Identification of in planta-expressed arbuscular mycorrhizal fungal proteins upon comparison of the root proteomes of Medicago truncatula colonised with two Glomus species

Fungal Genetics and Biology

Volumn 47, Issue 7, 2010, Pages 608-618

  Recorbet, Ghislaine ^a   Valot, Benoît ^b   Robert, Franck ^a   Gianinazzi Pearson, Vivienne ^a   Dumas Gaudot, Eliane ^a  

^a UNIVERSITÉ DE BOURGOGNE   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

Arbuscular mycorrhiza; Fungal proteins; Intra radical mycelium; MS MS; Mycorrhiza related proteins; Proteomics; Symbiosis; Two dimensional electrophoresis

Indexed keywords

FUNGAL PROTEIN;

ARTICLE; BARREL MEDIC; CONTROLLED STUDY; FUNGAL COLONIZATION; GLOMUS (FUNGUS); GLOMUS INTRARADICES; GLOMUS MOSSEAE; MYCORRHIZA; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT FUNGUS INTERACTION; PLANT ROOT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS;

ARBUSCULAR; FUNGI; GLOMUS; GLOMUS INTRARADICES; GLOMUS MOSSEAE; MEDICAGO TRUNCATULA;

EID: 77953542128     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.03.003     Document Type: Article

References (65)

