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. 2025 Apr 15;25:480. doi: 10.1186/s12870-025-06513-x

Quantitative proteomic analysis based on TMT reveals different responses of Haloxylon ammodendron and Haloxylon persicum to long-term drought

Fang Yang 1,2,3, Xuelian Ding 1,2,3, Guanghui Lv 1,2,3,✉
PMCID: PMC11998144  PMID: 40234745

Abstract

The essence of the plant drought tolerance mechanism lies in determining protein expression patterns, identifying key drought-tolerant proteins, and elucidating their association with specific functions within metabolic pathways. So far, there is limited information on the long-term drought tolerance of Haloxylon ammodendron and Haloxylon persicum grown in natural environments, as analyzed through proteomics. Therefore, this study conducted proteomic research on H. ammodendron and H. persicum grown in natural environments to identify their long-term drought-tolerant protein expression patterns. Totals of 71 and 348 differentially expressed proteins (DEPs) were identified in H. ammodendron and H. persicum, respectively. Bioinformatics analysis of DEPs reveals that H. ammodendron primarily generates a large amount of energy by overexpressing proteins related to carbohydrate metabolism pathways (pyruvate kinase, purple acid phosphatases and chitinase), and simultaneously encodes proteins capable of degrading misfolded/damaged proteins (tam3-transposase, enhancer of mRNA-decapping protein 4, and proteinase inhibitor I3), thus adapting to long-term drought environments. For H. persicum, most DEPs (enolase and UDP-xylose/xylose synthase) involved in metabolic pathways are up-regulated, indicating that it mainly adapts to long-term drought environments through mechanisms related to positive regulation of protein expression. These results offer crucial insights into how desert plants adapt to arid environments over the long term to maintain internal balance. In addition, the identified key drought-tolerant proteins can serve as candidate proteins for molecular breeding in the genus Haloxylon, aiming to develop new germplasm for desert ecosystem restoration.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12870-025-06513-x.

Keywords: Haloxylon ammodendron, Haloxylon persicum, Long-term drought, TMT proteomics, Key proteins for drought tolerance

Introduction

Drought has become one of the greatest environmental threats to plants [40]. Given that desert plants in arid regions are exposed to a long-term water-limited environment, analyzing their long-term drought tolerance strategies has become a major research focus.

Proteins are the direct effectors of plant responses to internal and external stimuli [39]. This effect is manifested not only in direct changes to enzyme types and activities at the metabolic level, but also through the regulation of transcription and translation levels. This leads to structural and functional alterations in plant cell membranes, cytoplasm, cytoskeleton, and various intracellular protein components, ultimately regulating plant adaptation to stress [95]. Proteomics is now one of the most commonly used techniques for studying the relationship between gene function and related molecular mechanisms [96]. In recent years, proteomics research has discovered a large number of proteins involved in key metabolic processes such as glucose and amino acid metabolism, redox homeostasis, stress response, photosynthesis, signal transduction, and protein processing [12, 29]. Therefore, studying the protein level responses of plants under adverse conditions is significant for understanding the physiological mechanisms of plant stress resistance.

Tandem mass tagging (TMT) and liquid chromatography-mass spectrometry (LC–MS/MS) techniques are crucial technical methods in proteomics analysis. With the advancement of LC–MS/MS, two prevalent quantitative proteomics methods have been developed, namely label-free quantification (LFQ) and isobaric tagging strategies (such as TMT) [36]. Compared to traditional two-dimensional gel electrophoresis (2-DE) technology, TMT-based quantitative proteomics offers a more efficient and accurate approach for analyzing a larger number of proteins [46].

H. ammodendron and H. persicum, as typical desert plants in arid regions, exhibit strong drought tolerance and environmental adaptability [63, 83]. Although H. ammodendron and H. persicum both belong to the genus Haloxylon and are found in desert regions, their habitats exhibit significant differences. The molecular mechanisms underlying their varying drought tolerance remain unclear. We have previously reported the responses of H. ammodendron and H. persicum to drought stress from morphological, physiological, biochemical, transcriptomic, and metabolomic perspectives [86–90]. However, there have been no reports on quantitative proteomic studies of assimilating branches of H. ammodendron and H. persicum under drought stress based on TMT analysis. To comprehensively uncover the molecular mechanisms underlying the long-term drought tolerance of H. ammodendron and H. persicum, this study utilized TMT and LC–MS/MS techniques for comprehensive protein kinetic analysis. This approach aimed to decipher their protein expression patterns related to long-term drought tolerance and identify key drought-tolerant proteins. This study lays a theoretical foundation for the subsequent functional verification of key drought-tolerant proteins, and holds significant importance for afforestation and vegetation restoration in the desert regions of northwest China.

Materials and methods

Sample plot setting

The experiment was performed during the peak season of plant growth from June to July 2021 at the field scientific observation station of the Ministry of Education in the temperate desert ecosystem of Jinghe County, Xinjiang University. Starting from the Dongdaqiao Management and Protection Station of the Ebinur Lake Wetland Nature Reserve, individual transects (0.1 km × 2.0 km wide) were set vertically to the Aqiksu River in areas with H. ammodendron and H. persicum: transect 1 (in the H. ammodendron distribution area) and transect 2 (in the H. persicum distribution area) (Fig. 1A). Based on the results of previous researchers [17], we selected two soil moisture environments, humid and arid. In each of the two soil moisture environments, set up a 50 m × 50 m sample plot (Fig. 1B). Along the diagonal of each sample plot, select 5 healthy H. ammodendron and H. persicum plants with similar height, crown width, and base diameter as experimental plants. To verify that the two soil moisture environments correspond to arid and humid habitats, soil moisture content was measured in two plots. The results indicated that the soil moisture content of HS was 12.88%, whereas that of LS was 3.80%, showing a significant difference (p < 0.05). Similarly, the soil moisture content of HB was 3.46%, while that of LB was 2.16%, also exhibiting a significant difference (p < 0.05) (Table S1).

Fig. 1.

