Effects of Fe and Mn Deficiencies on the Root Protein Profiles of Tomato (Solanum lycopersicum) Using Two-Dimensional Electrophoresis and Label-Free Shotgun Analyses
Abstract
:1. Introduction
2. Results
2.1. Effects of Fe and Mn Deficiencies on Leaf Pigments and Metal Concentrations
2.2. Identification of Root Proteins by Shotgun and 2-DE
2.3. Effect of Fe-Deficiency and Mn-Deficiency on the Root Proteome
2.4. GO-Enrichment Analysis of Differential Proteins
3. Discussion
3.1. The Cell Wall Is a Key Component to Fe and Mn Deficiencies
3.2. Contrasting Changes in Protein Profiles with Fe and Mn Deficiencies
3.2.1. Oxidoreductases and Oxidative Stress Responses
3.2.2. Coumarin Production
3.2.3. Protein and N Metabolism
3.2.4. Different Ways to Cope with a Common Problem: The Lack of Energy
3.3. A Possible Role of Extracellular Proteins in the Fe Deficiency Response
3.4. Mn Deficiency and Pathogen Response
4. Materials and Methods
4.1. Plant Material and Sampling
4.2. Experimental Design
4.3. Mineral Analysis, Chlorophyll Estimation and Photosynthetic Pigment Analysis
4.4. Root Iron Reductase Activity
4.5. Protein Extraction
4.6. Label-Free Liquid Chromatography-Tandem Mass Spectrometry (LC-MS/MS)
4.7. Protein 2-DE Separation of Root Samples
4.8. Gel Image and Statistical Analysis
4.9. Protein in Gel Digestion
4.10. Protein Identification by Nanoliquid Chromatography-Tandem Mass Spectrometry (nLC−ESI−MS/MS)
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Control | -Fe | -Mn | |
---|---|---|---|
SPAD | 42.4 ± 0.7 a | 13.6 ± 0.5 b | 29.6 ± 0.8 c |
Total Chl (Chl a + Chl b) | 323.9 ± 14.1 a | 88.0 ± 13.5 b | 219.5 ± 11.3 c |
Neoxanthin | 12.0 ± 0.6 a | 2.4 ± 0.2 b | 6.7 ± 0.4 c |
Violaxanthin (V) | 17.6 ± 0.9 a | 4.6 ± 0.5 b | 10.0 ± 0.7 c |
Taraxanthin | 0.2 ± 0.1 a | 0 a | 1.6 ± 0.2 b |
Antheraxanthin (A) | 0.8 ± 0.2 a | 1.9 ± 0.1 b | 1.3 ± 0.2 c |
Lutein | 44.8 ± 1.6 a | 15.3 ± 0.7 b | 24.5 ± 1.3 c |
Zeaxanthin (Z) | 0.2 ± 0.1 a | 3.1 ± 0.4 b | 0.3 ± 0.1 a |
(V + A + Z) | 18.6 ± 0.8 a | 9.5 ± 0.4 b | 11.5 ± 0.6 c |
Chl a/Chl b ratio | 3.0 ± 0.1 a | 2.8 ± 0.1 a | 3.0 ± 0.1 a |
(A + Z)/(V + A + Z) ratio | 0.06 ± 0.01 a | 0.53 ± 0.04 b | 0.14 ± 0.03 c |
# | Accession | UniProtKB | Description | Fold SG | Fold 2D | Mn |
---|---|---|---|---|---|---|
Oxidoreductases (6) | ||||||
1 | Solyc07g052510.4.1 | A0A3Q7HDZ4 | peroxidase (TPX1) | −0.76 | −3.00 | - |
2 | Solyc12g005790.2.1 | A0A3Q7JR84 | peroxidase 27 | −0.82 | + | |
3 | Solyc04g071890.3.1 | A0A3Q7G7T0 * | peroxidase | −1.06 | ||
