Rice Science ›› 2020, Vol. 27 ›› Issue (3): 184-200.DOI: 10.1016/j.rsci.2020.04.003
收稿日期:
2019-05-06
接受日期:
2019-10-31
出版日期:
2020-05-28
发布日期:
2020-01-17
. [J]. Rice Science, 2020, 27(3): 184-200.
Fig. 2. Overview of common techniques used in identification and quantification of rice phosphoproteome.2DE, Two-dimensional gel electrophoresis; 2D-DIGE, Two-dimensional differential gel electrophoresis; CBB, Coomassie brilliant blue; SCX, Strong cation exchange; SAX, Small-angle X-ray scattering; HILIC, Hydrophilic interaction liquid chromatography; IMAC, Immobilized metal affinity chromatography; MOAC, Metal oxide/hydroxide affinity chromatography; LC, Liquid chromatography; HPLC, High performance liquid chromatography; ESI-MS/MS; Electrospray ionization tandem mass spectrometry.
Treatment/Sample type | Proteomic approach; Subcellular fraction | Number of phosphoproteins and number of sites identified | Reference |
---|---|---|---|
GAs, BL, 2,4-D, ABA, cold or salt treatment of rice seedlings | Total protein extracts from leaf sheaths, leaf blades and roots, in vitro 32P labeling, 2DE; ESI-Q-TOF-MS/MS; MALDI-TOF-MS | 42 phosphoproteins identified, among them 13 were stress/hormonal responsive; 8 sites of phosphorylation in 6 phosphoproteins | Khan et al, 2005 |
Salt treatment of rice roots | Total protein extracts; 2DE; Pro-Q Diamond, SYPRO Ruby; MALDI-TOF/TOF PMF and MS/MS | 17 differentially up-regulated and 11 down-regulated phosphoproteins for Pro-Q Diamond dye; 26 up-regulated and 5 down-regulated phosphoproteins for SYPRO Ruby | Chitteti and Peng, 2007 |
Protoplast isolation from rice cell suspension | Nucleus and chromatin isolation; Total protein extracts; 2D-PAGE; Pro-Q Diamond; MALDI-TOF/TOF MS and LC/LC-MS/MS | 972 distinct protein spots and 509 proteins identified, which correspond to 269 unique proteins | Tan et al, 2007 |
ABA treatment of rice seedlings | Total protein; 2DE; Immunodetection of phospho-Ser and phospho-Thr; MALDI-TOF/TOF MS and MS/MS | 6 ABA responsive phosphoproteins out of 28 proteins | He and Li, 2008 |
Cd stress in leaves and root of rice seedlings | Total protein extracts; 2DE; Colloidal coomassie blue; MALDI-TOF/TOF PMF and MS/MS | 13 proteins in the roots and 12 proteins in the leaves | Ge et al, 2009 |
Drought treatment of rice seedlings | Total protein; 2DE; Immunodetection of phospho-Ser and phospho-Thr; MALDI-TOF/TOF MS and MS/MS | 3 drought-responsive differentially expressed proteins and 10 differentially phosphorylated (dp) phosphoproteins | Ke et al, 2009 |
Unfractionated whole-cell lysates of rice and Arabidopsis cells | Total protein extract; SCX prefractionation; Ti-HAMMOC; Zr-HAMMOC; Fe-IMAC using Phos-select; Nano-LC-MS/MS | 6 919 phosphopeptides from 3 393 proteins | Nakagami et al, 2010 |
Salinity, cold and drought stress | Genome sequences; Microarray gene expression analysis; Online databases and in silico search tools; RT-PCR | 132 proteins; 46 phosphatases were differentially expressed in 3 abiotic stresses | Singh et al, 2010 |
Heat (at 42 ºC) of rice seedlings | Total protein; 2DE; Pro-Q Diamond and coomassie, MALDI-TOF/TOF MS and MS/MS; Immunoblotting of ATP-β | 10 dp proteins | Chen et al, 2011 |
High salinity treatment of A. thaliana and rice plants | Microsomal fractions; Protein digestion; Enrichment using Zr4+-IMAC and TiO2 magnetic beads; Q-TOF Nano LC-MS/MS; Label-free quantification on Q-TOF, LTQ-FT and Q-Trap | 3 membrane phosphoproteins and 4 nonmembrane phosphoproteins; 15 phosphopeptides from rice microsomes | Chang et al, 2012 |
Cold stress (6 ºC and 15 ºC) of rice seedlings | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS | 12 up-regulated and 1 down-regulated phosphoprotein among 13 phosphoproteins | Chen et al, 2012 |
ABA treatment of rice inferior spiklets at 20 d after flowering | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS | 16 up-regulated and 15 down-regulated among 31 differentially regulated phosphoproteins | Zhang et al, 2012 |
Rice embryo germination | Total protein extracts; 2DE; Pro-Q Diamond; Coomassie brilliant blue and MALDI-TOF/TOF MS | About 500 phosphorylated protein spots were detected on each gel | Han et al, 2014a |
Poor grain-filling of rice inferior spikelets | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS and LC-ESI-MS/MS | 123 proteins in abundance and 43 phosphoproteins | Zhang et al, 2014 |
Rice pistils | Total protein; Fe3+-IMAC protein enrichment; HILIC and Nano-LC-MS/MS | 2 347 phosphorylation sites and 1 588 phosphoproteins | Wang K et al, 2014 |
Rice leaves in response to bacterial blight | Total protein; TiO2 MOAC and LC-MS/MS | 2 367 and 2 223 phosphosites on 1 334 and 1 297 proteins in 0 and 24 h after Xoo infection, respectively | Hou et al, 2015 |
Early stage of seed germination | Isolation of nuclei and extraction of nuclear proteins; Total protein; PolyMAC-Ti and MS/MS | 3 467 phosphopeptides and 102 nuclear phosphorproteins from rice embryos; 115 nuclear phosphoproteins identified after 24 h of imbibition | Li M et al, 2015 |
Early seed development | Total protein; TiO2 protein enrichment and LC-MS/MS | Pistils and seeds at 3 and 7 d after pollination resulted in 38 854 313 and 4 135 phosphopeptides, respectively. A total of 2487 proteins were dp | Qiu et al, 2015 |
Magnaporthe oryzae treatment of susceptible and resistant rice cultivars | Total protein extracts; Al(OH)3-MOAC; 2DE; Pro-Q Diamond; MALDI-TOF/TOF PMF and Nano LC-MS/MS | 1 522 unique peptides, of which 1 365 were dp | Li Y F et al, 2015 |
Developing rice anthers | Total protein; TiO2 MOAC and Nano UHPLC-MS/MS | 4 984 proteins and 3 203 phosphoproteins with 8 973 unique phosphorylation sites | Ye et al, 2015 |
Brassinosteroid treatment in rice | Total protein; TiO2 MOAC and LC-MS/MS | 4 034 phosphosites on 1 900 phosphoproteins and 1 821 brassinosteroid-responsive proteins | Hou et al, 2017 |
Callus, leaf, root, shoot meristem, young panicle, and mature panicle | Total protein extracts; Pro-Q diamond; TiO2 enrichment and LC-MS/MS | 7 171 unique phosphosites in 4 792 phosphopeptides from 2 657 identified phosphoproteins | Wang et al, 2017 |
Cd stress in rice seedlings | Total protein; iTRAQ labeling; TiO2 enrichment and LC-MS/MS | 2 454 phosphosites associated with 1 244 proteins, among them, 482 were dp | Zhong et al, 2017 |
Response to Cd stress in rice | 32 up-regulated and 1 down-regulated Cd tolerant, and 15 up-regulated and 4 down-regulated Cd sensitive among 53 differentially expressed phosphoproteins | Fang et al, 2019 |
Table 1 Summary of some quantitative studies in rice phosphoproteome study.
