Data-Independent Acquisition-Based Proteome and Phosphoproteome Profiling Reveals Early Protein Phosphorylation and Dephosphorylation Events in Arabidopsis Seedlings upon Cold Exposure
Abstract
:1. Introduction
2. Results
2.1. Proteome and Phosphoproteome Analyses of Arabidopsis Seedlings upon Short-Time Cold Stress
2.2. Identification of Early-Cold-Responsive Proteins
2.3. Protein Phosphorylation and Dephosphorylation Response Showed Distinct Patterns in Biological Processes or Pathways
2.4. Motif Analysis of Sequences Flanking p-Sites of Cold-Responsive Phosphopeptides
2.5. Cold Stimuli Induced Dynamic Protein Phosphorylation Modification
2.6. Cold-Induced Phosphorylation and Dephosphorylation in Phospholipid Signaling Proteins
2.7. Cold-Mediated Phosphorylation Modification in Cytoskeleton Proteins
2.8. Cold-Mediated Protein Phosphorylation in Calcium Signaling Proteins
2.9. MAPK Cascades Response upon Cold Stress
2.10. Phosphorylation Modification of Transcription Factors in Early Cold Response
2.11. Phosphorylation Modification of Proteins Belonging to COR Genes in Early Cold Response
2.12. Validation of Cold-Induced Protein Phosphorylation Level Changes
3. Discussion
4. Materials and Methods
4.1. Plant Growth and Cold Treatment
4.2. Protein Extraction and Peptides Preparation
4.3. Mass Spectrometric Acquisition
4.4. Mass Spectrometric Raw Data Analysis
4.5. Bioinformatic Analysis
4.6. Immunoblot Analysis
4.7. Parallel Reaction Monitoring
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Accession | Description | Fold 1 | Adjusted p Value | Fold | Adjusted p Value |
---|---|---|---|---|---|
30 min | PRM | DIA | |||
ATCG00710 | PSBH, Photosystem II reaction center protein H | 0.36 | 2.3 × 10−3 | 0.35 | 2.6 × 10−3 |
AT1G20340 | PETE2, Cupredoxin superfamily protein | 0.43 | 8.5 × 10−5 | 0.4 | 3.1 × 10−3 |
120 min | |||||
AT1G20340 | PETE2, Cupredoxin superfamily protein | 0.47 | 1.9 × 10−4 | 0.37 | 4.7 × 10−4 |
AT4G35750 | SEC14 cytosolic factor family protein | 0.42 | 5.8 × 10−4 | 0.42 | 2.4 × 10−6 |
ATCG00710 | PSBH, Photosystem II reaction center protein H | 0.46 | 4.0 × 10−3 | 0.47 | 8.2 × 10−3 |
AT3G46640 | LUX, Homeodomain-like superfamily protein | 0.64 | 8.0 × 10−2 | 0.65 | 1.5 × 10−3 |
AT4G12470 | AZI1, Azelaic acid induced 1 | 1.37 | 2.2 × 10−3 | 1.51 | 7.4 × 10−3 |
AT5G14920 | GASA14, Gibberellin-regulated family protein | 1.61 | 7.1 × 10−3 | 1.83 | 7.4 × 10−3 |
AT5G02160 | FIP, FTSH5 interacting protein | 2.02 | 1.3 × 10−3 | 2.18 | 4.7 × 10−4 |
