The signal peptide of the Medicago truncatula modular nodulin MtNOD25 operates as an address label for the specific targeting of proteins to nitrogen-fixing symbiosomes

Molecular Plant-Microbe Interactions

Volumn 22, Issue 1, 2009, Pages 63-72

  Hohnjec, Natalija ^a   Lenz, Frauke ^a   Fehlberg, Vera ^a   Vieweg, Martin F ^a   Baier, Markus C ^a   Hause, Bettina ^b   Küster, Helge ^a  

^a BIELEFELD UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

Author keywords

Alternative splicing; Confocal laser scanning microscopy; mRFP

Indexed keywords

GREEN FLUORESCENT PROTEIN; MEMBRANE PROTEIN; NODULIN; SIGNAL PEPTIDE; VEGETABLE PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ARTICLE; BARREL MEDIC; CONFOCAL MICROSCOPY; GENETICS; IN SITU HYBRIDIZATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SYMBIOSIS;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; BASE SEQUENCE; GREEN FLUORESCENT PROTEINS; IN SITU HYBRIDIZATION; MEDICAGO TRUNCATULA; MEMBRANE PROTEINS; MICROSCOPY, CONFOCAL; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PLANT ROOTS; PROTEIN SORTING SIGNALS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID; SYMBIOSIS;

MEDICAGO TRUNCATULA;

EID: 58249102865     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-22-1-0063     Document Type: Article

References (74)

