Complementary proteome and transcriptome profiling in phosphate-deficient arabidopsis roots reveals multiple levels of gene regulation

Molecular and Cellular Proteomics

Volumn 11, Issue 11, 2012, Pages 1156-1166

  Lan, Ping ^a   Li, Wenfeng ^a   Schmidt, Wolfgang ^a,b,c  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARBON; MEMBRANE LIPID; MESSENGER RNA; PHOSPHATE; PROTEOME; TRANSCRIPTOME;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; ENVIRONMENTAL CHANGE; EXHAUSTION; GENE ACTIVITY; GENE CONTROL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLYCOLYSIS; NONHUMAN; PHOSPHATE DEFICIENCY; PHOSPHATE METABOLISM; PLANT GROWTH; PLANT ROOT; POSTTRANSCRIPTIONAL GENE SILENCING; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RNA SEQUENCE; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARBON; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GLUCOSE; HOMEOSTASIS; ISOTOPE LABELING; LIPID BILAYERS; MODELS, BIOLOGICAL; PHOSPHATES; PLANT ROOTS; PROTEIN INTERACTION MAPS; PROTEOME; PROTEOMICS; RNA, MESSENGER;

ARABIDOPSIS;

EID: 84869236431     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.020461     Document Type: Article

References (44)

