An RNA sequencing transcriptome analysis reveals novel insights into molecular aspects of the nitrate impact on the nodule activity of Medicago truncatula

Plant Physiology

Volumn 164, Issue 1, 2014, Pages 400-411

  Cabeza, Ricardo ^a,b   Koester, Beke ^a   Liese, Rebecca ^a   Lingner, Annika ^a   Baumgarten, Vanessa ^a   Dirks, Jan ^a   Salinas Riester, Gabriela ^a   Pommerenke, Claudia ^a   Dittert, Klaus ^a   Schulze, Joachim ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; IRON; LEGHEMOGLOBIN; MEMBRANE PROTEIN; NITRATE REDUCTASE; NITRIC ACID DERIVATIVE; NODULIN; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; BARREL MEDIC; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NODULATION; PHYSIOLOGY; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY; SEQUENCE ANALYSIS;

ADENOSINE TRIPHOSPHATE; GENE EXPRESSION REGULATION, PLANT; IRON; LEGHEMOGLOBIN; MEDICAGO TRUNCATULA; MEMBRANE PROTEINS; NITRATE REDUCTASE; NITRATES; PLANT LEAVES; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; RNA, PLANT; ROOT NODULES, PLANT; SEQUENCE ANALYSIS, RNA;

EID: 84891809906     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.228312     Document Type: Article

References (77)