Treatment/Sample type | Proteomic approach; Subcellular fraction | Number of phosphoproteins and number of sites identified | Reference |
---|---|---|---|
GAs, BL, 2,4-D, ABA, cold or salt treatment of rice seedlings | Total protein extracts from leaf sheaths, leaf blades and roots, in vitro 32P labeling, 2DE; ESI-Q-TOF-MS/MS; MALDI-TOF-MS | 42 phosphoproteins identified, among them 13 were stress/hormonal responsive; 8 sites of phosphorylation in 6 phosphoproteins | Khan et al, 2005 |
Salt treatment of rice roots | Total protein extracts; 2DE; Pro-Q Diamond, SYPRO Ruby; MALDI-TOF/TOF PMF and MS/MS | 17 differentially up-regulated and 11 down-regulated phosphoproteins for Pro-Q Diamond dye; 26 up-regulated and 5 down-regulated phosphoproteins for SYPRO Ruby | Chitteti and Peng, 2007 |
Protoplast isolation from rice cell suspension | Nucleus and chromatin isolation; Total protein extracts; 2D-PAGE; Pro-Q Diamond; MALDI-TOF/TOF MS and LC/LC-MS/MS | 972 distinct protein spots and 509 proteins identified, which correspond to 269 unique proteins | Tan et al, 2007 |
ABA treatment of rice seedlings | Total protein; 2DE; Immunodetection of phospho-Ser and phospho-Thr; MALDI-TOF/TOF MS and MS/MS | 6 ABA responsive phosphoproteins out of 28 proteins | He and Li, 2008 |
Cd stress in leaves and root of rice seedlings | Total protein extracts; 2DE; Colloidal coomassie blue; MALDI-TOF/TOF PMF and MS/MS | 13 proteins in the roots and 12 proteins in the leaves | Ge et al, 2009 |
Drought treatment of rice seedlings | Total protein; 2DE; Immunodetection of phospho-Ser and phospho-Thr; MALDI-TOF/TOF MS and MS/MS | 3 drought-responsive differentially expressed proteins and 10 differentially phosphorylated (dp) phosphoproteins | Ke et al, 2009 |
Unfractionated whole-cell lysates of rice and Arabidopsis cells | Total protein extract; SCX prefractionation; Ti-HAMMOC; Zr-HAMMOC; Fe-IMAC using Phos-select; Nano-LC-MS/MS | 6 919 phosphopeptides from 3 393 proteins | Nakagami et al, 2010 |
Salinity, cold and drought stress | Genome sequences; Microarray gene expression analysis; Online databases and in silico search tools; RT-PCR | 132 proteins; 46 phosphatases were differentially expressed in 3 abiotic stresses | Singh et al, 2010 |
Heat (at 42 ºC) of rice seedlings | Total protein; 2DE; Pro-Q Diamond and coomassie, MALDI-TOF/TOF MS and MS/MS; Immunoblotting of ATP-β | 10 dp proteins | Chen et al, 2011 |
High salinity treatment of A. thaliana and rice plants | Microsomal fractions; Protein digestion; Enrichment using Zr4+-IMAC and TiO2 magnetic beads; Q-TOF Nano LC-MS/MS; Label-free quantification on Q-TOF, LTQ-FT and Q-Trap | 3 membrane phosphoproteins and 4 nonmembrane phosphoproteins; 15 phosphopeptides from rice microsomes | Chang et al, 2012 |
Cold stress (6 ºC and 15 ºC) of rice seedlings | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS | 12 up-regulated and 1 down-regulated phosphoprotein among 13 phosphoproteins | Chen et al, 2012 |
ABA treatment of rice inferior spiklets at 20 d after flowering | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS | 16 up-regulated and 15 down-regulated among 31 differentially regulated phosphoproteins | Zhang et al, 2012 |
Rice embryo germination | Total protein extracts; 2DE; Pro-Q Diamond; Coomassie brilliant blue and MALDI-TOF/TOF MS | About 500 phosphorylated protein spots were detected on each gel | Han et al, 2014a |
Poor grain-filling of rice inferior spikelets | Total protein extracts; 2DE; Coomassie brilliant blue; Pro-Q Diamond; MALDI-TOF/TOF MS and LC-ESI-MS/MS | 123 proteins in abundance and 43 phosphoproteins | Zhang et al, 2014 |
Rice pistils | Total protein; Fe3+-IMAC protein enrichment; HILIC and Nano-LC-MS/MS | 2 347 phosphorylation sites and 1 588 phosphoproteins | Wang K et al, 2014 |
