Studying Salt-Induced Shifts in Gene Expression Patterns of Glucosinolate Transporters and Glucosinolate Accumulation in Two Contrasting Brassica Species
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material and Growth Conditions
2.2. Bioinformatics Analyses
2.3. Biochemical Analyses
2.3.1. Malondialdehyde (MDA) Content
2.3.2. Hydrogen Peroxide (H2O2) Content
2.3.3. Total Free Amino Acids (TFA) Content
2.3.4. Total Soluble Protein (TSP) Content
2.3.5. Phenolic Compounds
2.4. Antioxidant Assays
2.5. RNA Extraction, cDNA Synthesis and qPCR Analysis
2.6. Measurement of Seed Glucosinolates Content
2.7. Statistical Analyses
3. Results
3.1. Bioinformatics Analysis
3.1.1. Identification of GTR Genes in Brassica Complex
3.1.2. Phylogenetic Analysis of GTR Proteins in Brassica Complex
3.1.3. Intron/Exon Composition of GTR Genes
3.1.4. Domain Analysis of GTR Proteins
3.1.5. Motif Analysis of GTR Proteins
3.1.6. Cis-Regulatory Elements Analysis of GTR Genes
3.2. Effect of NaCl Stress on Different Metabolites
3.3. Effect of NaCl on Enzymatic Antioxidant Activities
3.4. Effect of NaCl on Selected GTR Genes in Different Tissues
3.5. Determining the Effect of GTR Gene Expression on the Loading of Glucosinolates into the Seed
3.6. Predicting the Effect of NaCl Stress on Glucosinolates Content of B. napus and B. juncea
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Similarity (%) | |||||||||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
AtGTR1 | AtGTR2 | BnaGTR1A1 | BnaGTR1A2 | BnaGTR1A3 | BnaGTR1C1 | BnaGTR1C2 | BnaGTR1C3 | BnaGTR2A1 | BnaGTR2A2 | BnaGTR2A3 | BnaGTR2C1 | BnaGTR2C2 | BnaGTR2C3 | BjuGTR1A1 | BjuGTR1A2 | BjuGTR1A3 | BjuGTR1B1 | BjuGTR1B2 | BjuGTR1B3 | BjuGTR2A1 | BjuGTR2A2 | BjuGTR2A3 | BjuGTR2B1 | BjuGTR2B2 | BjuGTR2B3 | ||
Divergence (%) | AtGTR1 | 81.4 | 86.4 | 85.1 | 80.7 | 86.3 | 85.1 | 80.4 | 81.2 | 78.2 | 77.9 | 81.1 | 81.2 | 77.7 | 86.4 | 85.3 | 83.1 | 86.3 | 85.6 | 83.2 | 81.2 | 81.2 | 77.9 | 81.2 | 80.9 | 78.5 | |
AtGTR2 | 18.2 | 79.2 | 79.7 | 77.0 | 79.0 | 79.8 | 77.0 | 92.5 | 92.2 | 85.5 | 92.3 | 92.2 | 85.4 | 79.2 | 80.3 | 77.1 | 78.5 | 79.7 | 77.9 | 92.5 | 92.2 | 85.0 | 92.7 | 92.2 | 86.1 | ||