1. Ong, S. E., and Mann, M. (2005) Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 1, 252-262
2. Liberman, L. M., Sozzani, R., and Benfey, P. N. (2012) Integrative systems biology: an attempt to describe a simple weed. Curr. Opin. Plant Biol. 15, 162-167
3. Wu, P., Ma, L., Hou, X., Wang, M., Wu, Y., Liu, F., and Deng, X. W. (2003) Phosphate starvation triggers distinct alterations of genome expression in Arabidopsis roots and leaves. Plant Physiol. 132, 1260-1271 (Pubitemid 36872876)
4. Hammond, J. P., Bennett, M. J., Bowen, H. C., Broadley, M. R., Eastwood, D. C., May, S. T., Rahn, C., Swarup, R., Woolaway, K. E., and White, P. J. (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiol. 132, 578-596 (Pubitemid 36715059)
5. Misson, J., Raghothama, K. G., Jain, A., Jouhet, J., Block, M. A., Bligny, R., Ortet, P., Creff, A., Somerville, S., Rolland, N., Doumas, P., Nacry, P., Herrerra-Estrella, L., Nussaume, L., and Thibaud, M. C. (2005) A ge-nome- wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. U.S.A. 102, 11934-11939 (Pubitemid 41170828)
6. Bari, R., Datt, Pant, B., Stitt, M., and Scheible, W. R. (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988-999
7. Morcuende, R., Bari, R., Gibon, Y., Zheng, W., Pant, B. D., Bläsing, O., Usadel, B., Czechowski, T., Udvardi, M. K., Stitt, M., and Scheible, W. R. (2007) Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell Environ. 30, 85-112 (Pubitemid 44924284)
8. Müller, R., Morant, M., Jarmer, H., Nilsson, L., and Nielsen, T. H. (2007) Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol. 143, 156-171 (Pubitemid 46133626)
9. Marchive, C., Yehudai-Resheff, S., Germain, A., Fei, Z., Jiang, X., Judkins, J., Wu, H., Fernie, A. R., Fait, A., and Stern, D. B. (2009) Abnormal physiological and molecular mutant phenotypes link chloroplast polynucleotide phosphorylase to the phosphorus deprivation response in Arabidopsis. Plant Physiol. 151, 905-924
10. Lin, W. D., Liao, Y. Y., Yang, T. J., Pan, C. Y., Buckhout, T. J., and Schmidt, W. (2011) Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling. Plant Physiol. 155, 1383-1402
11. Hammond, J. P., Broadley, M. R., Craigon, D. J., Higgins, J., Emmerson, Z. F., Townsend, H. J., White, P. J., and May, S. T. (2005) Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. Plant Methods 1, 10
12. Wasaki, J., Yonetani, R., Kuroda, S., Shinano, T., Yazaki, J., Fujii, F., Shimbo, K., Yamamoto, K., Sakata, K., Sasaki, T., Kishimoto, N., Kikuchi, S., Yamagishi, M., and Osaki, M. (2003) Transcriptomic analysis of metabolic changes by phosphorus stress in rice plant roots. Plant Cell Environ. 26, 1515-1523 (Pubitemid 37124068)
13. Calderon-Vazquez, C., Ibarra-Laclette, E., Caballero-Perez, J., and Herrera- Estrella, L. (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and speciesspecific levels. J. Exp. Bot. 59, 2479-2497
14. Wang, Y. H., Garvin, D. F., and Kochian, L. V. (2002) Rapid induction of regulatory and transporter genes in response to phosphorus, potassium, and iron deficiencies in tomato roots. Evidence for cross talk and root/ rhizosphere-mediated signals. Plant Physiol. 130, 1361-1370 (Pubitemid 35358193)
15. Hernández, G., Ramirez, M., Valdes-Lopez, O., Tesfaye, M., Graham, M. A., Czechowski, T., Schlereth, A., Wandrey, M., Erban, A., Cheung, F., Wu, H. C., Lara, M., Town, C. D., Kopka, J., Udvardi, M. K., and Vance, C. P. (2007) Phosphorus stress in common bean: root transcript and metabolic responses. Plant Physiol. 144, 752-767 (Pubitemid 46944741)
16. Ideker, T., Thorsson, V., Ranish, J. A., Christmas, R., Buhler, J., Eng, J. K., Bumgarner, R., Goodlett, D. R., Aebersold, R., and Hood, L. (2001) Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 292, 929-934 (Pubitemid 32422490)
17. Rogers, S., Girolami, M., Kolch, W., Waters, K. M., Liu, T., Thrall, B., and Wiley, H. S. (2008) Investigating the correspondence between transcriptomic and proteomic expression profiles using coupled cluster models. Bioinformatics 24, 2894-2900
18. Griffin, T. J., Gygi, S. P., Ideker, T., Rist, B., Eng, J., Hood, L., and Aebersold, R. (2002) Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol. Cell. Proteomics 1, 323-333
19. Chen, G., Gharib, T. G., Huang, C. C., Taylor, J. M., Misek, D. E., Kardia, S. L., Giordano, T. J., Iannettoni, M. D., Orringer, M. B., Hanash, S. M., and Beer, D. G. (2002) Discordant protein and mRNA expression in lung adenocarcinomas. Mol. Cell. Proteomics 1, 304-313
20. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F., Gelb, M. H., and Aebersold, R. (1999) Quantitative analysis of complex protein mixtures using iso-tope- coded affinity tags. Nat. Biotechnol. 17, 994-999 (Pubitemid 29474856)