AGI | Name | Phosphopeptides 1 | p-Sites | Fold | adj_p | Fold | adj_p |
---|---|---|---|---|---|---|---|
PRM Data | DIA Data | ||||||
MAPK cascade kinases | |||||||
AT3G45640 | MPK3 | ICDFGLARPTSENDFMTEyVVTR | Y198 | 3.4 | 1.5 × 10−2 | 1.5 | 3.8 × 10−3 |
AT4G01370 | MPK4 | TKSETDFMtEyVVTR2 | T201;Y203 | 14.1 | 7.6 × 10−5 | 5.3 | 7.3 × 10−7 |
AT4G01370 | MPK4 | TKSETDFMtEYVVTR2 | T201 | 4.8 | 2.0 × 10−4 | 5.4 | 4.9 × 10−8 |
AT2G43790 | MPK6 | VTSESDFMtEyVVTR | T221;Y223 | 2.3 | 1.9 × 10−2 | 1.9 | 2.1 × 10−1 |
AT1G18150 | MPK8 | AAAAVASTLESEEADNGGGYsAR | S539 | 0.3 | 8.7 × 10−3 | 0.4 | 8.5 × 10−6 |
AT1G18150 | MPK8 | HHAsLPR | S495 | 0.5 | 4.1 × 10−3 | 0.4 | 1.3 × 10−4 |
AT3G18040 | MPK9 | SIASLVTtLESPPTSQHEGSDYR | T549 | 0.4 | 3.4 × 10−5 | 0.4 | 2.0 × 10−5 |
AT3G18040 | MPK9 | SQLtTIYR | T51 | 0.2 | 4.3 × 10−4 | 0.3 | 8.1 × 10−8 |
AT1G53510 | MPK18 | VAFNDTPTTVFWTDyVATR | Y189 | 2.6 | 5.5 × 10−2 | 2.9 | 2.7 × 10−6 |
AT4G29810 | MKK2 | FLTQSGtFKDGDLR2 | T31 | 0.5 | 2.0 × 10−3 | 0.5 | 3.5 × 10−5 |
AT1G51660 | MKK4 | ASPSQNRsPQNLHQLLPPPRPLSSSSSPTT | S344 | 2.3 | 2.5 × 10−3 | 2.4 | 9.9 × 10−4 |
AT1G53570 | MAPKKK3 | LSGVVsLESSTGR | S162 | 3.1 | 1.3 × 10−2 | 3.9 | 1.2 × 10−5 |
AT1G63700 | YDA | sPGSGGNFYTNSFFQEPSR | S794 | 2.1 | 7.4 × 10−5 | 2.5 | 2.3 × 10−4 |
AT3G13530 | MAPKKK7 | TPsSVSGNELAR | S452 | 0.3 | 2.3 × 10−2 | 0.2 | 6.4 × 10−8 |
AT4G08500 | MEKK1 | FKsFDLDK | S119 | 0.5 | 1.9 × 10−3 | 0.8 | 5.3 × 10−2 |
AT4G24100 | MAP4K5 | GVsAWNFDVR | S352 | 2.1 | 2.6 × 10−4 | 2.2 | 2.7 × 10−5 |
AT5G03730 | CTR1 | AStFLSSK | T704 | 12.2 | 1.7 × 10−4 | NA in CK | |
AT1G08720 | EDR1 | HNTFLsSK | S823 | 4.1 | 1.0 × 10−4 | NA in CK | |
AT3G06620 | RAF7 | NIGEGAPsWR | S59 | 0.2 | 1.8 × 10−2 | NA in CS120 | |
AT2G31010 | RAF13 | KTMsLPsSPHAYR | S465;S468 | 0.0 | 2.5 × 10−1 | NA in CS120 | |
AT1G79570 | RAF20 | TNsSLHEFGNK | S130 | 0.5 | 1.2 × 10−2 | 0.6 | 4.3 × 10−3 |
AT2G35050 | RAF24 | RNtLVtGGVR | T1134;T1137 | 1.2 | 6.5 × 10−1 | 1.1 | 8.9 × 10−1 |
AT5G57610 | RAF35 | ISGFDGMSsLGQPSYPNPHLQDR | S569 | 4.9 | 2.3 × 10−2 | NA in CK | |
Other kinases | |||||||
AT3G45780 | phot1 | ALsESTNLHPFMTK | S350 | 2.1 | 1.1 × 10−2 | 2.2 | 1.8 × 10−4 |
AT3G45780 | phot1 | MsENVVPSGR | S376 | 10.6 | 8.4 × 10−5 | 7.4 | 7.6 × 10−10 |
AT3G45780 | phot1 | MSENVVPsGR | S382 | 0.5 | 1.9 × 10−2 | 0.6 | 1.9 × 10−4 |
AT5G58140 | phot2 | sLEIFNPSSGK | S22 | 2.8 | 9.1 × 10−5 | 3.9 | 3.6 × 10−7 |
