Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants

Nature Communications

Volumn 4, Issue , 2013, Pages

  Marchive, Chloé ^a   Roudier, François ^b   Castaings, Loren ^a,c   Bréhaut, Virginie ^a   Blondet, Eddy ^b   Colot, Vincent ^b   Meyer, Christian ^a   Krapp, Anne ^a  

^a INSTITUT JEAN PIERRE BOURGIN   (France)

^b CNRS   (France)

^c MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NLP7; UNCLASSIFIED DRUG;

FUNGUS; MAMMAL; MOLECULAR ANALYSIS; NITRATE; NUTRIENT CYCLING; PHYSIOLOGICAL RESPONSE; SIGNALING;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; NONHUMAN; PLANT CELL; PLANT GENETICS; PLANT RESPONSE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

CELL NUCLEUS; GENE EXPRESSION REGULATION, PLANT; NITRATES; PLANTS; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84877735953     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2650     Document Type: Article

References (43)

1. Lawler, D., Lemaire, G. & Gastal, F. Plant Nitrogen: nitrogen, plant growth and crop yield. (eds Lea, P. & Morot-Gaudry, J. F.) 343-368 (Springer, 2001).
2. Crawford, M. N. Nitrate: nutrient and signal for plant growth. Plant Cell 7, 859-868 (1995).
3. Wang, R., Okamoto, M., Xing, X. & Crawford, N. M. Microarray analysis of the nitrate response in Arabidopsis roots and shoots reveals over 1, 000 rapidly responding genes and new linkages to glucose, trehalose-6-phosphate, iron, and sulfate metabolism. Plant Physiol. 132, 556-567 (2003). (Pubitemid 36715057)
4. Scheible, W. R. et al. 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. 136, 2483-2499 (2004).
5. Gutierrez, R. A. Systems biology for enhanced plant nitrogen nutrition. Science 336, 1673-1675 (2012).
6. Zhang, H. & Forde, B. G. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407-409 (1998). (Pubitemid 28063380)
7. Castaings, L. et al. The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J. 57, 426-435 (2009).
8. Rubin, G., Tohge, T., Matsuda, F., Saito, K. & Scheible, W. R. Members of the LBD family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21, 3567-3584 (2009).
9. Krouk, G., Mirowski, P., LeCun, Y., Shasha, D. E. & Coruzzi, G. M. Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol. 11, R123 (2010).
10. Schauser, L., Wieloch, W. & Stougaard, J. Evolution of NIN-like proteins in Arabidopsis, rice, and Lotus japonicus. J. Mol. Evol. 60, 229-237 (2005). (Pubitemid 40568861)
11. Fornerod, M., Ohno, M., Yoshida, M. & Mattaj, I. W. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060 (1997). (Pubitemid 27408519)
12. Fukuda, M. et al. CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311 (1997). (Pubitemid 27513316)
13. Haasen, D., Köhler, C., Neuhaus, G. & Merkle, T. Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine-rich nuclear export signals in Arabidopsis thaliana. Plant J. 20, 695-705 (1999).
14. Roudier, F. et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 18, 1928-1338 (2011).
15. Hu, H., Wang, Y. & Tsay, Y. F. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant J. 57, 264-278 (2009).
16. Wang, R., Xing, X., Wang, Y., Tran, A. & Craford, N. M. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol. 151, 472-478 (2009).
17. Ho, S. H., Lin, S. H., Hu, H. C. & Tsay, Y. F. CHL1 functions as a nitrate sensor in plants. Cell 18, 1184-1194 (2009).
18. Konishi, M. & Yanagisawa, S. Identification of a nitrate-responsive cis-element in the Arabidopsis NIR1 promoter defines the presence of multiple cis-regulatory elements for nitrogen response. Plant J. 63, 269-282 (2010).
19. Thomas-Chollier, M., Herrmann, C., Defrance, M., Sand, O., Thieffry, D. & van Helden, J. RSAT peak-motifs: motif analysis in full-size ChIP-seq datasets. Nucleic Acids Res. 40, e31 (2012).
20. Konishi, M. & Yanagisawa, S. The regulatory region controlling the nitrate-responsive expression of a nitrate reductase gene, NIA1, in Arabidopsis. Plant Cell Physiol. 52, 824-836 (2011).
