Differential gel electrophoresis (DIGE) to quantitatively monitor early symbiosis- and pathogenesis-induced changes of the Medicago truncatula root proteome

Journal of Proteomics

Volumn 73, Issue 4, 2010, Pages 753-768

  Schenkluhn, Leif ^a   Hohnjec, Natalija ^b   Niehaus, Karsten ^a   Schmitz, Udo ^b   Colditz, Frank ^b  

^a BIELEFELD UNIVERSITY   (Germany)

^b LEIBNIZ UNIVERSITY HANNOVER   (Germany)

Author keywords

Aphanomyces; Arbuscular mycorrhiza (AM); Differential gel electrophoresis (DIGE); Interactome; Medicago; Sinorhizobium

Indexed keywords

CARBOHYDRATE; CARBON; LECTIN; NITROGEN; PHYTOALEXIN; PROTEOME; SERINE PROTEINASE INHIBITOR;

APHANOMYCES; ARTICLE; BARREL MEDIC; CARBOHYDRATE METABOLISM; CARBON FIXATION; CONTROLLED STUDY; GEL ELECTROPHORESIS; MYCOSIS; NITROGEN FIXATION; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INDUCTION; SYMBIOSIS; TOXIN SYNTHESIS;

ANTIOXIDANTS; APHANOMYCES; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GLOMEROMYCOTA; MEDICAGO TRUNCATULA; PLANT DISEASES; PLANT PROTEINS; PLANT ROOTS; PROTEOME; SINORHIZOBIUM MELILOTI; SOIL MICROBIOLOGY; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SYMBIOSIS; TIME FACTORS;

APHANOMYCES; APHANOMYCES EUTEICHES; ARBUSCULAR; GLOMUS INTRARADICES; MEDICAGO; MEDICAGO TRUNCATULA; SINORHIZOBIUM; SINORHIZOBIUM MELILOTI;

EID: 75049085409     PISSN: 18743919     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jprot.2009.10.009     Document Type: Article

References (68)

