Role Of Proline Research Articles

Genetic engineering of drought- and salt-tolerant tomato via Δ1-pyrroline-5-carboxylate reductase S-nitrosylation.

Drought and soil salinization substantially impact agriculture. While proline's role in enhancing stress tolerance is known, the exact molecular mechanism by which plants process stress signals and control proline synthesis under stress is still not fully understood. In tomato (Solanum lycopersicum L.), drought and salt stress stimulate nitric oxide (NO) production, which boosts proline synthesis by activating Δ1-pyrroline-5-carboxylate synthetase (SlP5CS) and Δ1-pyrroline-5-carboxylate reductase (SlP5CR) genes and the P5CR enzyme. The crucial factor is stress-triggered NO production, which regulates the S-nitrosylation of SlP5CR at Cys-5, thereby increasing its NAD(P)H affinity and enzymatic activity. S-nitrosylation of SlP5CR enables tomato plants to better adapt to changing NAD(P)H levels, boosting both SlP5CR activity and proline synthesis during stress. By comparing tomato lines genetically modified to express different forms of SlP5CR, including a variant mimicking S-nitrosylation (SlP5CRC5W), we found that SlP5CRC5W plants show superior growth and stress tolerance. This is attributed to better P5CR activity, proline production, water use efficiency, reactive oxygen species scavenging, and sodium excretion. Overall, this study demonstrates that tomato engineered to mimic S-nitrosylated SlP5CR exhibits enhanced growth and yield under drought and salt stress conditions, highlighting a promising approach for stress-tolerant tomato cultivation.

Proline uptake promotes activation of lymphoid tissue inducer cells to maintain gut homeostasis.

Metabolic regulation is integral to the proper functioning of innate lymphoid cells, yet the underlying mechanisms remain elusive. Here, we show that disruption of exogenous proline uptake, either through dietary restriction or by deficiency of the proline transporter Slc6a7, in lymphoid tissue inducer (LTi) cells, impairs LTi activation and aggravates dextran sodium sulfate-induced colitis in mice. With an integrative transcriptomic and metabolomic analysis, we profile the metabolic characteristics of various innate lymphoid cell subsets and reveal a notable enrichment of proline metabolism in LTi cells. Mechanistically, defective proline uptake diminishes the generation of reactive oxygen species, previously known to facilitate LTi activation. Additionally, LTi cells deficient in Slc6a7 display downregulation of Cebpb and Kdm6b, resulting in compromised transcriptional and epigenetic regulation of interleukin-22. Furthermore, our study uncovers the therapeutic potential of proline supplementation in alleviating colitis. Therefore, these findings shed light on the role of proline in facilitating LTi activation and ultimately contributing to gut homeostasis.

Detoxification role of amino acids and phytochelatins on two populations of harmel plant under silver stress.

Two non-metallicolous and metallicolous populations of harmel plants were compared regarding the role of proline, cysteine, reducing sugars, hydrogen peroxide (H2O2), glutathione, thiol compounds, organic acids, total free amino acids, and lipid peroxidation in detoxification and tolerance of silver stress (0, 1, 2.5, 5, 10 ppm Ag). The results of the present research state that the effects of Ag were increased total free amino acids, glutathione, organic acids, proline, reducing sugars, thiol compounds, and cysteine, so the accumulation of these compounds was higher in metallicolous populations than non-metallicolous. On the other hand, non-metallicolous populations showed higher content of lipid peroxidation and H2O2 than metallicolous populations under Ag stresses. Also, the accumulation of phytochelatins (PC) was observed with increasing Ag concentration, which shows that compared to glutathione, non-protein thiols have a higher concentration. The number of organic acids (malic acids, fumaric, oxalic, and citric) except acetic acid increased in the leaves of harmel in both populations. According to the results of this research, the harmel metallophilic population has a crucial role in the tolerance and detoxification of Ag stress, so the antioxidant responses of the plant against Ag stress in the non-metallicolous population were lower than the metallicolous population. Based on the above results, it can be concluded that the harmel plant has a detoxification mechanism to deal with high concentrations of Ag.

