to restrict photosynthesis more directly than the metabolic limitations under water stress [81][23]. As photosynthesis is the major sink for photosynthetic electrons, water-stressed leaves with decreased photosynthesis are subjected to excess energy, leading to ROS formation that can impair ATP synthesis [82,83][24][25]. There is evidence that the activity of ribulose-1,5-bisphosphate carboxylase-oxygenase (Rubisco) decreases under water stress [84][26], which could be related to decreased ATP and Rubisco activase activity [82][24]. As CO2 availability is decreased, photorespiratory flux relatively increases in leaves of C3 plants under water deficit, contributing to electron sinks and resulting in high rates of H2O2 production [85][27]. The imbalance between the supply and demand of ATP or NADPH may be the main factor driving the metabolic pool-size changes induced by drought stress [86,87][28][29].
Osmotic adjustment, the accumulation of solutes, is one of the main strategies plants use to maintain positive turgor pressure in water-limited environments [88][30]. The osmolytes that are accumulated following drought stress are chemically diverse, including soluble sugars (e.g., glucose, fructose, sucrose, and trehalose); the raffinose family oligosaccharides (RFOs, e.g., raffinose, galactinol, and myo-inositol); amino acids (e.g., proline and GABA); quaternary ammonium compounds (e.g., glycine betaine); and polyamines (e.g., putrescine and spermidine) [27,89][31][32]. Many of these osmolytes are also involved in other abiotic stresses, such as salinity, cold, and flooding [90][33]. Soluble sugars are not only important for osmoregulation and the balance between the supply and utilization of carbon and energy in water-stressed plants; they also function as signaling molecules governing many changes in physiology and development [91][34]. Multiple time-course experiments revealed that sugars, such as RFOs, glucose, and fructose, generally accumulate earlier and more rapidly than many other metabolites in response to drought stress [92,93][35][36].
The accumulation of amino acids, such as proline and GABA, occurs later than sugars in response to drought [89,93][32][36]. Increased pools of amino acids require more nitrogen assimilation, which is inhibited when ATP is limited in the stressed plants. An alternative source of ammonium would be via glutamate dehydrogenase (GDH), which reversibly catalyzes the formation of glutamate by the amination of 2-oxoglutarate produced from the TCA cycle [94][37]. The GDH may become important for ammonium assimilation when plants are ATP-limited under drought stress, evidenced by the increased GDH activity in drought-stressed plants with the concomitant rise in proline levels [95][38]. The increase in branched-chain amino acids (BCAAs), such as leucine, isoleucine, and valine, is commonly observed in many plant species under drought stress [96,97][39][40]. The accumulation of BCAAs is probably associated with the high demand for the catabolism of BCAAs to fuel the alternative pathways of mitochondrial respiration during drought stress [97][40].

3.3. Cold Stress

3. Cold Stress

Cold stress impairs plant development, reduces plant growth and development, and causes crop economic loss. Cold stress can lead to various plant symptoms, including poor germination, stunted seedlings, yellowing of leaves, reduced leaf expansion and wilting, and severe membrane damage caused by acute dehydration associated with the formation of ice crystals [18][41]. The molecular basis and regulatory mechanisms for plant cold stress responses have been widely studied, including Ca2+ fluxes, inositol phosphates, mitogen activated protein (MAP)-kinase-mediated cascades, Ca-dependent protein kinases, and many transcription factors. Inducer of CBF Expression-1 (ICE1) and the C-repeat-binding factors (CBFs) are best-characterized transcripts that control an important regulon of target genes that include many of the downstream core genes [98,99][42][43]. About 10–15% of all the cold-regulated genes are activated by transcriptional activators C-repeat-binding factors/dehydration responsive element-binding factors (CBF1/DREB1b, CBF2/DREB1c, CBF3/DREB1a) [100,101][44][45].
Cold stress regulates GABA shunt and the accumulation of proline, raffinose, and galactinol [102,103][46][47]. Cold stress-induced transcripts for genes encoding enzymes involved in the induction of callose, fermentation, phospholipid, starch, sugar, flavonoid, protein amino acids, GABA, and terpenoid biosynthesis, and the repression of photorespiration, folic acid, betaine, sulfate assimilation, ethylene, fatty acid, gluconeogenesis, amino acids, brassinosteroids, and chlorophyll biosynthesis [102][46]. Metabolomic responses to cold stress have been widely studied in Arabidopsis thaliana traditionally and have recently expanded to crop, grass, and medicinal plants [104,105,106][48][49][50]. Cold stress was found to cause more changes to metabolite levels than heat stress [102,103][46][47]. Cold stress leads to an increase in a diverse range of metabolites, including proline, GABA, soluble sugars (e.g., glucose, fructose, inositol, galactinol, raffinose, sucrose, and trehalose), ascorbate, putrescine, citrulline, TCA-cycle intermediates, polyamines, and lipids [103,107,108,109,110,111][47][51][52][53][54][55]. Plants under cold stress showed an increase in the proportion of unsaturated fatty acids to stabilize the membranes and maintain membrane fluidity against freeze injury [102,103,112,113,114][46][47][56][57][58].

