Protein Dynamics in Young Maize Root Hairs in Response to Macro- and Micronutrient Deprivation

Journal of Proteome Research

Volumn 14, Issue 8, 2015, Pages 3362-3371

  Li, Zhi ^a   Phillip, Daniel ^a   Neuhäuser, Benjamin ^a   Schulze, Waltraud X ^a   Ludewig, Uwe ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

iron; macronutrient; micronutrient; nitrogen; nutrition; phosphorus; root hair; Zea mays

Indexed keywords

AHA11 PROTEIN; AHA2 PROTEIN; BIN 9 PROTEIN; FRUCTOSE BISPHOSPHATASE; GLCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; IRON; MAGNESIUM; MANGANESE; MITOCHONDRIAL PROTEIN; NITRITE REDUCTASE; NITROGEN; NUCLEAR PROTEIN; OXIDOREDUCTASE; PEROXIDASE; PHOSPHATE; PHOSPHATE TRANSPORTER; PHOSPHOGLYERATE KINASE; PHOSPHORUS; POTASSIUM; PROTEOME; PROTON PUMP; PYROPHOSPHATE FRUCTOSE 6 PHOSPHATE 1 PHOSPHOTRANSFERASE,; REGULATOR PROTEIN; RIBOSOME PROTEIN; TRACE ELEMENT; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ZINC; ZINC ION; PEPTIDE; PHOSPHOPEPTIDE;

AMINO ACID METABOLISM; AMINO ACID SYNTHESIS; ARTICLE; CARBOHYDRATE METABOLISM; CARBON METABOLISM; CITRIC ACID CYCLE; CONTROLLED STUDY; DENSITY; DOWN REGULATION; FATTY ACID SYNTHESIS; GLYCOLYSIS; GROWTH RATE; LIPID METABOLISM; MAIZE; MOLECULAR DYNAMICS; NITROGEN FIXATION; NITROGEN METABOLISM; NONHUMAN; NUTRIENT SOLUTION; NUTRITIONAL DEFICIENCY; PLANT GROWTH; PLANT NUTRIENT; POTASSIUM DEFICIENCY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; PROTEOMICS; RNA BINDING; ROOT DEVELOPMENT; ROOT HAIR; ROOT LENGTH; SECONDARY METABOLISM; SIGNAL TRANSDUCTION; SODIUM METABOLISM; SURFACE PROPERTY; UBIQUITINATION; UNINDEXED SEQUENCE; UPREGULATION; CLASSIFICATION; CLUSTER ANALYSIS; CROP PRODUCTION; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; KINETICS; LIQUID CHROMATOGRAPHY; METABOLISM; PLANT ROOT; PROCEDURES; TANDEM MASS SPECTROMETRY;

ZEA MAYS;

CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; CROP PRODUCTION; KINETICS; MAGNESIUM; METABOLIC NETWORKS AND PATHWAYS; MICRONUTRIENTS; NITROGEN; PEPTIDES; PHOSPHOPEPTIDES; PHOSPHORUS; PLANT PROTEINS; PLANT ROOTS; POTASSIUM; PROTEOME; PROTEOMICS; TANDEM MASS SPECTROMETRY; ZEA MAYS;

EID: 84938791236     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b00399     Document Type: Article

References (43)