Rice leaves in response to bacterial blight | Total protein; TiO2 MOAC and LC-MS/MS | 2 367 and 2 223 phosphosites on 1 334 and 1 297 proteins in 0 and 24 h after Xoo infection, respectively | Hou et al, 2015 |
Early stage of seed germination | Isolation of nuclei and extraction of nuclear proteins; Total protein; PolyMAC-Ti and MS/MS | 3 467 phosphopeptides and 102 nuclear phosphorproteins from rice embryos; 115 nuclear phosphoproteins identified after 24 h of imbibition | Li M et al, 2015 |
Early seed development | Total protein; TiO2 protein enrichment and LC-MS/MS | Pistils and seeds at 3 and 7 d after pollination resulted in 38 854 313 and 4 135 phosphopeptides, respectively. A total of 2487 proteins were dp | Qiu et al, 2015 |
Magnaporthe oryzae treatment of susceptible and resistant rice cultivars | Total protein extracts; Al(OH)3-MOAC; 2DE; Pro-Q Diamond; MALDI-TOF/TOF PMF and Nano LC-MS/MS | 1 522 unique peptides, of which 1 365 were dp | Li Y F et al, 2015 |
Developing rice anthers | Total protein; TiO2 MOAC and Nano UHPLC-MS/MS | 4 984 proteins and 3 203 phosphoproteins with 8 973 unique phosphorylation sites | Ye et al, 2015 |
Brassinosteroid treatment in rice | Total protein; TiO2 MOAC and LC-MS/MS | 4 034 phosphosites on 1 900 phosphoproteins and 1 821 brassinosteroid-responsive proteins | Hou et al, 2017 |
Callus, leaf, root, shoot meristem, young panicle, and mature panicle | Total protein extracts; Pro-Q diamond; TiO2 enrichment and LC-MS/MS | 7 171 unique phosphosites in 4 792 phosphopeptides from 2 657 identified phosphoproteins | Wang et al, 2017 |
Cd stress in rice seedlings | Total protein; iTRAQ labeling; TiO2 enrichment and LC-MS/MS | 2 454 phosphosites associated with 1 244 proteins, among them, 482 were dp | Zhong et al, 2017 |
Response to Cd stress in rice | 32 up-regulated and 1 down-regulated Cd tolerant, and 15 up-regulated and 4 down-regulated Cd sensitive among 53 differentially expressed phosphoproteins | Fang et al, 2019 |
Approach | Method | Advantage | Disadvantage |
---|---|---|---|
2D-DIGE | Deliver a visual map of all the proteins and allow the fractionation of thousands of proteins in a complex mixture | Relatively small scale, low sensitivity, poor detection of low-abundance phosphoproteins, and insufficient collected proteins for downstream enrichment methods | |
Stable isotope labeling quantification | SILAC | Lower experimental error | Allow up to only three samples |
HILEP, SILIP, SILIA | Applicable to entire plant and other plant tissues | Only be used in auxotrophic cells | |
iTRAQ and TMT | Allow multiplex up to 8 (iTARQ) and 10 (TMT); Labeling agent doesn’t affect overall peptide behavior thus minimizes experimental error | Reduced identification efficiency as much as 50% in multi-stage activation | |
Chemical derivatization (DiLeu) | Higher protein coverage and quantification efficiency; Cheaper than iTRAQ and TMT; Provide higher reproducibility in quantitation | ||
Label-free quantification | Signal intensity and spectral counting | Allow as many samples as possible | Time-consuming; Less degree of reproducibility in quantitation |
Absolute quantification | AQUA | Allow quantification of isoforms in low abundance and stoichiometry; Achieve accurate and sensitive quantification | |
AQUIP | Can determine the absolute amount of protein | ||
2D-DIGE, Two-dimensional differential gel electrophoresis; SILAC, Stable isotope labeling by amino acids in culture; HILEP, Hydroponic isotope labeling of entire plants; SILIP, Stable isotope labeling in planta; SILIA, Stable isotope labeling in Arabidopsis; iTRAQ, Isobaric tags for relative and absolute quantification; TMT, Tandem mass tags; AQUA, Absolute quantification of proteins; AQUIP, Absolute quantitation of isoforms of post-translationally modified proteins. |
Table 2 Different approach, methods, advantages and disadvantages of different phosphoproteome quantitation methods.
