AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip

Nature Communications

Volumn 6, Issue , 2015, Pages

  Medici, Anna ^a   Marshall Colon, Amy ^b,d   Ronzier, Elsa ^a,e   Szponarski, Wojciech ^a   Wang, Rongchen ^c   Gojon, Alain ^a   Crawford, Nigel M ^c   Ruffel, Sandrine ^a   Coruzzi, Gloria M ^b   Krouk, Gabriel ^a  

^a MONTPELLIER SUPAGRO   (France)

^b NEW YORK UNIVERSITY   (United States)

^c SECTION OF CELL AND DEVELOPMENTAL BIOLOGY   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITRATE; PHOSPHATE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HRS1; UNCLASSIFIED DRUG; ARABIDOPSIS PROTEIN; HRS1 PROTEIN, ARABIDOPSIS; NITRIC ACID DERIVATIVE; PRIMER DNA;

FERTILIZER APPLICATION; GENOME; IDENTIFICATION KEY; MOLECULAR ANALYSIS; PHOSPHATE; PLANT COMMUNITY; ROOT SYSTEM; SIGNALING;

ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; GENE CLUSTER; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PLANT ROOT; ROOT GROWTH; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; BIOLOGICAL MODEL; BIOLOGY; FLUORESCENCE MICROSCOPY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; MERISTEM; METABOLISM; PHYLOGENY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL MODEL;

ARABIDOPSIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; COMPUTATIONAL BIOLOGY; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; IMMUNOBLOTTING; LIKELIHOOD FUNCTIONS; MERISTEM; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; NITRATES; PHOSPHATES; PHYLOGENY; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84923885102     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7274     Document Type: Article

References (59)

