The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogen-limiting conditions by maintaining growth, nitrogen uptake, and assimilation

Plant Physiology

Volumn 147, Issue 3, 2008, Pages 1168-1180

  Kant, Surya ^a   Bi, Yong Mei ^a   Weretilnyk, Elizabeth ^b   Barak, Simon ^c   Rothstein, Steven J ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; THELLUNGIELLA; THELLUNGIELLA HALOPHILA;

ANION TRANSPORT PROTEIN; NITRATE TRANSPORTERS; NITROGEN;

ARTICLE; BRASSICACEAE; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANION TRANSPORT PROTEINS; BRASSICACEAE; GENE EXPRESSION REGULATION, PLANT; NITROGEN;

EID: 51549091065     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.118125     Document Type: Article

References (73)

1. Amtmann A, Bohnert HJ, Bressan RA (2005) Abiotic stress and plant genome evolution: search for new models. Plant Physiol 138: 127-130
2. Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8: 281
3. Bongue-Bartelsman M, Philips DA (1995) Nitrogen stress regulates gene expression of enzymes in the flavonoid biosynthetic pathway of tomato. Plant Physiol Biochem 33: 539-546
4. Cataldo DA, Haroon M, Schrader TE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6: 71-80
5. - uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol 127: 262-271
6. Chalker-Scott L (1999) Environmental significance of anthocyanins in plant stress responses. Photochem Photobiol 70: 1-9
7. Coruzzi GM (2003) Primary N-assimilation into amino acids in Arabidopsis. In CR Somerville, EM Meyerowitz, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, doi: 10.1199/tab.0010, www.aspb.org/publications/arabidopsis/
8. Coruzzi GM, Last RL (2000) Amino acids. In RG Buchanan, W Gruissem, R Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 358-410
9. Crawford NM (1995) Nitrate: nutrient and signal for plant growth. Plant Cell 7: 859-868
10. Crawford NM, Forde BG (2002) Molecular and developmental biology of inorganic nitrogen nutrition. In CR Somerville, EM Meyerowitz, eds, The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, doi: 10.1199/tab.0011, www.aspb.org/publications/arabidopsis/
11. Cren M, Hirel B (1999) Glutamine synthetase in higher plants: regulation of gene and protein expression from the organ to the cell. Plant Cell Physiol 40: 1187-1193
12. De Angeli A, Monachello D, Ephritikhine G, Frachisse JM, Thomine S, Gambale F, Barbier-Brygoo H (2006) The nitrate/proton antiporter AtCLCa mediates nitrate accumulation in plant vacuoles. Nature 442: 939-942
13. Delatte T, Trevisan M, Parker ML, Zeeman SC (2005) Arabidopsis mutants Atisa1 and Atisa2 have identical phenotypes and lack the same multimeric isoamylase, which influences the branch point distribution of amylopectin during starch synthesis. Plant J 41: 815-830
14. Dennis DT, Blakeley SD (2000) Carbohydrate metabolism. In RG Buchanan, W Gruissem, R Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 630-675
15. Diaz U, Saliba-Colombani V, Loudet O, Belluomo P, Moreau L, Daniel-Vedele F, Morot-Gaudry JF, Maselaux-Daubresse U (2006) Leaf yellowing and anthocyanin accumulation are two genetically independent strategies in response to nitrogen limitation in Arabidopsis thaliana. Plant Cell Physiol 47: 74-83
16. Ding L, Wang KJ, Jing GM, Biswas DK, Xu H, Li LF, Li YH (2005) Effects of nitrogen deficiency on photosynthetic traits of maize hybrids released in different years. Ann Bot (Lond) 96: 925-930
17. Doelling JH, Walker JM, Friedman EM, Thompson AR, Vierstra RD (2002) The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J Biol Chem 277: 33105-33114
18. Edwards JW, Walker EL, Coruzzi GM (1990) Cell-specific expression in transgenic plants reveals nonoverlapping roles for chloroplast and cytosolic glutamine synthetase. Proc Natl Acad Sci USA 87: 3459-3463
19. Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18: 1157-1161
20. Gibeaut DM, Hulett J, Cramer GR, Seemann JR (1997) Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiol 115: 317-319
21. Glass ADM (2003) Nitrogen use efficiency of crop plants: physiological constraints upon nitrate adsorption. Crit Rev Plant Sci 22: 453-470
22. Gong Q, Li P, Ma S, Rupassara SI, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44: 826-839
23. Good AG, Shrawat AK, Muench DG (2004) Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci 9: 597-605
24. Griffith M, Timonin M, Wong CEA, Gray GR, Akhter SR, Saldanha M, Rogers MA, Weretilnyk EA, Moffatt BA (2007) Thellungiella: an Arabidopsis-related model plant adapted to cold temperatures. Plant Cell Environ 30: 529-538
25. Hirel B, Gouis JL, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58: 2369-2387
26. Inan G, Zhang Q, Li P, Wang Z, Cao Z, Zhang H, Zhang C, Quist TM, Goodwin SM, Zhu J, et al (2004) Salt cress: a halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. Plant Physiol 135: 1718-1737
27. Kant P, Kant S, Gordon M, Shaked R, Barak S (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis response to multiple abiotic stresses. Plant Physiol 145: 814-830
28. + uptake in T. halophila. Plant Cell Environ 29: 1220-1234
29. - demand signaling in Arabidopsis. Plant Physiol 142: 1075-1086
30. Lea PJ, Azevedo RA (2006) Nitrogen use efficiency. 1. Uptake of nitrogen from the soil. Ann Appl Biol 149: 243-247
31. - uptake systems by N- and C-status of Arabidopsis plants. Plant J 18: 509-519
32. Li W, Wang Y, Okamoto M, Crawford NM, Siddiqi MY, Glass ADM (2007) Dissection of the AtNRT2.1:AtNRT2.2 inducible high-affinity nitrate transporter gene cluster. Plant Physiol 143: 425-433
33. Liu KH, Huang CY, Tsay YF (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11: 865-874
34. -ΔΔCT method. Methods 25: 402-408
35. Malamy JE (2005) Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28: 67-77
36. Malamy JE, Ryan KS (2001) Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127: 899-909
37. Marschner H (1995) Mineral Nutrition of Higher Plants, Ed 2. Academic Press, London
38. Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon:nitrogen availability. Plant Physiol 128: 472-481
39. McCullough DE, Girardin PH, Mihajlovic M, Aguilera A, Tollenaar M (1994) Influence of N supply on development and dry matter accumulation of an old and a new maize hybrid. Can J Plant Sci 74: 471-477
40. Miller AJ, Fan X, Orsel M, Smith SJ, Wells DM (2007) Nitrate transport and signalling. J Exp Bot 58: 2297-2306
41. Munos 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. Plant Cell 16: 2433-2447
42. Neff MM, Chory J (1998) Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiol 118: 27-36
43. Okamoto M, Kumar A, Li W, Wang Y, Siddiqi MY, Crawford NM, Glass ADM (2006) High-affinity nitrate transport in roots of Arabidopsis depends on expression of the NAR2-like gene AtNRT3.1. Plant Physiol 140: 1036-1046
44. Okamoto M, Vidmar JJ, Glass ADM (2003) Regulation of NRT1 and NRT2 gene families of Arabidopsis thaliana: responses to nitrate provision. Plant Cell Physiol 44: 304-317
45. Ono K, Terashima I, Watanabe A (1996) Interaction between nitrogen deficit of a plant and nitrogen content in the old leaves. Plant Cell Physiol 37: 1083-1089
46. Orsel M, Chopin F, Leleu O, Smith SJ, Krapp A, Daniel-Vedele F, Miller AJ (2006) Characterization of a two-component high-affinity nitrate uptake system in Arabidopsis: physiology and protein-protein interaction. Plant Physiol 142: 1304-1317
