Comparative Physiological, Biochemical, and Leaf Proteome Responses of Contrasting Wheat Varieties to Drought Stress
Abstract
:1. Introduction
2. Results
2.1. Growth and Physiological Responses of BW4074 and BW35695 Wheat Varieties towards Drought Stress
2.2. Drought Stress Increases the Levels of Photosynthetic Pigments Mainly in the Drought-Tolerant Wheat Variety
2.3. Drought Stress Induces Oxidative Stress in Wheat Tissues
2.4. Drought-Induced Accumulation of Osmoprotectants in Wheat Leaf and Root Tissues
2.5. The Drought-Tolerant Wheat Variety BW35695 Possesses Greater Antioxidant Enzyme Activities Compared to Drought-Susceptible BW4074 under Drought Stress
2.6. The Drought-Responsive Leaf Proteome of Two Contrasting Wheat Varieties
2.6.1. Drought Stress Modulates the Accumulation of Total Soluble Leaf Proteins of Wheat
2.6.2. Drought-Responsive Wheat Leaf Proteins Are Implicated in Diverse Functional Roles
Drought Stress Largely Downregulates Energy-Related Proteins, Particularly Those Associated with Photosynthesis
Drought Stress Upregulates Proteins Involved in Defense Response, Protein Homeostasis, and Transcription
Other Functional Categories of Drought-Responsive Wheat Leaf Proteins
Common Drought-Responsive Proteins between BW4074 and BW35695
2.7. Pathway Enrichment Analysis and Protein–Protein Interactions
2.7.1. KEGG Pathway Enrichment Analysis
2.7.2. Protein–Protein Interaction Analysis
2.8. Gene Expression Analysis Using qRT-PCR
3. Discussion
4. Materials and Methods
4.1. Plant Materials, Growth Conditions, and Drought Stress Treatments
4.2. Plant Growth Parameters, Relative Water Content, and Relative Shoot Water Loss Measurements
4.3. Biochemical Assays
4.3.1. Chlorophyll and Carotenoid Content
4.3.2. Lipid Peroxidation, Hydrogen Peroxide, and Superoxide Content
4.3.3. Proline and Glycine Betaine Content
4.3.4. Enzymatic Antioxidant Activity Assays
4.4. Leaf Protein Extraction, iTRAQ Labeling, LC-MS/MS, and Identification
4.4.1. Leaf Protein Extraction, iTRAQ Labeling, and Tandem Mass Spectrometry
4.4.2. Protein Identification and Quantification
4.4.3. Bioinformatics Analyses of Differentially Expressed Proteins
4.5. Gene Expression Analysis
4.6. Statistical Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Wheat Variety | Positively Identified Proteins | Drought-Responsive Proteins | Protein Regulation | |
---|---|---|---|---|
Up | Down | |||
BW4074 | 1062 | 69 | 41 | 28 |
BW35695 | 882 | 110 | 58 | 52 |
Accession a | Protein Name b | Ratio c | SD d | p-Value e | Family Name f |
---|---|---|---|---|---|
Primary Metabolism | |||||
A0A3B6QKI8 | GDSL esterase/lipase | −1.86 | 0.22 | 1.29 × 10−2 | GDSL lipase/esterase-like, plant |
A0A1D5URN5 | Fibronectin type III-LIKE domain-containing protein | −1.55 | 0.08 | 2.99 × 10−2 | Beta-D-xylosidase |
A0A077RPJ4 | Tryptophan synthase | −1.67 | 0.19 | 4.51 × 10−2 | Tryptophan synthase, alpha chain |
Q45NB2 | Glutamine synthetase | −1.68 | 0.26 | 3.75 × 10−2 | Glutamine synthetase |
