Auxin-mediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability

Plant, Cell and Environment

Volumn 37, Issue 1, 2014, Pages 162-174

  Mounier, Emmanuelle ^a   Pervent, Marjorie ^a   Ljung, Karin ^b   Gojon, Alain ^a   Nacry, Philippe ^a  

^a MONTPELLIER SUPAGRO   (France)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Arabidopsis thaliana; Lateral roots; Split root

Indexed keywords

BIOACCUMULATION; GROWTH; HERB; HETEROGENEITY; HOMOGENEITY; HORMONE; NITRATE; PHYSIOLOGICAL RESPONSE; ROOT ARCHITECTURE; ROOT COLONIZATION; SIGNALING;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ANION TRANSPORT PROTEIN; INDOLEACETIC ACID DERIVATIVE; NITRIC ACID DERIVATIVE; NRT1.1 PROTEIN, ARABIDOPSIS; PHYTOHORMONE; VEGETABLE PROTEIN;

ADAPTATION; ARABIDOPSIS; ARABIDOPSIS THALIANA; ARTICLE; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LATERAL ROOTS; METABOLISM; MUTATION; PH; PHYSIOLOGY; PLANT ROOT; REPORTER GENE; SIGNAL TRANSDUCTION; SPLIT ROOT; TRANSGENIC PLANT;

ARABIDOPSIS THALIANA; LATERAL ROOTS; SPLIT ROOT;

ADAPTATION, PHYSIOLOGICAL; ANION TRANSPORT PROTEINS; ARABIDOPSIS; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HYDROGEN-ION CONCENTRATION; INDOLEACETIC ACIDS; MODELS, BIOLOGICAL; MUTATION; NITRATES; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; SIGNAL TRANSDUCTION;

EID: 84897093926     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12143     Document Type: Article

References (55)