BnaGTR1A1 | 12.9 | 19.6 | 89.7 | 88.0 | 99.2 | 89.9 | 87.7 | 80.3 | 79.8 | 77.2 | 80.2 | 79.8 | 78.3 | 99.8 | 90.2 | 88.4 | 96.9 | 89.9 | 88.4 | 80.5 | 79.8 | 77.5 | 80.0 | 80.0 | 78.3 | ||
BnaGTR1A2 | 14.3 | 18.4 | 7.7 | 85.4 | 89.4 | 98.6 | 85.2 | 81.0 | 79.8 | 77.3 | 80.8 | 79.8 | 76.9 | 89.7 | 99.2 | 85.4 | 89.0 | 96.4 | 87.2 | 81.0 | 79.8 | 77.3 | 80.8 | 79.7 | 77.3 | ||
BnaGTR1A3 | 17.3 | 21.8 | 10.3 | 12.0 | 87.9 | 85.5 | 97.5 | 77.5 | 77.8 | 74.0 | 77.3 | 77.8 | 74.5 | 88.0 | 85.4 | 99.7 | 88.9 | 85.4 | 94.5 | 77.6 | 77.8 | 75.3 | 77.1 | 77.5 | 74.8 | ||
BnaGTR1C1 | 13.4 | 20.1 | 0.4 | 8.2 | 10.7 | 89.5 | 87.4 | 80.2 | 79.7 | 76.9 | 80.0 | 79.7 | 77.2 | 99.4 | 89.9 | 88.2 | 96.8 | 89.5 | 88.2 | 80.3 | 79.7 | 77.3 | 79.8 | 79.8 | 78.2 | ||
BnaGTR1C2 | 14.5 | 18.4 | 7.7 | 1.2 | 12.0 | 8.2 | 85.4 | 81.0 | 79.8 | 77.1 | 80.8 | 79.8 | 76.9 | 89.9 | 98.9 | 85.5 | 89.2 | 98.9 | 87.2 | 81.0 | 79.8 | 77.3 | 80.8 | 79.7 | 77.3 | ||
BnaGTR1C3 | 17.5 | 22.0 | 10.7 | 12.5 | 2.0 | 11.2 | 12.5 | 77.3 | 77.8 | 73.5 | 77.1 | 77.8 | 74.2 | 87.7 | 85.7 | 97.9 | 88.4 | 85.5 | 94.3 | 77.5 | 77.8 | 74.5 | 77.0 | 77.5 | 74.3 | ||
BnaGTR2A1 | 18.0 | 6.7 | 17.7 | 17.0 | 21.1 | 18.2 | 17.0 | 21.5 | 94.8 | 88.4 | 99.8 | 94.8 | 88.2 | 80.3 | 81.3 | 77.6 | 79.5 | 81.6 | 78.4 | 99.8 | 94.8 | 86.9 | 99.8 | 94.6 | 89.9 | ||
BnaGTR2A2 | 18.4 | 7.3 | 18.7 | 19.4 | 21.3 | 19.1 | 19.1 | 21.5 | 4.0 | 87.9 | 94.6 | 89.4 | 81.2 | 81.0 | 80.2 | 78.0 | 79.3 | 79.8 | 77.8 | 94.8 | 99.8 | 87.9 | 94.6 | 97.9 | 86.9 | ||
BnaGTR2A3 | 23.0 | 13.8 | 22.5 | 21.8 | 25.5 | 22.8 | 21.8 | 26.3 | 11.2 | 11.0 | 88.2 | 87.9 | 97.7 | 77.2 | 77.4 | 74.2 | 76.6 | 77.9 | 74.9 | 88.6 | 87.9 | 96.2 | 88.4 | 88.1 | 94.1 | ||
BnaGTR2C1 | 18.2 | 6.9 | 18.0 | 17.3 | 21.3 | 18.4 | 17.3 | 21.8 | 0.2 | 4.2 | 11.4 | 94.6 | 88.1 | 80.2 | 81.2 | 77.5 | 79.3 | 81.5 | 78.2 | 99.8 | 94.6 | 86.7 | 97.9 | 94.4 | 89.8 | ||
BnaGTR2C2 | 18.7 | 7.3 | 18.9 | 19.4 | 21.3 | 19.4 | 19.1 | 21.5 | 4.0 | 0.2 | 11.0 | 4.2 | 87.7 | 79.8 | 80.2 | 78.0 | 79.3 | 81.0 | 78.2 | 94.8 | 89.4 | 86.9 | 94.2 | 97.7 | 89.4 | ||
