MALDI mass spectrometry-assisted molecular imaging of metabolites during nitrogen fixation in the Medicago truncatula-Sinorhizobium meliloti symbiosis

Plant Journal

Volumn 75, Issue 1, 2013, Pages 130-145

  Ye, Hui ^a   Gemperline, Erin ^a   Venkateshwaran, Muthusubramanian ^a   Chen, Ruibing ^b   Delaux, Pierre Marc ^a   Howes Podoll, Maegen ^a   Ané, Jean Michel ^a   Li, Lingjun ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

DMAN; legume nodulation; MALDI MSI; Medicago truncatula; metabolites; nitrogen fixation; technical advance

Indexed keywords

DMAN; MALDI-MSI; MEDICAGO TRUNCATULA; NODULATION; TECHNICAL ADVANCES;

AMINO ACIDS; BIOMOLECULES; GENES; IMAGING TECHNIQUES; MASS SPECTROMETRY; METABOLITES; MOLECULAR IMAGING; NAPHTHALENE; PLANTS (BOTANY);

NITROGEN FIXATION;

1 (N DIMETHYL)AMINO 7 NAPHTHOL; 1-(N-DIMETHYL)AMINO-7-NAPHTHOL; 2,5-DIHYDROXYBENZOIC ACID; GENTISIC ACID; NAPHTHOL DERIVATIVE; NITROGEN;

ARTICLE; BARREL MEDIC; CHEMISTRY; GENE EXPRESSION REGULATION; MASS SPECTROMETRY; METABOLISM; METABOLOME; METHODOLOGY; MICROBIOLOGY; MOLECULAR IMAGING; NITROGEN FIXATION; NODULATION; PHENOTYPE; PHYSIOLOGY; PLANT ROOT; SINORHIZOBIUM MELILOTI; SYMBIOSIS;

GENE EXPRESSION REGULATION, PLANT; GENTISATES; MEDICAGO TRUNCATULA; METABOLOME; MOLECULAR IMAGING; NAPHTHOLS; NITROGEN; NITROGEN FIXATION; PHENOTYPE; PLANT ROOT NODULATION; PLANT ROOTS; ROOT NODULES, PLANT; SINORHIZOBIUM MELILOTI; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SYMBIOSIS;

BACTERIA (MICROORGANISMS); FABACEAE; MEDICAGO TRUNCATULA; RHIZOBIACEAE; SINORHIZOBIUM MELILOTI;

EID: 84879221641     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12191     Document Type: Article

References (82)