4 | Solyc10g076245.1.1 | A0A3Q7IJN4 * | peroxidase 70 | −1.40 | ||
5 | Solyc05g046000.4.1 | A0A3Q7GKW8 | peroxidase 27-like | −1.73 | ||
6 | Solyc10g076210.2.1 | A0A3Q7IJN4 * | peroxidase 1 | −3.00 | ||
Carbohydrate Metabolism (4) | ||||||
7 | Solyc05g050800.3.1 | A0A3Q7GLU0 | phosphoglycerate mutase family | −0.65 | ||
8 | Solyc08g080140.4.1 | A0A3Q7HT77 | bifunctional dTDP-4-dehydrorhamnose 3,5-epimerase/reductase | −0.81 | - | |
9 | Solyc07g052350.3.1 | A0A3Q7HBK4 | aconitate hydratase | −1.17 | −3.00 | |
10 | Solyc06g073190.3.1 | Q42896 | fructokinase-like | −2.30 | ||
Polysaccharide Metabolism (3) | ||||||
11 | Solyc12g098540.2.1 | A0A3Q7JEE6 * | apyrase | 1.91 | ||
12 | Solyc01g104950.4.1 | A0A3Q7EQN7 | beta-D-xylosidase 2 precursor | −0.90 | −1.14 | - |
13 | Solyc01g107590.3.1 | A0A3Q7ESC5 | cinnamyl alcohol dehydrogenase | −1.54 | - | |
Protein Metabolism (10) | ||||||
14 | Solyc08g067100.2.1 | K4CLT6 | eukaryotic aspartyl protease family | −0.61 | ||
15 | Solyc05g013820.4.1 | A0A3Q7GHJ1 | proteasome subunit beta type-7-A | −0.73 | - | |
16 | Solyc08g079920.2.1 | A0A3Q7HVI4 * | P69f protein | −1.16 | ||
17 | Solyc03g019690.1.1 | A0A3Q7FGU5 | Kunitz-type protease inhibitor | −1.60 | ||
18 | Solyc08g079930.2.1 | A0A3Q7HVI4 * | subtilisin-like protease | −1.79 | ||
19 | Solyc02g081700.1.1 | A0A3Q7F6F6 | proteasome subunit alpha type | −3.00 | ||
20 | Solyc08g082820.4.1 | A0A3Q7HX02 | glucose-regulated protein 78 | 1.69 | ||
21 | Solyc01g028810.3.1 | A0A3Q7ECG0 | chaperonin | −0.75 | ||
22 | Solyc01g099900.4.1 | A0A3Q7ENE9 | ribosomal protein L18 | 1.51 | ||
23 | Solyc12g008630.2.1 | A0A3Q7J3G4 | mitochondrial processing peptidase alpha subunit | −3.00 | ||
Aminoacid Metabolism (5) | ||||||
24 | Solyc01g080280.3.1 | A0A3Q7EI59 | chloroplast glutamine synthetase | −0.79 | ||
25 | Solyc06g060790.1.1 | A0A3Q7GXH5 | 3-isopropylmalate dehydratase | −1.11 | ||
26 | Solyc11g011380.2.1 | A0A3Q7IRF8 * | glutamine synthetase | −1.26 | ||
27 | Solyc12g005080.2.1 | A0A3Q7J1A5 | dihydrolipoyllysine-residue succinyltransferase component of 2-oxoglutarate dehydrogenase | −0.84 | ||
28 | Solyc09g008280.2.1 | P43282 | S-adenosylmethionine synthase | −3.00 | - | |
Signaling/Regulation (3) | ||||||
29 | Solyc08g076960.1.1 | A0A3Q7HTY9 | abscisic acid receptor PYL1 | −1.00 | ||
30 | Solyc07g062110.3.1 | A0A3Q7IAM5 | protein FLX-like 1 | −0.59 | ||
31 | Solyc02g093340.3.1 | A0A3Q7FDP2 | heterogeneous nuclear ribonucleoprotein A3 | −3.00 | ||
Miscellaneous (4) | ||||||
32 | Solyc01g102390.4.1 | A0A3Q7EP74 * | germin-like protein 5-1 | 1.12 | ||