Role of proline in regulating turfgrass tolerance to abiotic stress

Turfgrasses used on golf courses, sports fields and in urban landscapes have significant ecological and economic values. Various abiotic stresses are crucial in limiting the growth and development of turfgrass. As an important amino acid metabolite, proline can act as a signal to trigger plant responses to stress. Proline accumulation is not only a stress signal, but also alleviates plant damage by maintaining photosynthesis and the activities of antioxidant enzymes and the levels of non-enzymatic antioxidant compounds, thus reducing reactive oxygen species content, and regulating osmosis. A better understanding of mechanisms of proline response to abiotic stress in turfgrass is vital for the development of stress-tolerant germplasm. This review summarizes research progress into the role of proline in regulating growth and physiological and molecular adaptations to abiotic stress, with emphasis on drought, salt and temperature tolerance.

Anatomical and Physiological Performance of Jojoba Treated with Proline under Salinity Stress Condition

A field trial study was conducted for two consecutive seasons 2020 and 2021 in approximately 8-month-old jojoba plants to evaluate the physiological responses following salt treatment and the role of proline as a foliar application to enhance jojoba tolerance to salinity stress. Jojoba plants were irrigated once a week for four months with diluted seawater in concentrations of 5000, 10,000, and 15,000 ppm and tap water (control). Anti-stress proline was applied four times throughout the experiment, the first at the beginning of the experiment and another three times at 30-day intervals, at concentrations of 0, 300, and 450 ppm. The effect of proline treatments on jojoba plant behavior includes growth vegetative characteristics, namely plant height increase percentage (PHIP), shoot number increase percentage (NSIP), stem diameter increase percentage (SDIP), number of leaves, leaf thickness, leaf area, and fresh and dry weights of leaves, and chemical characteristics, namely chlorophyll a and b, total chlorophyll, carotenoids, leaf mineral contents (N, P, K, Na, and Cl), total phenolic content (TPC), and proline concentration. Moreover, the impacts of proline on hydrogen peroxide (H2O2), superoxide anion (O2•−), malondialdehyde (MDA), and ion leakage (IL) under salinity stress were investigated. Briefly, proline at 450 ppm enhanced all studied growth and physiological characteristics and promoted the antioxidant system of jojoba plants compared with the control and other treatments. The anatomical structure of leaves was also examined, and favorable variations in the anatomical structure were detected in the stressed and proline-treated plants. Exogenous application of proline enhanced most of this anatomical characteristic of jojoba leaf under saline stress. In conclusion, proline as a foliar application at 450 ppm under salinity stress of 10,000 ppm enhances jojoba tolerance to salinity stress by modifying the physicochemical and morphological characteristics of jojoba plants.

The Emerging Role of Proline in the Establishment and Functioning of Legume-Rhizobium Symbiosis.

High levels of some enzymes involved in proline synthesis and utilization were early found in soybean nodules, and rhizobial knockout mutants were shown to be defective in inducing nodulation and/or fixing nitrogen, leading to postulate that this amino acid may represent a main substrate for energy transfer from the plant to the symbiont. However, inconsistent results were reported in other species, and several studies suggested that proline metabolism may play an essential role in the legume-Rhizobium symbiosis only under stress. Different mechanisms have been hypothesized to explain the beneficial effects of proline on nodule formation and bacteroid differentiation, yet none of them has been conclusively proven. Here, we summarize these findings, with special emphasis on the occurrence of a legume-specific isoform of δ1-pyrroline-5-carboxylate synthetase, the enzyme that catalyses the rate-limiting step in proline synthesis. Data are discussed in view of recent results connecting the regulation of both, the onset of nodulation and proline metabolism, to the redox status of the cell. Full comprehension of these aspects could open new perspectives to improve the adaptation of legumes to environmental stress.

Plant growth regulators affecting corn (Zea mays L.) physiology and rab17 expression under drought conditions