Fig. 1

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The study area and sample layout map. A Study area; (B) Sample layout and plant selection. The distribution area of H. ammodendron: (A): humid and low salt (HS), (B): arid and low salt (LS). The distribution area of H. persicum: (C): humid and low salt (HB), D: arid and low salt (LB)

Sample collection

Collect assimilation branches from the upper, sunny parts of 5 plants labeled with H. ammodendron and H. persicum, grown under both arid and humid soil moisture conditions. Mix the collected assimilation branches from each plant evenly, and promptly freeze them in a liquid nitrogen tank for proteomic analysis. The protein data used for analysis for both H. ammodendron and H. persicum is the average of three biological replicates (n = 3).

Total protein extraction and protein quality tests

The samples were ground individually in liquid nitrogen and lysed with SDT lysis buffer (containing 100 mM NaCl) and a 1/100 volume of Dithiothreitol (DTT), followed by 5 min of ultrasonication on ice. After reacting at 95°C for 8–15 min and being placed in an ice bath for 2 min, the lysate was centrifuged at 12,000 × g for 15 min at 4°C. The supernatant was taken and added with sufficient IAM to react for 1 h at room temperature in the dark. Then, the samples were completely mixed with 4 × the volume of precooled acetone by vortexing and incubated at − 20°C for at least 2 h. The samples were then centrifuged at 12,000 × g for 15 min at 4°C, and the precipitate was collected. After washing with 1 mL of cold acetone, the pellet was completely dissolved in Dissolution Buffer (DB buffer) [79].

A bovine serum albumin (BSA) standard protein solution was prepared according to the instructions of a Bradford protein quantitative kit [8], with a gradient concentration ranging from 0 to 0.5 g/L. BSA standard protein solutions and sample solutions with different dilution multiples were added into 96-well plates to a volume of 20 µL. Each gradient was replicated three times. The plate was added with 180 μL of G250 dye solution and placed at room temperature for five minutes, and the absorbance at 595 nm was read. A standard curve was drawn using the absorbance of standard protein solutions, and the protein concentration of the sample was calculated from the curve. Twenty micrograms of the protein sample was loaded onto 12% SDS-PAGE gels for electrophoresis, where the concentrated gel was run at 80 V for 20 min, and the separation gel was run at 120 V for 90 min. The gel was stained by Coomassie brilliant blue R-250 and decolored until the bands were clearly visible.

TMT labeling of peptides and separation of fractions

One hundred microliters of 0.1 M triethylammonium bicarbonate (TEAB) buffer was added to reconstitute the sample, and 41 μL of acetonitrile-dissolved TMT labeling reagent was added, after which the sample was mixed with shaking for 2 h at room temperature. The reaction was stopped by adding 8% ammonia. All labeling samples were mixed with equal volumes, desalted, and lyophilized [59].

Mobile phase A (2% acetonitrile, pH adjusted to 10.0 using ammonium hydroxide) and B (98% acetonitrile) were used to develop an elution gradient. The lyophilized powder was dissolved in solution A and centrifuged at 14,000 g for 20 min at 4°C. The sample was fractionated using a C18 column (Waters BEH C18, 4.6 × 250 mm, 5 μm) on a Rigol L3000 HPLC system. The column oven was set to 45°C. The eluates were monitored at a UV wavelength of 214 nm, collected for a tube per minute, and finally combined into 10 fractions. All fractions were dried under vacuum, then they were reconstituted in 0.1% (v/v) formic acid (FA) in water.

Liquid chromatography-tandem mass spectroscopy

Fractional Separation: Prepare mobile phase A (2% acetonitrile, 98% water, adjusted to pH = 10 with ammonia) and B solution (98% acetonitrile, 2% water). Dissolve the freeze-dried powder in solution A and centrifuge at 14,000 g for 20 min at 4°C. Using the L-3000 HPLC system, the chromatographic column was Waters BEH C18 (4.6 × 250 mm, 5 μm), with a column temperature set at 45°C. Collect one tube per minute, merge into 10 fractions, freeze-dry and dissolve each with 0.1% formic acid.

TMT liquid phase parameters: Mobile phase A (100% water, 0.1% formic acid) and liquid B (80% acetonitrile, 0.1% formic acid) were prepared for LC. Samples of 1 μg of each fraction were injected into the LC–MS/MS system. An EASY-nLC™ 1200 nano-upgraded UHPLC system was used for identification. The precolumn (4.5 cm × 75 μm, 3 μm) and analytical column (25 cm × 150 μm, 1.9 μm) used in this project were both home-made.

TMT mass spectrometry parameters: The separated peptides were analyzed using a Q-Exactive™ HF-X mass spectrometer, with an ion source of Nanospray Flex™ (ESI), a spray voltage of 2.3 kV, and an ion transport capillary temperature of 320°C. Full scans ranged from m/z 350 to 1500, with a resolution of 60,000 (at m/z 200), an automatic gain control (AGC) target value of 3 × 106, and a maximum ion injection time of 20 ms. The top 40 precursors of the highest abundance in the full scan were selected and fragmented by higher energy collisional dissociation (HCD) and analyzed in MS/MS, where the resolution was 45,000 (at m/z 200) for 10 plex; the automatic gain control (AGC) target value was 5 × 104; the maximum ion injection time was 86 ms; the normalized collision energy was set as 32%; the intensity threshold was 1.2 × 105, and the dynamic exclusion parameter was 20 s. The raw data of MS detection were denoted as “.raw” [81].

The identification and quantitation of proteins

The resulting spectra from each run were searched against the 1859645-all_BAB_SAB.fasta_handled.fasta (24951 sequences) database by the search engines Proteome Discoverer 2.5 (PD, Thermo, HFX, and 480). The search parameters were set as follows. The mass tolerance for precursor ions was 10 ppm, and the mass tolerance for product ions was 0.02 Da. Carbamidomethyl was specified as a fixed modification; oxidation of methionine (M) and TMT plex were specified as dynamic modifications. Acetylation, TMT plex, Met-loss, and Met-loss + Acetyl were specified as N-terminal modifications. A maximum of two miscleavage sites were allowed.

To improve the quality of the analysis, the software PD was employed to further filter the retrieval results. Peptide Spectrum Matches (PSMs) with a credibility of more than 99% were identified as PSMs. The identified proteins contained at least one unique peptide. The identified PSMs and proteins that were retained had a false discovery rate (FDR) of no more than 1.0%. The protein quantification results were analyzed using the t-test in R (version 4.4.2) and adjusted by the Benjamini and Hochberg’s approach for controlling the false discovery rate. The proteins whose quantitation was significantly different between experimental and control groups, (padj < 0.05 and |log2FC|> 1 (FC > 2.0 or FC < 0.50 [fold change, FC]), were defined as differentially expressed proteins (DEPs) [55].

