The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation

BMC Plant Biology

Volumn 12, Issue , 2012, Pages

  Woo, Jongchan ^a   MacPherson, Cameron R ^a,d   Liu, Jun ^a   Wang, Huan ^a,c   Kiba, Takatoshi ^a   Hannah, Matthew A ^b   Wang, Xiu Jie ^c   Bajic, Vladimir B ^d   Chua, Nam Hai ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b Bayer Cropscience Belgium   (Belgium)

^c INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^d KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

Comparative analysis with AtGenExpress; Functional analysis; Hydroponic culture; Initial, Persistent, and Latent expression patterns; Micro array and tiling array; Organ specific; Phosphate starvation; Response and recovery; Roots and shoots; Whole seedling

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; PHOSPHATE; SODIUM CHLORIDE; TRANSCRIPTOME;

ANTIBODY SPECIFICITY; ARABIDOPSIS; ARTICLE; COLD; DNA MICROARRAY; DRUG EFFECT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; OSMOTIC PRESSURE; PLANT; PLANT GENE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ARABIDOPSIS; COLD TEMPERATURE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENETIC LOCI; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; OSMOTIC PRESSURE; PHOSPHATES; PLANT ROOTS; PLANT SHOOTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; TRANSCRIPTOME;

EID: 84860387015     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-12-62     Document Type: Article

References (52)