Finding methods, which may improve corn ( Zea mays L.) growth and physiology under drought stress, is of significance. Accordingly, the effects of different plant growth regulators (PGRs) including benzyl adenine (BA6), gibberellins (GA 3+7 ), proline (Pr), and BA6 + GA 3+7 + Pr (sub plots), at different drought levels including control (S1), moderate (S2) and severe (S3) (main plots) on the physiology and genetic contents of corn (Single Cross 704) plants were investigated. A two-year field research, as a split plot on the basis of a randomized complete block design with four replications, was conducted in the Research Field of Islamic Azad University, Isfahan, Iran in 2015–2016. Corn physiological parameters including carotenoids (Car), total chlorophyll (Chlt), chlorophyll a (Chla), chlorophyll b (Chlb), plasma membrane resistance (PR), and rab17 expression were determined. Analysis of variance and comparison of means indicated the experimental treatments significantly (P ≤ 0.01) affected the measured parameters. The combination of PGRs and drought stress was not significant on PR, and just drought stress had a significant effect on rab17 expression at P ≤ 0.01. The year parameter significantly affected corn Car and PR. Although stress decreased plant Car, and Chl contents, it increased PR. The tested PGRs significantly improved corn physiology and rab17 expression, and interestingly their effectiveness enhanced with increasing the level of stress (significant interaction of PGRs and drought stress). The role of proline as an RNA binding protein affecting RNA activity and rab17 expression and subsequent corn tolerance under drought stress has been suggested. • Plant growth regulators (PGRs) affecting corn physiology and genetic under drought. • Proline and its combination with benzyl adenine and gibberellins the most effective. • Suggesting proline as and RNA binding protein in the alleviation of drought stress. • The possibility of alleviating drought stress in corn plants using the tested PGRs.

Proline Dehydrogenase/Proline Oxidase (PRODH/POX) Is Involved in the Mechanism of Metformin-Induced Apoptosis in C32 Melanoma Cell Line.

The role of proline dehydrogenase/proline oxidase (PRODH/POX) in the mechanism of antineoplastic activity of metformin (MET) was studied in C32 melanoma cells. PRODH/POX is a mitochondrial enzyme-degrading proline that is implicated in the regulation of cancer cell survival/apoptosis. The enzyme is activated by AMP kinase (AMPK). It has been found that MET induced a significant decrease in cell viability and DNA biosynthesis accompanied by an increase in the expressions of AMPK and PRODH/POX in C32 cells. The mechanism for MET-dependent cytotoxicity on C32 cells was found at the level of PRODH/POX-induced ROS generation and activation of Caspase-3 and Caspase-9 expressions in these cells. The effects were not observed in MET-treated PRODH/POX knock-out C32 cells. Of interest is an MET-dependent increase in the concentration of proline, which is a substrate for PRODH/POX. This phenomenon is due to the MET-dependent inhibition of collagen biosynthesis, which is the main proline-utilizing process. It has been found that the underlying mechanism of anticancer activity of MET involves the activation of AMPK, PRODH/POX, increase in the cytoplasmic concentration of proline, inhibition of collagen biosynthesis, and stimulation of PRODH/POX-dependent ROS generation, which initiate the apoptosis of melanoma cells.

Perspectives, past, present and future: the proline cycle/proline-collagen regulatory axis

In the 35 years since the introduction of the “proline cycle”, its relevance to human tumors has been widely established. These connections are based on a variety of mechanisms discovered by many laboratories and have stimulated the search for small molecule inhibitors to treat cancer or metastases. In addition, the multi-layered connections of the proline cycle and the role of proline and hydroxyproline in collagen provide an important regulatory link between the extracellular matrix and metabolism.

Investigation of proline in superficial scald development during low temperature storage of ‘Dangshansuli’ pear fruit

The role of proline in superficial scald development in pear fruit was investigated in this study. During low temperature storage of ‘Dangshansuli’ pear fruit, superficial scald incidence and index accumulated in association with the alternation of α-farnesene and conjugated trienols (CTols). 14 out of 17 free amino acids were identified; proline content gradually decreased, which was consistent with the up-regulation of PbrP5CS activity and down-regulation of PbrProDH activity in its metabolic pathway. A total of 14 genes involved in proline metabolism were identified based on transcriptome annotation with diverse expression profiles. Results from correlation analysis among proline content further indicate that enzyme activity and gene expression profile, PbrProDH2, PbrProDH4, PbrProDH5 &PbrP5CS5 might play a critical role in proline metabolism during low temperature storage of ‘Dangshansuli’ fruit; thus, influencing superficial scald development which was then functionally validated using the transgenic pear fruit. Postharvest 1-MCP and diphenylamine (DPA) treatment inhibited the accumulation of CTols, and thus, mitigated superficial scald development and maintained higher proline content, in association with the up-regulated PbrP5CS activity, PbrP5CS4 &PbrP5CS5 mRNAs as well as the down-regulated PbrProDH activity &PbrProDH4 transcripts. In a further study, we found that exogenous application of proline alleviated superficial scald incidence and index. To that end, the results of our study confirmed that proline was involved in superficial scald development during pear storage.