A0A3B6FGE7 | Enoyl reductase (ER) domain-containing protein | 1.89 | 0.41 | 2.32 × 10−2 | Medium-chain dehydrogenase/ reductase |
A0A3B6DHI0 | Glutamate dehydrogenase | −2.08 | 0.19 | 4.52 × 10−2 | Glutamate dehydrogenase |
W5ACM8 | Delta-1-pyrroline-5-carboxylate synthase | 1.52 | 0.24 | 3.17 × 10−2 | Delta-l-pyrroline-5-carboxylate synthetase |
A0A3B6MSL2 | Aminocyclopropanecarboxylate oxidase | 1.58 | 0.36 | 2.09 × 10−2 | Plant 2-oxoglutarate-dependent oxidoreductases |
Protein synthesis/folding/degradation | |||||
W5I1R7 | 30S ribosomal protein S3, chloroplastic | 1.63 | 0.18 | 8.04 × 10−3 | Small ribosomal subunit protein uS3 |
A0A3B6TJK6 | Small ribosomal subunit protein uS10 domain-containing protein | 1.64 | 0.40 | 2.86 × 10−2 | Small ribosomal subunit protein uS10 |
W5H9B7 | Peptidyl-prolyl cis-trans isomerase | −1.57 | 0.21 | 3.52 × 10−2 | Cyclophilin-type peptidyl-prolyl cis-trans isomerase/CLD |
A0A2 × 0SLI3 | 40S ribosomal protein S6 | 1.94 | 0.33 | 4.09 × 10−2 | Small ribosomal subunit protein eS6-like |
A0A3B6QHV4 | Anion-transporting ATPase-like domain-containing protein | −1.68 | 0.25 | 2.63 × 10−2 | Arsenical pump ATPase, ArsA/GET3 |
Defense/ROS detoxification | |||||
A0A3B6HMK6 | Glutathione reductase | 1.94 | 0.66 | 4.69 × 10−2 | Glutathione reductase |
S6AWC2 | Cold induced 16 | 1.68 | 0.42 | 4.43 × 10−2 | Nodulin-related protein1/2 |
D8L9B5 | Putative PDI-like protein | −2.57 | 0.11 | 1.11 × 10−2 | Protein disulfide isomerase A6 |
Energy | |||||
A0A3B5Z298 | Phosphoglycerate kinase | −1.51 | 0.22 | 4.29 × 10−2 | Phosphoglycerate kinase family |
A0A3B6FUA0 | Fructose-bisphosphate aldolase | 1.71 | 0.27 | 2.64 × 10−3 | Fructose-bisphosphate aldolase, class I |
A0A3B6TBB9 | Ferredoxin--NADP reductase, chloroplastic | −2.02 | 0.31 | 1.77 × 10−2 | Ferredoxin-NADP reductase |
A0A3B6KSW8 | Glyceraldehyde-3-phosphate dehydrogenase | −1.68 | 0.18 | 4.84 × 10−2 | Glyceraldehyde-3-phosphate dehydrogenase, type 1 |
A0A3B6BY66 | Dihydrolipoyllysine-residue succinyltransferase | −1.61 | 0.18 | 3.67 × 10−2 | Dihydrolipoamide succinyltransferase |
A0A3B6BZB5 | Transketolase | −1.88 | 0.04 | 1.89 × 10−2 | Transketolase, bacterial-like |
Transcription | |||||
A0A3B6LV22 | H15 domain-containing protein | 1.50 | 0.19 | 4.14 × 10−3 | Linker histone H1/H5 |
A0A3B6A3G3 | Hyaluronan/mRNA-binding protein domain-containing protein | 1.99 | 0.59 | 2.54 × 10−2 | RNA binding protein HABP4/SERBP1-like |
Secondary metabolism | |||||
A0A3B6C785 | Zeta-carotene desaturase | −1.50 | 0.18 | 4.20 × 10−2 | Zeta-carotene desaturase |
A0A3B6DPV0 | AB hydrolase-1 domain-containing protein | −1.78 | 0.07 | 3.66 × 10−2 | Epoxide hydrolase-like |
Cell structure | |||||
A0A3B6SEK0 | Cyanobacterial aminoacyl-tRNA synthetase CAAD domain-containing protein | −1.87 | 0.19 | 2.29 × 10−2 | Protein curvature thylakoid I |
Unclear classification | |||||
A0A3B6FKP0 | PH domain-containing protein | 1.71 | 0.34 | 7.96 × 10−3 | Ricin B-like lectin EULS3-like |
A0A3B5XZW3 | Remorin C-terminal domain-containing protein | −1.65 | 0.02 | 1.98 × 10−2 | None predicted |