Approach | Method | Advantage | Disadvantage |
---|---|---|---|
2D-DIGE | Deliver a visual map of all the proteins and allow the fractionation of thousands of proteins in a complex mixture | Relatively small scale, low sensitivity, poor detection of low-abundance phosphoproteins, and insufficient collected proteins for downstream enrichment methods | |
Stable isotope labeling quantification | SILAC | Lower experimental error | Allow up to only three samples |
HILEP, SILIP, SILIA | Applicable to entire plant and other plant tissues | Only be used in auxotrophic cells | |
iTRAQ and TMT | Allow multiplex up to 8 (iTARQ) and 10 (TMT); Labeling agent doesn’t affect overall peptide behavior thus minimizes experimental error | Reduced identification efficiency as much as 50% in multi-stage activation | |
Chemical derivatization (DiLeu) | Higher protein coverage and quantification efficiency; Cheaper than iTRAQ and TMT; Provide higher reproducibility in quantitation | ||
Label-free quantification | Signal intensity and spectral counting | Allow as many samples as possible | Time-consuming; Less degree of reproducibility in quantitation |
Absolute quantification | AQUA | Allow quantification of isoforms in low abundance and stoichiometry; Achieve accurate and sensitive quantification | |
AQUIP | Can determine the absolute amount of protein | ||
2D-DIGE, Two-dimensional differential gel electrophoresis; SILAC, Stable isotope labeling by amino acids in culture; HILEP, Hydroponic isotope labeling of entire plants; SILIP, Stable isotope labeling in planta; SILIA, Stable isotope labeling in Arabidopsis; iTRAQ, Isobaric tags for relative and absolute quantification; TMT, Tandem mass tags; AQUA, Absolute quantification of proteins; AQUIP, Absolute quantitation of isoforms of post-translationally modified proteins. |
Rice tissue | Distribution of single (S) : double (D) : triple (T) : multiple (M) phosphorylated protein | Frequency of occurrence ratio (pS : pT : pY) | Reference |
---|---|---|---|
Unfractionated whole-cell lysates of rice cells | 84.8 : 12.3 : 2.9 | Nakagami et al, 2010 | |
Leaves from150 mmol/L NaCl treated rice roots | 75 : 25 : 0 | Shen et al, 2012 | |
Pistils | 98 : 2 : 0 (S : D : M) | 87 : 12 : 1 | Wang et al, 2014a |
Magnaporthe oryzae infected seedlings | 86 : 14 : 0 (S : D : M) | Li Y F et al, 2015 | |
Rice nucleus during the early stage of seed germination | 65 : 30 : 5 (S : D : M) | 64 : 31 : 5 | Li M et al, 2015 |
Developing rice anthers | 39 : 23 :14 : 24 (S : D : T : M) | 81.33: 17.06: 1.61 | Ye et al, 2015 |
Rice leaves in response to bacterial blight | (88.3‒89.9) : (11.0‒9.6) : (0.7‒0.5) (S : D : M) | (88.8‒89.2) : (10.6‒10.1) : (0.6‒0.7) | Hou et al, 2015 |
Pistils and seeds | 95.5 : 4.4 : 0.1 (S : D : M) | 90.93 : 8:84 : 0.23 | Qiu et al, 2015 |
ABA induced rice seedlings | 93.2 : 6.7 : 0.1 (S : D : M) | 90:93 : 8.84 : 0.23 | Qiu et al, 2017 |
Brassinosteroid treatment on rice seedlings | (92.9‒93.3) : (6.5‒6.8) : (> 0.3) (S : D : M) | 89.7 : 9.9 : 0.4 | Hou et al, 2017 |
Callus, leaf, root, shoot meristem, young panicle, and mature panicle | 64.82 : 24.83 : 7.29 : 3.06 (S : D : T : M) | 86.0 : 13.0 : 1.0 | Wang et al, 2017 |
Table 3 Distribution of phosphosites having single, double, triple and multiple sites and frequency of phosphosite in rice phosphoproteome study.
Rice tissue | Distribution of single (S) : double (D) : triple (T) : multiple (M) phosphorylated protein | Frequency of occurrence ratio (pS : pT : pY) | Reference |
---|---|---|---|
Unfractionated whole-cell lysates of rice cells | 84.8 : 12.3 : 2.9 | Nakagami et al, 2010 | |
Leaves from150 mmol/L NaCl treated rice roots | 75 : 25 : 0 | Shen et al, 2012 | |
Pistils | 98 : 2 : 0 (S : D : M) | 87 : 12 : 1 | Wang et al, 2014a |
Magnaporthe oryzae infected seedlings | 86 : 14 : 0 (S : D : M) | Li Y F et al, 2015 | |
Rice nucleus during the early stage of seed germination | 65 : 30 : 5 (S : D : M) | 64 : 31 : 5 | Li M et al, 2015 |
Developing rice anthers | 39 : 23 :14 : 24 (S : D : T : M) | 81.33: 17.06: 1.61 | Ye et al, 2015 |
Rice leaves in response to bacterial blight | (88.3‒89.9) : (11.0‒9.6) : (0.7‒0.5) (S : D : M) | (88.8‒89.2) : (10.6‒10.1) : (0.6‒0.7) | Hou et al, 2015 |
Pistils and seeds | 95.5 : 4.4 : 0.1 (S : D : M) | 90.93 : 8:84 : 0.23 | Qiu et al, 2015 |
ABA induced rice seedlings | 93.2 : 6.7 : 0.1 (S : D : M) | 90:93 : 8.84 : 0.23 | Qiu et al, 2017 |
Brassinosteroid treatment on rice seedlings | (92.9‒93.3) : (6.5‒6.8) : (> 0.3) (S : D : M) | 89.7 : 9.9 : 0.4 | Hou et al, 2017 |
Callus, leaf, root, shoot meristem, young panicle, and mature panicle | 64.82 : 24.83 : 7.29 : 3.06 (S : D : T : M) | 86.0 : 13.0 : 1.0 | Wang et al, 2017 |
[1] | Abbasi F M, Komatsu S.2004. A proteomic approach to analyze salt-responsive proteins in rice leaf sheath.Proteomics, 4(7): 2072-2081. |
[2] | Agrawal G K, Thelen J J J M.2006. Large scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape.Mol Cell Proteomics, 5(11): 2044-2059. |
[3] | Agrawal G K, Rakwal R.2008. Plant proteomics: Technologies, Strategies, and Applications. USA: John Wiley & Sons. |
[4] | Agrawal G K, Rakwal R.2011. Rice proteomics: A move toward expanded proteome coverage to comparative and functional proteomics uncovers the mysteries of rice and plant biology.Proteomics, 11(9): 1630-1649. |