21. Girin, T. et al. Identification of a 150 bp cis-acting element of the AtNRT2.1 promoter involved in the regulation of gene expression by the N and C status of the plant. Plant Cell Environ. 30, 1366-1380 (2007). (Pubitemid 47493859)
22. Blauwkamp, T. A., Chang, M. V. & Cadigan, K. M. Novel TCF-binding sites specify transcriptional repression by Wnt signalling. EMBO J. 27, 1436-1346 (2008).
23. MacDonald, B. T., Tamai, K. & He, X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell. 17, 9-26 (2009).
24. MacQuarrie, K. L., Fong, A. P., Morse, R. H. & Tapscott, S. J. Genome-wide transcription factor binding: beyond direct target regulation. Trends Genet. 27, 141-148 (2011).
25. Meier, I. & Somers, D. E. Regulation of nucleocytoplasmic trafficking in plants. Curr. Opin. Plant Biol. 14, 538-546 (2011).
26. Carmago, A. et al. Nitrate signaling by the regulatory gene NIT2 in Chlamydomonas. Plant Cell 19, 3491-3503 (2007).
27. Murthi, A. et al. Regulation of tRNA bidirectional nuclear-cytoplasmic trafficking in Saccharomyces cerevisiae. Mol. Biol. Cell. 21, 639-649 (2010).
28. Pierce, J. B., Eswara, M. B. & Mangroo, D. The ins and outs of nuclear re-export of retrogradely transported tRNAs in Saccharomyces cerevisiae. Nucleus 1, 224-230 (2010).
29. Johnstone, A. D., Mullen, R. T. & Mangroo, D. Plants, like mammals, but unlike Saccharomyces, do not regulate nuclear-cytoplasmic tRNA trafficking in response to nutrient stress. Plant Signal Behav. 6, 1183-1183 (2011).
30. Bernreiter, A. et al. Nuclear export of the transcription factor NirA is a regulatory checkpoint for nitrate induction in Aspergillus nidulans. Mol. Cell Biol. 27, 791-802 (2007). (Pubitemid 46174546)
31. Meur, G. et al. Nucleo-cytosolic shuttling of FoxO1 directly regulates mouse Ins2 but not Ins1 gene expression in pancreatic beta cells (MIN6). J. Biol. Chem. 286, 13647-13656 (2011).
32. Gendrel, A. V., Lippmann, Z., Martienssen, R. & Colot, V. Profiling histone modification patterns in plants using genomic tiling microarrays. Nat. Methods 2, 213-218 (2005). (Pubitemid 41122129)
33. Seifert, M., Gohr, A., Strickert, M. & Grosse, I. Parsimonious higher-order hidden Markov models for improved array-CGH analysis with applications to Arabidopsis thaliana. PLoS Comput. Biol 8, e1002286 (2012).
34. Crowe, M. L. et al. CATMA: a complete Arabidopsis GST database. Nucleic Acids Res. 31, 156-158 (2003).
35. Lurin, C. et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089-2103 (2004). (Pubitemid 39059730)
36. Ge, Y., Dudoit, S. & Speed, T. P. Resampling-based Multiple Testing for MicroarrayData Analysis. Test 12, 1 (2003).
37. Gagnot, S. et al. CATdb: a public access to Arabidopsis transcriptome data from the URGV-CATMA platform. Nucleic Acids Res. 36, D986-D990 (2008). (Pubitemid 351149857)
38. Daniel-Vedele, F. & Caboche, M. A tobacco cDNA clone encoding a GATA-1 zinc finger protein homologous to regulators of nitrogen metabolism in fungi. Mol. Gen. Genet. 240, 365-373 (1993). (Pubitemid 23285951)
39. Thomine, S., Lelièvre, F., Debarbieux, E., Schroeder, J. I. & Barbier-Brygoo, H. AtNRAMP3, a multispecific vacuolar metal transporter involved in plant responses to iron deficiency. Plant J. 34, 685-695 (2003). (Pubitemid 36720202)
40. Thévenin, J. et al. A new system for fast and quantitative analysis of heterologous gene expression in plants. New Phytol. 193, 504-512 (2012).
41. Carrington, J. C., Freed, D. D. & Leinicke, A. J. Bipartite signal sequence mediates nuclear translocation of the plant potyviral NIa protein. Plant Cell 3, 953-962 (1991). (Pubitemid 21913755)
42. Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6, 3901-3907 (1987).
43. 0 sequences of maize adh1 mRNA are required for enhanced translation under low-oxygen conditions. Plant Physiol. 112, 685-695 (1996).