The Unusual Role of Pro in Cu(II) Binding by His2-Cyclopentapeptide.

In this paper, we present findings from studying the interaction of copper(II) ions with the His2-cyclopentapeptide and the role of proline used for the purpose of potentiometric titration and UV-Vis, CD and EPR spectroscopic measurements. Experiments of two homodetic peptides differing by one amino acid residue were conducted for a ligand to metal ratio of 1:1 in the pH range 2.5–11.0. The presented studies reveal that peptides form only mononuclear complexes, and the CuH2L complex appears in the system first (for both L1 and L2). Study results show that the presence of Pro influences the structure of formed complexes and their stabilities and has a strong impact on the efficiency of copper(II) coordination.

Role of Proline in Mitigating the Deleterious Effects of Heat Stress in Chillies

Summary Chilli is a spicy crop which belongs to family Solanaceae. As a vegetable crop, it is considered as one of the major cultivated crops in the world seriously affected by the climatic changes, including elevation in temperature. Therefore, in this research various morpho-physiological characteristics of chilli were studied for heat tolerance under the influence of exogenous application of proline. This research was carried out in a growth room of the Institute of Horticultural Sciences, University of Agriculture, Faisalabad, Pakistan. Four chilli genotypes were evaluated under the applied conditions. Seeds were grown in plastic pots. Heat stress (40/32 ºC day and night temperature) was applied 30 days after the emergence. Foliar spray of proline (0, 5 and 10 mM) was applied during heat stress, and after 7 days of stress the plants were harvested. The results revealed that the inhibition of chilli growth by heat stress was successfully mediated by proline application. Morphological attributes such as the number of leaves per plant, root and shoot length, plant fresh and dry weight were reduced in response to heat stress, and physiological attributes such as photosynthetic rate, water use efficiency and chlorophyll contents were also reduced in response to heat stress, except transpiration rate and stomatal conductance, which increased under heat stress and showed recovery by proline application. Exogenous application of proline promoted tolerance against heat stress in chilli genotypes and enhanced growth. All the observed traits exhibited recovery in response to proline stimulus, indicating the role of proline in mitigating the consequences of heat stress. Recovery also depends on genetic capability of various cultivars.

Proline Concentration and Its Metabolism Are Regulated in a Leaf Age Dependent Manner But Not by Abscisic Acid in Pea Plants Exposed to Cadmium Stress.

The accumulation of proline is one of the defense mechanisms of plants against the harmful effects of adverse environmental conditions; however, when pea plants were treated for 12 h with CdCl2, the proline concentration decreased in the youngest A (not expanded) and B1 (expanded) leaves, and did not change significantly in the B2 (mature, expanded) or C (the oldest) leaves. After 24 h of cadmium (Cd) stress, the proline concentration remained low in A and B1 leaves, while in B2 and C leaves, it increased, and after 48 h, an increase in the proline concentration in the leaves at each stage of development was observed. The role of proline in the different phases of plant response to the Cd treatment is discussed. Changes in proline accumulation corresponded closely with changes in the transcript levels of PsP5CS2, a gene encoding D1-pyrroline-5-carboxylate synthetase involved in proline synthesis, and PsPDH1, a gene encoding proline dehydrogenase engaged in proline degradation. CdCl2 application induced the expression of PsProT1 and PsProT2, genes encoding proline transporters, especially during the first 12 h of treatment in A and B1 leaves. When the time courses of abscisic acid (ABA) and proline accumulation were compared, it was concluded that an increase in the proline concentration in the leaves of Cd-treated pea plants was more related to a decrease in chlorophyll concentration (leaves B2 and C) and an increase in the malondialdehyde level (A and B1 leaves) than with an increase in ABA concentration alone. Exogenous application of ABA (0.5, 5, 50 µM) significantly increased the proline concentration in the A leaves of pea plants only, and was accompanied by an elevated and repressed expression of PsP5CS2 and PsPDH1 in these leaves, respectively. The presented results suggest that under Cd stress, the accumulation of proline in leaves of pea plants may take place independently of the ABA signaling.

The role of prolines and glycine in the transmembrane domain of LAT.