[5] | Aryal U K, Krochko J E, Ross A R S.2012. Identification of phosphoproteins inArabidopsis thaliana leaves using polyethylene glycol fractionation, immobilized metal-ion affinity chromatography, two-dimensional gel electrophoresis and mass spectrometry. J Proteom Res, 11: 425-437. |
[6] | Bajguz A.2007. Metabolism of brassinosteroids in plants.Plant Physiol Biochem, 45: 95-107. |
[7] | Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B.2007. Quantitative mass spectrometry in proteomics: A critical review.Anal Bioanal Chem, 389(4): 1017-1031. |
[8] | Bantscheff M, Lemeer S, Savitski M M, Kuster B.2012. Quantitative mass spectrometry in proteomics: Critical review update from 2007 to the present.Anal Bioanal Chem, 404(4): 939-965. |
[9] | Batalha I L, Lowe C R, Roque A C.2012. Platforms for enrichment of phosphorylated proteins and peptides in proteomics.Trends Biotechnol, 30(2): 100-110. |
[10] | Benschop J J, Mohammed S, O’Flaherty M, Heck A J R, Slijper M, Menke F L H.2007. Quantitative phosphoproteomics of early elicitor signaling inArabidopsis. Mol Cell Proteomics, 6: 1198-1214. |
[11] | Berthet J, Rall T W, Sutherland E W.1957. The relationship of epinephrine and glucagon to liver phosphorylase: IV. Effect of epinephrine and glucagon on the reactivation of phosphorylase in liver homogenates.J Biol Chem, 224(1): 463-475. |
[12] | Bindschedler L V, Palmblad M, Cramer R.2008. Hydroponic isotope labelling of entire plants (HILEP) for quantitative plant proteomics: An oxidative stress case study.Phytochemistry, 69(10): 1962-1972. |
[13] | Bindschedler L V, Cramer R.2011. Quantitative plant proteomics.Proteomics, 11(4): 756-775. |
[14] | Boersema P J, Aye T T, van Veen T A, Heck A J, Mohammed S.2008. Triplex protein quantification based on stable isotope labeling by peptide dimethylation applied to cell and tissue lysates.Proteomics, 8: 4624-4632. |
[15] | Boex-Fontvieille E, Davanture M, Jossier M, Zivy M, Hodges M, Tcherkez G.2014. Photosynthetic activity influences cellulose biosynthesis and phosphorylation of proteins involved therein inArabidopsis leaves. J Exp Bot, 65: 4997-5010. |
[16] | Bonhomme L, Valot B, Tardieu F, Zivy M.2012. Phosphoproteome dynamics upon changes in plant water status reveal early events associated with rapid growth adjustment in maize leaves.Mol Cell Proteomics, 11(10): 957-972. |
[17] | Burnett G, Kennedy E P.1954. The enzymatic phosphorylation of proteins.J Biol Chem, 211(2): 969-980. |
[18] | Chandrasekhar K, Dileep A, Lebonah D E, Kumari J P.2014. A short review on proteomics and its applications.Int Lett Nat Sci, 17: 77-84. |
[19] | Chang I F, Hsu J L, Hsu P H, Sheng W A, Lai S J, Lee C, Chen C W, Hsu J C, Wang S Y, Wang L Y, Chen C C.2012. Comparative phosphoproteomic analysis of microsomal fractions ofArabidopsis thaliana and Oryza sativa subjected to high salinity. Plant Sci, 185/186: 131-142. |
[20] | Chen J H, Tian L, Xu H F, Tian D G, Luo Y M, Ren C M, Yang L M, Shi J S.2012. Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis.Plant Omics, 5(2): 194-199. |
[21] | Chen S X, Harmon A C.2006. Advances in plant proteomics.Proteomics, 6(20): 5504-5516. |
[22] | Chen X H, Zhang W F, Zhang B Q, Zhou J C, Wang Y F, Yang Q B, Ke Y Q, He H Q.2011. Phosphoproteins regulated by heat stress in rice leaves.Proteome Sci, 9: 37. |
[23] | Chitteti B R, Peng Z H.2007. Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res, 6(5): 1718-1727. |
[24] | Cohen P.2002. The origins of protein phosphorylation.Nat Cell Biol, 4(5): E127-E130. |
[25] | Cori G T, Green A A.1943. Crystalline muscle phosphorylase: II. Prosthetic group.J Biol Chem, 151: 31-38. |
[26] | Cunningham R, Ma D, Li L J.2012. Mass spectrometry-based proteomics and peptidomics for systems biology and biomarker discovery.Front Biol, 7(4): 313-335. |
[27] | Dietrich A, Mayer J E, Hahlbrock K.1990. Fungal elicitor triggers rapid, transient, and specific protein phosphorylation in parsley cell suspension cultures.J Biol Chem, 265(11): 6360-6368. |
[28] | Engelsberger W R, Schulze W X.2012. Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starvedArabidopsis seedlings. Plant J, 69(6): 978-995. |
[29] | Fageria N K.2007. Yield physiology of rice.J Plant Nutr, 30(6): 843-879. |
[30] | Fan S L, Meng Y Y, Song M Z, Pang C Y, Wei H L, Liu J, Zhan X J, Lan J Y, Feng C H, Zhang S X, Yu S X.2014. Quantitative phosphoproteomics analysis of nitric oxide-responsive phospho- proteins in cotton leaf.PLoS One, 9(4): e94261. |
[31] | Fang Y X, Deng X X, Lu X L, Zheng J J, Jiang H, Rao Y C, Zeng D L, Hu J, Zhang X Q, Xue D W.2019. Differential phosphop- roteome study of the response to cadmium stress in rice.Ecotox Environ Safe, 180: 780-788. |
[32] | Fíla J, Honys D.2012. Enrichment techniques employed in phosphoproteomics.Amino Acids, 43(3): 1025-1047. |
[33] | Fischer E H, Krebs E G.1955. Conversion of phosphorylaseb to phosphorylase a in muscle extracts. J Biol Chem, 216(1): 121-132. |
[34] | Fischer E H.2010. Phosphorylase and the origin of reversible protein phosphorylation.Biol Chem, 391: 131-137. |
[35] | Fitzgerald M A, McCouch S R, Hall R D.2009. Not just a grain of rice: The quest for quality. Trends Plant Sci, 14(3): 133-139. |