33 | Solyc03g025850.3.1 | Q9XEX8 | remorin 1 | −0.66 | ||
34 | Solyc03g113570.1.1 | A0A3Q7FQV4 * | germin-like protein | −0.91 | ||
35 | Solyc05g008460.4.1 | A0A3Q7GD18 | ATP synthase subunit beta | −1.66 |
# | Accession | UniProtKB | Description | Fold SG | Fold 2D | Fe |
---|---|---|---|---|---|---|
Oxidoreductases (18) | ||||||
36 | Solyc02g084780.4.1 | A0A3Q7F7C4 * | peroxidase superfamily protein | 1.53 | ||
37 | Solyc03g032000.4.1 | A0A3Q7G4N1 | thioredoxin reductase 2-like | 1.21 | ||
38 | Solyc08g081530.3.1 | A0A3Q7HU15 | monodehydroascorbate reductase | 0.96 | ||
2 | Solyc12g005790.2.1 | A0A3Q7JR84 | peroxidase 27 | 0.93 | - | |
39 | Solyc02g062510.3.1 | A0A3Q7F0H1 | peroxidase | 0.89 | ||
40 | Solyc10g076240.3.1 | A0A3Q7IJN4 | cationic peroxidase 1 | 0.79 | ||
41 | Solyc05g056540.4.1 | A0A3Q7HI60 | alcohol dehydrogenase 1B | 0.76 | ||
42 | Solyc02g084800.4.1 | A0A3Q7F7C4 | peroxidase 72 | 0.73 | ||
43 | Solyc10g050890.2.1 | A0A3Q7IH89 | nitrite reductase 2 | 0.68 | ||
44 | Solyc02g078650.4.1 | A0A3Q7F625 | polyphenol oxidase | 0.62 | ||
45 | Solyc11g072550.2.1 | A0A3Q7J0V5 | 4,5-dioxygenase-like protein | −0.63 | ||
46 | Solyc06g005150.3.1 | Q52QQ4 | ascorbate peroxidase | −0.64 | ||
47 | Solyc01g100360.4.1 | A0A3Q7ENY7 | dihydrolipoyl dehydrogenase 2 | −0.68 | ||
48 | Solyc09g007520.3.1 | A0A3Q7HVX4 | peroxidase | −0.78 | −0.74 | |
49 | Solyc09g011240.3.1 | A0A3Q7I069 | aldo-keto reductase 4B-like | −0.84 | ||
50 | Solyc06g059740.4.1 | A0A3Q7GTE7 | alcohol dehydrogenase 2 | −1.10 | ||
51 | Solyc07g043420.3.1 | Q40131 | 2-oxoglutarate-dependent dioxygenase 2 | −2.32 | ||
1 | Solyc07g052510.4.1 | A0A3Q7HDZ4 | peroxidase | −3.64 | - | |
Carbohydrate Metabolism (10) | ||||||
52 | Solyc05g005490.4.1 | Q5NE21 | carbonic anh isoform 1 | 1.95 | ||
53 | Solyc03g115990.3.1 | A0A3Q7GH43 | malate dehydrogenase | −0.66 | ||
54 | Solyc09g075450.3.1 | A0A3Q7I742 | fumarate hydratase | −0.69 | ||
55 | Solyc09g009260.3.1 | A0A3Q7HX95 | fructose-1,6-bisphosphate aldolase | −0.71 | ||
56 | Solyc04g011400.3.1 | A0A3Q7FZG5 | UDP-glucuronate decarboxylase 1 | −0.71 | ||
57 | Solyc10g083570.3.1 | A0A3Q7ILY0 | fructose-bisphosphate aldolase | −0.99 | ||
8 | Solyc08g080140.4.1 | A0A3Q7HT77 | bifunctional dTDP-4-dehydrorhamnose 3,5-epimerase/reductase | −1.72 | −1.65 | - |
58 | Solyc09g009020.3.1 | P26300 | enolase | −1.15 | ||
59 | Solyc04g011510.4.1 | A0A3Q7FZI5 | triosephosphate isomerase | −1.28 | ||
60 | Solyc10g085550.3.1 | A0A3Q7IN81 * | enolase | −2.06 | ||
Polysaccaride Metabolism (5) | ||||||