3.4. Heat Stress

4. Heat Stress

Heat stress can disrupt plant physiology by reducing membrane stability and inhibiting respiration and photosynthesis [115,116][59][60]. Heat and cold stresses shared many common responses, including the induction of osmolytes that function to reduce cellular dehydration, compatible solutes that are important to stabilize enzymes and membranes, chelating agents that can neutralize metals and inorganic ions, and energy sources [102,109,117][46][53][61].
Plants under heat shock and prolonged warming showed different responses. In response to heat shock, plants produce heat-shock proteins (HSPs) that function as molecular chaperons to defend against heat stress [118][62]. The heat-shock response is regulated by the transcription factor HSFs family. Part of heat-shock-affected genes was controlled by two major HSF genes, HsfA1a and HsfA1b [119][63]. HSFA1a/1b regulated genes encoding enzymes involved in signaling, transport processes, and the biosynthesis of osmolytes.
Several metabolomics studies have revealed the impacts of heat shock on plant central metabolism, including amino acids, organic acids, amines, and carbohydrates. Amino acids derived from oxaloacetate and pyruvate (asparagine, leucine, isoleucine, threonine, alanine, and valine), oxaloacetate precursors (fumarate and malate), amine-containing metabolites (β-alanine and GABA), and carbohydrates (maltose, sucrose, trehalose, galactinol, myo-inositol, raffinose, and monosaccharide cell-wall precursors) were reported to increase in response to heat shock [3,58,103,120][47][64][65][66]. The increase in free-amino acids during heat stress was associated with the breakdown of proteins [58,120][65][66]. The increase in the TCA-cycle intermediates under heat stress suggests that higher amounts of Coenzyme A may be important for increased biosynthetic and energy needs [103][47]. The induction of the raffinose biosynthesis pathway and accumulation of galactinol and raffinose during heat shock were mediated by galactinol synthase-1 (GolS1) controlled by HSFs [119][63]. In contrast to the short-term heat shock, plants exposed to prolonged warming enhance the glycolysis pathway but inhibit the TCA cycle [121][67]. Wheat (Triticum aestivum), under prolonged warming, showed an increase in tryptophan [122][68]. Cytokinins (CKs), fatty acid metabolism, flavonoid, terpenoid biosynthesis, and secondary metabolite biosynthesis were identified as the most important pathways involved in prolonged warming response [122][68].