[36] | Gallego-Bartolome J, Minguet E G, Grau-Enguix F, Abbas M, Locascio A, Thomas S G, Alabadí D, Blazquez M A.2012. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways inArabidopsis. Proc Natl Acad Sci USA, 109: 13446-13451. |
[37] | Gaspari M, Cuda G.2011. Nano LC-MS/MS: A robust setup for proteomic analysis.Methods Mol Biol, 790: 115-126. |
[38] | Gates M B, Tomer K B, Deterding L J.2010. Comparison of metal and metal oxide media for phosphopeptide enrichment prior to mass spectrometric analyses.J Am Soc Mass Spec, 21(10): 1649-1659. |
[39] | Ge C L, Wang Z G, Wan D Z, Ding Y, Wang Y L, Shang Q, Luo S S.2009. Proteomic study for responses to cadmium stress in rice seedlings.Rice Sci, 16(1): 33-44. |
[40] | Ghelis T, Bolbach G, Clodic G, Habricot Y, Miginiac E, Sotta B, Jeannette E.2008. Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes inArabidopsis seeds and suspension cells. Plant Physiol, 148(3): 1668-1680. |
[41] | Gruhler A, Schulze W X, Matthiesen R, Mann M, Jensen O N.2005. Stable isotope labeling ofArabidopsis thaliana cells and quantitative proteomics by mass spectrometry. Mol Cell Proteomics, 4(11): 1697-1709. |
[42] | Guo H Q, Li L, Aluru M, Aluru S, Yin Y H.2013. Mechanisms and networks for brassinosteroid regulated gene expression.Curr Opin Plant Biol, 16(5): 545-553. |
[43] | Gygi S P, Rist B, Gerber S A, Turecek F, Gelb M H, Aebersold R.1999. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags.Nat Biotechnol, 17: 994-999. |
[44] | Han C, Wang K, Yang P F.2014a. Gel-based comparative phosphoproteomic analysis on rice embryo during germination.Plant Cell Physiol, 55(8): 1376-1394. |
[45] | Han C, Yang P F, Sakata K, Komatsu S.2014b. Quantitative proteomics reveals the role of protein phosphorylation in rice embryos during early stages of germination.J Proteome Res, 13(3): 1766-1782. |
[46] | He H Q, Li J X.2008. Proteomic analysis of phosphoproteins regulated by abscisic acid in rice leaves.Biochem Biophl Res Co, 371(4): 883-888. |
[47] | Hou Y X, Qiu J H, Tong X H, Wei X J, Nallamilli B R, Wu W H, Huang S W, Zhang J.2015. A comprehensive quantitative phosphoproteome analysis of rice in response to bacterial blight.BMC Plant Biol, 15: 163. |
[48] | Hou Y X, Qiu J H, Wang Y F, Li Z Y, Zhao J, Tong X H, Lin H Y, Zhang J.2017. A quantitative proteomic analysis of brassinosteroid- induced protein phosphorylation in rice (Oryza sativa L.). Front Plant Sci, 8: 514. |
[49] | Howden A J M, Salek M, Miguet L, Pullen M, Thomas B, Knight M R, Sweetlove L J.2011. The phosphoproteome ofArabidopsis plants lacking the oxidative signal-inducible1 (OXI1) protein kinase. New Phytol, 190(1): 49-56. |
[50] | Hubbard M J, Cohen P.1993. On target with a new mechanism for the regulation of protein phosphorylation.Trends Biochem Sci, 18(5): 172-177. |
[51] | Ingebritsen T S, Foulkes J G, Cohen P.1983. The protein phosphatases involved in cellular regulation: 2. Glycogen metabolism.Eur J Biochem, 132(2): 263-274. |
[52] | Javier G B, Minguet E G, Federico G E, Mohamad A, Locascio A, Thomas S G, Alabadí D, Miguel A B.2012. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways inArabidopsis. Proc Natl Acad Sci USA, 109: 13446-13451. |
[53] | Johnson L N, Barford D.1993. The effects of phosphorylation on the structure and function of proteins.Annu Rev Biophys Biomol Struct, 22: 199-232. |
[54] | Johnson L N, Lewis R J.2001. Structural basis for control by phosphorylation.Chem Rev, 101: 2209-2242. |
[55] | Jones J D G, Dangl J L.2006. The plant immune system.Nature, 444: 323-329. |
[56] | Ke Y Q, Han G Q, He H Q, Li J X.2009. Differential regulation of proteins and phosphoproteins in rice under drought stress.Biochem Biophys Res Commun, 379(1): 133-138. |
[57] | Kersten B, Agrawal G K, Iwahashi H, Rakwal R.2006. Plant phosphoproteomics: A long road ahead.Proteomics, 6(20): 5517-5528. |
[58] | Kersten B, Agrawal G K, Durek P, Neigenfind J, Schulze W, Walther D, Rakwal R.2009. Plant phosphoproteomics: An update.Proteomics, 9(4): 964-988. |
[59] | Khan M, Takasaki H, Komatsu S.2005. Comprehensive phosphoproteome analysis in rice and identification of phosphoproteins responsive to different hormones/stresses.J Proteome Res, 4(5): 1592-1599. |
[60] | Kline J C, De Luca C J.2014. Error reduction in EMG signal decomposition.J Neurophysiol, 112(11): 2718-2728. |
[61] | Kline-Jonakin K G, Barrett-Wilt G A, Sussman M R.2011. Quantitative plant phosphoproteomics.Curr Opin Plant Biol, 14(5): 507-511. |
[62] | Krebs E G, Fischer E H.1956. The phosphorylase b to a converting enzyme of rabbit skeletal muscle.Biochimi Biophys Acta, 20: 150-157. |
[63] | Kresge N, Simoni R D, Hill R L.2011. The Process of reversible phosphorylation: The work of Edmond H. Fischer.J Biol Chem, 286(3): e1-e2. |
[64] | Kweon H K, Håkansson K.2006. Selective zirconium dioxide- based enrichment of phosphorylated peptides for mass spectrometric analysis.Anal Chem, 78(6): 1743-1749. |
[65] | Leibler D C.2002. Introduction to Proteomics: Tools for the New Biology. Totowa NJ: Humana press. |
[66] | Levene P A, Alsberg C L.1906. The cleavage products of vitellin.J Biol Chem, 2: 127-133. |
[67] | Li M, Yin X J, Sakata K, Yang P F, Komatsu S.2015. Proteomic analysis of phosphoproteins in the rice nucleus during the early stage of seed germination.J Proteome Res, 14(7): 2884-2896. |