1. Barsch, A., Carvalho, H.G., Cullimore, J.V., and, Niehaus, K., (2006a) GC-MS based metabolite profiling implies three interdependent ways of ammonium assimilation in Medicago truncatula root nodules. J. Biotechnol. 127, 79-83.
2. Barsch, A., Tellström, V., Patschkowski, T., Küster, H., and, Niehaus, K., (2006b) Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Mol. Plant-Microbe Interact. 19, 998-1013.
3. Becana, M., and, Klucas, R.V., (1992) Oxidation and reduction of leghemoglobin in root nodules of leguminous plants. Plant Physiol. 98, 1217-1221.
4. Benedito, V.A., Torres-Jerez, I., Murray, J.D., et al. (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J. 55, 504-513.
5. Benloch, R., Navarro, C., Beltran, J.P., and, Canas, L.A., (2003) Floral development of the model legume Medicago truncatula: ontogeny studies as a tool to better characterize homeotic mutations. Sex. Plant Reprod. 15, 231-241.
6. Bergersen, F.J., Kennedy, C., and, Hill, S., (1982) Influence of low oxygen concentration on derepression of nitrogenase in Klebsiella pneumoniae. J. Gen. Microbiol. 128, 909-915.
7. Borowiec, A., Lechward, K., Tkacz-Stachowska, K., and, Skladanowski, A.C., (2006) Adenosine as a metabolic regulator of tissue function: production of adenosine by cytoplasmic 5'-nucleotidases. Acta Biochim. Pol. 53, 269-278.
8. Branca, A., Paape, T.D., Zhou, P., et al. (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc. Natl Acad. Sci. USA, 108, E864-E870.
9. Brechenmacher, L., Lei, Z., Libault, M., Findley, S., Sugawara, M., Sadowsky, M.J., Sumner, L.W., and, Stacey, G., (2010) Soybean metabolites regulated in root hairs in response to the symbiotic bacterium Bradyrhizobium japonicum. Plant Physiol. 153, 1808-1822.
10. Broeckling, C.D., Huhman, D.V., Farag, M.A., Smith, J.T., May, G.D., Mendes, P., Dixon, R.A., and, Sumner, L.W., (2005) Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J. Exp. Bot. 56, 323-336.
11. Catoira, R., Galera, C., de Billy, F., Penmetsa, R.V., Journet, E.P., Maillet, F., Rosenberg, C., Cook, D., Gough, C., and, Denarie, J., (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell, 12, 1647-1666.
12. Cha, S.W., Zhang, H., Ilarslan, H.I., Wurtele, E.S., Brachova, L., Nikolau, B.J., and, Yeung, E.S., (2008) Direct profiling and imaging of plant metabolites in intact tissues by using colloidal graphite-assisted laser desorption ionization mass spectrometry. Plant J. 55, 348-360.
13. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., Kopka, J., and, Udvardi, M.K., (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487-512.
14. Desbrosses, G.G., Kopka, J., and, Udvardi, M.K., (2005) Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol. 137, 1302-1318.
15. D'Haeze, W., and, Holsters, M., (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology, 12, 79R-105R.
16. Edwards, E.L., Rodrigues, J.A., Ferreira, J., Goodall, D.M., Rauter, A.P., Justino, J., and, Thomas-Oates, J., (2006) Capillary electrophoresis-mass spectrometry characterisation of secondary metabolites from the antihyperglycaemic plant Genista tenera. Electrophoresis, 27, 2164-2170.
17. Farag, M.A., Huhman, D.V., Lei, Z.T., and, Sumner, L.W., (2007) Metabolic profiling and systematic identification of flavonoids and isoflavonoids in roots and cell suspension cultures of Medicago truncatula using HPLC-UV-ESI-MS and GC-MS. Phytochemistry, 68, 342-354.
18. Farag, M.A., Huhman, D.V., Dixon, R.A., and, Sumner, L.W., (2008) Metabolomics reveals novel pathways and differential mechanistic and elicitor-specific responses in phenylpropanoid and isoflavonoid biosynthesis in Medicago truncatula cell cultures. Plant Physiol. 146, 387-402.
19. Gallardo, K., Le Signor, C., Vandekerckhove, J., Thompson, R.D., and, Burstin, J., (2003) Proteomics of Medicago truncatula seed development establishes the time frame of diverse metabolic processes related to reserve accumulation. Plant Physiol. 133, 664-682.
20. Garrocho-Villegas, V., Gopalasubramaniam, S.K., and, Arredondo-Peter, R., (2007) Plant hemoglobins: what we know six decades after their discovery. Gene, 398, 78-85.