61 | Solyc03g123630.4.1 | A0A3Q7GM93 * | pectinesterase/pectinesterase inhibitor U1 precursor | 0.61 | ||
12 | Solyc01g104950.4.1 | A0A3Q7EQN7 | beta-D-xylosidase 2 precursor | −0.74 | −0.62 | - |
13 | Solyc01g107590.3.1 | A0A3Q7ESC5 | cinnamyl alcohol dehydrogenase | −1.37 | - | |
62 | Solyc08g079080.5.1 | A0A3Q7HT63 | acid beta-fructofuranosidase | −2.56 | ||
63 | Solyc01g111230.3.1 | A0A3Q7EVU4 | dirigent protein | −3.00 | ||
Protein Metabolism (35) | ||||||
64 | Solyc06g072220.1.1 | A0A3Q7GYL5 | Kunitz trypsin inhibitor | 1.50 | ||
65 | Solyc01g080010.2.1 | A0A3Q7EHP2 | xyloglucan endoglucanase inhibitor | 0.95 | ||
66 | Solyc12g088670.2.1 | O49877 | cysteine protease CYP1 | 0.74 | ||
67 | Solyc09g007640.4.1 | A0A3Q7HWG9 | serine carboxypeptidase-like 50 | 0.67 | ||
68 | Solyc02g068740.3.1 | A0A3Q7F1L3 | glycine cleavage system H family | −0.58 | ||
69 | Solyc01g099760.3.1 | A0A3Q7F894 | LeMA-1 putatve Mg-dependent ATPase 1 | −0.74 | −0.74 | |
70 | Solyc02g083710.3.1 | A0A3Q7F6N7 | 26S proteasome non-ATPase regulatory subunit 4 | −0.80 | ||
71 | Solyc04g076190.1.1 | A0A3Q7G5A8 | aspartic proteinase nepenthesin-1 | −1.20 | ||
72 | Solyc04g080960.4.1 | A0A3Q7GB74 | pre-pro-cysteine proteinase | −1.23 | ||
73 | Solyc01g100320.3.1 | A0A3Q7ENV3 | disulfide-isomerase-like protein | −0.57 | ||
74 | Solyc07g049450.3.1 | A0A3Q7HDI6 | protein disulfide isomerase family | −0.61 | ||
75 | Solyc08g079170.3.1 | A0A3Q7HV43 | heat shock protein STI | −0.61 | ||
76 | Solyc08g079260.3.1 | A0A3Q7HV74 | tetratricopeptide repeat-containing | −0.63 | ||
77 | Solyc01g106260.3.1 | A0A3Q7FBU5 | heat shock protein 70 | −0.64 | ||
78 | Solyc07g042250.3.1 | Q9M5A8 | chaperonin 21 precursor | −0.65 | ||
79 | Solyc01g088610.4.1 | A0A3Q7F3J4 | 10 kDa chaperonin 1 | −0.95 | ||
80 | Solyc06g065520.3.1 | A0A3Q7GYZ2 | T-complex protein eta subunit | −0.89 | ||
81 | Solyc03g121330.3.1 | A0A3Q7FVJ9 | 60S ribosomal protein L28, putative | −0.61 | ||
82 | Solyc01g096580.3.1 | A0A3Q7F6F2 | ribosomal protein S10p/S20e | −0.62 | ||
83 | Solyc09g010100.3.1 | Q2MI68 * | 30S ribosomal protein S11 | −0.63 | ||
84 | Solyc09g005720.3.1 | A0A3Q7HVY6 | 60S ribosomal protein L23A | −0.69 | ||
85 | Solyc12g044720.2.1 | A0A3Q7JA54 | 60S ribosomal L28-like protein | −0.69 | ||
86 | Solyc03g096360.4.1 | A0A3Q7FPS6 | 60S ribosomal protein L35a-2 | −0.70 | ||
87 | Solyc06g073430.4.1 | A0A3Q7ITW7 * | 40S ribosomal protein S29 | −0.72 | ||
88 | Solyc11g017070.2.1 | A0A3Q7JK86 | eukaryotic translation initiation factor 3 subunit I | −0.73 | ||
89 | Solyc06g008170.3.1 | K4CUW3 | 50S ribosomal protein L14 | −0.80 | ||
