Time-Course of Metabolic and Proteomic Responses to Different Nitrate/Ammonium Availabilities in Roots and Leaves of Maize
Abstract
:1. Introduction
2. Results and Discussion
2.1. Plant Growth and Metabolic Status of Roots and Leaves
2.2. Comparative Proteomic Analyses in Roots and Leaves of Maize during Exposure to Different N Sources
2.3. Proteomic Changes Involved in Nitrogen (N) Assimilation and Amino Acid Metabolism
2.4. Changes in Proteins Involved in Photosynthesis, Energy, and Carbon Metabolism
2.5. Root Proteomic Changes Involved in Cell Water Homeostasis and Cell Wall Metabolism
2.6. Proteomic Changes Related to Protein Synthesis and Folding
2.7. Stress Responses and Other Functions
3. Materials and Methods
3.1. Plant Material and Nutritional Treatments
3.2. Determination of the Contents of Nitrate, Ammonium, Amino Acids, Sucrose and Reducing Sugars
3.3. Protein Extraction, Gel Electrophoresis and in-Gel Digestion
3.4. Mass Spectrometry Analysis
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
2-ME | 2-Mercaptoethanol |
CBB | Coomassie Brilliant Blue |
DPs | Differentially abundant Proteins |
FA | Formic acid |
NUP | Number of unique peptides |
OPA | o-Phthalaldehyde |
SDS | Sodium dodecyl sulfate |
SI | Spectrum intensity |
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Condition | Time (h) | Total N Plant−1 (mg g−1 FW) | Inorganic N/Organic N Roots | Inorganic N/Organic N Leaves |
---|---|---|---|---|
0 | 3.37 ± 0.02 (a) | 0.50 ± 0.07 (bc) | 0.24 ± 0.03 (abc) | |
Nitrate (n) | 6 | 3.73 ± 0.06 (ab) | 0.80 ± 0.01 (de) | 0.23 ± 0.01 (ab) |
30 | 4.25 ± 0.10 (cd) | 1.28 ± 0.10 (f) | 0.26 ± 0.02 (bc) | |
54 | 4.38 ± 0.10 (cd) | 0.91 ± 0.07 (e) | 0.34 ± 0.01 (c) | |
Ammonium (a) | 6 | 4.13 ± 0.04 (bc) | 0.49 ± 0.08 (bc) | 0.28 ± 0.01 (bc) |
30 | 4.55 ± 0.03 (de) | 0.34 ± 0.03 (ab) | 0.21 ± 0.01 (ab) | |
54 | 4.50 ± 0.06 (cde) | 0.13 ± 0.01 (a) | 0.14 ± 0.01 (a) | |
Nitrate + Ammonium (na) | 6 | 4.34 ± 0.14 (cd) | 0.74 ± 0.02 (cde) | 0.28 ± 0.03 (bc) |
30 | 4.90 ± 0.10 (e) | 0.74 ± 0.07 (cde) | 0.28 ± 0.02 (bc) | |
54 | 4.60 ± 0.06 (de) | 0.61 ± 0.04 (bcd) | 0.30 ± 0.04 (bc) |
Parameter | Root | Leaf |
---|---|---|
n. of total peptides | 39,516 | 31,739 |
Average of peptides per sample (±SE, n = 27) | 1464 ± 15 | 1176 ± 11 |
Average of peptides per condition (±SE, n = 9) | 4391 ± 55 | 3527 ± 50 |
Average of unique peptide per protein (±SE) | 6.8 ± 0.3 | 6.4 ± 0.4 |
Average amino acid coverage % (±SE) | 22.5 ± 0.8 | 22.4 ± 0.9 |
n. of identified proteins | 336 | 246 |
n. of differentially accumulated proteins (%) | 51 (15%) | 48 (19%) |
ID | Entry—Protein Name | FC | Differences | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
V | h (n) | h (a) | h (na) | |||||||||||
t | s | i | 06 | 30 | 54 | 06 | 30 | 54 | 06 | 30 | 54 | |||
Nitrogen assimilation | ||||||||||||||
R74 | B6SY01—Ferredoxin-nitrite reductase | 7.57 | * | abc | d | cd | abc | ab | a | abc | bcd | abc | ||