1. Raghothama KG. Phosphate Acquisition. Annual Review of Plant Physiology and Plant Molecular Biology 1999, 50:665-693. 10.1146/annurev.arplant.50.1.665, 15012223.
2. Schachtman DP, Reid RJ, Ayling S. Phosphorus Uptake by Plants: From Soil to Cell. Plant Physiology 1998, 116:447-453. 10.1104/pp.116.2.447, 1539172, 9490752.
3. Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 2003, 157:423-447.
4. Ma W, Ma L, Li J, Wang F, Sisak I, Zhang F. Phosphorus flows and use efficiencies in production and consumption of wheat, rice, and maize in China. Chemosphere 2011, 84:814-821. 10.1016/j.chemosphere.2011.04.055, 21570104.
5. MacDonald GK, Bennett EM, Potter PA, Ramankutty N. Agronomic phosphorus imbalances across the world's croplands. Proc Natl Acad Sci U S A 2011, 108:3086-3091. 10.1073/pnas.1010808108, 3041096, 21282605.
6. Chebud Y, Naja GM, Rivero R. Phosphorus run-off assessment in a watershed. J Environ Monit 2011, 13:66-73. 10.1039/c0em00321b, 21069224.
7. Howarth R, Sharpley A, Walker D. Sources of nutrient pollution to coastal waters in the United States: Implications for achieving coastal water quality goals. Estuaries and Coasts 2002, 25:656-676.
8. Moss B. Water pollution by agriculture. Philos Trans R Soc Lond B Biol Sci 2008, 363:659-666. 10.1098/rstb.2007.2176, 2610176, 17666391.
9. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, Bligny R, Ortet P, Creff A, Somerville S, Rolland N, et al. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 2005, 102:11934-11939. 10.1073/pnas.0505266102, 1188001, 16085708.
10. Morcuende R, Bari R, Gibon Y, Zheng W, Pant BD, BlÄSing O, Usadel B, Czechowski T, Udvardi MK, 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, 17177879.
11. Muller R, Morant M, Jarmer H, Nilsson L, Nielsen TH. Genome-wide analysis of the Arabidopsis leaf transcriptome reveals interaction of phosphate and sugar metabolism. Plant Physiol 2007, 143:156-171. 1761981, 17085508.
12. Nilsson L, Muller R, Nielsen TH. Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol Plant 2010, 139:129-143. 10.1111/j.1399-3054.2010.01356.x, 20113436.
13. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, Perez-Perez J, Solano R, Leyva A, Paz-Ares J. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 2010 6(9). pii: e1001102..
14. Thibaud M, Arrighi J, Bayle V, Chiarenza S, Creff A, Bustos R, Paz-Ares J, Poirier Y, Nussaume L. Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. Plant J 2010, 64(5):775-89. 10.1111/j.1365-313X.2010.04375.x, 21105925.
15. Ji H, Jiang H, Ma W, Johnson DS, Myers RM, Wong WH. An integrated software system for analyzing ChIP-chip and ChIP-seq data. Nat Biotech 2008, 26:1293-1300.
16. Saeed AI, Bhagabati NK, Braisted JC, Liang W, Sharov V, Howe EA, Li J, Thiagarajan M, White JA, Quackenbush J. TM4 microarray software suite. Methods Enzymol 2006, 411:134-193.
17. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 2003, 34:374-378.
18. Zhang H, Forde BG. An Arabidopsis MADS Box Gene That Controls Nutrient-Induced Changes in Root Architecture. Science 1998, 279:407-409. 10.1126/science.279.5349.407, 9430595.
19. de Folter S, Immink RGH, Kieffer M, Parenicová L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, et al. Comprehensive Interaction Map of the Arabidopsis MADS Box Transcription Factors. The Plant Cell Online 2005, 17:1424-1433.
20. Zhong R, Lee C, Zhou J, McCarthy RL, Ye Z-H. A Battery of Transcription Factors Involved in the Regulation of Secondary Cell Wall Biosynthesis in Arabidopsis. The Plant Cell Online 2008, 20:2763-2782.
21. Zhou J, Lee C, Zhong R, Ye Z-H. MYB58 and MYB63 Are Transcriptional Activators of the Lignin Biosynthetic Pathway during Secondary Cell Wall Formation in Arabidopsis. The Plant Cell Online 2009, 21:248-266.
22. Wilson K, Long D, Swinburne J, Coupland G. A Dissociation Insertion Causes a Semidominant Mutation That Increases Expression of TINY, an Arabidopsis Gene Related to APETALA2. The Plant Cell Online 1996, 8:659-671.
23. Franco-Zorrilla JM, Martín AC, Leyva A, Paz-Ares J. Interaction between Phosphate-Starvation, Sugar, and Cytokinin Signaling in Arabidopsis and the Roles of Cytokinin Receptors CRE1/AHK4 and AHK3. Plant Physiology 2005, 138:847-857. 10.1104/pp.105.060517, 1150402, 15923327.
24. Qin F, Sakuma Y, Tran L-SP, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y. Miyazono K-i, et al: Arabidopsis DREB2A-Interacting Proteins Function as RING E3 Ligases and Negatively Regulate Plant Drought Stress-Responsive Gene Expression. The Plant Cell Online 2008, 20:1693-1707.
25. Albrecht V, Ritz O, Linder S, Harter K, Kudla J. The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. EMBO J 2001, 20:1051-1063. 10.1093/emboj/20.5.1051, 145464, 11230129.
26. Nelson DC, Flematti GR, Riseborough J-A, Ghisalberti EL, Dixon KW, Smith SM. Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proceedings of the National Academy of Sciences 2010, 107:7095-7100.
27. Despres C, DeLong C, Glaze S, Liu E, Fobert PR. The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 2000, 12:279-290. 139764, 10662863.
28. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 2000, 97:11632-11637. 10.1073/pnas.190309197, 17252, 11005831.