Linker for activation in T cells (LAT) is a critical regulator of T-cell development and function. It organises signalling events at the plasma membrane. However, the mechanism, which controls LAT localisation at the plasma membrane, is not fully understood. Here, we studied the impact of helix-breaking amino acids, two prolines and one glycine, in the transmembrane segment on localisation and function of LAT. Using insilico analysis, confocal and super-resolution imaging and flow cytometry, we demonstrate that central proline residue destabilises transmembrane helix by inducing a kink. The helical structure and dynamics are further regulated by glycine and another proline residue in the luminal part of LAT transmembrane domain. Replacement of these residues with aliphatic amino acids reduces LAT dependence on palmitoylation for sorting to the plasma membrane. However, surface expression of these mutants is not sufficient to recover function of nonpalmitoylated LAT in stimulated T cells. These data indicate that geometry and dynamics of LAT transmembrane segment regulate its localisation and function in immune cells.

БИДАЙ ДƏНДЕРІН ПРАЙМИНГТЕУДІҢ МЫС ИОНДАРЫ БАР ОРТАДА ӨСКІНДЕРДІҢ ДАМУЫ МЕН ПРОЛИН МӨЛШЕРІНЕ ƏСЕРІ

In addition to antioxidants, compounds called osmoprotectants also play a special role in relieving the negative effects of oxidative stress that occurs in plants. These include glycinbetaine, proline, and mannitol. Among them, the biological role of proline is most common among plants. The results of this study are related to the development of pre- sowing processing (priming) of grains of various varieties of spring wheat to increase its resistance to heavy metals, yield and seed quality. The study is aimed not only at increasing seed germination, growth and development of their seedlings under heavy metal exposure, but also at determining the amount of proline in sprouted seeds after priming. It was carried out under the above-mentioned conditions of different concentrations of priming and copper salt solution and studied how Proline levels change in wheat sprouts. The obtained results show for the fi rst time that the relationship between antioxidants and osmoprotectants changes during oxidative stress caused by heavy metal. Key words: proline, pre-sowing priming, heavy metals, osmoprotectants.

Studies on role of proline, hydrogen peroxide and total antioxidant activity in Wheat (Triticum aestivum L.) under drought stress after anthesis

The investigation was conducted to evaluate the effect of drought stress on role of proline, hydrogen peroxide and total antioxidant activity (TAA) of two wheat varieties viz. WH 1105 (Drought sensitive) and WH 1025 (Drought sensitive) after anthesis. Drought was given by only pre sown irrigation. Analysis of data revealed that drought stress results an increase in proline and hydrogen peroxide (H2O2) contents in leaves and developing grains of both wheat varieties after anthesis, however more increase in imino amino acid proline was observed in WH 1025 which is ascribed to improved drought tolerance through osmotic adjustment of cellular contents. Drought sensitive wheat variety WH 1105 had accumulated higher hydrogen peroxide (H2O2) than WH 1025. Stress tolerance to plants is determined by the pool size of antioxidants and protective plant pigments particularly carotenoids. This study also revealed that the total antioxidant activity (TAA) was increased in leaves and developing grains of both wheat varieties with higher and significant increase in WH 1025 than WH 1105.

Proline Accumulation in Pollen Grains as Potential Target for Improved Yield Stability Under Salt Stress.

Seed yield, a major determinant for the commercial success of grain crops, critically depends on pollen viability, which is dramatically reduced by environmental stresses, such as drought, salinity, and extreme temperatures. Salinity, in particular, is a major problem for crop yield known to affect about 20% of all arable land and cause huge economic losses worldwide. Flowering plants are particularly sensitive to environmental stress during sexual reproduction, and even a short exposure to stressing conditions can severely hamper reproductive success, and thus reduce crop yield. Since proline is required for pollen fertility and accumulates in plant tissues in response to different abiotic stresses, a role of proline in pollen protection under salt stress conditions can be envisaged. In this perspective, we analyze old and new data to evaluate the importance of pollen development under saline conditions, and discuss the possibility of raising proline levels in pollen grains as a biotechnological strategy to stabilize seed yield in the presence of salt stress. The overall data confirm that proline is necessary to preserve pollen fertility and limit seed loss under stressful conditions. However, at present, we have not enough data to conclude whether or not raising proline over wildtype levels in pollen grains can effectively ameliorate seed yield under saline conditions, and further work is still required.