R64 | B4FR61—Glutamine synthetase (cytosol) | 2.60 | * | a | a | a | ab | c | c | a | a | cb | ||
R189 | A0A1D6NFK0—Glutamate synthase 1 [NADH] chloroplastic | 8.54 | * | * | a | ab | a | a | ab | b | a | a | ab | |
R103 | B5U8J8—Asparagine synthetase | n.d. | * | a | a | a | a | b | c | a | a | a | ||
R68 | B4G043—Ferredoxin-NADP reductase | 5.48 | * | cb | cb | c | cb | ab | a | cb | ab | abc | ||
Amino acid metabolism | ||||||||||||||
R6 | B6U4D6—Phenylalanine ammonia-lyase | 2.88 | * | bc | abc | bc | bc | a | a | c | abc | ab | ||
R107 | P80608—Cysteine synthase | 2.74 | * | a | bc | ab | ab | ab | c | a | bc | abc | ||
R49 | A0A1D6FUX8—S-adenosylmethionine synthase | 2.16 | * | b | a | ab | ab | ab | ab | b | ab | ab | ||
R96 | K7TSD2—Serine hydroxymethyltransferase | 2.08 | * | b | ab | ab | ab | ab | a | ab | a | a | ||
Carbon metabolism | ||||||||||||||
R207 | C0PMR3—Glucose-6-phosphate 1-dehydrogenase (cytosol) | 7.66 | * | ab | b | ab | a | ab | ab | ab | ab | ab | ||
R85 | A0A1D6J424—Glucose-6-phosphate 1-dehydrogenase (chloroplast) | 224 | * | ab | b | ab | ab | a | a | ab | ab | ab | ||
R57 | A0A1D6NVZ7—Transketolase 1 | 2.98 | * | * | ab | a | ab | ab | a | a | b | ab | a | |
R231 | Q8L5G8—Phosphotransferase | 7.59 | * | ab | b | ab | a | ab | ab | a | ab | ab | ||
R168 | A0A1D6NR86—Pyrophosphate-fructose 6-phosphate 1-phosphotransferase subunit beta | 2.85 | * | a | b | ab | a | a | a | a | b | ab | ||
R243 | B4F820—Triosephosphate isomerase a | 3.67 | * | a | ab | abc | a | ab | c | abc | abc | bc | ||
R19 | C0HHU2—2,3-bisphosphoglycerate-independent phosphoglycerate mutase 1 | 2.35 | * | a | ab | ab | a | ab | c | a | a | cb | ||
R119 | A0A1D6H4C4—Citrate synthase | 2.87 | * | ab | ab | a | a | ab | b | a | ab | a | ||
R28 | Q9SAZ6—Phosphoenolpyruvate carboxylase | 3.20 | * | * | a | ab | a | ab | ab | b | a | ab | ab | |
Cell water homeostasis | ||||||||||||||
R290 | B6T7A1—Voltage-gated potassium channel beta subunit | 2.21 | * | * | ab | c | bc | ab | ab | ab | a | abc | abc | |
R127 | B6T634—Aquaporin PIP2.1 | 2.75 | * | ab | ab | b | ab | ab | a | ab | b | b | ||
R193 | A0A1R3N4Y1—Aquaporin PIP2-5 | 5.52 | * | * | a | abc | c | ab | abc | ab | abc | abc | bc | |
R285 | B6TNY0—Aquaporin TIP2.1 | 2.81 | * | * | ab | ab | b | ab | a | ab | ab | ab | ab | |
Cell wall metabolism | ||||||||||||||
R92 | A0A1D6IMH7—Hydroxyproline-rich glycoprotein family protein | 4.07 | * | b | a | a | ab | ab | ab | ab | a | ab | ||
R154 | B6UD26—O-methyltransferase ZRP4 | 3.66 | * | ab | ab | ab | a | a | b | ab | ab | ab | ||
Protein synthesis and folding | ||||||||||||||
R58 | C0PCQ6—40S ribosomal protein S2-1 | 3.21 | * | c | a | ab | bc | abc | abc | bc | ab | abc | ||
R255 | A0A1D6PYT7—Ribosomal protein S25 | 2.80 | * | bc | ab | ab | c | abc | a | abc | ab | ab | ||
R309 | A0A1D6FKZ4—60S acidic ribosomal protein P2-5 | 6.66 | * | a | b | ab | ab | ab | a | ab | ab | ab | ||