AT3G50500 | SnRK2.2 | SSVLHsQPKsTVGTPAYIAPEILLR | S173;S177 | 14.4 | 1.5 × 10−3 | 18.9 | 8.0 × 10−8 |
AT3G50500 | SnRK2.2 | StVGTPAYIAPEILLR | T178 | 5.8 | 1.2 × 10−4 | 9.4 | 1.2 × 10−7 |
AT4G40010 | SnRK2.7 | SSVLHsQPK2 | S154 | 5.4 | 1.1 × 10−4 | 4.3 | 3.6 × 10−10 |
AT4G40010 | SnRK2.7 | StVGTPAYVAPEVLSR | T159 | 5.9 | 5.6 × 10−4 | NA in CK | |
AT4G33950 | OST1 | sTVGTPAYIAPEVLLK | S175 | 12.3 | 1.3 × 10−6 | NA in CK | |
AT4G33950 | OST1 | SSVLHsQPKsTVGTPAYIAPEVLLK | S171;S175 | 279.9 | 1.2 × 10−5 | NA in CK | |
AT2G17290 | CPK6 | NsLNISMR2 | S536 | 2.3 | 6.1 × 10−3 | 1.7 | 1.8 × 10−2 |
AT3G53930 | ATG1B | SSYGFsVER | S349 | 2.4 | 1.1 × 10−4 | NA in CK | |
AT4G21390 | B120 | NTDTsVVVADLTK | S480 | 0.1 | 2.2 × 10−2 | NA in CS120 | |
AT4G27300 | SD11 | NVPDISSsLSLR | S798 | 0.4 | 2.8 × 10−2 | NA in CS120 | |
AT4G33080 | NDR6 | KLAFsTVGTPDYIAPEVLLK | S300 | 5.9 | 1.1 × 10−2 | NA in CK | |
AT5G28290 | NEK3 | HRPVDLsANDTSR | S333 | 0.0 | 2.4 × 10−4 | NA in CS120 | |
AT5G64940 | ATH13 | SVsIAGIFLPR | S31 | 0.1 | 2.1 × 10−3 | NA in CS120 | |
AT1G68830 | STN7 | TVTEtIDEISDGRKtVWWNR | T541;T551 | 0.2 | 3.4 × 10−3 | NA in CS120 | |
AT2G07180 | PBL17 | SVtLYEASSDSQGTR | T392 | 4.2 | 1.7 × 10−2 | NA in CK | |
AT3G48750 | CDC2 | TFtHEVVTLWYR | T161 | 0.5 | 6.3 × 10−3 | 0.5 | 4.7 × 10−3 |
AT1G30570 | HERK2 | LNtLAASTMGR | T498 | 0.2 | 1.7 × 10−3 | NA in CS120 | |
Phosphatases | |||||||
AT3G55270 | MKP1 | YVSKtPLSR | T474 | 9.4 | 2.2 × 10−5 | NA in CK | |
AT4G21670 | CPL1 | DETALPVsSRPTDPR | S839 | 12.5 | 3.2 × 10−2 | NA in CK | |
AT3G50110 | PEN3 | TDDIVPCPPGsSPR | S86 | 4.9 | 5.6 × 10−4 | 1.9 | 1.5 × 10−5 |
Transcription factors | |||||||
AT2G04880 | WRKY1 | VVTHNNMLDSEVDDKEGDANKtPQSSTLQSITK | T391 | 0.1 | 1.3 × 10−2 | NA in CS120 | |
AT2G46830 | CCA1 | IsSNITDPWK | S475 | -- | -- | NA in CK | |
AT3G16857 | ARR1 | SIFsFDNTK | S374 | 12.6 | 1.7 × 10−2 | NA in CK | |
AT3G26744 | ICE1 | DLSSVPDFLsAR | S172 | 4.6 | 1.5 × 10−2 | NA in CK | |
AT4G16110 | ARR2 | GPDsGTAAGGSNSDPFPANLR | S12 | 2.7 | 6.7 × 10−3 | NA in CK | |
AT2G40620 | bZIP18 | LGSGSGsASDSAGPSAPR | S83 | 2.4 | 8.1 × 10−5 | 1.6 | 2.6 × 10−3 |
AT3G09600 | RVE8 | VIsPQHELATLR | S157 | 2.6 | 7.2 × 10−4 | 2.3 | 2.8 × 10−6 |
AT4G16150 | CAMTA5 | ETHEVHAAPAtPGNSYSSSItDHLSPK | T154;T164 | 14.6 | 1.9 × 10−3 | 5.0 | 5.5 × 10−8 |
AT4G16150 | CAMTA5 | ETHEVHAAPAtPGNSYSSSITDHLSPK | T154 | 1.9 | 4.5 × 10−3 | 2.3 | 9.0 × 10−6 |
E3 ligases | |||||||
AT2G39810 | HOS1 | SIsLPTQPNYSSKPVQEALK | S17 | 2.1 | 2.8 × 10−4 | 2.3 | 4.2 × 10−7 |