21. Gilles-Gonzalez, M.A., Ditta, G.S., and, Helinski, D.R., (1991) A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature, 350, 170-172.
22. Gloux, K., and, Lerudulier, D., (1989) Transport and catabolism of proline betaine in salt-stressed Rhizobium meliloti. Arch. Microbiol. 151, 143-148.
23. Goldmann, A., Boivin, C., Fleury, V., Message, B., Lecoeur, L., Maille, M., and, Tepfer, D., (1991) Betaine use by rhizosphere bacteria: genes essential for trigonelline, stachydrine, and carnitine catabolism in Rhizobium meliloti are located on pSym in the symbiotic region. Mol. Plant-Microbe Interact. 4, 571-578.
24. Gordon, A.J., Thomas, B.J., and, James, C.L., (1995) The location of sucrose synthase in root nodules of white clover. New Phytol. 130, 523-530.
25. Graham, P.H., and, Vance, C.P., (2003) Legumes: importance and constraints to greater use. Plant Physiol. 131, 872-877.
26. Grimsrud, P.A., den Os, D., Wenger, C.D., Swaney, D.L., Schwartz, D., Sussman, M.R., Ané, J.M., and, Coon, J.J., (2010) Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiol. 152, 19-28.
27. Harada, K., and, Fukusaki, E., (2009) Profiling of primary metabolite by means of capillary electrophoresis-mass spectrometry and its application for plant science. Plant Biotechnol. 26, 47-52.
28. Hartwig, U.A., Maxwell, C.A., Joseph, C.M., and, Phillips, D.A., (1990a) Effects of alfalfa nod gene-inducing flavonoids on nodABC transcription in Rhizobium meliloti strains containing different nodD genes. J. Bacteriol. 172, 2769-2773.
29. Hartwig, U.A., Maxwell, C.A., Joseph, C.M., and, Phillips, D.A., (1990b) Chrysoeriol and luteolin released from alfalfa seeds induce nod genes in Rhizobium meliloti. Plant Physiol. 92, 116-122.
30. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., and, Bohnert, H.J., (2000) Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 463-499.
31. Hölscher, D., Shroff, R., Knop, K., Gottschaldt, M., Crecelius, A., Schneider, B., Heckel, D.G., Schubert, U.S., and, Svatoš, A., (2009) Matrix-free UV-laser desorption/ionization (LDI) mass spectrometric imaging at the single-cell level: distribution of secondary metabolites of Arabidopsis thaliana and Hypericum species. Plant J. 60, 907-918.
32. Jones, D.L., (1998) Organic acids in the rhizosphere-a critical review. Plant Soil, 205, 25-44.
33. Jun, J.H., Song, Z., Liu, Z., Nikolau, B.J., Yeung, E.S., and, Lee, Y.J., (2010) High-spatial and high-mass resolution imaging of surface metabolites of Arabidopsis thaliana by laser desorption-ionization mass spectrometry using colloidal silver. Anal. Chem. 82, 3255-3265.
34. Kahn, M.L., Kraus, J., and, Somerville, J.E., (1985) A model of nutrient exchange in the Rhizobium-legume symbiosis. In Nitrogen Fixation Research Progress (, Evans, H.J., Bottomley, P.J., and, Newton, W.E., eds). Dordrecht, The Netherlands: Martinus Nijhoff, pp. 193-199.
35. Kaspar, S., Peukert, M., Svatoš, A., Matros, A., and, Mock, H.P., (2011) MALDI-imaging mass spectrometry-an emerging technique in plant biology. Proteomics, 11, 1840-1850.
36. Kessmann, H., Edwards, R., Geno, P.W., and, Dixon, R.A., (1990) Stress responses in alfalfa (Medicago sativa L.): V Constitutive and elicitor-induced accumulation of isoflavonoid conjugates in cell suspension cultures. Plant Physiol. 94, 227-232.
37. Kueger, S., Steinhauser, D., Willmitzer, L., and, Giavalisco, P., (2012) High-resolution plant metabolomics: from mass spectral features to metabolites and from whole-cell analysis to subcellular metabolite distributions. Plant J. 70, 39-50.
38. Lee, S., Valentine, S.J., Reilly, J.P., and, Clemmer, D.E., (2012a) Analyzing a mixture of disaccharides by IMS-VUVPD-MS. Int. J. Mass Spectrom. 309, 161-167.
39. Lee, Y.J., Perdian, D.C., Song, Z.H., Yeung, E.S., and, Nikolau, B.J., (2012b) Use of mass spectrometry for imaging metabolites in plants. Plant J. 70, 81-95.
40. Li, Y., Shrestha, B., and, Vertes, A., (2007) Atmospheric pressure molecular imaging by infrared MALDI mass spectrometry. Anal. Chem. 79, 523-532.