1. Abadjieva A., Pauwells K., Hilven P., Crabeel M. A new yeast metabolon involving at least the two first enzymes of arginine biosynthesis. J. Biol. Chem. 2001, 276:42869-42880.
2. Aloui A., Recorbet G., Golotte A., Robert F., Valot B., Gianinazzi-Pearson V., Aschi-Smiti S., Dumas-Gaudot E. On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 2009, 9:420-433.
3. Amiour N., Recorbet G., Robert F., Gianinazzi S., Dumas-Gaudot E. Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol. Plant-Microbe Interact. 2006, 9:988-997.
4. Arnér E.S., Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 2000, 267:6102-6109.
5. Avis J.M., Clarke P.R. Ran, a GTPase involved in nuclear processes: its regulators and effectors. J. Cell Sci. 1996, 109:2423-2427.
6. Bago B., Pfeffer P.E., Douds D.D., Brouillette J., Bécard G., Shachar-Hill Y. Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol. 1999, 121:263-271.
7. Bago B., Pfeffer P.E., Shachar-Hill Y. Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol. 2000, 124:948-958.
8. Bago B., Pfeffer P., Shachar-Hill Y. Could the urea cycle be translocating nitrogen in the arbuscular mycorrhizal symbiosis?. New Phytol. 2001, 149:4-8.
9. Bago B., Pfeffer P.E., Zipfel W., Lammers P., Shachar-Hill Y. Tracking metabolism and imaging transport in arbuscular mycorrhizal fungi. Plant Soil 2002, 244:189-497.
10. Balestrini R., Lanfranco L. Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 2006, 16:509-524.
11. Bestel-Corre G., Dumas-Gaudot E., Poinsot V., Dieu M., van Tuinen D., Remacle J., Gianinazzi-Pearson V., Gianinazzi S. Proteome analysis and identification of symbiosis-related proteins from Medicago truncatula Gaertn. by two-dimensional electrophoresis and mass spectrometry. Electrophoresis 2002, 23:122-137.
12. Bestel-Corre G., Gianinazzi S., Dumas-Gaudot E. Impact of sewage sludges on the symbiotic proteome of Medicago truncatula. Phytochem. 2004, 65:1651-1659.
13. Bidochka M.J., Khachatourians G.G. Identification of Beauveria bassiana extracellular protease as a virulence factor in pathogenicity toward the migratory grasshopper, Melanoplus sanguinipes. J. Invertebr. Pathol. 1990, 56:362-370.
14. Charles H., Heddi A., Guillaud J., Nardon C., Nardon P. A molecular survey of symbiotic interactions between the weevil Sitophilus oryzae and its endosymbiotic bacteria: over-expression of a chaperonin. Biochem. Biophys. Res. Comm. 1997, 239:769-774.
15. Cruz C., Egsgaard H., Trujillo C., Requena N., Martins-Loução M.A., Jakobsen I. Enzymatic evidence fot the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol. 2007, 144:782-792.
16. Deguchi Y., Banba M., Shimoda Y., Chechetka S.A., Suzuri R., Okusako Y., Ooki Y., Toyokura K., Suzuki A., Uchiumi T., Higashi S., Abe M., Kouchi H., Izui K., Hata S. Transcriptome profiling of Lotus japonicus roots during arbuscular mycorrhiza development and comparison with that of nodulation. DNA Res. 2007, 14:117-133.
17. Dickson S. The Arum-Paris continuum of mycorrhizal symbioses. New Phytol. 2004, 163:187-200.
18. Dumas-Gaudot E., Guillaume P., Tahiri-Alaoui A., Gianinazzi-Pearson V., Gianinazzi S. Changes in polypeptide patterns in tobacco roots colonized by two Glomus species. Mycorrhiza 1994, 4:215-221.
19. Dupont F. Metabolic pathways of the wheat (Triticum aestivum) endosperm amyloplast revealed by proteomics. BMC Plant Biol. 2008, 8:39-57.
20. Feddermann N., Boller T., Salzer P., Elfstrand S., Wiemken A., Elfstrand M. Medicago truncatula shows distinct patterns of mycorrhiza-related gene expression after inoculation with three different arbuscular mycorrhizal fungi. Planta 2008, 227:671-680.
21. Gomez S.K., Javot H., Deewatthanawong P., Torres-Jerez I., Tang Y., Blancaflor E.B., Udvardi M.K., Harrison M.J. Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 2009, 9:10.
22. Görg A., Postel W., Weser J., Günther S., Strahler J.R., Hanash S.M., Somerlot L. Elimination of point streaking on silver stained two-dimensional gels by addition of iodoacetamide to the equilibration buffer. Electrophoresis 1987, 8:122-124.
23. Güimil S., Chang H.S., Zhu T., Sesma A., Osbourn A., Roux C., Ioannidis V., Oakeley E.J., Docquier M., Descombes P., Briggs S.P., Paszkowski U. Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl. Acad. Sci. USA 2005, 102:8066-8070.
24. Haynes P.A., Roberts T.H. Subcellular shotgun proteomics in plants: looking beyond the usual suspects. Proteomics 2007, 7:2963-2975.
25. He W., Wang Y., Liu W., Zhou C.Z. Crystal structure of Saccharomyces cerevisiae 6-phosphogluconate dehydrogenase Gnd1. BMC Struct. Biol. 2007, 14:7-38.
26. Heupel S., Roser B., Kuhn H., Lebrun M.H., Villalba F., Requena N. Erl1, a novel Era-like GTPase from Magnaporthe oryzae, is required for full root virulence and is conserved in the mutualistic symbiont Glomus intraradices. Mol. Plant-Microbe Interact. 2009, 23:67-81.
27. Hohnjec N., Vieweg A., Puhler A., Becker A., Kuster H. 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. 2005, 137:1283-1301.
28. Jin H., Pfeffer P.E., Douds D.D., Piotrowski E., Lammers P.J., Shachar-Hill Y. The uptake, metabolism, transport and transfer of nitrogen in an arbuscular mycorrhizal symbiosis. New Phytol. 2005, 168:687-696.
29. Jun J., Abubaker J., Rehrer C., Pfeffer P.E., Shachar-Hill Y., Lammers P.J. Expression in an arbuscular mycorrhizal fungus of genes putatively involved in metabolism, transport, the cytoskeleton and the cell cycle. Plant Soil 2002, 244:141-148.
30. Lanfranco L., Novero M., Bonfante P. The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol. 2005, 137:1319-1330.
31. Liu J., Blaylock L.A., Endre G., Cho J., Town C.D., VandenBosch K.A., Harrison M.J. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 2003, 15:2106-2123.
32. Liu J., Maldonado-Mendoza I., Lopez-Meyer M., Cheung F., Town C.D., Harrison M.J. Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J. 2007, 50:529-544.
33. MacDonald R.M., Lewis M. The occurrence of some acid phosphatases and dehydrogenases in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. New Phytol. 1978, 80:135-141.