1. Gruber, B. D., Giehl, R. F., Friedel, S. & von Wiren, N. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163, 161-179 (2013).
2. Peret, B., Clement, M., Nussaume, L. & Desnos, T. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci. 16, 442-450 (2011).
3. Alvarez, J. M., Vidal, E. A. & Gutierrez, R. A. Integration of local and systemic signaling pathways for plant N responses. Curr. Opin. Plant Biol. 15, 185-191 (2012).
4. Vidal, E. A. & Gutierrez, R. A. A systems view of nitrogen nutrient and metabolite responses in Arabidopsis. Curr. Opin. Plant Biol. 11, 521-529 (2008).
5. Gojon, A., Nacry, P. & Davidian, J. C. Root uptake regulation: a central process for NPS homeostasis in plants. Curr. Opin. Plant Biol. 12, 328-338 (2009).
6. Krouk, G., Crawford, N. M., Coruzzi, G. M. & Tsay, Y. F. Nitrate signaling: adaptation to fluctuating environments. Curr. Opin. Plant Biol. 13, 266-273 (2010).
7. Camacho-Cristobal, J. J. et al. PRD, an Arabidopsis AINTEGUMENTA-like gene, is involved in root architectural changes in response to phosphate starvation. Planta 228, 511-522 (2008).
8. Svistoonoff, S. et al. Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genet. 39, 792-796 (2007).
9. Ticconi, C. A. et al. ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability. Proc. Natl Acad. Sci. USA 106, 14174-14179 (2009).
10. Ticconi, C. A., Delatorre, C. A., Lahner, B., Salt, D. E. & Abel, S. Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. Plant J. 37, 801-814 (2004).
11. Rubio, V. et al. A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15, 2122-2133 (2001).
12. Bustos, R. et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6, e1001102 (2010).
13. Miura, K. et al. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl Acad. Sci. USA 102, 7760-7765 (2005).
14. Vidal, E. A., Tamayo, K. P. & Gutierrez, R. A. Gene networks for nitrogen sensing, signaling, and response in Arabidopsis thaliana. Wiley Interdiscip. Rev. Syst. Biol. Med. 2, 683-693 (2010).
15. Walch-Liu, P. & Forde, B. G. Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. Plant J. 54, 820-828 (2008).
16. Kant, S., Peng, M. & Rothstein, S. J. Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in arabidopsis. PLoS Genet. 7, e1002021 (2011).
17. Lin, W. Y., Huang, T. K. & Chiou, T. J. Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 26, 454-464 (2013).
18. Peng, M. et al. Adaptation of Arabidopsis to nitrogen limitation involves induction of anthocyanin synthesis which is controlled by the NLA gene. J. Exp. Bot. 59, 2933-2944 (2008).
19. Khamis, S., Lamaze, T., Lemoine, Y. & Foyer, C. Adaptation of the photosynthetic apparatus in maize leaves as a result of nitrogen limitation: relationships between electron transport and carbon assimilation. Plant Physiol. 94, 1436-1443 (1990).
20. Krouk, G. et al. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18, 927-937 (2010).
21. Ho, C. H., Lin, S. H., Hu, H. C. & Tsay, Y. F. CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194 (2009).
22. 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).
23. 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).
24. Wang, R. et al. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136, 2512-2522 (2004).
25. Hu, H. C., Wang, Y. 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).
26. Sawaki, N. et al. A nitrate-inducible GARP family gene encodes an autorepressible transcriptional repressor in rice. Plant Cell Physiol. 54, 506-517 (2013).
27. Waters, M. T. et al. GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21, 1109-1128 (2009).
28. Kerstetter, R. A., Bollman, K., Taylor, R. A., Bomblies, K. & Poethig, R. S. KANADI regulates organ polarity in Arabidopsis. Nature 411, 706-709 (2001).
29. Liu, H. et al. Overexpressing HRS1 confers hypersensitivity to low phosphate-elicited inhibition of primary root growth in Arabidopsis thaliana. J. Integr. Plant Biol. 51, 382-392 (2009).
30. Bolle, C. et al. GABI-DUPLO: a collection of double mutants to overcome genetic redundancy in Arabidopsis thaliana. Plant J. 75, 157-171 (2013).
31. Wang, R. et al. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 136, 2512-2522 (2004).
32. Wang, R., Xing, X., Wang, Y., Tran, A. & Crawford, N. M. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol. 151, 472-478 (2009).
33. Konishi, M. & Yanagisawa, S. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 4, 1617 (2013).
34. Marchive, C. et al. Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4, 1713 (2013).
35. Canales, J., Moyano, T. C., Villarroel, E. & Gutiérrez, R. A. Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front. Plant Sci. 5, 22 (2014).
36. Bargmann, B. O. et al. TARGET: a transient transformation system for genomewide transcription factor target discovery. Mol. Plant 6, 978-980 (2013).
37. Para, A. et al. Hit-and-run transcriptional control by bZIP1 mediates rapid nutrient signaling in Arabidopsis. Proc. Natl Acad. Sci. USA 111, 10371-10376 (2014).
38. Katari, M. S. et al. VirtualPlant: a software platform to support systems biology research. Plant Physiol. 152, 500-515 (2010).
39. Du, Z., Zhou, X., Ling, Y., Zhang, Z. & Su, Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res. 38, W64-W70 (2010).
40. Bailey, T. L. et al. MEME Suite: tools for motif discovery and searching. Nucleic Acids Res. 37, W202-W208 (2009).
41. Giraud, E. et al. TCP transcription factors link the regulation of genes encoding mitochondrial proteins with the circadian clock in Arabidopsis thaliana. Plant Cell 22, 3921-3934 (2010).
42. Franco-Zorrilla, J. M. et al. DNA-binding specificities of plant transcription factors and their potential to define target genes. Proc. Natl Acad. Sci. USA 111, 2367-2372 (2014).
43. Obertello, M., Krouk, G., Katari, M. S., Runko, S. J. & Coruzzi, G. M. Modeling the global effect of the basic-leucine zipper transcription factor 1 (bZIP1) on nitrogen and light regulation in Arabidopsis. BMC Sys. Biol. 4, 111 (2010).
44. Krouk, G. et al. A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PLoS Comput. Biol. 5, e1000326 (2009).
45. Supek, F., Bosnjak, M., Skunca, N. & Smuc, T. REVIGO summarizes and visualizes long lists of gene ontology terms. PLoS ONE 6, e21800 (2011).
46. Alvarez, J. M. et al. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J. 80, 1-13 (2014).
47. Nero, D., Krouk, G., Tranchina, D. & Coruzzi, G. M. A system biology approach highlights a hormonal enhancer effect on regulation of genes in a nitrate responsive "biomodule". BMC Sys. Biol. 3, 59 (2009).
48. Tsukagoshi, H., Busch, W. & Benfey, P. N. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143, 606-616 (2010).
49. Lu, D., Wang, T., Persson, S., Mueller-Roeber, B. & Schippers, J. H. Transcriptional control of ROS homeostasis by KUODA1 regulates cell expansion during leaf development. Nat. Commun. 5, 3767 (2014).
50. Bargmann, B. O. et al. A map of cell type-specific auxin responses. Mol. Sys. Biol. 9, 688 (2013).
51. Wu, C. et al. HRS1 acts as a negative regulator of abscisic acid signaling to promote timely germination of Arabidopsis seeds. PLoS ONE 7, e35764 (2012).
52. Mito, T., Seki, M., Shinozaki, K., Ohme-Takagi, M. & Matsui, K. Generation of chimeric repressors that confer salt tolerance in Arabidopsis and rice. Plant Biotechnol. J. 9, 736-746 (2011).
53. Kellermeier, F. et al. Analysis of the root system architecture of arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26, 1480-1496 (2014).
54. Delgado-Baquerizo, M. et al. Decoupling of soil nutrient cycles as a function of aridity in global drylands. Nature 502, 672-676 (2013).
55. Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462-469 (2003).
56. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743 (1998).
57. Tamura, K. et al. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739 (2011).
58. Santoni, V., Vinh, J., Pflieger, D., Sommerer, N. & Maurel, C. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem J. 373, 289-296 (2003).
59. Nemhauser, J. L., Hong, F. & Chory, J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126, 467-475 (2006).