90 | Solyc03g112360.1.1 | A0A3Q7FRG1 | 60S ribosomal protein L27A | −0.82 | ||
91 | Solyc10g086010.2.1 | A0A3Q7IMU3 | 60S ribosomal L4 | −0.97 | ||
22 | Solyc01g099900.4.1 | A0A3Q7ENE9 | 60S ribosomal protein L18-2 | −0.99 | + | |
92 | Solyc01g099890.2.1 | A0A3Q7ENE9 * | PUA domain-containing protein | −1.27 | ||
93 | Solyc12g096300.2.1 | A0A3Q7JEJ5 | 40S ribosomal protein S6 | −1.55 | ||
94 | Solyc07g005560.3.1 | Q9AXQ5 | eukaryotic translation initiation factor 5A | −0.84 | ||
95 | Solyc03g083390.4.1 | A0A3Q7FN48 | protein BOBBER 1 | −0.66 | ||
96 | Solyc08g074290.3.1 | A0A3Q7HSI3 | myosin heavy chain-like protein | −0.86 | ||
97 | Solyc02g087300.1.1 | A0A3Q7FW84 | transducin/WD40 repeat-like | −1.00 | ||
Aminoacid Metabolism (9) | ||||||
98 | Solyc01g112280.3.1 | A0A3Q7EV39 | N-acyl-L-amino-acid amidohydrolase | 0.61 | ||
99 | Solyc05g053810.3.1 | A0A3Q7GNF6 | serine hydroxymethyltransferase | −0.76 | −0.76 | |
100 | Solyc02g082830.3.1 | A0A3Q7F688 | phosphoserine aminotransferase 2 | −0.93 | ||
101 | Solyc04g074480.3.1 | A0A3Q7H097 | 3-deoxy-D-arabinoheptulosonate 7-phosphate (DAHP) synthase 2 | −1.17 | ||
28 | Solyc09g008280.2.1 | P43282 | S-adenosyl-L-methionine synthase | −1.29 | - | |
102 | Solyc12g098490.2.1 | A0A3Q7JE99 | serine hydroxymethyltransferase | −1.32 | ||
103 | Solyc10g083970.1.1 | A0A3Q7IMD9 | S-adenosylmethionine synthase | −1.60 | −1.00 | |
104 | Solyc12g099000.3.1 | A0A3Q7JEH3 | S-adenosylmethionine synthase | −0.94 | ||
105 | Solyc04g076790.3.1 | A0A3Q7G863 | serine hydroxymethyltransferase | −1.84 | ||
Signaling/Regulation (11) | ||||||
106 | Solyc09g091000.4.1 | A0A3Q7I801 | pathogenesis-related protein STH-2 | 1.90 | ||
107 | Solyc09g082780.3.1 | A0A3Q7I7U0 | stem-specific protein TSJT1 | 0.64 | ||
108 | Solyc09g090990.2.1 | A0A3Q7I9H4 * | major allergen Mal d 1 | 0.66 | ||
109 | Solyc12g088720.2.1 | A0A3Q7JBV0 | polyadenylate-binding protein | −0.62 | ||
110 | Solyc12g014210.3.1 | A0A3Q7J5F6 | UBP1-associated protein 2C-like | −0.62 | ||
111 | Solyc03g096460.4.1 | Q672Q3 | wound/stress protein precursor | −1.10 | ||
112 | Solyc04g074040.3.1 | A0A3Q7H017 | serine/arginine-rich splicing factor | −1.12 | ||
113 | Solyc02g071180.3.1 | A0A3Q7F2T0 | RNA polymerase II degradation factor-like protein (DUF1296) | −1.21 | ||
114 | Solyc09g009030.4.1 | A0A3Q7HYW7 | histone deacetylase HDT1 | −1.46 | ||
115 | Solyc01g109660.2.1 | A0A3Q7IGH7 * | glycine-rich RNA-binding protein | −0.62 | ||
116 | Solyc12g095960.3.1 | A0A3Q7JDH7 | Insulin-like growth factor 2 mRNA-binding protein 2 | −0.92 | ||