The functional analysis of proteins and DEPs

To identify significant differences in protein expression between arid low-salt and humid low-salt conditions, the data was subjected to logarithmic transformation and centering using R (version 4.4.2). Gene Ontology (GO, http://www.geneontology.org) and InterPro (IPR) functional analyses were conducted using the InterProScan program (5.25–64.0) against non-redundant protein databases (including Pfam, PRINTS, ProDom, SMART, ProSite, and PANTHER), and the databases ofClusters of Orthologous Groups of Protein (KOG, http://www.ncbi.nlm.nih.gov/COG/) and Kyoto Encyclopedia of Genes and Genomes (KEGG, http://www.genome.jp/kegg) were used to analyze the protein families and pathways [31]. The DEPs were used for volcano maps, cluster heat maps, and enrichment analyses of GO, IPR, and KEGG results [26]. The probable protein–protein interactions (PPI) were predicted using the STRING-DB server (version 10.1, http://string.embl.de/) and visualized in Cytoscape software (version 3.10.0) [3]. Utilize the CytoHubba plugin within the Cytoscape software to identify key drought-tolerant proteins and subnetworks within the PPI [82].

Results

Protein identification and evaluation

Mass spectrometry analysis obtained a total of 438700 secondary spectra and 165109 effective spectra. Totals of 66715 peptide segments and 6325 proteins were identified. The total number of quantifiable proteins in all samples was 6290 (Table S2). The distribution of peptide lengths indicated that the majority of peptide lengths were within the range of 7–20 amino acid residues, a result that met the quality control criteria (Fig. 2A). The repeatability of the protein quantification was evaluated by using the coefficient of variation (CV) to test whether the quantitative results of the samples were statistically consistent. The cumulative curve of all protein CV values in the corresponding samples increased very rapidly, indicating excellent repeatability of the sample as a whole (Fig. 2B). In addition, PCA analysis revealed that the two principal components (PC1 and PC2) accounted for 68.45% and 12.6% of the variance, respectively. Samples from both H. ammodendron and H. ammodendron soil moisture environments were significantly distant from each other on the PC1 score plot, suggesting distinct protein expression trends.

Fig. 2.

Fig. 2

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Protein identification and evaluation. A Peptide length distribution range. B Repetitive CV analysis. C Principal component analysis (PCA) of H. ammodendron and H. persicum samples under two soil moisture environments. HS and HB respectively represent the moist and low-salt habitats of H. ammodendron and H. persicum; LS and LB respectively represent the arid and low-salt habitats of H. ammodendron and H. persicum

Quantification and annotation of DEPs

A total of 71 DEPs (34 up-regulated and 37 down-regulated) were identified in H. ammodendron (Fig. 3A, Table S3). Among them, the levels of eight DEPs increased by more than three times, while the levels of 37 DEPs decreased by 0.49–0.11 times, and there were eight unknown DEPs. In addition, the protein with the highest fold change was an unknown protein (FC = 7.34), followed by lipoxygenase (LOX, FC = 7.33). This indicates that lipid metabolism plays a crucial role in the drought tolerance of H. ammodendron.

Fig. 3.

Fig. 3

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Volcano plots of differentially expressed proteins in a long-term arid environment. A Differentially expressed proteins in H. ammodendron. B Differentially expressed proteins in H. persicum. Black indicates proteins with insignificant differences, red indicates up-regulated proteins, and green indicates down-regulated proteins

A total of 348 DEPs (186 up-regulated and 162 down-regulated) were identified in H. persicum (Fig. 3B, Table S4). The protein with the most up-regulated expression level was the proteinase inhibitor I3 (FC = 17.96), followed by enolase involved in the glycolysis pathway (FC = 13.83) and UDP xylose/xylose synthase involved in amino sugar and nucleotide sugar metabolism (FC = 12.66). This indicates that under drought stress, H. persicum can reduce cell damage and enhance glucose metabolism by overexpressing protease inhibitor activity, thereby generating a large amount of energy in response to long-term drought conditions.

Subcellular localization of DEPs

Subcellular localization information analysis and KOG functional classification pathway analysis were conducted to characterize the biological functions of DEPs in long-term arid environments. Subcellular localization information showed that under long-term drought conditions, most proteins in H. ammodendron were located in the cytoplasm (five DEPs up-regulated and six down-regulated; 37.93%), followed by chloroplasts (two proteins up-regulated and three down-regulated; 17.24%) (Fig. 4A).

Fig. 4.

Fig. 4

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Subcellular localization of DEPs in long-term arid environments. A Subcellular localization of DEPs in H. ammodendron. B Subcellular localization of DEPs in H. persicum

The proteins in H. persicum were mostly located in the cytoplasm (22 up-regulated and 21 down-regulated; 26.88%), followed by the nucleus (nine up-regulated and 14 down-regulated; 14.38%) (Fig. 4B). This suggested that the cytoplasm plays a crucial role in the drought tolerance of H. ammodendron and H. persicum.

Acetyl CoA acetyltransferase and acyl CoA synthase located in the peroxisomes, as well as ABA/WDS proteins induced in response to stress and located in the nucleus, were down-regulated in both H. ammodendron and H. persicum. The monodehydroascorbate reductase located in the cytoplasm was only up-regulated in H. ammodendron. In addition, the up-regulated enzymes L-ascorbate peroxidase, glutathione S-transferase, catalase, and peroxidase were located in the cytoplasm and peroxisome of H. persicum. The results indicated differences in the subcellular localization and distribution of DEPs in response to drought environments between H. ammodendron and H. persicum in the medium and long term. In addition, subcellular localization can predict the specific location of DEPs within cells, providing research directions for understanding the function of proteins in drought environments.

KOG function annotation for DEPs

Long-term drought up-regulated proteins associated with carbohydrate transport and metabolism, replication, recombination, and repair in H. ammodendron (Fig. 5A, Table S5). In H. persicum, proteins related to amino acid transport and metabolism, carbohydrate transport and metabolism, and cytoskeleton were up-regulated, whereas proteins involved in nuclear structure, chromosome structure, ribosome structure, and transcription were down-regulated (Fig. 5B, Table S6). The KOG analysis of the function and specific metabolic pathways of proteins provides a reference for further research on the role of DEPs in H. ammodendron and H. persicum under long-term drought conditions.