[68] | Li Y F, Ye Z J, Nie Y F, Zhang J, Wang G L, Wang Z Z.2015. Comparative phosphoproteome analysis ofMagnaporthe oryzae- responsive proteins in susceptible and resistant rice cultivars. J Proteomic, 115: 66-80. |
[69] | Lipmann F A, Levene P A.1932. Serinephosphoric acid obtained on hydrolysis of vitellinic acid.J Biol Chem, 98: 109-114. |
[70] | Macek B, Mann M, Olsen J V.2009. Global and site-specific quantitative phosphoproteomics: Principles and applications.Annu Rev Pharmacol Toxicol, 49: 199-221. |
[71] | Magdeldin S, Enany S, Yoshida Y, Xu B, Zhang Y, Zureena Z, Lokamani I, Yaoita E, Yamamoto T.2014. Basics and recent advances of two dimensional-polyacrylamide gel electrophoresis.Clin Proteom, 11(1): 16. |
[72] | Mandell D J, Chorny I, Groban E S, Wong S E, Levine E, Rapp C S, Jacobson M P.2007. Strengths of hydrogen bonds involving phosphorylated amino acid side chains.J Am Chem Soc, 129: 820-827. |
[73] | Meleady P.2018. Two-dimensional gel electrophoresis and 2D-DIGE.Methods Mol Biol, 1664: 3-14. |
[74] | Molina H, Horn D M, Tang N, Mathivanan S, Pandey A.2007. Global proteomic profiling of phosphopeptides using electron transfer dissociation tandem mass spectrometry.Proc Natl Acad Sci USA, 104(7): 2199-2204. |
[75] | Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K.2010. Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants.Plant Physiol, 153(3): 1161-1174. |
[76] | Neilson K A, Ali N A, Muralidharan S, Mirzaei M, Mariani M, Assadourian G, Lee A, van Sluyter S C, Haynes P A.2011. Less label, more free: Approaches in label-free quantitative mass spectrometry.Proteomics, 11(4): 535-553. |
[77] | Niittylä T, Fuglsang A T, Palmgren M G, Frommer W B, Schulze W X.2007. Temporal analysis of sucrose-induced phosphorylation changes in plasma membrane proteins ofArabidopsis. Mol Cell Proteomics, 6(10): 1711-1726. |
[78] | Nilsson C L.2012. Advances in quantitative phosphoproteomics.Anal Chem, 84(2): 735-746. |
[79] | Nishi H, Shaytan A, Panchenko A R.2014. Physicochemical mechanisms of protein regulation by phosphorylation.Front Genet, 5: 270. |
[80] | Nühse T S, Stensballe A, Jensen O N, Peck S C.2004. Phospho- proteomics of theArabidopsis plasma membrane and a new phosphorylation site database. Plant Cell, 16(9): 2394-2405. |
[81] | Oda Y, Huang K, Cross F R, Cowburn D, Chait B T.1999. Accurate quantitation of protein expression and site-specific phosphorylation.Proc Natl Acad Sci USA, 96(12): 6591-6596. |
[82] | Ong S E, Blagoev B, Kratchmarova I, Kristensen D B, Steen H, Pandey A, Mann M.2002. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics.Mol Cell Proteomics, 1(5): 376-386. |
[83] | Ong S E, Mann M.2005. Mass spectrometry-based proteomics turns quantitative.Nat Chem Biol, 1: 252-262. |
[84] | Ozlu N, Akten B, Timm W, Haseley N, Steen H, Steen J.2010. Phosphoproteomics.Wiley Interdiscip Rev: Syst Biol Med, 2(3): 255-276. |
[85] | Qiu J H, Hou Y X, Tong X H, Wang Y F, Lin H Y, Liu Q, Zhang W, Li Z Y, Nallamilli B R, Zhang J.2015. Quantitative phosphoproteomic analysis of early seed development in rice (Oryza sativa L.). Plant Mol Biol, 90(3): 249-265. |
[86] | Qiu J H, Hou Y X, Wang Y F, Li Z Y, Zhao J, Tong X H, Lin H Y, Wei X J, Ao H J, Zhang J.2017. A comprehensive proteomic survey of ABA-induced protein phosphorylation in rice (Oryza sativa L.). Int J Mol Sci, 18(1): E60. |
[87] | Reiland S, Finazzi G, Endler A, Willig A, Baerenfaller K, Grossmann J, Gerrits B, Rutishauser D, Gruissem W, Rochaix J D.2011. Comparative phosphoproteome profiling reveals a function of the STN8 kinase in fine-tuning of cyclic electron flow (CEF).Proc Natl Acad Sci USA, 108: 12955-12960. |
[88] | Reinders J, Sickmann A.2005. State-of-the-art in phospho- proteomics.Proteomics, 5(16): 4052-4061. |
[89] | Ross P L, Huang Y N, Marchese J N, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin D J.2004. Multiplexed protein quantitation inSaccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics, 3(12): 1154-1169. |
[90] | Schaff J E, Mbeunkui F, Blackburn K, Bird D M, Goshe M B.2008. SILIP: A novel stable isotope labeling method for in planta quantitative proteomic analysis.Plant J, 56(5): 840-854. |
[91] | Schmidt S R, Schweikart F, Andersson M E.2007. Current methods for phosphoprotein isolation and enrichment.J Chromatogr B Analyt Technol Biomed Life Sci., 849: 154-162. |
[92] | Schulze W X, Schneider T, Starck S, Martinoia E, Trentmann O.2012. Cold acclimation induces changes inArabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J, 69(3): 529-541. |
[93] | Shen F, Hu Y, Guan P, Ren X.2012. Ti4+-phosphate functionalized cellulose for phosphopeptides enrichment and its application in rice phosphoproteome analysis.J Chromatogr B Analyt Technol Biomed Life Sci, 902: 108-115. |
[94] | Silva-Sanchez C, Li H Y, Chen S X.2015. Recent advances and challenges in plant phosphoproteomics.Proteomics, 15: 1127-1141. |
[95] | Singh A, Giri J, Kapoor S, Tyagi A K, Pandey G K.2010. Protein phosphatase complement in rice: Genome-wide identification and transcriptional analysis under abiotic stress conditions and reproductive development.BMC Genom, 11: 435. |