29. Zhang L-Y, Bai M-Y, Wu J, Zhu J-Y, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, et al. Antagonistic HLH/bHLH Transcription Factors Mediate Brassinosteroid Regulation of Cell Elongation and Plant Development in Rice and Arabidopsis. The Plant Cell Online 2009, 21:3767-3780.
30. Pandey SP, Somssich IE. The Role of WRKY Transcription Factors in Plant Immunity. Plant Physiology 2009, 150:1648-1655. 10.1104/pp.109.138990, 2719123, 19420325.
31. Jung K-H, Seo Y-S, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC. The Submergence Tolerance Regulator Sub1A Mediates Stress-Responsive Expression of AP2/ERF Transcription Factors. Plant Physiology 2010, 152:1674-1692. 10.1104/pp.109.152157, 2832257, 20107022.
32. Yang C-Y, Hsu F-C, Li J-P, Wang N-N, Shih M-C. The AP2/ERF Transcription Factor AtERF73/HRE1 Modulates Ethylene Responses during Hypoxia in Arabidopsis. Plant Physiology 2011, 156:202-212. 10.1104/pp.111.172486, 3091062, 21398256.
33. Ascencio-Ibáñez JT, Sozzani R, Lee T-J, Chu T-M, Wolfinger RD, Cella R, Hanley-Bowdoin L. Global Analysis of Arabidopsis Gene Expression Uncovers a Complex Array of Changes Impacting Pathogen Response and Cell Cycle during Geminivirus Infection. Plant Physiology 2008, 148:436-454. 10.1104/pp.108.121038, 2528102, 18650403.
34. Wang Y, Zhang W-Z, Song L-F, Zou J-J, Su Z, Wu W-H. Transcriptome Analyses Show Changes in Gene Expression to Accompany Pollen Germination and Tube Growth in Arabidopsis. Plant Physiology 2008, 148:1201-1211. 10.1104/pp.108.126375, 2577266, 18775970.
35. Oono Y, Seki M, Satou M, Iida K, Akiyama K, Sakurai T, Fujita M, Yamaguchi-Shinozaki K, Shinozaki K. Monitoring expression profiles of Arabidopsis genes during cold acclimation and deacclimation using DNA microarrays. Functional & Integrative Genomics 2006, 6:212-234. 10.1007/s10142-005-0014-z, 3504448, 23213575.
36. Hanada K, Sawada Y, Kuromori T, Klausnitzer R, Saito K, Toyoda T, Shinozaki K, Li W-H, Hirai MY. Functional Compensation of Primary and Secondary Metabolites by Duplicate Genes in Arabidopsis thaliana. Molecular Biology and Evolution 2011, 28:377-382. 10.1093/molbev/msq204, 3002239, 20736450.
37. Lee J-Y, Colinas J, Wang JY, Mace D, Ohler U, Benfey PN. Transcriptional and posttranscriptional regulation of transcription factor expression in Arabidopsis roots. Proceedings of the National Academy of Sciences 2006, 103:6055-6060.
38. Osuna D, Usadel B, Morcuende R, Gibon Y, Bläsing OE, Höhne M, Günter 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. The Plant Journal 2007, 49:463-491. 10.1111/j.1365-313X.2006.02979.x, 17217462.
39. Ramel F, Sulmon C, Cabello-Hurtado F, Taconnat L, Martin-Magniette M-L, Renou J-P, El Amrani A, Couee I, Gouesbet G. Genome-wide interacting effects of sucrose and herbicide-mediated stress in Arabidopsis thaliana: novel insights into atrazine toxicity and sucrose-induced tolerance. BMC Genomics 2007, 8:450. 10.1186/1471-2164-8-450, 2242805, 18053238.
40. Journot-Catalino N, Somssich IE, Roby D, Kroj T. The Transcription Factors WRKY11 and WRKY17 Act as Negative Regulators of Basal Resistance in Arabidopsis thaliana. The Plant Cell Online 2006, 18:3289-3302.
41. Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and unicellular algae. Genes Dev 2001, 15(16):2122-33. 10.1101/gad.204401, 312755, 11511543.
42. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 2007, 39(8):1033-7. 10.1038/ng2079, 17643101.
43. Cheng Y, Zhou W, EI Sheery NI, Peters C, Li M, Wang X, Huang J. Characterization of the Arabidopsis glycerophosphodiester phosphodiesterase (GDPD) family reveals a role of the plastid-localized AtGDPD1 in maintaining cellular phosphate homeostasis under phosphate starvation. Plant J 2011, 66(5):781-95. 10.1111/j.1365-313X.2011.04538.x, 21323773.
44. Essigmann B, Guler S, Narang RA, Linke D, Benning C. Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana. PNAS 1998, 95(4):1950-5. 10.1073/pnas.95.4.1950, 19220, 9465123.
45. Cruz-Rumirez A, Oropeza-Aburto A, Razo-Hernandez F, Ramirez-Chavez E, Herrera-Estrella L. Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Genes Dev 2006, 103(17):6765-70.
46. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 2001, 126(2):875-82. 10.1104/pp.126.2.875, 111176, 11402214.
47. Tominaga R, Iwata M, Sano R, Inoue K, Okada K, Wada T. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 2008, 135(7):1335-45. 10.1242/dev.017947, 18305006.
48. Lelandais-Brière C, Jovanovic M, Torres GAM, Perrin Y, Lemoine R, Corre-Menguy F, Hartmann C. Disruption of AtOCT1, an organic cation transporter gene, affects root development and carnitine-related responses in Arabidopsis. The Plant Journal 2007, 51:154-164. 10.1111/j.1365-313X.2007.03131.x, 17521409.
49. Bari R, Datt Pant B, Stitt M, Scheible W-R. PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants. Plant Physiology 2006, 141:988-999. 10.1104/pp.106.079707, 1489890, 16679424.
50. Rouached H, Arpat A, Poirier Y. Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 2010, 3(2):288-99. 10.1093/mp/ssp120, 20142416.
51. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S. Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation. Current Biology 2007, 17:678-682. 10.1016/j.cub.2007.02.047, 17363254.
52. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 2007, 19:118-130. 10.1105/tpc.106.047761, 1820965, 17259263.