1. Datta, S.; Kim, C. M.; Pernas, M.; Pires, N. D.; Proust, H.; Tam, T.; Vijayakumar, P.; Dolan, L. Root hairs: development, growth and evolution at the plant-soil interface Plant Soil 2011, 346, 1-14 10.1007/s11104-011-0845-4
2. Bates, T. R.; Lynch, J. P. Root hairs confer a competitive advantage under low phosphorus availability Plant Soil 2001, 236, 243-250 10.1023/A:1012791706800
3. Gahoonia, T. S.; Nielsen, N. E. Phosphorus (P) uptake and growth of a root hairless barley mutant (bald root barley, brb) and wild type in low- and high-P soils Plant, Cell Environ. 2003, 26, 1759-1766 10.1046/j.1365-3040.2003.01093.x
4. Gilroy, S.; Jones, D. L. Through form to function: root hair development and nutrient uptake Trends Plant Sci. 2000, 5, 56-60 10.1016/S1360-1385(99)01551-4
5. Clowes, F. A. L. Pattern in root meristem development in angiosperms New Phytol. 2000, 146, 83-94 10.1046/j.1469-8137.2000.00614.x
6. Nestler, J.; Liu, S.; Wen, T. J.; Paschold, A.; Marcon, C.; Tang, H. M.; Li, D.; Li, L.; Meeley, R. B.; Sakai, H.; Bruce, W.; Schnable, P. S.; Hochholdinger, F. Roothairless5, which functions in maize (Zea mays L.) root hair initiation and elongation encodes a monocot-specific NADPH oxidase Plant J. 2014, 79, 729-740 10.1111/tpj.12578
7. Masucci, J. D.; Rerie, W. G.; Foreman, D. R.; Zhang, M.; Galway, M. E.; Marks, M. D.; Schiefelbein, J. W. The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana Development 1996, 122, 1253-1260
8. Schiefelbein, J.; Huang, L.; Zheng, X. Regulation of epidermal cell fate in Arabidopsis roots: the importance of multiple feedback loops Front. Plant Sci. 2014, 5, 47 10.3389/fpls.2014.00047
9. Wen, T. J.; Hochholdinger, F.; Sauer, M.; Bruce, W.; Schnable, P. S. The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis Plant Physiol. 2005, 138, 1637-1643 10.1104/pp.105.062174
10. Hochholdinger, F.; Wen, T. J.; Zimmermann, R.; Chimot-Marolle, P.; da Costa e Silva, O.; Bruce, W.; Lamkey, K. R.; Wienand, U.; Schnable, P. S. The maize (Zea mays L.) roothairless 3 gene encodes a putative GPI-anchored, monocot-specific, COBRA-like protein that significantly affects grain yield Plant J. 2008, 54, 888-898 10.1111/j.1365-313X.2008.03459.x
11. Ma, Z.; Bielenberg, D. G.; Brown, K. M.; Lynch, J. P. Regulation of root hair density by phosphorus availability in Arabidopsis thaliana Plant, Cell Environ. 2001, 24, 459-467 10.1046/j.1365-3040.2001.00695.x
12. Foehse, D.; Jungk, A. Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants Plant Soil 1983, 74, 359-368 10.1007/BF02181353
13. Pitts, R. J.; Cernac, A.; Estelle, M. Auxin and ethylene promote root hair elongation in Arabidopsis Plant J. 1998, 16, 553-560 10.1046/j.1365-313x.1998.00321.x
14. Nadeem, M.; Mollier, A.; Morel, C.; Vives, A.; Prudhomme, L.; Pellerin, S. Relative contribution of seed phosphorus reserves and exogenous phosphorus uptake to maize (Zea mays L.) nutrition during early growth stages Plant Soil 2011, 346, 231-244 10.1007/s11104-011-0814-y
15. White, P. J.; Veneklaas, E. J. Nature and nurture: the importance of seed phosphorus Plant Soil 2012, 357, 1-8 10.1007/s11104-012-1128-4
16. Nagy, R.; Vasconcelos, M.; Zhao, S.; McElver, J.; Bruce, W.; Amrhein, N.; Raghothama, K.; Bucher, M. Differential regulation of five Pht1 phosphate transporters from maize (Zea mays L.) Plant Biol. (Berlin, Ger.) 2006, 8, 186-197 10.1055/s-2005-873052
17. Nestler, J.; Schutz, W.; Hochholdinger, F. Conserved and unique features of the maize (Zea mays L.) root hair proteome J. Proteome Res. 2011, 10, 2525-2537 10.1021/pr200003k
18. Lan, P.; Li, W.; Lin, W. D.; Santi, S.; Schmidt, W. Mapping gene activity of Arabidopsis root hairs Genome Biol. 2013, 14, R67 10.1186/gb-2013-14-6-r67
19. Brechenmacher, L.; Nguyen, T. H.; Hixson, K.; Libault, M.; Aldrich, J.; Pasa-Tolic, L.; Stacey, G. Identification of soybean proteins from a single cell type: the root hair Proteomics 2012, 12, 3365-73 10.1002/pmic.201200160
20. Scheible, W. R.; Morcuende, R.; Czechowski, T.; Fritz, C.; Osuna, D.; Palacios-Rojas, N.; Schindelasch, D.; Thimm, O.; Udvardi, M. K.; Stitt, M. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen Plant Physiol. 2004, 136, 2483-2499 10.1104/pp.104.047019
21. Krouk, G.; Crawford, N. M.; Coruzzi, G. M.; Tsay, Y. F. Nitrate signaling: adaptation to fluctuating environments Curr. Opin. Plant Biol. 2010, 13, 265-272 10.1016/j.pbi.2009.12.003