[96] | Stokes M P, Farnsworth C L, Moritz A, Silva J C, Jia X Y, Lee K A, Guo A L, Polakiewicz R D, Comb M J.2012. PTMScan direct: Identification and quantification of peptides from critical signaling proteins by immunoaffinity enrichment coupled with LC-MS/MS.Mol Cell Proteomics, 11(5): 187-201. |
[97] | Sutherland E W, Wosilait W D.1955. Inactivation and activation of liver phosphorylase.Nature, 175: 169-170. |
[98] | Tan F, Li G S, Chitteti B R, Peng Z H.2007. Proteome and phosphoproteome analysis of chromatin associated proteins in rice (Oryza sativa). Proteomics, 7: 4511-4527. |
[99] | Trinidad J C, Specht C G, Thalhammer A, Schoepfer R, Burlingame A L.2006. Comprehensive identification of phosphorylation sites in postsynaptic density preparations.Mol Cell Proteomics, 5(5): 914-922. |
[100] | Unlu M, Morgan M E, Minden J S.1997. Difference gel electrophoresis: A single gel method for detecting changes in protein extracts.Electrophoresis, 18(11): 2071-2077. |
[101] | Walton A, Stes E, de Smet I, Goormachtig S, Gevaert K.2015. Plant hormone signalling through the eye of the mass spectrometer.Proteomics, 15: 1113-1126. |
[102] | Wang K, Zhao Y, Li M, Gao F, Yang M K, Wang X, Li S Q, Yang P F.2014. Analysis of phosphoproteome in rice pistil.Proteomics, 14(20): 2319-2334. |
[103] | Wang P C, Xue L, Batelli G, Lee S, Hou Y J, van Oosten M J, Zhang H M, Tao W A, Zhu J K.2013. Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action.Proc Natl Acad Sci USA, 110: 11205-11210. |
[104] | Wang W F, Bai M Y, Wang Z Y.2014. The brassinosteroid signaling network: A paradigm of signal integration.Curr Opin Plant Biol, 21: 147-153. |
[105] | Wang Y F, Tong X H, Qiu J H, Li Z Y, Zhao J, Hou Y X, Tang L Q, Zhang J.2017. A phosphoproteomic landscape of rice (Oryza sativa) tissues. Physiol Plant, 160(4): 458-475. |
[106] | Wang Z Y, Bai M Y, Oh E, Zhu J Y.2012. Brassinosteroid signaling network and regulation of photomorphogenesis.Annu Rev Genet, 46: 701-724. |
[107] | Watson T J, Sparkman D O.2007. Introduction to Mass Spectrometry: Instrumentation, Applications, and Strategies of Data Interpretation. Chichester West Sussex, England: John Wiley & Sons, Ltd. |
[108] | Wu K J, Shaler T A, Becker C H.1994. Time-of-flight mass spectrometry of underivatized single-stranded DNA oligomers by matrix-assisted laser desorption.Anal Chem, 66(10): 1637-1645. |
[109] | Xiang F, Ye H, Chen R B, Fu Q, Li L J.2010. N, N-dimethyl leucines as novel isobaric tandem mass tags for quantitative proteomics and peptidomics.Anal Chem, 82(7): 2817-2825. |
[110] | Yang Z, Guo G Y, Zhang M Y, LiuC Y, Hu Q, Lam H, Cheng H, Xue Y, Li J Y, Li N.2013. Stable isotope metabolic labeling- based quantitative phosphoproteomic analysis ofArabidopsis mutants reveals ethylene-regulated time-dependent phosphoproteins and putative substrates of constitutive triple response 1 kinase. Mol Cell Protemics, 12(12): 3559-3582. |
[111] | Yao X D, Freas A, Ramirez J, Demirev P A, Fenselau C.2001. Proteolytic 18O labeling for comparative proteomics: Model studies with two serotypes of adenovirus.Anal Chem, 73(13): 2836-2842. |
[112] | Ye J Y, Zhang Z B, Long H F, Zhang Z M, Hong Y, Zhang X M, You C J, Liang W Q, Ma H, Lu P L.2015. Proteomic and phosphoproteomic analyses reveal extensive phosphorylation of regulatory proteins in developing rice anthers.Plant J, 84: 527-544. |
[113] | Yi E C, Li X J, Cooke K, Lee H, Raught B, Page A, Aneliunas V, Hieter P, Goodlett D R, Aebersold R.2005. Increased quantitative proteome coverage with 13C/12C-based, acid- cleavable isotope-coded affinity tag reagent and modified data acquisition scheme.Proteomics, 5(2): 380-387. |
[114] | Yoshida S.1972. Physiological aspects of grain yield.Ann Rev Plant Physiol, 23: 437-464. |
[115] | Zhang H T, Zhou H J, Berke L, Heck A J R, Mohammed S, Scheres B, Menke F L H.2013. Quantitative phosphoproteomics after auxin-stimulated lateral root induction identifies a SNX1 phosphorylation site required for growth.Mol Cell Proteomics, 12(5): 1158-1169. |
[116] | Zhang J, Guo D, Chang Y X, You C J, Li X W, Dai X X, Weng Q J, Zhang J W, Chen G X, Li X H, Liu H F, Han B, Zhang Q F, Wu C Y.2007. Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analyzing 13804 T-DNA flanking sequences from an enhancer-trap mutant library.Plant J, 49: 947-959. |
[117] | Zhang Z X, Chen J, Lin S S, Li Z, Cheng R H, Fang C X, Chen H F, Lin W X.2012. Proteomic and phosphoproteomic determination of ABA’s effects on grain-filling ofOryza sativa L. inferior spikelets. Plant Sci, 185/186: 259-273. |
[118] | Zhang Z X, Zhao H, Tang J, Li Z, Li Z, Chen D M, Lin W X.2014. A proteomic study on molecular mechanism of poor grain-filling of rice (Oryza sativa L.) inferior spikelets. PLoS One, 9(2): e89140. |
[119] | Zhao Y M, Jensen O N.2009. Modification-specific proteomics: Strategies for characterization of post-translational modifications using enrichment techniques.Proteomics, 9: 4632-4641. |
[120] | Zhong M, Li S F, Huang F L, Qiu J H, Zhang J, Sheng Z H, Tang S Q, Wei X J, Hu P S.2017. The phosphoproteomic response of rice seedlings to cadmium stress.Int J Mol Sci, 18: E2055. |
[121] | Zuo J R, Li J Y.2014. Molecular dissection of complex agronomic traits of rice: A team effort by Chinese scientists in recent years. Nat Sci Rev, 1(2): 253-276. |
No related articles found! |
阅读次数 | ||||||
全文 |
|
|||||
摘要 |
|
|||||