47. Orsel M, Eulenburg K, Krapp A, Daniel-Vedele F (2004) Disruption of the nitrate transporter genes AtNRT2.1 and AtNRT2.2 restricts growth at low external nitrate concentration. Planta 219: 714-721
48. Ortiz-Monasterio JI, Sayre KD, Rajaram S, McMahon M (1997) Genetic progress in wheat yield and nitrogen use efficiency under four nitrogen regimes. Crop Sci 37: 898-904
49. Paul MJ, Driscoll SP (1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source:sink imbalance. Plant Cell Environ 20: 110-116
50. Peng M, Bi YM, Zhu T, Rothstein SJ (2007a) Genome-wide analysis of Arabidopsis responsive transcriptome to nitrogen limitation and its regulation by the ubiquitin ligase gene NLA. Plant Mol Biol 65: 775-797
51. Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007b) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50: 320-337
52. Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agron J 91: 357-363
53. Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A (2006) 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 Physiol 140: 909-921
54. Rosen H (1957) A modified ninhydrin colorimetric analysis for amino acids. Arch Biochem Biophys 67: 10-15
55. Sagi M, Dovrat A, Kipnis T, Lips SH (1997) Ionic balance and the production of biomass and organic nitrogen as affected by salinity and N source in annual ryegrass (Lolium multiflorum Lam). J Plant Nutr 20: 1291-1316
56. Shapiro BM, Stadtman ER (1970) The regulation of glutamine synthetase in microorganisms. Annu Rev Microbiol 24: 501-524
57. Siedow JN, Day DA (2000) Respiration and photorespiration. In RG Buchanan, W Gruissem, R Jones, eds, Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD, pp 676-725
58. Stitt M (1999) Nitrate regulation of metabolism and growth. Curr Opin Plant Biol 2: 178-186
59. Taira M, Valtersson U, Burkhardt B, Ludwig RA (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16: 2048-2058
60. Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135: 1697-1709
61. Tsay YF, Chiu CC, Tsai CB, Ho CH, Hsu PK (2007) Nitrate transporters and peptide transporters. FEBS Lett 581: 2290-2300
62. + homeostasis under salinity stress. Plant J 48: 342-353
63. Wang R, Liu D, Crawford NM (1998) The Arabidopsis CHL1 protein plays a major role in high affinity nitrate uptake. Proc Natl Acad Sci USA 95: 15134-15139
64. Wang ZL, Li PH, Fredricksen M, Gong ZZ, Kim CS, Zhang C, Bohnert HJ, Zhu JK, Bressan RA, Hasegawa PM, et al (2004) Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci 166: 609-616
65. Wilkinson JQ, Crawford NM (1991) Identification of the Arabidopsis CHL3 gene as the nitrate reductase structural gene NIA2. Plant Cell 3: 461-471
66. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57: 391-399
67. Wirth J, Chopin F, Santoni V, Viennois G, Tillard P, Krapp A, Lejay L, Daniel-Vedele F, Gojon A (2007) Regulation of root nitrate uptake at the NRT2.1 protein level in Arabidopsis thaliana. J Biol Chem 282: 23541-23552
68. Wong CE, Li Y, Labbe A, Guevara D, Paulo N, Whitty B, Diaz C, Golding GB, Gray GR, Weretilnyk EA, et al (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140: 1437-1450
69. Wong CE, Li Y, Whitty BR, Diaz-Camino C, Akhter SR, Brandle JE, Golding GB, Weretilnyk EA, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58: 561-574
70. Yu X, Sukumaran S, Marton L (1998) Differential expression of the Arabidopsis Nia1 and Nia2 genes. Plant Physiol 116: 1091-1096
71. Zhang H, Rong H, Pilbeam D (2007) Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana. J Exp Bot 58: 2329-2338
72. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6: 66-72
73. Zhuo D, Okamoto M, Vidmar JJ, Glass ADM (1999) Regulation of a putative high-affinity nitrate transporter (Nrt2;1At) in roots of Arabidopsis thaliana. Plant J 17: 563-568