1. Alunni, B., Kevei, Z., Redondo-Nieto, M., Kondorosi, A., Mergaert, P., and Kondorosi, E. 2007. Genomic organization and evolutionary insights on GRP and NCR genes, two large nodule-specific gene families in Medicago truncatula. Mol. Plant-Microbe Interact. 20:1138-1148.
2. Auriac, M. C., and Timmers, A. C. 2007. Nodulation studies in the model legume Medicago truncatula: advantages of using the constitutive EF1alpha promoter and limitations in detecting fluorescent reporter proteins in nodule tissues. Mol. Plant-Microbe Interact. 20:1040-1047.
3. Bairoch, A., Boeckmann, B., Ferro, S., and Gasteiger, E. 2004. Swiss-Prot: Juggling between evolution and stability Brief. Bioinform. 5:39-55.
4. Bevan, M. W. 1984. Binary Agrobacterium tumefaciens vectors for plant transformation. Nucleic Acids Res. 12:8711-8721.
5. Boutet, E., Lieberherr, D., Tognolli, M., Schneider, M., and Bairoch, A. 2007. UniProtKB/Swiss-Prot: the manually annotated section of the UniProt KnowledgeBase. Methods Mol. Biol. 406:89-112.
6. Brewin, N. J. 1991. Development of the legume root nodule. Annu. Rev. Cell Biol. 7:191-226.
7. Bullock, W. C., Fernandez, J. M., and Short, J. M. 1987. XL1Blue: a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. BioTechniques 5:376-379.
8. Carvalho, H. G., Lopes-Cardoso, I. A., Lima, L. M., Melo, P. M., and Cullimore, J. V. 2003. Nodule-specific modulation of glutamine synthetase in transgenic Medicago truncatula leads to inverse alterations in asparagine synthetase expression. Plant. Physiol. 133:243-252.
9. Catalano, C. M., Lane, W. S., and Sherrier, D. J. 2004. Biochemical characterization of symbiosome membrane proteins from Medicago truncatula root nodules. Electrophoresis 25:519-531.
10. Chen, M.-H., Huang, L.-F., Li, H.-M., Chen, Y.-R., and Yu, S.-M. 2004. Signal peptide-dependent targeting of a rice α-amylase and cargo proteins to plastids and extracellular compartments of plant cells. Plant Physiol. 135:1367-1377.
11. 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.
12. Coque, L., Neogi, P., Pislariu, C., Wilson, K. A., Catalano, C., Avadhani, M., Sherrier, D. J., and Dickstein, R. 2008. Transcription of ENOD8 in Medicago truncatula nodules directs ENOD8 esterase to developing and mature symbiosomes. Mol. Plant-Microbe Interact. 21:404-410.
13. Crespi, M., and Galvez, S. 2000. Molecular mechanisms in root nodule development. J. Plant Growth Regul. 19:155-166.
14. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. 2004. Web-Logo: a sequence logo generator. Genome Res. 14:1188-1190.
15. Cullimore, J., and Dénarié, J. 2003. How legumes select their sweet talking symbionts. Science 302:575-578.
16. Day, D. A., Kaiser, B. N., Thomson, R., Udvardi, M. K., Moreau, S., and Puppo, A. 2001. Nutrient transport across symbiotic membranes from legume nodules. Aust. J. Plant Physiol. 28:667-674.
17. Doyle, J., and Luckow, M. A. 2003. The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol. 131:900-910.
18. El Yahyaoui, F., Küster, H., Ben Amor, B., Hohnjec, N., Pühler, A., Becker, A., Gouzy, J., Vernié, T., Gough, C., Niebel, A., Godiard, L., and Gamas, P. 2004. Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol. 136:3159-3176.
19. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. 2007. Locating proteins in the cell using TargetP, SignalP, and related tools. Nat. Protocols 2:953-971.
20. Fedorova, M., van de Mortel, J., Matsumoto, P. A., Cho, J., Town, C. D., VandenBosch, K. A., Gantt, J. S., and Vance, C. P. 2002. Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol. 130:519-537.
21. Frühling, M., Albus, U., Hohnjec, N., Geise, G., Pühler, A., and Perlick, A. M. 2000. A small gene family of broad bean codes for late nodulins containing conserved cysteine clusters. Plant Sci. 152:67-77.
22. Gamas, P., Niebel, F. D. C., Lescure, N., and Cullimore, J. V. 1996. Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. Mol. Plant-Microbe Interact. 9:233-242.
23. Ganter, G., Allen, T., and Dunn, K. 1998. The cDNA sequence of nms32/34 (Accession No. AF077405), a gene whose message is specific to the infected cells of alfalfa root nodules (PGR98-155). Plant Physiol. 118:330.
24. Geurts, R., and Bisseling, T. 2002. Rhizobium Nod factor perception and signalling. Plant Cell 14 (Suppl.):S239-249.