Fig. 5.

Fig. 5

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Functional classification of DEPs in long-term arid environments. A KOG functional classification diagram of DEPs in H. ammodendron. B KOG functional classification diagram of DEPs in H. persicum. The horizontal axis represents the functional classification of annotations, while the vertical axis indicates the number of proteins that are annotated to each corresponding function

GO enrichment analysis of DEPs in long-term arid environments

GO annotation classifies protein expression into three classes: biological processes (BP), molecular functions (MF), and cellular components (CC). In BP and MF analysis, the up-regulated DEPs in H. ammodendron were significantly enriched in "chitin catabolism process (GO: 0006032, enriched protein: chitinase)" and "metal ion binding (GO: 0046872, enriched proteins: two purple acid phosphatases, two lipoxygenases, and pyruvate kinase) (Fig. 6A, Table S7). All enriched proteins are involved in carbohydrate transport, metabolism, and signal transduction processes. The down-regulated DEPs significantly enriched the pathways of "ATP hydrolysis coupled proton transport (p = 6.77 × 10−5)" in BP analysis and "hydrogen ion transmembrane transporter activity" in MF analysis (Fig. 6B, Table S7). All enriched proteins involved in these pathways are involved in energy production and conversion processes. GO analysis results indicate that the long-term drought environment had the greatest impact on carbohydrate transport and metabolism, signal transduction, and the energy production and conversion processes of H. ammodendron.

Fig. 6.

Fig. 6

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GO enrichment analysis of DEPs in long-term arid environments. A GO enrichment histogram of upregulated DEPs in H. ammodendron. B GO enrichment histogram of downregulated DEPs in H. ammodendron. C GO enrichment histogram of upregulated DEPs in H. persicum. D GO enrichment histogram of downregulated DEPs in H. persicum. BP, biological processes; MF, molecular function; CC, cellular component. The percentage on the y-axis represents the ratio of DEPs related to the GO process to the total DEPs of GO annotations

In BP analysis, the up-regulated DEPs in H. persicum were significantly enriched in the "response to stress" category (GO: 0006950, p = 0.0010). Among them, nine DEPs (including two L-ascorbate peroxidases, peroxidases, ABA/WDS induced proteins, dehydrin, glutathione peroxidases, calmodulin-binding protein 60, and Major latex proteins) were all associated with the antioxidant system. In the MF analysis, the most significant change was observed in "lyase activity (GO: 0016829, p = 0.0013)", where seven enriched proteins (phosphoenolpyruvate carboxylase, carbohydrate, fructose bisphosphate aldolase, glutamate decarboxylase, two isoprenoid synthases, and aluminum synthases) were involved in carbohydrate transport and metabolism, inorganic ion transport and metabolism, amino acid transport and metabolism, as well as terpene skeleton biosynthesis pathways (Fig. 6C, Table S8). In BP analysis, the most representative of the down-regulated DEPs is the "oxidation reduction process (GO: 0055114, 17 DEPs)" (Fig. 6D, Table S8). The most significant functional differences were observed between the “nucleosome” (GO: 0000786, p = 0.013) of CC and “oxidoreductase activity” (GO: 0016491, p = 8.43 × 10−5) of the MF categories. The enriched proteins in the CC category were all linker histone H1/H5, proteins that connect DNA and histones (Fig. 6D, Table S8). These results indicate that under long-term drought conditions, H. persicum can respond to the environment by modulating its osmotic regulation function and secondary metabolite synthesis, while also regulating the expression of related genes.

KEGG enrichment analysis of DEPs

The up-regulated expression of DEPs in H. ammodendron was concentrated in the pathways of “linoleic acid metabolism” (two proteins: lipoxygenase) and “alpha-linolenic acid metabolism” (two proteins: lipoxygenase) (Fig. 7A, Table S9). In addition, linoleic acid metabolism and alpha-linolenic acid metabolism are upstream of jasmonic acid (JA) biosynthesis, indicating that H. ammodendron up-regulates lipoxygenase activity to express endogenous hormone levels in response to long-term drought. The down-regulated DEPs were in metabolic pathways such as “valine, leucine, and isoleucine degradation”, “degradation and metabolism of fatty acids”, and “ascorbate and aldarate metabolism” (Fig. 7B, Table S9).

Fig. 7.

Fig. 7

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KEGG enrichment analysis of DEPs in long-term arid environments. A KEGG enrichment analysis of up-regulated DEPs in H. ammodendron. B KEGG enrichment analysis of down-regulated DEPs in H. ammodendron. C KEGG enrichment analysis of up-regulated DEPs in H. persicum. D KEGG enrichment analysis of down-regulated DEPs in H. persicum. The horizontal axis in the figure represents the ratio of DEPs in the corresponding pathway to the total number of identified proteins in that pathway. The higher the value, the greater the enrichment of differential proteins in that pathway. The color of the dot represents the p-value of the hypergeometric test, with colors ranging from purple to red. The redder the color, the smaller the p-value, indicating greater reliability and statistical significance of the test. The size of the dot represents the number of differentially expressed proteins in the corresponding pathway, and the larger the dot, the more differentially expressed proteins in that pathway

Most of the up-regulated DEPs in H. persicum were related to the pathways of “Biosynthesis of secondary metabolites” (36 species), “Carbon metabolism” (13 species), “Biosynthesis of amino acids” (11 species), and “Glycolysis / Gluconeogenesis” (8 species) (Fig. 7C, Table S10). In addition, KEGG enrichment analysis revealed significant enrichment in pathways such as photosynthesis-antenna proteins, phenylpropanoid biosynthesis, and carbon fixation in photosynthetic organisms (Fig. 7C, Table S10). This indicates that H. persicum responds to long-term drought by increased expression of proteins related to carbohydrates and secondary metabolites, while the high expression of proteins related to photosynthesis represents the response to cell damage caused by drought. The down-regulated DEPs are primarily enriched in pathways such as "tryptophan metabolism (4 types)", "glyoxylate and dicarboxylate metabolism (5 types)", and "carbon metabolism (11 types)". (Fig. 7D, Table S10). The changes in the expression and quantity of DEPs indicate that plants are undergoing positive and complex responses to counteract adverse external environmental changes.