41. Li, Y., Shrestha, B., and, Vertes, A., (2008) Atmospheric pressure infrared MALDI imaging mass spectrometry for plant metabolomics. Anal. Chem. 80, 407-420.
42. Lodwig, E.M., Hosie, A.H.F., Bourdès, A., Findlay, K., Allaway, D., Karunakaran, R., Downie, J.A., and, Poole, P.S., (2003) Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature, 422, 722-726.
43. Lois, A.F., Ditta, G.S., and, Helinski, D.R., (1993) The oxygen sensor FixL of Rhizobium meliloti is a membrane protein containing four possible transmembrane segments. J. Bacteriol. 175, 1103-1109.
44. Masson-Boivin, C., Giraud, E., Perret, X., and, Batut, J., (2009) Establishing nitrogen-fixing symbiosis with legumes: how many rhizobium recipes? Trends Microbiol. 17, 458-466.
45. Maxwell, C.A., Hartwig, U.A., Joseph, C.M., and, Phillips, D.A., (1989) A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91, 842-847.
46. Mitra, R.M., and, Long, S.R., (2004) Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiol. 134, 595-604.
47. Nemes, P., and, Vertes, A., (2007) Laser ablation electrospray ionization for atmospheric pressure, in vivo, and imaging mass spectrometry. Anal. Chem. 79, 8098-8106.
48. Northen, T.R., Yanes, O., Northen, M.T., Marrinucci, D., Uritboonthai, W., Apon, J., Golledge, S.L., Nordström, A., and, Siuzdak, G., (2007) Clathrate nanostructures for mass spectrometry. Nature, 449, 1033-1036.
49. Ott, T., Sullivan, J., James, E.K., Flemetakis, E., Gunther, C., Gibon, Y., Ronson, C., and, Udvardi, M., (2009) Absence of symbiotic leghemoglobins alters bacteroid and plant cell differentiation during development of Lotus japonicus root nodules. Mol. Plant-Microbe Interact. 22, 800-808.
50. Pachuta, S.J., and, Cooks, R.G., (1987) Mechanisms in molecular SIMS. Chem. Rev. 87, 647-669.
51. Penmetsa, R.V., and, Cook, D.R., (2000) Production and characterization of diverse developmental mutants of Medicago truncatula. Plant Physiol. 123, 1387-1397.
52. Peters, N.K., Frost, J.W., and, Long, S.R., (1986) A plant flavone, luteolin, induces expression of Rhizobium meliloti nodulation genes. Science, 233, 977-980.
53. Phillips, D.A., Joseph, C.M., and, Maxwell, C.A., (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol. 99, 1526-1531.
54. Reyrat, J.M., David, M., Blonski, C., Boistard, P., and, Batut, J., (1993) Oxygen-regulated in vitro transcription of Rhizobium meliloti nifA and fixK genes. J. Bacteriol. 175, 6867-6872.
55. Rose, C.M., Venkateshwaran, M., Grimsrud, P.A., Westphall, M.S., Sussman, M.R., Coon, J.J., and, Ané, J.M., (2012) Medicago PhosphoProtein Database: a repository for Medicago truncatula phosphoprotein data. Front. Plant Sci. 3, 122.
56. Samac, D.A., Peñuela, S., Schnurr, J.A., Hunt, E.N., Foster-Hartnett, D., Vandenbosch, K.A., and, Gantt, J.S., (2011) Expression of coordinately regulated defence response genes and analysis of their role in disease resistance in Medicago truncatula. Mol. Plant Pathol. 12, 786-798.
57. Santana, M.A., Pihakaski-Maunsbach, K., Sandal, N., Marcker, K.A., and, Smith, A.G., (1998) Evidence that the plant host synthesizes the heme moiety of leghemoglobin in root nodules. Plant Physiol. 116, 1259-1269.
58. Shimma, S., and, Seto, M., (2007) Mass microscopy to reveal distinct localization of Heme B (m/z 616) in colon cancer liver metastasis. J. Mass Spectrom. Soc. Jpn, 55, 145-148.
59. Shroff, R., and, Svatoš, A., (2009) Proton sponge: a novel and versatile MALDI matrix for the analysis of metabolites using mass spectrometry. Anal. Chem. 81, 7954-7959.
60. Shroff, R., Rulisek, L., Doubsky, J., and, Svatoš, A., (2009) Acid-base-driven matrix-assisted mass spectrometry for targeted metabolomics. Proc. Natl Acad. Sci. USA, 106, 10092-10096.
61. Starker, C.G., Parra-Colmenares, A.L., Smith, L., Mitra, R.M., and, Long, S.R., (2006) Nitrogen fixation mutants of Medicago truncatula fail to support plant and bacterial symbiotic gene expression. Plant Physiol. 140, 671-680.
62. Stitt, M., Muller, C., Matt, P., Gibon, Y., Carillo, P., Morcuende, R., Scheible, W.R., and, Krapp, A., (2002) Steps towards an integrated view of nitrogen metabolism. J. Exp. Bot. 53, 959-970.