BnaGTR2C3 | 22.5 | 13.8 | 22.0 | 22.0 | 24.7 | 22.3 | 22.0 | 25.2 | 11.6 | 11.2 | 2.0 | 11.8 | 11.2 | 77.5 | 77.2 | 74.7 | 76.9 | 78.0 | 75.7 | 88.4 | 87.7 | 95.8 | 88.1 | 87.9 | 94.6 | ||
BjuGTR1A1 | 12.9 | 19.6 | 0.0 | 7.7 | 10.3 | 0.4 | 7.7 | 10.7 | 17.7 | 18.7 | 22.5 | 18.0 | 18.9 | 22.0 | 90.2 | 88.4 | 97.1 | 89.9 | 88.4 | 80.5 | 79.8 | 77.5 | 80.0 | 80.0 | 78.3 | ||
BjuGTR1A2 | 14.1 | 18.0 | 7.5 | 0.6 | 11.8 | 7.9 | 1.0 | 12.3 | 16.8 | 18.9 | 21.3 | 17.0 | 18.9 | 21.5 | 7.5 | 85.4 | 89.5 | 96.7 | 87.7 | 81.3 | 80.2 | 77.7 | 81.2 | 80.0 | 77.7 | ||
BjuGTR1A3 | 17.0 | 21.5 | 10.1 | 11.8 | 0.2 | 10.5 | 11.8 | 1.8 | 20.8 | 21.1 | 25.2 | 21.1 | 21.1 | 24.5 | 10.1 | 11.6 | 89.2 | 85.4 | 94.8 | 77.8 | 78.0 | 75.3 | 77.3 | 77.6 | 74.9 | ||
BjuGTR1B1 | 12.9 | 19.6 | 2.4 | 8.2 | 9.4 | 2.8 | 8.2 | 9.9 | 17.7 | 18.2 | 22.5 | 18.0 | 18.4 | 22.0 | 2.4 | 7.9 | 9.2 | 89.4 | 89.2 | 79.7 | 79.3 | 77.3 | 79.2 | 79.5 | 77.5 | ||
BjuGTR1B2 | 14.1 | 19.4 | 8.2 | 3.2 | 12.5 | 8.6 | 3.4 | 12.5 | 16.6 | 18.0 | 21.1 | 16.8 | 18.0 | 20.8 | 8.2 | 3.2 | 12.3 | 8.4 | 87.4 | 81.6 | 81.0 | 77.9 | 81.6 | 81.0 | 78.3 | ||
BjuGTR1B3 | 16.1 | 20.1 | 9.6 | 10.7 | 3.8 | 10.1 | 11.0 | 4.2 | 19.4 | 20.3 | 24.2 | 19.6 | 20.3 | 23.2 | 9.6 | 10.5 | 3.6 | 8.6 | 11.0 | 78.5 | 78.2 | 76.0 | 78.2 | 78.0 | 75.7 | ||
BjuGTR2A1 | 18.0 | 6.7 | 17.7 | 17.0 | 21.1 | 18.2 | 17.0 | 21.5 | 0.0 | 4.0 | 11.2 | 0.2 | 4.0 | 11.6 | 17.7 | 16.8 | 20.8 | 17.7 | 16.6 | 19.4 | 94.8 | 86.9 | 98.0 | 94.6 | 90.1 | ||
BjuGTR2A2 | 18.4 | 7.3 | 18.7 | 19.4 | 21.3 | 19.1 | 19.1 | 21.5 | 4.0 | 0.0 | 11.0 | 4.2 | 0.2 | 11.2 | 18.7 | 18.9 | 21.1 | 18.2 | 18.0 | 20.3 | 4.0 | 86.9 | 94.6 | 97.9 | 89.4 | ||
BjuGTR2A3 | 24.7 | 16.3 | 25.0 | 24.2 | 27.3 | 25.2 | 24.2 | 28.3 | 14.1 | 13.8 | 4.0 | 14.3 | 13.8 | 4.4 | 25.0 | 23.7 | 27.3 | 25.0 | 23.5 | 26.3 | 14.1 | 13.8 | 87.3 | 87.3 | 91.7 | ||
BjuGTR2B1 | 18.0 | 6.5 | 18.4 | 17.0 | 21.5 | 18.9 | 17.0 | 22.0 | 1.6 | 4.2 | 11.0 | 1.8 | 4.2 | 11.4 | 18.4 | 16.8 | 21.3 | 18.4 | 16.6 | 19.6 | 1.6 | 4.2 | 13.6 | 94.4 | 89.6 | ||