PPI network analysis of DEPs

A protein–protein interaction network analysis was performed using a confidence level (score ≥ 0.5) to determine the interactions between specific DEPs in H. ammodendron and H. persicum. Five major interacting proteomes were identified in the protein interaction network of H. ammodendron, including 13 DEPs (Fig. S1, Table S11). Most of the proteins in these five clusters were down-regulated, and their functions were related to carbohydrate transport and metabolism (e.g., purple acid phosphatase and pyruvate kinase), amino acid transport and metabolism (Xaa-Pro aminopeptidase, alanine-glyoxylate aminotransferase AGT2), antioxidant and defense (aldehyde dehydrogenase, monodehydroascorbate reductase), energy production and conversion (NADH-ubiquinone oxidoreductase), lipid transport and metabolism (Acyl-CoA synthase), and translation, ribosomal structure and biogenesis (elongation factor Ts, large subunit ribosomal protein L3e. Based on the interaction network, the top ten protein nodes were screened using the CytoHubba plugin (Fig. 8). Xaa-Pro aminopeptidase, aldehyde dehydrogenase (ALDH), and monodehydroascorbate reductase (MDHAR) were ranked as the top three most important proteins.

Fig. 8.

Fig. 8

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PPI network analysis of DEPs in H. ammodendron. In the interaction network, each node represents a protein, with its degree indicating the number of edges directly connected to it. The size of a node signifies the number of interacting proteins; the larger the node and the darker its color, the stronger the interaction between the two proteins

Among the 348 DEPs in H. persicum, 132 (76 up-regulated and 56 down-regulated) formed an interaction network (Fig. S2, Table S12). The top 58 protein nodes were screened using the CytoHubba plugin (Fig. 9). The DEPs (17 protein nodes) that interact with urease involved in arginine biosynthesis were the most common. Next was Lysyl-tRNA synthetase (class II) involved in aminoacyl-tRNA biosynthesis, ALDH for antioxidant functions and defense, Xaa-Pro aminopeptidase and glutamine synthetase for amino acid transport and metabolism, elongation factor Tu for translation, ribosomal structure and biogenesis, and heat shock 70 kDa protein involved in posttranslational modification, protein turnover, and chaperones, with 12 protein nodes. These proteins may play key roles in the drought tolerance of H. persicum.

Fig. 9.

Fig. 9

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PPI network analysis of DEPs in H. persicum. In the interaction network, each node represents a protein, with its degree indicating the number of edges directly connected to it. The size of a node signifies the number of interacting proteins; the larger the node and the darker its color, the stronger the interaction between the two proteins

Screening of key drought-tolerant proteins in H. ammodendron and H. persicum

Significant differences in entries or pathways between H. ammodendron and H. persicum were analyzed based on the GO and KEGG enrichment analysis results. Then, repeated proteins with more than one connection point were selected from the control group to further screen for key drought-tolerance proteins. A total of 17 candidate proteins (six up-regulated and 11 down-regulated) were screened from H. ammodendron, and these were involved in energy production and transformation, amino acid transport and metabolism, lipid transport and metabolism, carbohydrate transport and metabolism, translation, ribosome structure and biogenesis, and ROS clearance processes (Table S13). A total of 110 drought-tolerance candidate key proteins (73 up-regulated and 37 down-regulated) were screened from the H. persicum, among which proteins involved in signal transduction, carbohydrate transport and metabolism, lipid transport and metabolism, amino acid transport and metabolism, energy production and transformation, inorganic ion transport and metabolism, coenzyme transport and metabolism and transcription and translation processes were overexpressed (Table S14).

Discussion

Based on the proteomic analysis, 71 differentially expressed proteins (34 up-regulated and 37 down-regulated) related to drought tolerance were identified in H. ammodendron and 348 differentially expressed proteins (186 up-regulated and 162 down-regulated) in H. persicum. There were significant differences in the number, expression patterns (up-regulation/down-regulation), and magnitude of changes in drought tolerance-related proteins between the two species. Proteins related to carbohydrate metabolism and uncharacterized proteins in H. ammodendron were up-regulated, while proteins related to carbohydrate metabolism, photosynthesis, amino acid metabolism, secondary metabolism, and antioxidant defense were up-regulated in H. persicum. One possible explanation is that H. ammodendron may have a higher initial osmotic potential that allows the species to maintain cellular functions for longer periods under drought conditions before needing to respond [54]. In contrast, H. persicum is more severely limited by water and has a higher ability to respond to drought. The observed changes are discussed under the main functional categories reflecting metabolism (Tables S15, S16).

Proteins related to the regulation of gene expression

The structural changes in plant genomes are occasionally induced by transposable elements (TE) activated by environmental stresses [16]. Its expression is induced in drought-tolerant barley exposed to drought conditions, leading to different levels of DNA methylation in drought-sensitive and drought-tolerant cultivars [32]. Therefore, the activation of Tam3-transportase is one of the mechanisms for achieving self-protection and self-repair in H. ammodendron. This also stimulates the expression of other genes responsible for stress response [19]. The inconsistent changes in the abundance of two Tam3-transportases in H. persicum indicate that the regulatory mechanism of H. persicum in maintaining genome integrity and stability is more complex.

Research has shown that histone deacetylation promotes gene expression and further affects plant morphology, development, and stress resistance [84]. In this study, the abundance of transcription-related histones and histone deacetylase complex subunits in H. persicum were decreased, indicating that an increase in histone content and a decrease in histone deacetylation are a means of inhibiting the expression of certain genes under drought stress. However, the target genes regulated in this way remain unclear.

The diversity of mRNA decay pathways in eukaryotes highlights the importance of ineffective transcripts as a mechanism to ensure correct gene expression and prevent the accumulation of abnormal mRNAs [10]. The mRNA-decapping enhancer (EDC) protein has been identified as an enhancer for decapping reactions and is a key control point for the main decay pathway of mRNA [50]. In arid environments, the up-regulation of enhancer of mRNA-degrading protein 4 (OsEDC4) regulates the degradation of ineffective or abnormal mRNAs in H. ammodendron, thereby enhancing its drought tolerance. OsEDC4 and CCR4-NOT transcription complex subunit 2, which catalyze deacetylation, were downregulated in H. persicum, but the up-regulation of RNA binding proteins (RNA-binding protein Sam68 and related KH domain proteins) and RNA helicase (ATP-dependent RNA helicase) to some extent prevents incorrect folding of RNA molecules.