AT1G67900 | NPY8 | ALLAAHNIDPSNPNAAAFStTTSIAAPEDR | T549 | 0.3 | 3.1 × 10−3 | NA in CS120 | |
AT2G23140 | PUB4 | SGPLAATTsAATR | S492 | 0.3 | 4.4 × 10−2 | NA in CS120 | |
AT3G08020 | PHD finger protein | ATFGSVTQFPAASTsEGNHVDDK | S615 | 2.1 | 1.5 × 10−2 | NA in CK | |
AT3G26730 | RING/U-boxprotein | NQTQsLsPPDVSR | S428;S430 | 2.0 | 2.9 × 10−2 | NA in CK | |
AT3G60080 | BTL13 | TVsGLGIGMR | S282 | 0.3 | 1.0 × 10−2 | NA in CS120 | |
AT5G15440 | EDL1 | RNsLLGGSENGPPPQK | S273 | 2.1 | 4.9 × 10−3 | NA in CK | |
AT5G65683 | WAVH2 | FGFLSNPStPR | T50 | 0.1 | 1.2 × 10−2 | NA in CS120 | |
Others | |||||||
AT2G38750 | ANN4 | KAsKsFFVEDEER | S46;S48 | 2.2 | 9.3 × 10−4 | 1.9 | 1.5 × 10−4 |
AT4G35920 | MCA1 | STsNVSSGHDLLSR | S278 | 0.4 | 6.0 × 10−4 | 0.4 | 2.6 × 10−5 |
AT5G03280 | EIN2 | AAPTSNFTVGSDGPPsFR | S645 | 2.0 | 8.9 × 10−3 | 2.3 | 7.0 × 10−3 |
AT5G03280 | EIN2 | SLSGEGGsGTGSLSR | S655 | 2.4 | 1.4 × 10−3 | 2.1 | 2.9 × 10−3 |
AT5G03280 | EIN2 | TPGsIDSLYGLQR | S757 | 1.6 | 2.3 × 10−2 | 1.7 | 1.2 × 10−1 |
AT1G20440 | COR47 | NNVPEHEtPTVATEESPATTTEVTDR | T14 | 0.3 | 1.1 × 10−3 | 0.4 | 1.5 × 10−3 |
AT1G76180 | ERD14 | KKDETKPEEtPIASEFEQK | T46 | 0.1 | 7.0 × 10−6 | 0.2 | 4.2 × 10−7 |
AT2G23120 | LEA protein | AYGAEGHQEPTPGLGGGSTDAPtPSGDAPAATTTDAK | T67 | 0.4 | 3.9 × 10−3 | 0.4 | 6.1 × 10−5 |
AT3G57410 | VLN3 | AAALAALTSAFNSsSGR | S773 | 0.4 | 2.9 × 10−4 | 0.3 | 1.8 × 10−2 |
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Tan, J.; Zhou, Z.; Feng, H.; Xing, J.; Niu, Y.; Deng, Z. Data-Independent Acquisition-Based Proteome and Phosphoproteome Profiling Reveals Early Protein Phosphorylation and Dephosphorylation Events in Arabidopsis Seedlings upon Cold Exposure. Int. J. Mol. Sci. 2021, 22, 12856. https://doi.org/10.3390/ijms222312856
Tan J, Zhou Z, Feng H, Xing J, Niu Y, Deng Z. Data-Independent Acquisition-Based Proteome and Phosphoproteome Profiling Reveals Early Protein Phosphorylation and Dephosphorylation Events in Arabidopsis Seedlings upon Cold Exposure. International Journal of Molecular Sciences. 2021; 22(23):12856. https://doi.org/10.3390/ijms222312856
Chicago/Turabian StyleTan, Jinjuan, Zhongjing Zhou, Hanqian Feng, Jiayun Xing, Yujie Niu, and Zhiping Deng. 2021. "Data-Independent Acquisition-Based Proteome and Phosphoproteome Profiling Reveals Early Protein Phosphorylation and Dephosphorylation Events in Arabidopsis Seedlings upon Cold Exposure" International Journal of Molecular Sciences 22, no. 23: 12856. https://doi.org/10.3390/ijms222312856