Review on Role of Proline on Coffee Under Drought Conditions

Drought is one of the major constraints that limiting production of crop worldwide. Plants tolerate drought by many ways like morphological, physiological and biochemical tolerance mechanisms. Plants develop mechanisms to tolerant abiotic stress by osmotic adjustment that is usually accomplished by uptake of inorganic ions, as well as the accumulation of proline. Proline is a universal osmo-protectant and acts as an osmolyte and antioxidant, and it is one of the most important compatible solutes that play a vital role in osmotic adjustment in crops under drought stress. Accumulation of proline considered as adaptive mechanisms in drought-tolerant coffee genotypes. In general, more attention on biochemical traits for drought tolerant mechanisms on coffee should be given. Therefore, looking for high proline accumulation genotype under drought conditions is important for further coffee breeding program to release drought tolerant genotypes. Keywords: Coffee, Drought, Tolerant, Proline Accumulation DOI : 10.7176/JEES/9-10-01 Publication date :October 31 st 2019

Development of a direct ESI-MS method for measuring the tannin precipitation effect of proline-rich peptides and in silico studies on the proline role in tannin-protein interactions

Tannins are a heterogeneous class of polyphenols that are present in several plants and foods. Their ability to interact and precipitate proline-rich proteins leads to different effects such as astringency or antidiarrheal activity. Thus, evaluation of the tannin content in plant extracts plays a key role in understanding their potential use as pharmaceuticals and nutraceuticals. Several methods have been proposed to study tannin-protein interactions but few of them are focused on quantification. The purpose of the present work is to set up a suitable and time efficient method able to quantify the extent of tannin protein precipitation. Bradykinin, chosen as a model, was incubated with increasing concentrations of 1,2,3,4,6-penta-O-galloyl-β-d-glucose and tannic acid selected as reference of tannic compounds. Bradykinin not precipitated was determined by a mass spectrometer TSQ Quantum Ultra Triple Quadrupole (direct infusion analysis). The results were expressed as PC50, which is the concentration able to precipitate 50% of the protein. The type of tannin-protein interaction was evaluated also after precipitate solubilisation. The involvement of proline residues in tannin-protein interactions was confirmed by repeating the experiment using a synthesized peptide (RR-9) characterized by the same bradykinin sequence, but having proline residues replaced by glycine residues: no interaction occurred between the peptide and the tannins. Moreover, modelling studies on PGG-BK and PGG-RR-9 were performed to deeply investigate the involvement of prolines: a balance of hydrophobic and H-bond contacts stabilizes the PGG-BK cluster and the proline residues exert a crucial role thus allowing the PGG molecules to elicit a sticking effect.

Synthesis versus degradation: directions of amino acid metabolism during Arabidopsis abiotic stress response.

During abiotic stress low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, darkness) and are degraded. Metabolic adaptation is crucial for abiotic stress resistance in plants, and accumulation of specific amino acids as well as secondary metabolites derived from amino acid metabolism has been implicated in increased tolerance to adverse environmental conditions. The role of proline, which is synthesized during Arabidopsis stress response to act as a compatible osmolyte, has been well established. However, conclusions drawn about potential functions of other amino acids such as leucine, valine, and isoleucine are not entirely consistent. This study reevaluates published datasets with a special emphasis on changes in the free amino acid pool and transcriptional regulation of the associated anabolic and catabolic pathways. In order to gain a comprehensive overview about the general direction of amino acid metabolism under abiotic stress conditions a complete map of all currently known enzymatic steps involved in amino acid synthesis and degradation was assembled including also the initial steps leading to the synthesis of secondary metabolites. Microarray datasets and amino acid profiles of Arabidopsis plants exposed to dehydration, high salinity, extended darkness, cold, and heat were systematically analyzed to identify trends in fluxes of amino acid metabolism. Some high abundant amino acids such as proline, arginine, asparagine, glutamine, and GABA are synthesized during abiotic stress to act as compatible osmolytes, precursors for secondary metabolites, or storage forms of organic nitrogen. In contrast, most of the low abundant amino acids are not synthesized but they accumulate due to increased protein turnover under conditions inducing carbohydrate starvation (dehydration, salt stress, extended darkness) and are degraded.