BjuGTR2B2 | 18.4 | 7.5 | 18.2 | 19.1 | 21.1 | 18.7 | 18.9 | 21.3 | 4.8 | 1.2 | 11.0 | 5.0 | 1.4 | 11.2 | 18.2 | 18.7 | 20.8 | 17.7 | 17.5 | 19.8 | 4.8 | 1.2 | 13.6 | 5.0 | 89.4 | ||
BjuGTR2B3 | 22.5 | 12.7 | 21.8 | 22.5 | 25.2 | 22.3 | 22.5 | 25.7 | 9.4 | 9.0 | 6.1 | 9.6 | 9.0 | 5.8 | 21.8 | 22.0 | 25.0 | 22.0 | 21.3 | 24.0 | 9.4 | 9.0 | 8.8 | 9.4 | 9.4 |
Gene | Coefficients | Estimate | Standard Error | t-Value | Pr (>|t|) | Significance | Cumulative % Variance Explained |
---|---|---|---|---|---|---|---|
(Intercept) | 137.31 | 5.67 | 24.2 | 1.3 × 10−14 | *** | - | |
GTR2A21 | Stem | 21.46 | 7.84 | 2.73 | 0.0153 | * | 52.57 |
Root | 0.93 | 0.53 | 1.73 | 0.1027 | — | 60.52 | |
GTR2B1/C22 | Flower | 14.73 | 3.69 | 3.98 | 0.0010 | ** | 49.83 |
GTR2A13 | Flower | 19.01 | 8.50 | 2.23 | 0.0409 | * | 45.33 |
Root | 9.54 | 4.30 | 2.21 | 0.0425 | * | 58.82 | |
GTR1A2/B14 | Root | 2.22 | 1.00 | 2.22 | 0.0417 | * | 47.17 |
Stem | 16.59 | 7.96 | 2.08 | 0.0548 | — | 59.02 |
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Fatima, S.; Khan, M.O.; Iqbal, N.; Iqbal, M.M.; Qamar, H.; Imtiaz, M.; Hundleby, P.; Wei, Z.; Ahmad, N. Studying Salt-Induced Shifts in Gene Expression Patterns of Glucosinolate Transporters and Glucosinolate Accumulation in Two Contrasting Brassica Species. Metabolites 2024, 14, 179. https://doi.org/10.3390/metabo14040179
Fatima S, Khan MO, Iqbal N, Iqbal MM, Qamar H, Imtiaz M, Hundleby P, Wei Z, Ahmad N. Studying Salt-Induced Shifts in Gene Expression Patterns of Glucosinolate Transporters and Glucosinolate Accumulation in Two Contrasting Brassica Species. Metabolites. 2024; 14(4):179. https://doi.org/10.3390/metabo14040179
Chicago/Turabian StyleFatima, Samia, Muhammad Omar Khan, Nadia Iqbal, Muhammad Mudassar Iqbal, Huma Qamar, Muhammad Imtiaz, Penny Hundleby, Zhengyi Wei, and Niaz Ahmad. 2024. "Studying Salt-Induced Shifts in Gene Expression Patterns of Glucosinolate Transporters and Glucosinolate Accumulation in Two Contrasting Brassica Species" Metabolites 14, no. 4: 179. https://doi.org/10.3390/metabo14040179