1. Remy W., Taylor T.N., Hass H., and Kerp H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91 (1994) 11841-11843
2. Markmann K., and Parniske M. Evolution of root endosymbiosis with bacteria: how novel are nodules?. Trends Plant Sci 14 (2009) 77-86
3. Wang H., Moore M.J., Soltis P.S., Bell C.D., Brockington S.F., Alexandre R., et al. Rosid radiation and the rapid rise of angiosperm-dominated forests. Proc Natl Acad Sci USA 106 (2009) 3853-3858
4. Oldroyd G.E.D., and Downie J.A. Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9 (2006) 351-357
5. Riely B.K., Lougnon G., Ané J.-M., and Cook D.R. The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49 (2007) 208-216
6. Akiyama K., Matsuzaki K., and Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435 (2005) 824-827
7. Olah B., Briere C., Becard G., Denarie J., and Gough C. Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44 (2005) 195-207
8. Zhang S., Liu Y., and Klessig D.F. Multiple levels of tobacco WIPK activation during the induction of cell death by fungal elicitins. Plant J 23 (2000) 339-347
9. Nürnberger T., Brunner F., Kemmerling B., and Piater L. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198 (2004) 249-266
10. Genre A., Ortu G., Bertoldo C., Martino E., and Bonfante P. Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol 149 (2009) 1424-1434
11. Genre A., Chabaud M., Timmers T., Bonfante P., and Barker D.G. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17 (2005) 3489-3499
12. Hardham A.R., Jones D.A., and Takemoto D. Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10 (2007) 342-348
13. Hardham A.R., Takemoto D., and White R.G. Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8 (2008) 63
14. Hammond-Kosack K.E., and Jones J.D.G. Resistance gene-dependent plant defense responses. Plant Cell 8 (1996) 1773-1791
15. Scheidle H., Groß A., and Niehaus K. The lipid A substructure of the Sinorhizobium meliloti lipopolysaccharides is sufficient to suppress the oxidative burst in host plants. New Phytol 165 (2005) 559-566
16. Tellström V., Usadel B., Thimm O., Stitt M., Küster H., and Niehaus K. The Lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiol 143 (2007) 1-13
17. Gianinazzi-Pearson V., Dumas-Gaudot E., Gollotte A., Tahiri-Alaoui A., and Gianinazzi S. Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133 (1996) 45-57
18. Salzer P., Corbière H., and Boller T. Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208 (1999) 319-325
19. Harrison M.J., and Dixon R.A. Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular-arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6 (1993) 643-654
20. Liu J.Y., Maldonado-Mendoza I.E., Lopez-Meyer M., Cheung F., Town C.D., VandenBosch K.A., et al. The arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50 (2007) 529-544
21. Hagedorn D.J. Aphanomyces root rot. In: Hagedorn D.J. (Ed). Compendium of Pea Diseases (1989), American Phytopathology Society (APS) Press, St. Paul 25-28
22. Levenfors J.P., Wikström M., Persson L., and Gerhardson B. Pathogenicity of Aphanomyces spp. from different leguminous crops in Sweden. Eur J Plant Path 109 (2003) 535-543
23. Gaulin E., Jacquet C., Bottin A., and Dumas B. Root rot disease of legumes caused by Aphanomyces euteiches. Mol Plant Pathol 8 (2007) 539-548
24. Colditz F., Nyamsuren O., Niehaus K., Eubel H., Braun H.-P., and Krajinski F. Proteomic approach: identification of Medicago truncatula proteins induced in roots after infection with the pathogenic oomycete Aphanomyces euteiches. Plant Mol Biol 55 (2004) 109-120
25. Colditz F., Braun H.-P., Jacquet C., Niehaus K., and Krajinksi F. Proteomic profiling unravels insights into the molecular background underlying increased Aphanomyces euteiches-tolerance of Medicago truncatula. Plant Mol Biol 59 (2005) 387-406
26. Colditz F., Niehaus K., and Krajinski F. Silencing of PR-10-like proteins in Medicago truncatula results in an antagonistic induction of other PR proteins and in an increased tolerance upon infection with the oomycete Aphanomyces euteiches. Planta 226 (2007) 57-71
27. Trapphoff T., Beutner C., Niehaus K., and Colditz F. Induction of distinct defense-associated protein patterns in Aphanomyces euteiches (oomycota)-elicited and -inoculated Medicago truncatula cell-suspension cultures: a proteome and phosphoproteome approach. Mol Plant-Microbe Intract 4 (2009) 421-436
28. Boisson-Dernier A., Chabaud M., Rosenberg C., and Barker D. Agrobacterium rhizogenes-based transformation of Medicago truncatula. Mol Plant Microbe Interact 14 (2001) 695-700
29. Williams K.R., LoPresti M., and Stone K. Internal protein sequencing of SDS-PAGE-separated proteins: optimization of an in gel digest protocol. In: Marshak D. (Ed). Techniques in Protein Chemistry (1997), Academic Press, San Diego 97-190
30. Nyamsuren O., Colditz F., Rosendahl S., Tamasloukht M., Bekel T., Meyer F., et al. Transcriptional profiling of Medicago truncatula roots after infection with Aphanomyces euteiches (oomycota) identifies novel genes upregulated during this pathogenic interaction. Physiol Mol Plant Path 63 (2003) 17-26
31. Abad L.R., D'Urzo M.P., Liu D., Narasimhan M.L., Reuveni M., Zhu J.K., et al. Antifungal activity of tobacco osmotin has specificity and involves plasma membrane permeabilization. Plant Sci 118 (1996) 11-23
32. Hanselle T., Ichinoseb Y., and Barz W. Biochemical and molecular biological studies on infection (Ascochyta rabiei)-induced thaumatin-like proteins from chickpea plants (Cicer arietinum L.). Z Naturforsch 56 (2001) 1095-1107
33. Park C.-J., Kim K.-J., Shin R., Park J.M., Shin Y.-C., and Paek K.-H. Pathogenesis-related protein 10 from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37 (2004) 186-198
34. Van Loon L.C., Rep M., and Pieterse C.M.J. Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44 (2006) 1-28
35. Wang X., Zafian P., Choudhary M., and Lawton M. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc Natl Acad Sci USA 93 (1996) 2598-2602
36. Markovic-Housley Z., Degano M., Lamba D., von Roepenack-Lahaye E., Clemens S., Susani M., et al. Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. J Mol Biol 325 (2003) 123-133