25. Graham, M. A., Silverstein, K. A., Cannon, S. B., and VandenBosch, K. A. 2004. Computational identification and characterization of novel genes from legumes. Plant Physiol. 135:1179-1197.
26. Györgyey, J., Vaubert, D., Jimenez-Zurdo, J. I., Charon, C., Troussard, L., Kondorosi, A., and Kondorosi, E. 2000. Analysis of Medicago truncatula nodule expressed sequence tags. Mol. Plant-Microbe Interact. 13:62-71.
27. Haseloff, J. 1999. GFP variants for multispectral imaging of living cells. Methods Cell Biol. 58:139-151.
28. Haseloff, J., Siemering, D. R., Prasher, D. C., and Hodge, S. 1997. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 94:2122-2127.
29. Hohnjec, N., Perlick, A. M., Pühler, A., and Küster, H. 2003. The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol. Plant-Microbe Interact. 16:903-915.
30. Hohnjec, N., Vieweg, M. F., Pühler, A., Becker, A., and Küster, H. 2005. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137:1283-1301.
31. Journet, E. P., van Tuinen, D., Gouzy, J., Crespeau, H., Carreau, V., Farmer, M. J., Niebel, A., Schiex, T., Jaillon, O., Chatagnier, O., Godiard, L., Micheli, F., Kahn, D., Gianinazzi-Pearson, V., and Gamas, P. 2002. Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res. 30:5579-5592.
32. Kaijalainen, S., Schroda, M., and Lindström, K. 2002. Cloning of nodule-specific cDNAs of Galega orientalis. Physiol. Plant. 114:588-593.
33. Kiss, G. B., Vincze, É., Végh, Z., Tóth, G., and Soós, J. 1990a. Identification and cDNA cloning of a new nodule-specific gene, Nms-25 (nodulin 25) of Medicago sativa. Plant Mol. Biol. 14:467-475.
34. Kiss, G. B., Csanádi, G., Kálmán, K., Kaló, P., and Ökrész, L. 1993. Construction of a basic genetic map for alfalfa using RFLP, RAPD, isozyme and morphological markers. Mol. Gen. Genet. 238:129-137.
35. Küster, H., Perlick, A. M., and Pühler, A. 1994. Members of a broad bean nodulin family with partial homologies to the alfalfa nodulin 25 are composed of two types of amino acid repeats flanked by unique amino acid sequence termini. Plant Mol. Biol. 24:143-157.
36. Küster, H., Quandt, H.-J., Broer, I., Perlick, A. M., and Pühler, A. 1995. The promoter of the Vicia faba L. VfENOD-GRP3 gene encoding a glycine-rich early nodulin mediates a predominant gene expression in the interzone II-III region of transgenic Vicia hirsuta root nodules. Plant Mol. Biol. 29:759-772.
37. Küster, H., Frühling, M., Pühler, A., and Perlick, A. M. 1996. The modular nodulins Nvf-28/32 of broad bean (Vicia faba L.): alternative exon combinations account for different modular structures. Mol. Gen. Genet. 252:648-657.
38. Küster, H., Pühler, A., and Perlick, A. M. 1999. Analysis of genes encoding modular nodulins from Vicia hirsuta and Vicia faba. Plant Sci. 149:1-11.
39. Küster, H., Hohnjec, N., Krajinski, F., El Yahyaoui, F., Manthey, K., Gouzy, J., Dondrup, M., Meyer, F., Kalinowski, J., Brechenmacher, L., van Tuinen, D., Gianinazzi-Pearson, V., Pühler, A., Gamas, P., and Becker, A. 2004. Construction and validation of cDNA-based Mt6k-RIT macro- and microarrays to explore root endosymbioses in the model legume Medicago truncatula. J. Biotechnol. 108:95-113.
40. Liu, J., Miller, S. S., Graham, M., Bucciarelli, B., Catalano, C. M., Sherrier, D. J., Samac, D. A., Ivashuta, S., Fedorova, M., Matsumoto, P., Gantt, J. S., and Vance, C. P. 2006. Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiol. 141:167-177.
41. Meade, H. M., and Signer, E. R. 1977. Genetic mapping of Rhizobium meliloti. Proc. Natl. Acad. Sci. U.S.A. 74:2076-2078.
42. Mergaert, P., Nikovics, K., Kelemen, Z., Maunoury, N., Vaubert, D., Kondorosi, A., and Kondorosi, E. 2003. A novel family in Medicago truncatula consisting of more than 300 nodule-specific genes coding for small, secreted polypeptides with conserved cysteine motifs. Plant Physiol. 132:161-73.
43. Nam, Y. W., Penmetsa, R. V., Endre, G., Uribe, P., Kim, D., and Cook, D. R. 1999. Construction of a bacterial artificial chromosome library of Medicago truncatula and identification of clones containing ethylene-response genes. Theor. Appl. Genet. 98:638-646.