1. Bagchi R, Salehin M, Adeyemo OS, Salazar C, Shulaev V, Sherrier DJ, Dickstein R (2012) Functional assessment of the Medicago truncatula NIP/LATD protein demonstrates that it is a high-affinity nitrate transporter. Plant Physiol 160: 906-916
2. Baier MC, Barsch A, Küster H, Hohnjec N (2007) Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol 145: 1600-1618
3. Becana M, Matamoros MA, Udvardi M, Dalton DA (2010) Recent insights into antioxidant defenses of legume root nodules. New Phytol 188: 960-976
4. Becker A, Bergès H, Krol E, Bruand C, Rüberg S, Capela D, Lauber E, Meilhoc E, Ampe F, de Bruijn FJ, et al (2004) Global changes in gene expression in Sinorhizobium meliloti 1021 under microoxic and symbiotic conditions. Mol Plant Microbe Interact 17: 292-303
5. Blumenthal JM, Russelle MP, Vance CP (1997) Localized and internal effect of nitrate on symbiotic dinitrogen fixation. Physiol Plant 101: 59-66
6. Boscari A, Del Giudice J, Ferrarini A, Venturini L, Zaffini AL, Delledonne M, Puppo A (2013) Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol 161: 425-439
7. Bouguyon E, Gojon A, Nacry P (2012) Nitrate sensing and signaling in plants. Semin Cell Dev Biol 23: 648-654
8. Castaings L, Camargo A, Pocholle D, Gaudon V, Texier Y, Boutet-Mercey S, Taconnat L, Renou JP, Daniel-Vedele F, Fernandez E, et al (2009) The nodule inception-like protein 7 modulates nitrate sensing and metabolism in Arabidopsis. Plant J 57: 426-435
9. Cesar AI, Minchin FR, Gordon AJ, Nath AK (1997) Possible causes of the physiological decline in soybean nitrogen fixation in the presence of nitrate. J Exp Bot 48: 905-913
10. Colditz F, Braun HP (2010) Medicago truncatula proteomics. J Proteomics 73: 1974-1985
11. Delorenzo C, Iannetta PPM, Fernandezpascual M, James EK, Lucas MM, Sprent JI, Witty JF, Minchin FR, Defelipe MR (1993) Oxygen diffusion in lupin nodules. 2. Mechanisms of diffusion barrier operation. J Exp Bot 44: 1469-1474
12. Denison RF, Harter BL (1995) Nitrate effects on nodule oxygen permeability and leghemoglobin (nodule oximetry and computer modeling). Plant Physiol 107: 1355-1364
13. Denison RF, Kinraide TB (1995) Oxygen-induced membrane depolarizations in legume root-nodules (possible evidence for an osmoelectrical mechanism controlling nodule gas-permeability). Plant Physiol 108: 235-240
14. Dillies MA, Rau A, Aubert J, Hennequet-Antier C, Jeanmougin M, Servant N, Keime C, Marot G, Castel D, Estelle J, et al (2013) A comprehensive evaluation of normalization methods for Illumina highthroughput RNA sequencing data analysis. Brief Bioinform 14: 671-683
15. Elumalai RP, Nagpal P, Reed JW (2002) A mutation in the Arabidopsis KT2/ KUP2 potassium transporter gene affects shoot cell expansion. Plant Cell 14: 119-131
16. Fei H, Vessey JK (2009) Stimulation of nodulation in Medicago truncatula by low concentrations of ammonium: quantitative reverse transcription PCR analysis of selected genes. Physiol Plant 135: 317-330
17. Ferguson BJ, Indrasumunar A, Hayashi S, Lin MH, Lin YH, Reid DE, Gresshoff PM (2010) Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 52: 61-76
18. Fischinger SA, Drevon JJ, Claassen N, Schulze J (2006) Nitrogen from senescing lower leaves of common bean is re-translocated to nodules and might be involved in a N-feedback regulation of nitrogen fixation. J Plant Physiol 163: 987-995
19. Fischinger SA, Schulze J (2010a) The argon-induced decline in nitrogenase activity commences before the beginning of a decline in nodule oxygen uptake. J Plant Physiol 167: 1112-1115
20. 2 fixation for the efficiency of symbiotic nitrogen fixation in pea at vegetative growth and during pod formation. J Exp Bot 61: 2281-2291
21. Forde BG (2000) Nitrate transporters in plants: structure, function, and regulation. Biochim Biophys Acta 1465: 219-235
22. Forde BG, Walch-Liu P (2009) Nitrate and glutamate as environmental cues for behavioural responses in plant roots. Plant Cell Environ 32: 682-693
23. Fujikake H, Yamazaki A, Ohtake N, Sueyoshi K, Matsuhashi S, Ito T, Mizuniwa C, Kume T, Hashimoto S, Ishioka NS, et al (2003) Quick and reversible inhibition of soybean root nodule growth by nitrate involves a decrease in sucrose supply to nodules. J Exp Bot 54: 1379-1388
24. Gachomo EW, Jimenez-Lopez JC, Kayodé APP, Baba-Moussa L, Kotchoni SO (2012) Structural characterization of plant defensin protein superfamily. Mol Biol Rep 39: 4461-4469
25. Gan YB, Bernreiter A, Filleur S, Abram B, Forde BG (2012) Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol 53: 1003-1016
26. Gordon AJ, Minchin FR, James CL, Komina O (1999) Sucrose synthase in legume nodules is essential for nitrogen fixation. Plant Physiol 120: 867-878
27. Gordon AJ, Skøt L, James CL, Minchin FR (2002) Short-term metabolic responses of soybean root nodules to nitrate. J Exp Bot 53: 423-428
28. Hofmann NR (2012) Nicotianamine in zinc and iron homeostasis. Plant Cell 24: 373
29. Horchani F, Prévot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, et al (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155: 1023-1036
30. Hummon AB, Lim SR, Difilippantonio MJ, Ried T (2007) Isolation and solubilization of proteins after TRIzol extraction of RNA and DNA from patient material following prolonged storage. Biotechniques 42: 467-472
31. 2 concentration on nodule activity in soybean. Plant Physiol 91: 315-321
32. Hwang JH, Ellingson SR, Roberts DM (2010) Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett 584: 4339-4343
33. Iannetta PPM, Delorenzo C, James EK, Fernandezpascual M, Sprent JI, Lucas MM, Witty JF, Defelipe MR, Minchin FR (1993) Oxygen diffusion in lupin nodules. 1. Visualization of diffusion barrier operation. J Exp Bot 44: 1461-1467
34. Iannetta PPM, James EK, Sprent JI, Minchin FR (1995) Time-course of changes involved in the operation of the oxygen diffusion barrier in white lupin nodules. J Exp Bot 46: 565-575
35. Jones R, Ougham H, Thomas H, Waaland S (2013). The Molecular Life of Plants, Ed 1. Wiley-Blackwell and American Society of Plant Biologists, Hoboken, NJ.
36. Kanayama Y, Watanabe I, Yamamoto Y (1990) Inhibition of nitrogen fixation in soybean plants supplied with nitrate. I. Nitrite accumulation and formation of nitrosylleghemoglobin in nodules. Plant Cell Physiol 31: 341-346