3.5. Salinity Stress

5. Salinity Stress

Salinity stress negatively impacts plants’ water and nutrients uptake, growth and development, photosynthesis, and protein biosynthesis [123][69]. Salinity stress may induce both osmotic and ion stresses [124][70]. A previous study showed that the high-voltage electrical discharge treatment could improve the germination and early growth of wheat in drought and salinity conditions [125][71]. The main difference between osmotic adjustment induced by salinity and drought stresses is the total amount of water available. In addition to low water potential, the concentration of harmful ions, such as Na+, Cl−, or SO42−, increased associated with salinity stress, causing specific ion toxicity effects [126][72]. NaCl is the most abundant salt in plants under salinity stress. A high concentration of Na+ and/or Cl− in cells inhibits photosynthesis [127][73]. The transport systems, such as K+–Na+ transporter (HKT1), Na+–H+ antiporter SOS1 (salt overly sensitive 1) AtNHX1, and calcium-regulated transporters SOS2/SOS3, are important in regulating Na+ compartmentation during salinity stress [128,129,130,131,132][74][75][76][77][78].
Metabolomics has been extensively used to characterize the salinity responses of various plant species. Central metabolites, including sugars, polyols, and amino acids, play important roles in osmotic adjustment, cell turgor pressure maintenance, signaling molecules, carbon storage, and free-radical scavenging [17][79]. A variety of plants under salt stress were reported to accumulate osmolytes as soluble sugars (sucrose, trehalose, and raffinose) and sugar alcohols (sorbitol, galactinol, and mannitol) [133,134,135,136,137,138][80][81][82][83][84][85]. Amino acids, such as proline, can also function as osmolytes to protect plants under salt stress in many varieties [38,139,140,141][86][87][88][89]. For example, Tibetan wild barley (Hordeum spontaneum) and cultivated barley (H. vulgare) under salt stress were reported with changes in amino acids, including proline, alanine, aspartate, glutamate, threonine, and valine, with genotype-dependent manners [142][90]. Eight amino acids and amines, including 4-hydroxy-proline, asparagine, alanine, arginine, phenylalanine, citrulline, glutamine, and proline, were reported to be significantly increased in multiple barley varieties under salt stress [138][85]. Both Thellungiella halophila and Arabidopsis thaliana under salinity stresses showed an increase in proline and sugars. Triticum durum Desf. Exposed to salinity stress showed an accumulation in proline, GABA, threonine, leucine, glutamic acid, glycine, mannose, and fructose, and the depletion of organic acids, including TCA-cycle intermediates [143][91]. Rice (Oryza sativa) pretreated with chemical priming reagent hydrogen sulfide (H2S) showed better growth and development under salt stress with elevated levels of ascorbic acid, glutathione, redox states, and the enhanced activities of ROS- and methylglyoxal-detoxifying enzymes [17][79].
The biomarkers for salt-tolerant varieties vary between species. Three halophytes, Sesuvium portulacastrum, Spartina maritima, and Salicornia brachiate, were compared under salinity stress [144][92]. Proline increased in Sesuvium portulacastrum and Spartina maritima, while glycine betaine and polyols increased in Spartina maritima and Salicornia brachiate [144][92]. Salinity-resistant Lotus japonicus seedlings showed an increase in threonine, serine, ononitol, glucuronic acids, and gulonic acids, and decreased asparagine and glutamine [145][93]. Salt-tolerant cultivar barley (Hordeum vulgare) showed increased proline, carbohydrates, hexose phosphates, and TCA-cycle intermediates [142,146][90][94]. Salt-tolerant rice (Oryza sativa) showed increased concentrations of amino acids, serotonin, and gentisic acid, and decreased concentrations of TCA intermediates [147][95]. Salinity-resistant transgenic tobacco (Nicotiana) plants showed an increase in proline, glutathione, and trehalose, and a decrease in fructose [148][96]. Omeprazole-treated tomato (Solanum lycopersicum) with improved salinity tolerance showed increased polyamine conjugates, alkaloids, sesquiterpene lactones, and abscisic acid, and a decrease in auxins and cytokinin, and gibberellic acid [149][97]. Sugar-beet (Beta vulgaris subsp. vulgaris) seedlings under salinity stress showed an increase in malic acid and 2-oxoglutaric acid in the short-term treatment and an increase in betaine and melatonin in the long-term treatment [150][98]. Hulless barley (Hordeum distichon) under salinity stress showed increased tryptophan, glutamic acid, phenylalanine, cinnamic acid, inosine 5-monophosphate, and abscisic acid [151][99].

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