44. Nothwehr, S. F., and Gordon, J. I. 1990. Targeting of proteins into the eukaryotic secretory pathway: signal peptide structure/function relationships. BioEssays 12:479-484.
45. Oldroyd, G. E., and Downie, J. A. 2006. Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol. 9:351-357.
46. Parniske, M. 2000. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr. Opin. Plant Biol. 3:320-328.
47. Pawlowski, K. 1997. Nodule-specific gene expression. Physiol. Plant. 99:617-631.
48. Peng, T., and Dickstein, R. 1994. Regulation of plant nodule-specific genes expressed in alfalfa nodules arrested at early-stage of development. Plant Sci. 101:65-73.
49. Perlick, A. M., and Pühler, A. 1993. A survey of transcripts expressed specifically in root nodules of broadbean (Vicia faba L.). Plant Mol. Biol. 22:957-970.
50. Pridmore, R. D. 1987. New and versatile cloning vectors with kanamycin-resistance marker. Gene 56:309-312.
51. Quackenbush, J., Cho, J., Lee, D., Liang, F., Holt, I., Karamycheva ,S., Parvici, B., Pertea, G., Sultana, R., and White, J. 2001. The TIGR Gene Indices: analysis of gene transcript sequences in highly sampled eukaryotic species. Nucleic Acids Res. 29:159-164.
52. Quandt, H. J., Pühler, A., and Broer, I. 1993. Transgenic root nodules of Vicia hirsuta: A fast and efficient system for the study of gene expression in indeterminate-type nodules. Mol. Plant-Microbe Interact. 6:699-706.
53. Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R., and Lopez, R. 2005. InterProScan: protein domains identifier. Nucleic Acids Res. 33:W116-120.
54. Saalbach, G., Erik, P., and Wienkoop, S. 2002. Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes. Proteomics 2:325-337.
55. Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U.S.A.
56. Schaarschmidt, S., Roitsch, T., and Hause, B. 2006. Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J. Exp. Bot. 57:4015-4023.
57. Schultze, M., and Kondorosi, A. 1998. Regulation of symbiotic root nodule development. Annu. Rev. Genet. 32:33-57.
58. Smit, P., Raedts, J., Portyanko, V., Debelle, F., Gough, C., Bisseling, T., and Geurts, R. 2005. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789-1791.
59. Stougaard, J., Joergenson, J. E., Christensen, T., Kuhle, A., and Marcker, K. A. 1990. Interdependence and nodule specificity of cis-acting regulatory elements in the soybean leghemoglobin lbc3 and N23 gene promoters. Mol. Gen. Genet. 220:353-360.
60. Swiderski, M. R., Zaborowska, Z., and Legocki, A. B. 2000. Identification of new nodulin cDNAs from yellow lupine by differential display. Plant Sci. 151:75-83.
61. Thoquet, P., Gherardi, M., Journet, E. P., Kereszt, A., Ane, J. M., Prosperi, J. M., and Huguet, T. 2002. The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol. 2:1.
62. 2-fixing plants. Nature 378:629-632.
63. 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.
64. van Kammen, A. 1984. Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Mol. Biol. Rep. 2:43-45.
65. 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.
66. Végh, Z., Vincze, É., Kadirov, R., Tóth, G., and Kiss, G. B. 1990. The nucleotide sequence of a nodule-specific gene, Nms-25 of Medicago sativa: its primary evolution via exon-shuffling and retrotransposon-mediated DNA rearrangements. Plant Mol. Biol. 15:295-306.
67. Vieweg, M. F., Frühling, M., Quandt, H.-J., Heim, U., Bäumlein, H., Pühler, A., Küster, H., and Perlick, A. M. 2004. The promoter of the Vicia faba L. leghemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and nonlegume plants. Mol. Plant-Microbe Interact. 17:62-69.
68. von Heijne, G. 1986. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14:4683-4690.
69. Wienkoop, S., and Saalbach, G. 2003. Proteome analysis. Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiol. 131:1080-1090.
70. Zhu, H., Kim, D.-J., Baek, J.-M., Choi, H.-K., Ellis, L. C., Küster, H., McCombie, W. R., Peng, H.-M., and Cook, D. R. 2003. Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organization. Plant Physiol. 131:1018-1026.
71. DFCI Medicago truncatula Gene Index: compbio.dfci.harvard.edu/tgi
72. Medicago genome sequencing project: www.medicago.org/genome
73. National Center for Biotechnology Information website: www.ncbi.nlm.nih.gov
74. University of California-Berkeley WebLogo3 software: weblogo.berkeley. edu/logo.cgi