R87 | C4JA45—60S ribosomal protein L5-1 homolog b | 2.52 | * | a | b | b | ab | ab | b | ab | b | ab | ||
R122 | B6T267—Ribosomal protein L15 | 18.7 | * | bc | ab | abc | c | abc | abc | abc | a | abc | ||
R4 | B7ZZ42—Heat shock 70 kDa protein 3 | 2.25 | * | bc | a | abc | bc | abc | ab | c | a | ab | ||
R100 | B6U0V6—Endoplasmin | 5.19 | * | ab | ab | ab | a | ab | a | ab | b | ab | ||
R188 | B6SXW8—RuBisCO large subunit-binding protein sub. alpha | 3.92 | * | a | ab | ab | a | ab | a | a | b | ab | ||
R297 | A0A1D6FAH0—T-complex protein 1 subunit epsilon | 4.66 | * | ab | ab | a | ab | ab | a | ab | b | ab | ||
R131 | B4FZZ2—Peptidyl-prolyl cis-trans isomerase | 4.68 | * | c | a | ab | c | a | ab | bc | a | ab | ||
R216 | A0A1D6LN79—Peptidyl-prolyl cis-trans isomerase | 15.7 | * | d | a | abc | cd | abcd | abcd | bcd | ab | abcd | ||
R145 | A0A1D6F8L7—Coatomer subunit gamma | 3.43 | * | a | ab | ab | a | a | a | a | b | a | ||
R205 | A0A1D6PJW1—Proteasome subunit alpha type | n.d. | * | * | a | a | a | b | a | a | a | a | a | |
R230 | B4FB55—Ras-related protein ARA-3 | 2.40 | * | * | ab | b | b | a | ab | ab | ab | b | ab | |
Stress response and other functions | ||||||||||||||
R105 | C0P848—Formate dehydrogenase, mitochondrial | 14.2 | * | a | a | a | a | a | b | a | ab | ab | ||
R99 | B8A2B4—Guanine nucleotide-binding protein beta subunit-like protein a | 2.22 | * | abc | a | c | ab | a | bc | bc | ab | bc | ||
R112 | A5H452—Peroxidase 70 | 2.75 | * | c | a | abc | abc | abc | abc | bc | ab | ab | ||
R133 | A0A1D6E530—Peroxidase | 3.56 | * | ab | b | ab | ab | ab | ab | a | ab | ab | ||
R300 | B6SIU4—Peroxidase | n.d. | * | bc | ab | c | abc | ab | a | abc | abc | ab | ||
R31 | C0PH85—Tubulin beta chain | 2.88 | * | * | d | cb | cb | c | ab | a | c | bc | abc | |
R79 | Q6RW10—Allene oxide synthase | 2.27 | * | a | b | ab | a | ab | ab | ab | ab | ab | ||
R225 | A0A1D6HSR3—Putative carboxylesterase 15 | n.d. | * | a | a | a | a | b | c | a | ab | b | ||
R236 | A0A1D6QNT6—Peroxisomal fatty acid beta-oxidation multifunctional protein a | 3.86 | * | a | ab | ab | ab | ab | ab | a | b | ab | ||
R271 | Q71RX2—Isopentenyl pyrophosphate isomerase | n.d. | * | * | ab | c | bc | a | abc | abc | a | bc | bc | |
R272 | B6TKK2—Gibberellin receptor GID1L2 | n.d. | * | ab | ab | b | ab | ab | ab | a | a | ab | ||
R301 | B6TP36—Prohibitin | 3.56 | * | ab | bc | abc | a | abc | abc | ab | c | abc | ||
R318 | B6T7H0—Glutathione S-transferase 6 | n.d. | * | a | ab | b | a | a | a | a | a | a |
ID | Entry—Protein Name | FC | Differences | |||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
V | h (n) | h (a) | h (na) | |||||||||||
t | s | i | 06 | 30 | 54 | 06 | 30 | 54 | 06 | 30 | 54 | |||
Nitrogen assimilation | ||||||||||||||
L149 | B6SY01—Ferredoxin-nitrite reductase | 3.00 | * | a | ab | b | a | a | ab | ab | a | ab | ||
L177 | B6TE43—Glutamine synthetase (chloroplast) | 3.92 | * | ab | ab | ab | ab | a | a | b | ab | a | ||