Miscellaneous (3) | ||||||
117 | Solyc03g115110.4.1 | A0A3Q7FRU0 | ATP synthase subunit gamma | 1.13 | ||
118 | Solyc06g062380.3.1 | A0A3Q7GUF9 | acid phosphatase-like protein 1 | 0.72 | ||
119 | Solyc11g039980.3.1 | A0A3Q7JLN4 | ATP synthase subunit alpha | 0.63 |
# | Accession | UniProtKB | Description | −Fe SG | −Fe 2D | −Mn SG | −Mn 2D |
---|---|---|---|---|---|---|---|
22 | Solyc01g099900.4.1 | A0A3Q7ENE9 | ribosomal protein L18 | 1.51 | −0.99 | ||
2 | Solyc12g005790.2.1 | A0A3Q7JR84 | peroxidase 27 | −0.82 | 0.93 | ||
1 | Solyc07g052510.4.1 | A0A3Q7HDZ4 | peroxidase (TPX1) | −0.76 | −3.00 | −3.64 | |
13 | Solyc01g107590.3.1 | A0A3Q7ESC5 | cinnamyl alcohol dehydrogenase | −1.54 | −1.37 | ||
8 | Solyc08g080140.4.1 | A0A3Q7HT77 | bifunctional dTDP-4-dehydrorhamnose 3,5-epimerase/reductase | −0.81 | −1.72 | −1.65 | |
12 | Solyc01g104950.4.1 | A0A3Q7EQN7 | beta-D-xylosidase 2 | −0.90 | −1.14 | −0.74 | −0.62 |
28 | Solyc09g008280.2.1 | P43282 | S-adenosylmethionine synthase | −3.00 | −1.29 |
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Ceballos-Laita, L.; Takahashi, D.; Uemura, M.; Abadía, J.; López-Millán, A.F.; Rodríguez-Celma, J. Effects of Fe and Mn Deficiencies on the Root Protein Profiles of Tomato (Solanum lycopersicum) Using Two-Dimensional Electrophoresis and Label-Free Shotgun Analyses. Int. J. Mol. Sci. 2022, 23, 3719. https://doi.org/10.3390/ijms23073719
Ceballos-Laita L, Takahashi D, Uemura M, Abadía J, López-Millán AF, Rodríguez-Celma J. Effects of Fe and Mn Deficiencies on the Root Protein Profiles of Tomato (Solanum lycopersicum) Using Two-Dimensional Electrophoresis and Label-Free Shotgun Analyses. International Journal of Molecular Sciences. 2022; 23(7):3719. https://doi.org/10.3390/ijms23073719
Chicago/Turabian StyleCeballos-Laita, Laura, Daisuke Takahashi, Matsuo Uemura, Javier Abadía, Ana Flor López-Millán, and Jorge Rodríguez-Celma. 2022. "Effects of Fe and Mn Deficiencies on the Root Protein Profiles of Tomato (Solanum lycopersicum) Using Two-Dimensional Electrophoresis and Label-Free Shotgun Analyses" International Journal of Molecular Sciences 23, no. 7: 3719. https://doi.org/10.3390/ijms23073719
APA StyleCeballos-Laita, L., Takahashi, D., Uemura, M., Abadía, J., López-Millán, A. F., & Rodríguez-Celma, J. (2022). Effects of Fe and Mn Deficiencies on the Root Protein Profiles of Tomato (Solanum lycopersicum) Using Two-Dimensional Electrophoresis and Label-Free Shotgun Analyses. International Journal of Molecular Sciences, 23(7), 3719. https://doi.org/10.3390/ijms23073719