63. Stoeckli, M., Chaurand, P., Hallahan, D.E., and, Caprioli, R.M., (2001) Imaging mass spectrometry: a new technology for the analysis of protein expression in mammalian tissues. Nat. Med. 7, 493-496.
64. Subramanian, S., Stacey, G., and, Yu, O., (2006) Endogenous isoflavones are essential for the establishment of symbiosis between soybean and Bradyrhizobium japonicum. Plant J. 48, 261-273.
65. Subramanian, S., Stacey, G., and, Yu, O., (2007) Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci. 12, 282-285.
66. 2 fixation in legumes? Plant Signal Behav. 6, 32-36.
67. 2 fixation efficiency in the model legume Medicago truncatula. Plant, Cell Environ. 33, 2162-2172.
68. Suzuki, H., Reddy, M.S., Naoumkina, M., Aziz, N., May, G.D., Huhman, D.V., Sumner, L.W., Blount, J.W., Mendes, P., and, Dixon, R.A., (2005) Methyl jasmonate and yeast elicitor induce differential transcriptional and metabolic re-programming in cell suspension cultures of the model legume Medicago truncatula. Planta, 220, 696-707.
69. Takáts, Z., Wiseman, J.M., and, Cooks, R.G., (2005) Ambient mass spectrometry using desorption electrospray ionization (DESI): instrumentation, mechanisms and applications in forensics, chemistry, and biology. J. Mass Spectrom. 40, 1261-1275.
70. Trinchant, J.C., Boscari, A., Spermato, G., Van de Sype, G., and, Le Rudulier, D., (2004) Proline betaine accumulation and metabolism in alfalfa plants under sodium chloride stress. Exploring its compartmentalization in nodules. Plant Physiol. 135, 1583-1594.
71. Turner, G.L., and, Gibson, A.H., (1980) Measurement of nitrogen fixation by indirect means. In Methods for Evaluating Biological Nitrogen Fixation (, Bergersen, F.J., ed.). Chichester, UK: John Wiley & Sons, pp. 111-138.
72. Udvardi, M.K., and, Day, D.A., (1997) Metabolite transport across symbiotic membranes of legume nodules. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 493-523.
73. Vaclavik, L., Cajka, T., Hrbek, V., and, Hajslova, J., (2009) Ambient mass spectrometry employing direct analysis in real time (DART) ion source for olive oil quality and authenticity assessment. Anal. Chim. Acta, 645, 56-63.
74. Vasse, J., de Billy, F., Camut, S., and, Truchet, G., (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J. Bacteriol. 172, 4295-4306.
75. Venkateshwaran, M., and, Ané, J.M., (2011) Legumes and nitrogen fixation: physiological, molecular, evolutionary perspective and applications. In The Molecular Basis of Nutrient Use Efficiency in Crops (, Hawkesford, M., and, Barraclough, P., eds). Oxford, UK: John Wiley & Sons, pp. 443-489.
76. Wang, H.L., Chen, J.H., Wen, J.Q., Tadege, M., Li, G.M., Liu, Y., Mysore, K.S., Ratet, P., and, Chen, R.J., (2008) Control of compound leaf development by FLORICAULA/LEAFY ortholog SINGLE LEAFLET1 in Medicago truncatula. Plant Physiol. 146, 1759-1772.
77. Wang, D., Griffitts, J., Starker, C., Fedorova, E., Limpens, E., Ivanov, S., Bisseling, T., and, Long, S., (2010) A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science, 327, 1126-1129.
78. Wasson, A.P., Pellerone, F.I., and, Mathesius, U., (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell, 18, 1617-1629.
79. Wiseman, J.M., Ifa, D.R., Song, Q.Y., and, Cooks, R.G., (2006) Tissue imaging at atmospheric pressure using desorption electrospray ionization (DESI) mass spectrometry. Angew. Chem. Int. Ed. Engl. 45, 7188-7192.
80. Woo, H.K., Northen, T.R., Yanes, O., and, Siuzdak, G., (2008) Nanostructure-initiator mass spectrometry: a protocol for preparing and applying NIMS surfaces for high-sensitivity mass analysis. Nat. Protoc. 3, 1341-1349.
81. Zahran, H.H., (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol. Mol. Biol. Rev. 63, 968-989.
82. Zhang, N., Venkateshwaran, M., Boersma, M., Harms, A., Howes-Podoll, M., den Os, D., Ané, J.M., and, Sussman, M.R., (2012) Metabolomic profiling reveals suppression of oxylipin biosynthesis during the early stages of legume-rhizobia symbiosis. FEBS Lett. 586, 3150-3158.