Proteins related to protein synthesis and turnover

Protein synthesis and turnover are fundamental metabolic processes in plants for coping with drought stress [75, 78]. DEPs related to protein biosynthesis include various ribosomal proteins, elongation factors, and tRNA-synthetases. The abundance of these proteins decreased under drought stress. This means that protein synthesis in both H. ammodendron and H. persicum was weakened, suggesting that the plants attempt to conserve energy and shift from a growth mechanism to a protective mechanism [20]. Meanwhile, the companion protein (DnaJ homologous subfamily A member 2), which is associated with correct protein folding in H. ammodendron, plays an important role in maintaining protein stability and repairing damaged proteins [29]. The results indicate that the integrity of the protein structure is necessary for enhancing the drought tolerance of H. ammodendron.

When plants are subjected to drought stress, protein degradation is normally enhanced [59]. Most proteins related to protein degradation in H. persicum such as Proteinase inhibitor I3 (FC = 17.96) were up-regulated. This is consistent with the findings of protein expression research on Hippophae rhamnoides under drought stress [22]. This may help hydrolyze proteins damaged during drought stress to release their amino acids for reuse. Eukaryotic translation initiation factor 2 (eIF2) plays an important role in regulating mRNA translation and the production of specific proteins [65]. Extension factor promotes the movement of the ribosome toward the 3' end of the mRNA [80], and it works in synergy with ribosome recycling factor (RRF) to recover ribosomes, an important factor in the synthesis of new proteins [75, 78]. The eukaryotic translation initiation factor 2C (FC = 3.47) and elongation factor Tu (FC = 4.32) in H. persicum were significantly increased, indicating that the amino acids released by proteases may be reused for new protein synthesis.

Proteins associated with the cell cycle and programmed cell death

The cytoskeleton is crucial for maintaining the morphology and internal structure of eukaryotic cells, and it is closely related to material transport and cellular structure [23]. Actin is a component of the cytoskeleton system that allows for cellular movement and processes [57]. Up-regulation of actin and related proteins helps maintain the cell structure of H. persicum in arid environments. Plants respond to abiotic stress by altering intracellular molecular pathways through real-time regulation of the cell cycle [56]. Cyclin-dependent kinases (CDKs) control the transitions through cell cycle stages [56]. The S-M checkpoint control protein CID1 plays an important role in cell cycle regulation, as it is involved in monitoring the status and integrity of DNA replication [77]. The increase in CDK2 activity and the decrease in CID1 activity indicate that to maintain life activities, H. persicum must balance the inhibitory effects caused by drought stress with cell cycle control and adaptation to dynamic environmental conditions. In addition, the levels of apoptosis-related proteins such as Apoptotic ATPase were decreased in both species, possibly due to drought stress reducing the clearance of damaged cells in both species.

Drought-responsive proteins related to signal transduction

Under stress conditions, the first response of plants is to activate various signaling pathways [62]. GTP binding proteins, also known as G proteins, are important signaling molecules in eukaryotes [13]. The AIG1 guanine nucleotide-binding (G) domain is an important component of the G protein-coupled receptor (GPCR) signaling pathway [97]. The upregulation of the AIG1 guanine nucleotide-binding (G) domain activates the G protein, thereby prompting H. ammodendron to initiate multiple signaling pathways in response to drought environments.

Jasmonic acid (JA) is an endogenous signaling molecule involved in multiple developmental processes and is closely related to plant resistance to abiotic stress [74]. Research has shown that JA effectively enhances plant drought tolerance by increasing organic osmotic protectants and antioxidant enzyme activity [66]. 12-oxophytic acid reductase (OPR) is a key enzyme in the biosynthesis of JA [2]. Therefore, up-regulation of OPR increases the synthesis of JA in H. persicum, serving as a messenger molecule to coordinate various physiological activities during drought stress. Ca2+ plays an important role as a second messenger in various signaling pathways [5]. Therefore, the up-regulation of proteins related to the Ca2+ signaling pathway activates Ca2+ signal sensing proteins (calmodulin-binding protein60, EF-hand domain, Ca2+/calmodulin-dependent protein phosphatase and IQ motif) and transduces specific Ca2+ signals to appropriate effectors in response to drought.

Regulation of photosynthesis-related proteins in arid environments

The photosynthesis of plants, including the light response (light dependence) and dark response (carbon fixation), is typically inhibited under drought stress [75, 78]. In physiological responses, the net photosynthetic rate (Pn), intercellular carbon dioxide concentration (Ci), transpiration rate (Tr), and stomatal conductance (Gs) of H. ammodendron were significantly inhibited by drought stress (Fig. S3, Table S17). Consistent with these physiological responses, drought stress significantly decreased ATPase activity in H. ammodendron. ATPase is a key enzyme in photophosphorylation and plays an important role in the energy conversion process of photosynthesis [33]. This indicates that drought stress inhibits the energy conversion process during the photosynthesis of H. ammodendron, leading to a setback in photosynthesis. This finding aligns with previous research results [69].

In physiological response, drought stress had no significant effect on the photosynthesis of H. persicum (Fig. S3). At the molecular level, H. persicum resists light damage through an active repair mechanism. Among them, the upregulation of four light-harvesting chlorophyll a/b-binding (LHCB) proteins converts excess light energy into heat (non-photochemical quenching), thereby reducing the excitation pressure on photosystem II (PSII). Simultaneously, the upregulation of three phytocyanin domain proteins accelerates electron transfer and hinders the formation of free radical chains [9]. The 22 kDa protein of photosystem II protects the oxygen-evolving complex and maintains its water-splitting function,Photosystem I subunit IV promotes Fe-S cluster repair and prevents oxidative damage caused by electron accumulation [40]. In addition, under arid conditions, the expression of phosphoenolpyruvate carboxylase (PEPC), pyruvate phosphate dikinase (PPDK), and NADP+-dependent malic enzyme (NADP-ME), which are involved in the carbon fixation process in H. persicum, is up-regulated. Up-regulation of PEPC, PPDK, and NADP-ME activates the Hatch-Slack pathway of C4 photosynthesis. Concentrated CO₂ inhibits the oxygenation activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), reducing hydrogen peroxide (H₂O₂) produced by photorespiration. Simultaneously, it maintains the Calvin cycle electron flow and prevents excessive photosynthesis (Veronika et al. 2014). This indicates that under drought conditions, H. persicum achieves active repair of photodamage at the molecular level through a three-tiered defense network consisting of light energy allocation optimization (LHCB), photosystem repair enhancement (PS subunit), and metabolic pathway activation (C4 enzyme), without significant fluctuations in physiological photosynthetic efficiency. This "invisible repair" strategy may be a key mechanism for its adaptation to extreme arid habitats.