1. Alboresi A., Gestin C., Leydecker M.T., Bedu M., Meyer C. & Truong H.N. (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant, Cell & Environment 28, 500-512.
2. Andersen S.U., Buechel S., Zhao Z., Ljung K., Novak O., Busch W., Schuster C. & Lohmann J.U. (2008) Requirement of B2-type cyclin-dependent kinases for meristem integrity in Arabidopsis thaliana. The Plant Cell 20, 88-100.
3. Burns I.G. (1991) Short-term and long-term effects of a change in the spatial-distribution of nitrate in the root zone on n uptake, growth and root development of young lettuce plants. Plant, Cell & Environment 14, 21-33.
4. - concentration. Journal of Experimental Botany 29, 453-464.
5. Colón-Carmona A., You R., Haimovitch-Gal T. & Doerner P. (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. The Plant Journal 20, 503-508.
6. Crawford N.M. & Glass A.D.M. (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389-395.
7. Drew M.C. (1975) Comparison of effects of a localized supply of phosphate, nitrate, ammonium and potassium on growth of seminal root system, and shoot, in barley. New Phytologist 75, 479-490.
8. Edlund A., Eklof S., Sundberg B., Moritz T. & Sandberg G. (1995) A microscale technique for gas chromatography-mass spectrometry measurements of picogram amounts of indole-3-acetic acid in plant tissues. Plant Physiology 108, 1043-1047.
9. Farley R.A. & Fitter A.H. (1999) Temporal and spatial variation in soil resources in a deciduous woodland. Journal of Ecology 87, 688-696.
10. Forde B.G. (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review of Plant Biology 53, 203-224.
11. Fransen B., de Kroon H. & Berendse F. (1998) Root morphological plasticity and nutrient acquisition of perennial grass species from habitats of different nutrient availability. Oecologia 115, 351-358.
12. + transporter genes AtNrt2.1 and AtAmt1.1 in Arabidopsis: relation with long distance and local controls by N status of the plant. The Plant Journal 26, 143-155.
13. Gojon A., Nacry P. & Davidian J.C. (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Current Opinion in Plant Biology 12, 328-338.
14. Gojon A., Krouk G., Perrine-Walker F. & Laugier E. (2011) Nitrate transceptor(s) in plants. Journal of Experimental Botany 62, 2299-2308.
15. Guo F.Q., Wang R.C., Chen M.S. & Crawford N.M. (2001) The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1. (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. The Plant Cell 13, 1761-1777.
16. Guo F.Q., Young J. & Crawford N.M. (2003) The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in arabidopsis. The Plant Cell 15, 107-117.
17. Herr J.M. (1971) New clearing-squash technique for study of ovule development in angiosperms. American Journal of Botany 58, 785-790.
18. Ho C.H., Lin S.H., Hu H.C. & Tsay Y.-F. (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 1184-1194.
19. Hodge A. (2006) Plastic plants and patchy soils. Journal of Experimental Botany 25, 401-411.
20. Hodge A. (2009) Root decisions. Plant, Cell & Environment 32, 628-640.
21. Hodge A., Stewart J., Robinson D., Griffiths B.S. & Fitter A.H. (1998) Root proliferation, soil fauna and plant nitrogen capture from nutrient-rich patches in soil. The New Phytologist 139, 479-494.
22. Hodge A., Robinson D., Griffiths B.S. & Fitter A.H.L. (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant, Cell & Environment 22, 811-820.
23. Hodge A., Stewart J., Robinson D., Griffiths B.S. & Fitter A.H. (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. The Journal of Ecology 88, 150-164.
24. Holsbeeks I., Lagatie O., Van Nuland A., Van de Velde S. & Thevelein J.M. (2004) The eukaryotic plasma membrane as a nutrient-sensing device. Trends in Biochemical Sciences 29, 556-564.
25. Jefferson R.A. (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Molecular Biology Reporter 5, 387-405.
26. Kanno Y., Hanada A., Chiba Y., Ichikawa T., Nakazawa M., Matsui M., Koshiba T., Kamiya Y. & Seo M. (2012) Identification of an abscisic acid transporter by functional screening using the receptor complex as a sensor. Proceedings of the National Academy of Sciences of the United States of America 109, 9653-9658.
27. - demand signaling in Arabidopsis. Plant Physiology 142, 1075-1086.
28. Krouk G., Lacombe B., Bielach A., etal. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Developmental Cell 18, 927-937.
29. Lainé P., Ourry A. & Boucaud J. (1995) Shoot control of nitrate uptake rates by roots of Brassica-Napus L - effects of localized nitrate supply. Planta 196, 77-83.
30. - uptake systems by N- and C-status of Arabidopsis plants. The Plant Journal 18, 509-519.
31. Lejay L., Gansel X., Cerezo M., Tillard P., Muller C., Krapp A., von Wiren N., Daniel-Vedele F. & Gojon A. (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. The Plant Cell 15, 2218-2232.
32. Lejay L., Wirth J., Pervent M., Cross J.M.F. Tillard P. & Gojon A. (2008) Oxidative pentose phosphate pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiology 146, 2036-2053.
33. Lima J.E., Kojima S., Takahashi H. & von Wirén N. (2010) Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. The Plant Cell 22, 3621-3633.
34. Linkohr B.I., Williamson L.C., Fitter A.H. & Leyser H.M. (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal 29, 751-760.
35. Liu K.H. & Tsay Y.-F. (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO Journal 22, 1005-1013.
36. - reduction. Plant Physiology 132, 958-967.
37. Muños S., Cazettes C., Fizames C., Gaymard F., Tillard P., Lepetit M., Lejay L. & Gojon A. (2004) Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. The Plant Cell 16, 2433-2447.
38. Nacry P., Canivenc G., Muller B., Azmi A., Van Onckelen H., Rossignol M. & Doumas P. (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis. Plant Physiology 138, 2061-2074.
39. Nacry P., Bouguyon E. & Gojon A. (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant and Soil. doi: 10.1007/s11104-013-1645-9.
40. Remans T., Nacry P., Pervent M., Filleur S., Diatloff E., Mounier E., Tillard P., Forde B.G. & Gojon A. (2006a) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences of the United States of America 103, 19206-19211.
41. Remans T., Nacry P., Pervent M., Girin T., Tillard P., Lepetit M. & Gojon A. (2006b) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiology 140, 909-921.
42. Robinson D. (1994) The response of plants to non uniform supplies of nutrients. New Phytologist 127, 635-674.
43. Robinson D., Hodge A., Griffiths B.S. & Fitter A.H. (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 265, 431-435.
44. Ruffel S., Krouk G., Ristova D., Shasha D., Birnbaum K.D. & Coruzzi G.M. (2011) Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proceedings of the National Academy of Sciences of the United States of America 108, 18524-18529.
45. Tsay Y.-F., Schroeder J.I., Feldmann K.A. & Crawford N.M. (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705-713.
46. Tsay Y.-F., Chiu C.C., Tsai C.B., Ho C.H. & Hsu P.K. (2007) Nitrate transporters and peptide transporters. Febs Letters 581, 2290-2300.
47. Ulmasov T., Murfett J., Hagen G. & Guilfoyle T.J. (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell 9, 1963-1971.
48. Vidal E.A., Araus V., Lu C., Parry G., Green P.J., Coruzzi G.M. & Gutiérrez R.A. (2010) Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 107, 4477-4482.
49. van Vuuren M.M.I., Robinson D. & Griffiths B.S. (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant and Soil 178, 185-192.
50. Walch-Liu P. & Forde B.G. (2008) Nitrate signalling mediated by the NRT1.1 nitrate transporter antagonises L-glutamate-induced changes in root architecture. The Plant Journal 54, 820-828.
51. Walch-Liu P., Liu L.H., Remans T., Tester M. & Forde B.G. (2006) Evidence that L-glutamate can act as an exogenous signal to modulate root growth and branching in Arabidopsis thaliana. Plant and Cell Physiology 47, 1045-1057.
52. Wang R., Xing X., Wang Y., Tran A. & Crawford N.M. (2009) A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiology 151, 472-478.
53. Zhang H.M. & Forde B.G. (1998) An Arabidopsis MADS box gene that controls nutrient induced changes in root architecture. Science 279, 407-409.
54. Zhang H.M., Jennings A., Barlow P.W. & Forde B.G. (1999) Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96, 6529-6534.
55. Zhang H.M., Rong H.L. & Pilbeam D. (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. Journal of Experimental Botany 58, 2329-2338.