22. Morcuende, R.; Bari, R.; Gibon, Y.; Zheng, W.; Pant, B. D.; Blasing, O.; Usadel, B.; Czechowski, T.; Udvardi, M. K.; Stitt, M.; Scheible, W. R. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus Plant, Cell Environ. 2007, 30, 85-112 10.1111/j.1365-3040.2006.01608.x
23. Osuna, D.; Usadel, B.; Morcuende, R.; Gibon, Y.; Blasing, O. E.; Hohne, M.; Gunter, M.; Kamlage, B.; Trethewey, R.; Scheible, W. R.; Stitt, M. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings Plant J. 2007, 49, 463-491 10.1111/j.1365-313X.2006.02979.x
24. Lin, W. D.; Liao, Y. Y.; Yang, T. J.; Pan, C. Y.; Buckhout, T. J.; Schmidt, W. Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling Plant Physiol. 2011, 155, 1383-402 10.1104/pp.110.166520
25. Gifford, M. L.; Dean, A.; Gutierrez, R. A.; Coruzzi, G. M.; Birnbaum, K. D. Cell-specific nitrogen responses mediate developmental plasticity Proc. Natl. Acad. Sci. U. S. A. 2008, 105, 803-808 10.1073/pnas.0709559105
26. Rappsilber, J.; Ishihama, Y.; Mann, M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics Anal. Chem. 2003, 75, 663-70 10.1021/ac026117i
27. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26, 1367-72 10.1038/nbt.1511
28. Cox, J.; Neuhauser, N.; Michalski, A.; Scheltema, R. A.; Olsen, J. V.; Mann, M. Andromeda: a peptide search engine integrated into the MaxQuant environment J. Proteome Res. 2011, 10, 1794-805 10.1021/pr101065j
29. Zauber, H.; Schulze, W. X. Proteomics wants cRacker: automated standardized data analysis of LC-MS derived proteomic data J. Proteome Res. 2012, 11, 5548-5555 10.1021/pr300413v
30. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing J. R Stat Soc. Ser. B 1995, 57, 289-300
31. Thimm, O.; Blasing, O.; Gibon, Y.; Nagel, A.; Meyer, S.; Kruger, P.; Selbig, J.; Muller, L. A.; Rhee, S. Y.; Stitt, M. MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes Plant J. 2004, 37, 914-939 10.1111/j.1365-313X.2004.02016.x
32. Tanz, S. K.; Castleden, I.; Hooper, C. M.; Vacher, M.; Small, I.; Millar, H. A. SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis Nucleic Acids Res. 2013, 41, D1185-D1191 10.1093/nar/gks1151
33. Schulze, W. X.; Usadel, B. Quantitation in mass-spectrometry-based proteomics Annu. Rev. Plant Biol. 2010, 61, 491-516 10.1146/annurev-arplant-042809-112132
34. Marschner, P. Marschners Mineral Nutrition of Higher Plants; Academic Press: London, 2011.
35. Li, J.; Wu, X. D.; Hao, S. T.; Wang, X. J.; Ling, H. Q. Proteomic response to iron deficiency in tomato root Proteomics 2008, 8, 2299-2311 10.1002/pmic.200700942
36. Lan, P.; Li, W.; Wen, T. N.; Shiau, J. Y.; Wu, Y. C.; Lin, W.; Schmidt, W. iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis Plant Physiol. 2011, 155, 821-834 10.1104/pp.110.169508
37. Engelsberger, W. R.; Schulze, W. X. Nitrate and ammonium lead to distinct global dynamic phosphorylation patterns when resupplied to nitrogen-starved Arabidopsis seedlings Plant J. 2012, 69, 978-995 10.1111/j.1365-313X.2011.04848.x
38. Hopff, D.; Wienkoop, S.; Luthje, S. The plasma membrane proteome of maize roots grown under low and high iron conditions J. Proteomics 2013, 91, 605-618 10.1016/j.jprot.2013.01.006
39. Zargar, S. M.; Fujiwara, M.; Inaba, S.; Kobayashi, M.; Kurata, R.; Ogata, Y.; Fukao, Y. Correlation analysis of proteins responsive to Zn, Mn, or Fe deficiency in Arabidopsis roots based on iTRAQ analysis Plant Cell Rep. 2015, 34, 157-166 10.1007/s00299-014-1696-2
40. Stetter, M. G.; Schmid, K.; Ludewig, U. Uncovering Genes and Ploidy Involved in the High Diversity in Root Hair Density, Length and Response to Local Scarce Phosphate in Arabidopsis thaliana PLoS One 2015, 10, e0120604 10.1371/journal.pone.0120604
41. Schaaf, G.; Ludewig, U.; Erenoglu, B. E.; Mori, S.; Kitahara, T.; von Wiren, N. ZmYS1 functions as a proton-coupled symporter for phytosiderophore- and nicotianamine-chelated metals J. Biol. Chem. 2004, 279, 9091-9096 10.1074/jbc.M311799200
42. Nadeem, M.; Mollier, A.; Morel, C.; Vives, A.; Prudhomme, L.; Pellerin, S. Maize (Zea mays L.) endogenous seed phosphorus remobilization is not influenced by exogenous phosphorus during germination and early growth stages Plant Soil 2012, 357, 13-25 10.1007/s11104-011-1111-5
43. Schreiber, L.; Franke, R.; Lessire, R. Biochemical characterization of elongase activity in corn (Zea mays L.) roots Phytochemistry 2005, 66, 131-138 10.1016/j.phytochem.2004.11.022