Proteins related to carbohydrate and energy metabolism

Under drought stress, the growth and development of plants require large amounts of energy [94]. This energy is produced through carbohydrate metabolism such as glycolysis and the tricarboxylic acid (TCA) cycle [24]. In this study, most of the proteins related to carbohydrate metabolism in H. ammodendron were up-regulated. Among them, pyruvate kinase (PK) participates in the final step of glycolysis (the second ATP generation step of glycolysis) and plays a crucial role in energy production and controlling glycolysis in response to ATP demand [43]. Therefore, an increase in its abundance may be necessary for the enhancement and reduction of ATP by H. ammodendron.

Chitinase (Chi), a glycoside hydrolase capable of hydrolyzing the natural polymer chitin, participates in chitin degradation during biotic stress and is up-regulated in response to drought. Research has shown that under drought conditions, Chi transcripts and proteins are increased [91], and they are unique to drought-tolerant species [48]. In addition, Chi plays a key role in alleviating oxidative stress by directly interacting with reactive oxygen species (ROS) and neutralizing superoxide radicals (O2−) and hydrogen peroxide (H2O2), effectively clearing ROS [72]. The dual function of Chi may be the key to the long-term drought tolerance of H. ammodendron.

In H. persicum, most of the proteins involved in carbohydrate metabolism were up-regulated, while most of the proteins related to energy metabolism were down-regulated. Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and enolase (ENO)are key enzymes in the sugar degradation pathway, and GAPDH converts 3-phosphoglyceraldehyde to 1,3-diphosphoglycerate, a reaction that helps to break down glucose to produce energy [25]. Consistent with previous research findings, the overexpression of GAPDH and ENO indicates that plants enhance their glycolysis rate and generate more energy in response to drought stress [9]. This may be one of the natural mechanisms by which H. persicum adapts to long-term drought conditions.

The proteins involved in the energy metabolism of H. persicum included H+-ATPases, and most were down-regulated in expression. The decrease in protein abundance may be a mechanism by which H. persicum accumulates sugar metabolism related proteins (GAPDH, ENO, β-glucosidase, sucrose synthase and UDP-xylose/xylose synthase) as an additional source of energy [38].

Proteins involved in amino acid biosynthesis and nitrogen metabolism

Amino acids act as intermediates of final metabolites in several metabolic pathways and participate in the regulation of multiple metabolic pathways and physiological activities [35, 41]. Alanine aminotransferase (AlaAT) catalyzes the reversible reaction of alanine and 2-oxoglutarate to pyruvate and glutamate. This pyridoxal phosphate-dependent enzyme plays a critical role in plant metabolism by linking primary carbon metabolism with amino acid synthesis [37]. At present, the regulation of AlaAT activity in plants has only been studied under the stresses of hypoxia and nitrogen deficiency. AlaAT is involved in the degradation of alanine after hypoxia stress relief [52]. Low nitrogen-induced overexpression of AlaAT increases the efficiency of nitrogen assimilation [18, 64]. Therefore, for wild-type H. ammodendron, down-regulation of alanine-xylate aminotransferase AGT2 activity inhibits the synthesis of pyruvate but can promote its synthesis through glycolysis pathway; this may be a special growth regulation strategy for drought resistance in the long-term evolution of H. ammodendron.

Xaa-Pro aminopeptidase (PAP) is an N-terminal exopeptidase that specifically catalyzes the cleavage of proline or hydroxyproline from the N-termini of peptides [44]. Research has shown that AtPAP1 increases the activity of PAP, thereby increasing the accumulation of free proline in plant cells and positively controlling plant tolerance to salt and drought stress [68]. The main biological functions of proline include osmotic regulation, regulation of nitrogen and energy metabolism, and protection of the cell membrane system in plant cells [58]. In this study, PAP activity was reduced in H. ammodendron and overexpressed in H. persicum. A possible reason may be that the overexpression of PAP in H. persicum increased the content of free proline, thereby improving osmotic regulation and energy metabolism to protect cells from drought stress; although both H. ammodendron and H. persicum belong to the genus Haloxylon, they may have different regulatory strategies in response to drought stress. In addition, ferredoxin-nitrite reductase (NiR, FC = 8.60) and glutamine synthetase (GS, FC = 6.36) are key enzymes in the natural nitrogen cycle [42]. NiR can degrade nitrite into NO or NH3, which are then assimilated into amino acids by GS and glutamate synthase [34, 53]. Therefore, the overexpression of NiR and GS significantly enhances nitrogen assimilation in H. persicum, thereby regulating its growth and development to adapt to long-term drought. This finding aligns with previous research results [1].

Proteins related to lipid metabolism and secondary metabolism

Lipids have multiple functions in plant tissues, including components of cell membranes, storage molecules for metabolic energy, and signaling factors in response to stressors [67, 93]. Changes in lipid biosynthesis, biofilm rearrangement, and specific fatty acid changes can reduce the damage to cell membranes caused by abiotic stress [11]. In this study, Lipoxygenase (LOX), which is only involved in linoleic acid metabolism, and Hydroxyindole-O-methyltransferase and related SAM-dependent methyltransferases (HIOMT), which are involved in melatonin biosynthesis, were up-regulated among the seven DEPs related to lipid metabolism and secondary metabolism in H. ammodendron. LOX is a non-heme iron dioxygenase that catalyzes the conversion of polyunsaturated fatty acids (linoleic acid and linolenic acid) into hydroperoxide fatty acids that participate in the formation of stress-related plant growth regulators such as JA and methyl jasmonate (MeJA) [6]. Melatonin is a tryptophan-derived molecule with pleiotropic activity [27]. It can regulate plant growth and development, improve plant stress resistance, maintain cell membrane integrity, prevent chlorophyll degradation, and regulate plant circadian rhythms and photoperiod [49]. Melatonin is involved in the final step in HIOMT-catalyzed melatonin synthesis [27]. Therefore, the metabolism of linoleic acid and the pleiotropic activity of melatonin may coordinate various physiological activities to help H. ammodendron adapt to long-term drought environments.