37. Kanayama Y, Yamamoto Y (1990) Effects of nitrate on nucleotide levels in soybean nodules. Plant Cell Physiol 31: 893-895
38. Kato K, Kanahama K, Kanayama Y (2010) Involvement of nitric oxide in the inhibition of nitrogenase activity by nitrate in Lotus root nodules. J Plant Physiol 167: 238-241
39. Kereszt A, Mergaert P, Kondorosi E (2011) Bacteroid development in legume nodules: evolution of mutual benefit or of sacrificial victims? Mol Plant Microbe Interact 24: 1300-1309
40. Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238: 106-119
41. Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010a) Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13: 266-273
42. Krouk G, Mirowski P, LeCun Y, Shasha DE, Coruzzi GM (2010b) Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate. Genome Biol 11: R123
43. 2 favours nitrate reduction in the roots of wild-type tobacco (Nicotiana tabacum cv. Gat.) and significantly alters N-metabolism in transformants lacking functional nitrate reductase in the roots. J Exp Bot 53: 2351-2367
44. Ligaba A, Maron L, Shaff J, Kochian L, Piñeros M (2012) Maize ZmALMT2 is a root anion transporter that mediates constitutive root malate efflux. Plant Cell Environ 35: 1185-1200
45. Liu JP, Magalhaes JV, Shaff J, Kochian LV (2009) Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. Plant J 57: 389-399
46. Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24: 133-141
47. Masalkar P, Wallace IS, Hwang JH, Roberts DM (2010) Interaction of cytosolic glutamine synthetase of soybean root nodules with the Cterminal domain of the symbiosome membrane nodulin 26 aquaglyceroporin. J Biol Chem 285: 23880-23888
48. Matamoros MA, Baird LM, Escuredo PR, Dalton DA, Minchin FR, Iturbe-Ormaetxe I, Rubio MC, Moran JF, Gordon AJ, Becana M (1999) Stressinduced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol 121: 97-112
49. Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R (2011) Nitric oxide in legume-rhizobium symbiosis. Plant Sci 181: 573-581
50. Minchin FR (1997) Regulation of oxygen diffusion in legume nodules. Soil Biol Biochem 29: 881-888
51. Morère-Le Paven MC, Viau L, Hamon A, Vandecasteele C, Pellizzaro A, Bourdin C, Laffont C, Lapied B, Lepetit M, Frugier F, et al (2011) Characterization of a dual-affinity nitrate transporter MtNRT1.3 in the model legume Medicago truncatula. J Exp Bot 62: 5595-5605
52. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. NatMethods 5: 621-628
53. 2 fixation by peas (Pisum sativum L.) in response to short-term nitrate exposure. Plant Soil 346: 275-287
54. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59: 25-35
55. Nookaew I, PapiniM, Pornputtapong N, Scalcinati G, Fagerberg L, Uhlén M, Nielsen J (2012) A comprehensive comparison of RNA-Seq-based transcriptome analysis from reads to differential gene expression and cross-comparison with microarrays: a case study in Saccharomyces cerevisiae. Nucleic Acids Res 40: 10084-10097
56. Okamoto S, Ohnishi E, Sato S, Takahashi H, Nakazono M, Tabata S, KawaguchiM(2009) Nod factor/nitrate-induced CLE genes that drive HAR1-mediated systemic regulation of nodulation. Plant Cell Physiol 50: 67-77
57. Okubara PA, Fujishige NA, Hirsch AM, Berry AM (2000) Dg93, a noduleabundant mRNA of Datisca glomerata with homology to a soybean early nodulin gene. Plant Physiol 122: 1073-1079
58. Ott T, van Dongen JT, Gunther C, Krusell L, Desbrosses G, Vigeolas H, Bock V, Czechowski T, Geigenberger P, Udvardi MK (2005) Symbiotic leghemoglobins are crucial for nitrogen fixation in legume root nodules but not for general plant growth and development. Current Biology 15: 531-535
59. Reid DE, Ferguson BJ, Gresshoff PM (2011) Inoculation-and nitrateinduced CLE peptides of soybean control NARK-dependent nodule formation. Mol Plant Microbe Interact 24: 606-618
60. Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Martin-Magniette ML, van der Merwe MJ, Kakar K, Gouzy J, Fernie AR, et al (2008) Systemic signaling of the plant nitrogen status triggers specific transcriptome responses depending on the nitrogen source in Medicago truncatula. Plant Physiol 146: 2020-2035
61. Schubert S (1995) Nitrogen assimilation by legumes-processes and ecological limitations. Fert Res 42: 99-107
62. Schuller KA, Minchin FR, Gresshoff PM (1988) Nitrogenase activity and oxygen diffusion in nodules of soybean cv Bragg and a supernodulating mutant: effects of nitrate. J Exp Bot 39: 865-877
63. Schwarz G, Boxer DH, Mendel RR (1997) Molybdenum cofactor biosynthesis. The plant protein Cnx1 binds molybdopterin with high affinity. J Biol Chem 272: 26811-26814
64. 2 fixation by nitrate. Crit Rev Plant Sci 7: 1-23
65. Tamai S, Iida H, Yokota S, Sayano T, Kiguchiya S, Ishihara N, Hayashi JI, Mihara K, Oka T (2008) Characterization of the mitochondrial protein LETM1, which maintains the mitochondrial tubular shapes and interacts with the AAA-ATPase BCS1L. Journal of Cell Science 121: 2588-2600
66. Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37: 914-939
67. Tsay YF, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72: 705-713
68. Udvardi M, Poole PS (2013) Transport and metabolism in legume-rhizobia symbioses. Annu Rev Plant Biol 64: 781-805
69. Van de VeldeW, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H, et al (2010) Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122-1126
70. Vessey JK, Walsh KB, Layzell DB (1998) Oxygen limitation of N-2 fixation in stem-girdled and nitrate-treated soybean. Physiologia Plantarum 73: 113-121
71. Vessey JK, Waterer J (1992) In search of the mechanism of nitrate inhibition of nitrogenase activity in legume nodules: recent developments. Physiol Plant 84: 171-176
72. Walch-Liu P, Ivanov II, Filleur S, Gan YB, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot (Lond) 97: 875-881
73. Wang D, Griffitts J, Starker C, Fedorova E, Limpens E, Ivanov S, Bisseling T, Long SR (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126-1129
74. Wang YY, Hsu PK, Tsay YF (2012) Uptake, allocation and signaling of nitrate. Trends Plant Sci 17: 458-467
75. Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10: 57-63
76. Wienkoop S, Saalbach G (2003) Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol 131: 1080-1090
77. Wilson ID, Neill SJ, Hancock JT (2008) Nitric oxide synthesis and signalling in plants. Plant Cell Environ 31: 622-631