21. Tian, Q., Stepaniants, S. B., Mao, M., Weng, L., Feetham, M. C., Doyle, M. J., Yi, E. C., Dai, H., Thorsson, V., Eng, J., Goodlett, D., Berger, J. P., Gunter, B., Linseley, P. S., Stoughton, R. B., Aebersold, R., Collins, S. J., Hanlon, W. A., and Hood, L. E. (2004) Integrated genomic and proteomic analyses of gene expression in mammalian cells. Mol. Cell. Proteomics 3, 960-969 (Pubitemid 40361231)
22. Baginsky, S., Kleffmann, T., von Zychlinski, A., and Gruissem, W. (2005) Analysis of shotgun proteomics and RNA profiling data from Arabidopsis thaliana chloroplasts. J. Proteome Res. 4, 637-640 (Pubitemid 40548175)
23. Li, K., Xu, C., Zhang, K., Yang, A., and Zhang, J. (2007) Proteomic analysis of roots growth and metabolic changes under phosphorus deficit in maize (Zea mays L.) plants. Proteomics 7, 1501-1512 (Pubitemid 46775881)
24. Torabi, S., Wissuwa, M., Heidari, M., Naghavi, M. R., Gilany, K., Hajirezaei, M. R., Omidi, M., Yazdi-Samadi, B., Ismail, A. M., and Salekdeh, G. H. (2009) A comparative proteome approach to decipher the mechanism of rice adaptation to phosphorous deficiency. Proteomics 9, 159-170
25. Yao, Y., Sun, H., Xu, F., Zhang, X., and Liu, S. (2011) Comparative proteome analysis of metabolic changes by low phosphorus stress in two Brassica napus genotypes. Planta 233, 523-537
26. Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., and Selbach, M. (2011) Global quantification of mammalian gene expression control. Nature 473, 337-342
27. Nakamura, Y., Awai, K., Masuda, T., Yoshioka, Y., Takamiya, K., and Ohta, H. (2005) A novel phosphatidylcholine-hydrolyzing phospholipase C induced by phosphate starvation in Arabidopsis. J. Biol. Chem. 280, 7469-7476 (Pubitemid 40349638)
28. Plaxton, W. C., and Tran, H. T. (2011) Metabolic adaptations of phosphatestarved plants. Plant Physiol. 156, 1006-1015
29. Chiou, T. J., Aung, K., Lin, S. I., Wu, C. C., Chiang, S. F., and Su, C. L. (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18, 412-421 (Pubitemid 43951302)
30. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., Nussaume, L., and Desnos, T. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39, 792-796 (Pubitemid 46848591)
31. Estelle, M. A., and Somerville, C. (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206, 200-206
32. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
33. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628 (Pubitemid 351911867)
34. Kent, W. J. (2002) BLAT-the BLAST-like alignment tool. Genome Res. 12, 656-664
35. Clark, G., Konopka-Postupolska, D., Hennig, J., and Roux, S. (2010) Is annexin 1 a multifunctional protein during stress responses? Plant Signal Behav. 5, 303-307
36. Bayle, V., Arrighi, J. F., Creff, A., Nespoulous, C., Vialaret, J., Rossignol, M., Gonzalez, E., Paz-Ares, J., and Nussaume, L. (2011) Arabidopsis thaliana high-affinity phosphate transporters exhibit multiple levels of posttranslational regulation. Plant Cell 23, 1523-1535
37. Chen, J., Liu, Y., Ni, J., Wang, Y., Bai, Y., Shi, J., Gan, J., Wu, Z., and Wu, P. (2011) OsPHF1 regulates the plasma membrane localization of lowand high-affinity inorganic phosphate transporters and determines inorganic phosphate uptake and translocation in rice. Plant Physiol. 157, 269-278
38. Mahfouz, M. M., Kim, S., Delauney, A. J., and Verma, D. P. (2006) Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 18, 477-490 (Pubitemid 43951307)
39. Swaraz, A. M., Park, Y. D., and Hur, Y. (2011) Knock-out mutations of Arabidopsis SmD3-b induce pleotropic phenotypes through altered transcript splicing. Plant Sci. 180, 661-671
40. Shimojima, M. (2011) Biosynthesis and functions of the plant sulfolipid. Prog. Lipid Res. 50, 234-239
41. Nakamura, Y., Koizumi, R., Shui, G., Shimojima, M., Wenk, M. R., Ito, T., and Ohta, H. (2009) Arabidopsis lipins mediate eukaryotic pathway of lipid metabolism and cope critically with phosphate starvation. Proc. Natl. Acad. Sci. U.S.A. 106, 20978-20983
42. May, A., Spinka, M., and Köck, M. (2012) Arabidopsis thaliana PECP1 - Enzymatic characterization and structural organization of the first plant phosphoethanolamine/phosphocholine phosphatase. Biochim. Biophys. Acta 1824, 319-325
43. Hammond, J. P., Broadley, M. R., and White, P. J. (2004) Genetic responses to phosphorus deficiency. Ann. Bot. 94, 323-332 (Pubitemid 41301649)
44. May, A., Berger, S., Hertel, T., and Köck, M. (2011) The Arabidopsis thaliana phosphate starvation responsive gene AtPPsPase1 encodes a novel type of inorganic pyrophosphatase. Biochim. Biophys. Acta 1810, 178-185