Accession a | Protein Name b | Ratio c | SD d | p-Value e | Family Name f |
---|---|---|---|---|---|
Primary Metabolism | |||||
A0A3B6UC94 | Acid phosphatase | 2.05 | 0.28 | 5.05 × 10−4 | Acid phosphatase, plant |
A0A3B6FKL0 | Nucleoside phosphorylase domain-containing protein | 1.66 | 0.27 | 3.78 × 10−3 | Phosphorylase superfamily |
A0A3B6B442 | Aspartate/glutamate/uridylate kinase domain-containing protein | −1.92 | 0.34 | 4.08 × 10−2 | Glutamate/acetylglutamate kinase |
A0A3B6TUD9 | Thiamine thiazole synthase, chloroplastic | −1.74 | 0.13 | 3.42 × 10−2 | Thiamine thiazole synthase |
A0A3B6NHD8 | O-methyltransferase ZRP4 | 1.56 | 0.41 | 3.89 × 10−2 | O-methyltransferase COMT-type |
A0A3B5ZXG4 | Glycosyltransferase | −1.50 | 0.12 | 2.23 × 10−2 | UDP-glucuronosyl/UDP-glucosyltransferase |
A0A3B6MS26 | Glucose-6-phosphate 1-epimerase | −2.37 | 0.15 | 1.86 × 10−3 | Glucose-6-phosphate 1-epimerase |
A0A3B6KPK9 | Beta-glucosidase | 2.27 | 0.88 | 4.53 × 10−2 | Cellulase degradation glycosyl hydrolase 3 |
Energy | |||||
P24065 | Photosystem II CP47 reaction center protein | −2.02 | 0.12 | 1.01 × 10−2 | Photosystem II CP47 reaction centre protein |
A0A3B6AYY2 | 23 kDa subunit of oxygen evolving system of photosystem II | 1.56 | 0.35 | 4.27 × 10−2 | PsbP |
A0A3B6N1I7 | Photosystem I reaction center subunit II, chloroplastic | −1.57 | 0.19 | 1.60 × 10−2 | Photosystem I PsaD |
A0A3B6LQN1 | Chlorophyll A-B binding protein, chloroplastic | −1.63 | 0.11 | 2.36 × 10−2 | Chlorophyll A-B binding protein |
A0A3B6JMT4 | Glyceraldehyde-3-phosphate dehydrogenase | −2.20 | 0.42 | 4.92 × 10−2 | Glyceraldehyde-3-phosphate dehydrogenase, type 1 |
W5C4P1 | Uncharacterized protein | −1.92 | 0.08 | 1.06 × 10−2 | Oxygen-evolving enhancer protein 3, plants |
W5AY52 | Chlorophyll A-B binding protein, chloroplastic | −1.67 | 0.08 | 1.53 × 10−3 | Chlorophyll A-B binding protein |
W5D4R0 | Photosystem II 22 kDa protein, chloroplastic | −1.63 | 0.13 | 5.52 × 10−3 | Chlorophyll A-B binding protein |
A0A3B6QKY1 | Aconitate hydratase | 2.05 | 0.47 | 5.72 × 10−3 | Aconitase/Iron-responsive element-binding protein 2 |
P58386 | Photosystem I P700 chlorophyll A apoprotein A2 | −2.39 | 0.09 | 2.93 × 10−3 | Photosystem I PsaB |
A0A3B6QDB2 | Photosystem II protein D1 | −1.57 | 0.14 | 2.89 × 10−2 | Photosynthetic reaction centre, L/M |
P58311 | Photosystem I P700 chlorophyll A apoprotein A1 | −2.39 | 0.04 | 9.95 × 10−3 | Photosystem I PsaA |
A0A3B6HUR4 | Chlorophyll A-B binding protein, chloroplastic | −1.91 | 0.09 | 4.14 × 10−3 | Chlorophyll A-B binding protein |
A0A3B6AWZ1 | Chlorophyll A-B binding protein, chloroplastic | −1.58 | 0.05 | 3.46 × 10−3 | Chlorophyll A-B binding protein |
W5F8Z5 | Chlorophyll A-B binding protein, chloroplastic | −1.69 | 0.07 | 1.88 × 10−4 | Chlorophyll A-B binding protein |
A0A3B5Z4J5 | ATP synthase subunit b, chloroplastic OS = Triticum aestivum | −1.55 | 0.09 | 2.09 × 10−2 | ATPase, FO complex, subunit b/b’ |
P69415 | Photosystem I iron-sulfur center | −1.65 | 0.06 | 3.97 × 10−2 | Photosystem I protein PsaC |