Glycerophoryl diester phosphodiesterase (GDPD) is a key enzyme in the phospholipid metabolism pathway of organisms, playing an important role in maintaining lipid remodeling [73, 76]. Research has shown that phosphatid dicylglycerol acyltransferase (PDAT) plays a critical physiological role in transferring fatty acids from membrane lipids to beta oxidation, thereby maintaining membrane lipid homeostasis in Arabidopsis leaves [14, 85]. Therefore, the overexpression of GDPD and PDAT plays a crucial role in maintaining phospholipid remodeling in H. persicum to adapt to arid environments. This also partly explains the absence of significant changes in malondialdehyde (MDA) content (Fig. S4A, Table S17).

The synthesis and accumulation of secondary metabolites in plants are the result of long-term natural selection directed by environmental conditions [92]. Specific ecological conditions have been selected for unique physiological and biochemical mechanisms in plants [28]. Plant terpenoids are a diverse class of natural products, and their synthesis in plants may involve isoprene end-to-end or isoprene ring formation [45, 47, 60]. Isoprene is the most abundant volatile organic compound (VOC) emitted by terrestrial plants and is an important molecule for ameliorating abiotic stress [15, 61]. Isoprene synthase (ISPS) relies on the methylerythritol-4-phosphate (MEP) pathway to catalyze the synthesis of isoprene from dimethylally diphosphate (DMADP) [7, 15]. Triterpenoids are rich in the epidermal layer of stems and leaves, and they can help prevent dehydration [30, 70]. Research has demonstrated a positive correlation between beta-amyloid synthase (β-AS) activity and triterpenoid saponin biosynthesis, and upregulation of β-AS activity contributes to the high-level accumulation of soybean saponins [21]. Therefore, the increased activities of ISPS and β-AS may promote the biosynthesis of triterpenoid ring structures in H. persicum, prevent leaf dehydration, and confer potential resistance to drought conditions.

Proteins related to antioxidant and defense responses

Reactive oxygen species (ROS) are byproducts of aerobic metabolism in plant cells [71]. Drought stress is believed to accelerate the accumulation of ROS in plant cells, ultimately leading to cell damage [4]. Therefore, it is necessary to actively control ROS levels to protect plants from drought-induced oxidative stress. In physiological responses, the ROS metabolite (H2O2) in H. ammodendron significantly increased (Fig. S4B, Table S17), accompanied by an increase in peroxidase (POD) activity in response to drought (Fig. S5A, Table S17). At the molecular level, only the expression abundance of Monodehydroascorbate (MDHAR) increased in H. ammodendron. MDHAR participates in the ascorbate–glutathione cycle (AsA-GSH), reducing monodehydroascorbic acid to ascorbic acid, thereby maintaining cellular antioxidant capacity [51]. This indicates that H. ammodendron catalyzes the decomposition of H2O2 via POD, while MDHAR is involved in the regeneration of ascorbic acid. The two enzymes work synergistically to effectively reduce ROS levels and protect cells from oxidative stress damage.

Under drought stress, there is a certain accumulation of H2O2 content in H. persicum, but it is not significant (Fig. S4A, Table S17). The activities of POD, superoxide dismutase (SOD), and catalase (CAT) decreased (Fig. S5, Table S17). Contrary to physiological responses, most proteins related to antioxidant defense in H. persicum were upregulated, including CAT, POD, as well as L-ascorbate peroxidase (APX), glutathione peroxidase (GPX), and glutathione S-transferase (GST) involved in the AsA-GSH pathway. This indicates that H. persicum compensates for the decrease in antioxidant enzyme activity by encoding antioxidant-related proteins.

Other functional categories and uncharacterized proteins

In this study, there were 21 uncharacterized proteins in H. ammodendron and 56 in H. persicum. Although there were many changes in the expression levels of these proteins, it is difficult to draw firm conclusions. The exact functions of these proteins in combating drought remain unclear. Future functional studies on uncharacterized proteins will further deepen our understanding of the drought tolerance of H. ammodendron and H. persicum and contribute to the development of drought-tolerant crops.

Conclusions

This study elucidated the molecular mechanisms underlying long-term drought tolerance in typical desert plants (H. ammodendron and H. persicum) at the protein level. It addressed the deficiencies in previous research. The findings reveal that H. ammodendron and H. persicum might employ distinct mechanisms to cope with the adverse effects of drought. H. ammodendron primarily responds to drought by enhancing energy production and maintaining genomic integrity, whereas H. persicum appears to perceive limited soil water availability through mechanisms associated with up-regulation of protein expression. This involves enhancing photosynthesis, ROS clearance, and osmotic regulation to bolster drought tolerance. Both species demonstrate unique adaptation strategies to drought, yet further research is warranted to fully understand their drought tolerance mechanisms. The identification of key drought-tolerant proteins can provide regulatory targets for future functional validation of proteins.

Supplementary Information

Supplementary Material 1. (1.1MB, zip)

Acknowledgements

We thank LetPub (www.letpub.com.cn) for its linguistic assistance during the preparation of this manuscript.

Authors’ contributions

F.Y., X.D. and G.L. conceived the study; F.Y. collected data, analyzed data and drafted the text; all authors edited the manuscript.

Funding

This work was supported by [National Natural Science Foundation of China (Youth Fund)] (32301307), Central Government Guides Local Special Fund Projects for Science and Technology Development (ZYYD2025ZY04) and [Natural Science Foundation of Xinjiang Uygur Autonomous Region] (2023D01C186).

Data availability

No datasets were generated or analysed during the current study.

Declarations

Ethics approval and consent to participate

The author declares that the experimental research on the plants described in this article complies with institutional, national, and international guidelines. We conducted on-site research in accordance with local laws and obtained sampling permits from relevant authorities. The collection of assimilating branches of Haloxylon ammodendron and Haloxylon persicum was carried out with full permission from Xinjiang University. Sampling from the Ebinur Lake Wetland Nature Reserve in Jinghe County, Xinjiang.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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Supplementary Materials

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