37. Narasimhan M.L., Coca M.A., Jin J., Yamauchi T., Ito Y., Kadowaki T., et al. Osmotin is a homolog of mammalian adiponectin and controls apoptosis in yeast through a homolog of mammalian adiponectin receptor. Mol Cell 17 (2005) 171-180
38. Fernandes H., Bujacz A., Bujacz G., Jelen F., Jasinski M., Kachlicki P., et al. Cytokinin-induced structural adaptability of a Lupinus luteus PR-10 protein. FEBS J 276 (2009) 1596-1609
39. Koiwa H., Bressan R.A., and Hasegawa P.M. Regulation of protease inhibitors and plant defense. Trends Plant Sci 2 (1997) 379-385
40. Tian M., Huitema E., Da Cunha L., Torto-Alalibo T., and Kamoun S. A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J Biol Chem 279 (2004) 26370-26377
41. Tian M., Bendedetti B., and Kamoun S. A second kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 138 (2005) 1785-1793
42. Ryan C.A. Protease inhibitors: genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28 (1990) 425-449
43. Valueva T.A., Revina T.A., Kladnitskaya G.V., and Mosolov V.V. Kunitz-type proteinase inhibitors from intact and Phytophthora-infected potato tubers. FEBS Lett 426 (1998) 131-134
44. Kusumawati L., Imin N., and Djordjevic M.A. Characterization of the secretome of suspension cultures of Medicago species reveals proteins important for defense and development. J Proteom Res 7 (2008) 4508-4520
45. Nyamsuren O., Firnhaber C., Hohnjec N., Becker A., Küster H., and Krajinski F. Suppression of the pathogen-inducible Medicago truncatula putative protease-inhibitor MtTi2 does not influence root infection by Aphanomyces euteiches but results in transcriptional changes from wildtype roots. Plant Sci 173 (2007) 84-95
46. Esteban R., Dopico B., Muňoz F.J., Romo S., and Labrador E. A seedling specific vegetative lectin gene is related to development in Cicer arietinum. Physiol Plant 115 (2002) 619-626
47. Frenzel A., Tiller N., Hause B., and Krajinski F. The conserved arbuscular mycorrhiza-specific transcription of the secretory lectin MtLec 5 is mediated by a short upstream sequence containing specific protein binding sites. Planta 224 (2006) 792-800
48. Diaz C.L., Melchers L.S., Hooykaas P.J.J., Lugtenberg B.J.J., and Kijne J.W. Root lectin as a determinant of host specificity in the Rhizobium-legume symbiosis. Nature 338 (1989) 579-581
49. Higgins V.J. Role of phytoalexin medicarpin in 3 leaf spot diseases of Alfalfa. Physiol Plant Pathol 2 (1972) 289-300
50. Farag M.A., Huhman D.V., Dixon R.A., and Sumner L.W. Metabolomics reveals novel pathways and differential mechanistic and elicitor-specific responses in phenylpropanoid and isoflavonoid biosynthesis in Medicago truncatula cell cultures. Plant Physiol 146 (2008) 387-402
51. Takezawa D., Ramachandiran S., Paranjape V., and Poovaiah B.W. Dual regulation of a chimeric plant seine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem 271 (1996) 8126-8132
52. Xu L., and Massague J. Nucleocytoplasmic shuttling of signal transducers. Nat Rev Mol Cell Biol 5 (2004) 209-219
53. Lee Y., Lee H.-S., Lee J.-S., Kim S.-K., and Kim S.-H. Hormone- and light-regulated nucleocytoplasmic transport in plants: current status. J Exp Bot 59 (2008) 3229-3245
54. Penheiter A.R., Duff S.M.G., and Sarath G. Soybean root nodule acid phosphatase. Plant Physiol 114 (1997) 597-604
55. Fridborg I., Grainger J., Page A., Coleman M., Findlay K., and Angell S. TIP, a novel host factor linking callose degradation with the cell-to-cell movement of Potato virus X. Mol Plant Microbe Interact 16 (2003) 132-140
56. Böttner S., Iven T., Carsjens C.S., and Dröge-Laser W. Nuclear accumulation of the ankyrin repeat protein ANK1 enhances the auxin-mediated transcription accomplished by the bZIP transcription factors BZI-1 and BZI-2. Plant J 58 (2009) 914-926
57. Kim S.-H., Arnold D., Lloyd A., and Roux S.J. Antisense expression of an Arabidopsis Ran-binding protein renders transgenic roots hypersensitive to auxin and alters auxin-induced root growth and development by arresting mitotic progress. Plant Cell 13 (2001) 2619-2630
58. Seo M., Akaba S., Oritani T., Delarue M., Bellini C., Caboche M., et al. Higher activity of an aldehyde oxidase in the auxin-overproducing superroot1 mutant of Arabidopsis thaliana. Plant Physiol 116 (1998) 687-693
59. Hodge A., Berta G., Doussan C., Merchan F., and Crespi M. Plant root growth, architecture and function. Plant Soil 321 (2009) 153-187
60. Mathesius U., Schlamann H.R.M., Spaink H.P., Sautter C., Rolfe B.G., and Djordjevic M.A. Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides. Plant J 14 (1998) 23-34
61. van Noorden G.E., Kerim T., Goffard N., Wiblin R., Pellerone F.I., Rolfe B.G., et al. Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti. Plant Physiol 144 (2007) 1115-1131
62. Mathesius U. Comparative proteomic studies of root-microbe interactions. J Proteom 72 (2009) 353-366
63. Campanella J.J., Smith S.M., Leibu D., Wexler S., and Ludwig-Müller J. The auxin conjugate hydrolase family of Medicago truncatula and their expression during the interaction with two symbionts. J Plant Growth Regul 27 (2008) 26-38
64. Schoonheim P.J., and Veiga H. da Costa Pereira D, Friso G, van Wijk KJ, de Boer AH. A comprehensive analysis of the 14-3-3 interactome in barley leaves using a complementary proteomics and two-hybrid approach. Plant Physiol 143 (2007) 670-683
65. Bonanomi A., Wiemken A., Boller T., and Salzer P. Local induction of a mycorrhiza-specific class III chitinase gene in cortical cells of Medicago truncatula containing developing or mature arbuscules. Plant Biol 3 (2001) 194-199
66. Dudley M.E., Jacobs T.W., and Long S.R. Microscopic studies of cell divisions induced in alfalfa roots by Rhizobium meliloti. Planta 171 (1987) 289-301
67. Cook D., Dreyer D., Bonnet D., Howell M., Nony E., and VandenBosch K. Transient induction of a peroxidase gene in Medicago truncatula precedes infection by Rhizobium meliloti. Plant Cell 7 (1995) 43-55
68. Hurkman WJ, Tanaka CK. Solubilization of Plant Membrane Proteins for Analysis by Two-Dimensional Gel Electrophoresis Plant Physiol;81:802-806.