Amino acid metabolism | ||||||||||||||
L193 | B6TQ06—Aminomethyltransferase | 2.31 | * | ab | ab | b | ab | a | ab | ab | ab | ab | ||
L22 | C0P5Y3—5-methyltetrahydropteroyltriglutamate -homocysteine methyltransferase 1 (MetE) | 3.57 | * | ab | a | ab | ab | ab | b | ab | ab | ab | ||
L194 | A0A1D6KDZ0—Shikimate kinase family protein | 2.85 | * | abc | ab | c | ab | ab | c | abc | a | bc | ||
Photosynthesis | ||||||||||||||
L31 | P04966—Photosystem I P700 chlorophyll a apoprotein A1 | 2.48 | * | a | ab | b | a | b | ab | ab | b | ab | ||
L85 | P04967—Photosystem I P700 chlorophyll a apoprotein A2 | 2.62 | * | a | bc | ab | ab | c | ab | ab | ab | ab | ||
L132 | B6U534—Photosystem I reaction center subunit V | 3.85 | * | c | c | a | bc | c | a | bc | bc | ab | ||
L196 | B4FLT7—Photosystem I H subunit1 | 2.99 | * | * | bcd | d | ab | abc | cd | a | ab | bcd | a | |
L113 | B6SP64—Oxygen evolving enhancer protein 3 containing protein | 2.34 | * | a | a | b | a | a | b | a | a | b | ||
L162 | B8A3D1—Pyruvate phosphate dikinase regulatory protein, chloroplastic a | 6.68 | * | a | a | ab | a | a | b | a | a | ab | ||
L212 | B6TKB3—Triose phosphate/phosphate translocator, non-green plastid, chloroplast | n.d. | * | a | a | ab | a | a | b | a | a | b | ||
Energy metabolism | ||||||||||||||
L115 | B6T908—ATP synthase B chain | 8.19 | * | * | ab | abc | c | a | ab | abc | ab | abc | bc | |
L225 | B6SP77—ATP synthase C chain | 77.8 | * | a | a | b | a | a | ab | a | a | ab | ||
L155 | B6T168—ATP synthase epsilon chain | 3.09 | * | a | abc | bc | a | abc | bc | abc | ab | c | ||
L130 | B4FK49—Nucleoside diphosphate kinase | 4.88 | * | * | a | ab | abc | abc | abc | bc | abc | ab | c | |
L236 | C0HHC4—Nucleoside diphosphate kinase | 7.24 | * | a | a | b | a | a | b | a | a | b | ||
Carbon metabolism | ||||||||||||||
L192 | A0A1D6N8I0—2,3-bisphosphoglycerate-independent phosphoglycerate mutase 1 | 4.77 | * | ab | a | ab | ab | ab | ab | ab | ab | b | ||
L191 | B8A0W7—Enolase 1 a | 13.1 | * | a | a | abc | ab | a | bc | a | a | c | ||
L110 | B4FZU8—Malate dehydrogenase | 2.31 | * | a | a | b | a | a | b | a | a | b | ||
Protein synthesis and folding | ||||||||||||||
L69 | A0A0B4J303—Eukaryotic initiation factor4a | 3.01 | * | abc | a | abc | ab | ab | bc | ab | a | c | ||
L111 | A0A1D6LAB8—RNA helicase4 | 3.98 | * | a | a | a | a | a | a | a | a | b | ||
L205 | A0A1X7YHC0—30S ribosomal protein S2, chloroplastic a | n.d. | * | ab | ab | a | ab | ab | a | b | ab | a | ||
L127 | C0PEC4—30S ribosomal protein S5 chloroplastic | 4.70 | * | ab | ab | b | ab | a | b | ab | ab | ab | ||
L211 | P08530—30S ribosomal protein S8, chloroplastic | 3.27 | * | ab | a | bc | ab | ab | bc | ab | a | c | ||
L137 | B4FR40—30S ribosomal protein S9 chloroplastic | n.d. | * | ab | a | a | ab | b | a | ab | ab | a | ||
L145 | B6UGL6—40S ribosomal protein S5 | 2.27 | * | * | a | a | b | a | a | b | a | a | b | |