A0A3B6PUD8 | Photosystem II 10 kDa polypeptide, chloroplastic | −1.64 | 0.08 | 5.55 × 10−3 | Photosystem II PsbR |
F6K744 | Chlorophyll A-B binding protein, chloroplastic | −2.27 | 0.06 | 1.71 × 10−3 | Chlorophyll A-B binding protein |
A0A3B6U9Q7 | Cytochrome b/b6 C-terminal region profile domain-containing protein | −3.44 | 0.21 | 1.90 × 10−2 | Cytochrome b6/f complex, subunit IV |
Protein synthesis/folding/degradation | |||||
W5ASA4 | Uncharacterized protein | 1.61 | 0.41 | 4.51 × 10−2 | Small ribosomal subunit protein uS19 |
A0A3B6JIR3 | Heat shock cognate 70kDa protein | 1.55 | 0.34 | 4.59 × 10−2 | Heat shock protein 70 family |
A0A3B6B204 | Large ribosomal subunit protein uL23 N-terminal domain-containing protein | 1.59 | 0.16 | 5.55 × 10−4 | Large ribosomal subunit protein uL23 |
W5D739 | KOW domain-containing protein | 1.64 | 0.24 | 4.49 × 10−3 | Large ribosomal subunit protein uL24 |
A0A3B6MTE3 | Peptidylprolyl isomerase | 1.64 | 0.38 | 3.20 × 10−2 | Peptidyl-prolyl cis-trans isomerase FKBP18-like |
A0A3B6N0K3 | 50S ribosomal protein L17, chloroplastic | 1.51 | 0.21 | 3.22 × 10−3 | Large ribosomal subunit protein bL17 |
A0A3B6A2B9 | 60S ribosomal protein L37a | 2.54 | 0.42 | 9.27 × 10−3 | Large ribosomal subunit protein eL43 |
A0A3B6QGX5 | 60S ribosomal protein L6 | 1.65 | 0.29 | 4.00 × 10−2 | Large ribosomal subunit protein eL6 |
A0A3B6UD00 | 50S ribosomal protein L20 | 1.83 | 0.45 | 1.28 × 10−2 | Large ribosomal subunit protein bL20 |
Transporters | |||||
A0A3B6GKQ2 | Non-specific lipid-transfer protein | 1.71 | 0.40 | 1.31 × 10−2 | Plant non-specific lipid-transfer protein/Par allergen |
A0A3B5YX09 | Chloroplast inner envelope protein | −1.50 | 0.10 | 2.53 × 10−2 | Protein TIC110, chloroplastic |
A0A3B6I0D3 | STI1/HOP DP domain-containing protein | 1.74 | 0.39 | 1.84 × 10−2 | None predicted |
Transcription | |||||
A0A3B6LSN3 | MBD domain-containing protein | 1.52 | 0.18 | 7.18 × 10−3 | Methyl-CpG-binding domain-containing protein 10/11 |
Q8LRU5 | HMG-I/Y protein HMGa | 1.60 | 0.40 | 3.88 × 10−2 | High-mobility group protein HMGA |
A0A3B6MXZ6 | H15 domain-containing protein | 1.84 | 0.44 | 4.79 × 10−2 | Linker histone H1/H5 |
A0A3B6GNG0 | Histone H2B | 1.53 | 0.24 | 5.14 × 10−3 | Histone H2B |
Defense/ROS detoxification | |||||
A0A3B6EFA0 | Uncharacterized protein | 2.66 | 0.73 | 4.24 × 10−3 | Nodulin-related protein ½ family |
Q8W428 | Chitinase | −1.56 | 0.17 | 9.40 × 10−3 | Glycoside hydrolase, family 19 |
A0A172WCB1 | Cold-responsive LEA/RAB-related COR protein | 3.23 | 1.19 | 1.01 × 10−2 | None predicted |
A0A3B6TZ07 | GH18 domain-containing protein | 1.84 | 0.28 | 1.98 × 10−3 | Glycoside hydrolase 18 family chitinases |
A0A3B6MJX1 | Pathogen-related protein | −2.00 | 0.13 | 1.68 × 10−2 | Pathogen-related defense protein |
Secondary metabolism | |||||
A0A3B6TV37 | Amine oxidase domain-containing protein | 1.67 | 0.33 | 2.10 × 10−2 | Flavin monoamine oxidase and related enzymes |
A0A3B6QDX1 | Delta-aminolevulinic acid dehydratase | −1.59 | 0.17 | 8.35 × 10−3 | Delta-aminolevulinic acid dehydratase family |