34. Maldonado-Mendoza I.E., Dewbre G.R., van Buuren M.L., Versaw W.K., Harrison M.J. Methods to estimate the proportion of plant and fungal RNA in an arbuscular mycorrhiza. Mycorrhiza 2002, 12:67-74.
35. Massoumou M., van Tuinen D., Chatagnier O., Arnould C., Brechenmacher L., Sanchez L., Selim S., Gianinazzi S., Gianinazzi-Pearson V. Medicago truncatula gene responses specific to arbuscular mycorrhiza interactions with different species and genera of Glomeromycota. Mycorrhiza 2007, 17:223-234.
36. Mathesius U. Conservation and divergence of signalling pathways between roots and soil microbes - the Rhizobium-legume symbiosis compared to the development of lateral roots. Mycorrhizal interact. nematode-induced galls Plant Soil 2003, 255:105-119.
37. Mathesius U., Keijzers G., Natera S.H., Weinmann J.J., Djordjevic M.A., Rolfe B.G. Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting. Proteomics 2001, 1:1424-1440.
38. Munkvold L., Kjøller R., Vestberg M., Rosendahl S., Jakobsen I. High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol. 2004, 164:357-364.
39. Oeljeklaus S., Meyer H.E., Warscheid B. Advancements in plant proteomics using quantitative mass spectrometry. J. Proteom. 2008, 72:545-554.
40. Parniske M. Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease?. Curr. Opin. Plant Biol. 2000, 3:320-328.
41. Pauwells K., Abadjieva A., Hilven P., Stankiewcz A., Crabeel M. The N-acetylglutamate synthase/N-acetylglutamate kinase metabolon of Saccharomyces cerevisiae allows co-ordinated feedback regulation of the first two steps in arginine biosynthesis. Eur. J. Biochem. 2003, 270:1014-1024.
42. Pazkowski U. Mutualism and parasitism: the yin and yang of plant symbioses?. Curr. Opin. Plant Biol. 2006, 9:364-370.
43. Perfect S.E., Green J.R. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol. Plant Pathol. 2001, 2:101-108.
44. Phillips J.M., Hayman D.S. Improved procedures for clearing and staining parasite and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Brit. Mycol. Soc. 1970, 55:158-161.
45. Ramagli L.S., Rodriguez L.W. Quantification of microgram amounts of protein in two-dimensional polyacrylamide gel electrophoresis sample buffer. Electrophoresis 1985, 6:559-563.
46. Recorbet G., Rogniaux H., Gianinazzi-Pearson V., Dumas-Gaudot E. Fungal proteins in the extra-radical phase of mycorrhiza: a shotgun proteomic picture. New Phytol. 2009, 181:248-260.
47. Reddy P.V., Lam C.K., Belanger F.C. Mutualistic fungal endophytes express a proteinase that is homologous to proteases suspected to be important in fungal pathogenicity. Plant Physiol. 1996, 111:1209-1218.
48. Remy W., Taylor T.N., Hass H., Kerp H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl. Acad. Sci. USA 1994, 91:11841-11843.
49. Rohrbough J.G., Galgiani J.N., Wysocki V.H. The application of proteomic techniques to fungal protein identification and quantification. Ann. NY Acad. Sci. 2007, 1111:133-146.
50. Rospert S., Junne T., Glick B.S., Schatz G. Cloning and disruption of the gene encoding yeast mitochondrial chaperonin 10, the homolog of E. coli groES. FEBS Lett. 1993, 335:358-360.
51. Ruepp A., Zollner A., Maier D., Albermann K., Hani J., Mokrejs M., Tetko I., Güldener U., Mannhaupt G., Münsterkötter M., Mewes H.W. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Res. 2004, 14:5539-5545.
52. Saito M. Enzyme activities of the internal hyphae and germinated spores of an arbuscular mycorrhizal fungus, Gigaspora margarita Becker § Hall. New Phytol. 1995, 129:425-431.
53. Sanchez L., Weidmann S., Arnould C., Bernard A.R., Gianinazzi S., Gianinazzi-Pearson V. Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol. 2005, 139:1065-1077.
54. Schüssler A., Schwarzott D., Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 2001, 105:1413-1421.
55. Seddas P., Arnould C., Tollot M., Arias C., Gianinazzi-Pearson V. Spatial monitoring of gene activity in extraradical and intraradical developmental stages of arbuscular mycorrhizal fungi by direct fluorescent in situ RT-PCR. Fungal Genet. Biol. 2008, 45:1155-1165.
56. Seddas P., Arias C., Arnould C., van Tuinen D., Godfroy O., Ait Ben Hassou H., Gouzy J., Morandi D., Dessaint F., Gianinazzi-Pearson V. Symbiosis-related plant genes modulate molecular responses in an arbuscular mycorrhizal fungus during early root interactions. Mol. Plant-Microbe Interact. 2009, 22:341-351.
57. Smith S.E., Smith F.A., Jakobsen I. Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol. 2004, 162:511-524.
58. Sreedhar L., Kobayashi D.Y., Bunting T.E., Hillman B.I., Belanger F.C. Fungal proteinase expression in the interaction of the plant pathogen Magnaporthe poae with its host. Gene 1999, 235:121-129.
59. St-Arnaud M., Hamel C., Vimard B., Caron M., Fortin J.A. Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol. Res. 1996, 100:328-332.
60. Sturn A., Quackenbush J., Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics 2002, 18:207-208.
61. Tollot M., Wong Sak Hoi J., van Tuinen D., Arnould C., Chatagnier O., Dumas B., Gianinazzi-Pearson V., Seddas P.M. An STE12 gene identified in the mycorrhizal fungus Glomus intraradices restores infectivity of a hemibiotrophic plant pathogen. New Phytol. 2009, 181:693-707.
62. Trouvelot A., Kough J.L., Gianinazzi-Pearson V. Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. Physiol. Genet. Aspects Mycorrhizae 1986, 217-221. INRA, Paris. V. Gianinazzi-Pearson, S. Gianinazzi (Eds.).
63. Tunlid A., Rosen S.E., Rask L. Purification and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys oligospora. Microbiol. 1994, 140:1687-1695.
64. Valot B., Dieu M., Recorbet G., Raes M., Gianinazzi S., Dumas-Gaudot E. Identification of membrane-associated proteins regulated by the arbuscular mycorrhizal symbiosis. Plant Mol. Biol. 2005, 59:565-580.
65. Vieweg M.F., Hohnjec N., Küster H. Two genes encoding different truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatula. Planta 2005, 220:757-766.