L118 | A0A1D6P3R8—40S ribosomal protein S14 | 2.15 | * | ab | a | ab | ab | b | ab | a | ab | ab | ||
L88 | B6SNQ7—40S ribosomal protein S16 | n.d. | * | a | a | ab | a | a | b | ab | a | ab | ||
L171 | B6UF84—50S ribosomal protein L3 | 2.23 | * | ab | a | ab | ab | ab | ab | ab | ab | b | ||
L195 | B6SK79—60S ribosomal protein L4 | 3.28 | * | ab | a | ab | ab | ab | ab | ab | b | b | ||
L216 | B6SHW0—60S ribosomal protein L6 | 2.33 | * | a | a | ab | ab | a | ab | a | ab | b | ||
L126 | A0A1D6GM13—60S ribosomal protein L10 a | 2.40 | * | ab | a | ab | ab | ab | ab | ab | a | b | ||
L239 | B6TM00—60 ribosomal protein L14 | 2.66 | * | * | ab | a | bc | bc | bc | bc | ab | ab | c | |
L240 | B6SJH2—60S ribosomal protein L17 | 2.65 | * | a | a | b | a | a | b | a | a | b | ||
L15 | A0A1X7YIM9—RuBisCO large subunit-binding protein subunit alpha, chloroplastic a | 2.10 | * | c | a | bc | c | abc | c | c | ab | c | ||
L19 | B7ZZ42—Heat shock 70 kDa protein 3 | 2.73 | * | ab | a | ab | ab | b | ab | b | ab | b | ||
L64 | C3UZ63—HSP protein | 6.72 | * | abc | a | cb | abc | abc | bc | ab | abc | c | ||
L70 | A0A1D6LIK1—Peptidyl-prolyl cis-trans isomerase | 2.04 | * | d | abcd | a | cd | abc | ab | bcd | abcd | a | ||
L204 | B4FZZ2—Peptidyl-prolyl cis-trans isomerase | n.d. | * | b | a | a | c | a | a | bc | a | a | ||
L243 | A0A1D6FAW5—Peptidyl-prolyl cis-trans isomerase | n.d. | * | b | a | a | b | a | a | b | a | a | ||
L154 | B6TCN7—Threonine endopeptidase | 3.58 | * | a | ab | abc | a | a | c | ab | a | bc | ||
Stress response and other functions | ||||||||||||||
L76 | A1XCI5—Lipoxygenase | 4.44 | * | * | a | a | a | a | a | b | a | a | ab | |
L189 | B6T2W9—Thylakoid lumenal 19 kDa protein | 2.84 | * | b | a | ab | a | ab | ab | ab | a | ab | ||
L201 | B6SU36—Thylakoid lumenal 16.5 kDa protein | 10.3 | * | a | ab | b | ab | a | ab | ab | ab | ab | ||
L143 | B6T7W8—Cortical cell-delineating protein | 2.57 | * | ab | a | b | ab | ab | b | ab | a | b | ||
L180 | K7UGI3—Putative thioredoxin superfamily protein | 4.52 | * | abc | a | bcd | abcd | ab | cd | ab | a | d | ||
L208 | C4J9Y2—Aluminum-induced protein homolog1 | 10.5 | * | ab | a | b | a | a | ab | ab | a | ab |
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Prinsi, B.; Espen, L. Time-Course of Metabolic and Proteomic Responses to Different Nitrate/Ammonium Availabilities in Roots and Leaves of Maize. Int. J. Mol. Sci. 2018, 19, 2202. https://doi.org/10.3390/ijms19082202
Prinsi B, Espen L. Time-Course of Metabolic and Proteomic Responses to Different Nitrate/Ammonium Availabilities in Roots and Leaves of Maize. International Journal of Molecular Sciences. 2018; 19(8):2202. https://doi.org/10.3390/ijms19082202
Chicago/Turabian StylePrinsi, Bhakti, and Luca Espen. 2018. "Time-Course of Metabolic and Proteomic Responses to Different Nitrate/Ammonium Availabilities in Roots and Leaves of Maize" International Journal of Molecular Sciences 19, no. 8: 2202. https://doi.org/10.3390/ijms19082202