A0A3B5Y2F9 | Dienelactone hydrolase domain-containing protein | 1.60 | 0.22 | 2.30 × 10−3 | Dienelactone hydrolase family |
Cell structure | |||||
W5FAY5 | Actin | −1.50 | 0.15 | 3.53 × 10−2 | Actin family |
Unclear classification | |||||
A0A3B6GTL4 | DJ-1/PfpI domain-containing protein | −1.79 | 0.11 | 5.38 × 10−4 | Protein/nucleic acid deglycase DJ-1 |
A0A3B6TRL4 | Thylakoid membrane protein slr0575 | −1.78 | 0.19 | 1.58 × 10−2 | Protein of unknown function DUF2854 |
A0A3B6AVR1 | Uncharacterized protein | −1.63 | 0,06 | 4.05 × 10−2 | RidA family |
A0A3B6N353 | Pentacotripeptide-repeat region of PRORP domain-containing protein | 2.10 | 0.41 | 3.42 × 10−3 | Tetratricopeptide-like helical domain superfamily |
W5CRR3 | DUF538 domain-containing protein | −2.38 | 0.13 | 1.91 × 10−3 | Protein of unknown function DUF538 |
A0A3B5ZXF0 | Protein kinase domain-containing protein | 1.92 | 0.44 | 9.42 × 10−3 | None predicted |
Accession | Protein Name | Ratio a | BW4074 vs. BW35698 Ratio p-Value b | |
---|---|---|---|---|
BW4074 | BW35698 | |||
Primary Metabolism | ||||
A0A3B6MJZ2 | 5-methyltetrahydropteroyltriglutamate-homocysteine S-methyltransferase | 1.47 | 1.37 | 3.39 × 10−1 |
A0A1D5URN5 | Fibronectin type III-like domain-containing protein | −1.55 | −1.15 | 3.30 × 10−3 * |
Protein synthesis/folding/degradation | ||||
A0A3B6TJK6 | Small ribosomal subunit protein uS10 domain-containing protein | 1.64 | 1.44 | 3.98 × 10−1 |
A0A3B6MTE3 | Peptidylprolyl isomerase | 1.28 | 1.64 | 1.28 × 10−1 |
W5D1D3 | 30S ribosomal protein S20, chloroplastic | −1.27 | 1.36 | 2.49 × 10−3 * |
Energy | ||||
A0A3B6QKY1 | Aconitate hydratase | 1.26 | 2.05 | 1.83 × 10−2 * |
P69415 | Photosystem I iron-sulfur center | −1.46 | −1.65 | 4.52 × 10−1 |
Transcription | ||||
A0A3B6LSN3 | MBD domain-containing protein | 1.36 | 1.52 | 2.86 × 10−1 |
Unclear classification | ||||
A0A3B6MQA1 | RRM domain-containing protein | 1.20 | −1.24 | 9.37 × 10−4 * |
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© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
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Moloi, S.J.; Alqarni, A.O.; Brown, A.P.; Goche, T.; Shargie, N.G.; Moloi, M.J.; Gokul, A.; Chivasa, S.; Ngara, R. Comparative Physiological, Biochemical, and Leaf Proteome Responses of Contrasting Wheat Varieties to Drought Stress. Plants 2024, 13, 2797. https://doi.org/10.3390/plants13192797
Moloi SJ, Alqarni AO, Brown AP, Goche T, Shargie NG, Moloi MJ, Gokul A, Chivasa S, Ngara R. Comparative Physiological, Biochemical, and Leaf Proteome Responses of Contrasting Wheat Varieties to Drought Stress. Plants. 2024; 13(19):2797. https://doi.org/10.3390/plants13192797
Chicago/Turabian StyleMoloi, Sellwane J., Ali O. Alqarni, Adrian P. Brown, Tatenda Goche, Nemera G. Shargie, Makoena J. Moloi, Arun Gokul, Stephen Chivasa, and Rudo Ngara. 2024. "Comparative Physiological, Biochemical, and Leaf Proteome Responses of Contrasting Wheat Varieties to Drought Stress" Plants 13, no. 19: 2797. https://doi.org/10.3390/plants13192797