Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming

Frontiers in Plant Science

Volumn 2, Issue AUG, 2011, Pages

  Voll, Lars Matthias ^a   Horst, Robin Jonathan ^a,f,g,h   Voitsik, Anna Maria ^a   Zajic, Doreen ^a   Samans, Birgit ^b   Pons Kühnemann, Jörn ^b   Doehlemann, Gunther ^c   Münch, Steffen ^d   Wahl, Ramon ^e   Molitor, Alexandra ^b,f,g,h   Hofmann, Jörg ^a   Schmiedl, Alfred ^a   Waller, Frank ^b,f,g,h   Deising, Holger Bruno ^d   Kahmann, Regine ^c   Kämper, Jörg ^e   Kogel, Karl Heinz ^b   Sonnewald, Uwe ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^d MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^e UNIVERSITY OF KARLSRUHE   (Germany)

^f UNIVERSITY OF WASHINGTON   (United States)

^g KWS SAAT SE   (Germany)

^h UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Barley; Blumeria graminis f.sp. hordei; Colletotrichum graminicola; Compatible interaction; Maize; Metabolite analysis; Transcriptome analysis; Ustilago maydis

Indexed keywords

EID: 84879549763     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2011.00039     Document Type: Article

References (56)

1. Banuett, F. (1995). Genetics of Ustilago maydis, a fungal pathogen that induces tumors in maize. Annu. R e v. Genet. 29, 179-208.
2. Bergstrom, G. C., and Nicholson, R. L. (1999). The biology of corn anthrac-nose - knowledge for improved management. Plant Dis. 83, 596-608.
3. Biemelt, S., and Sonnewald, U. (2006). Plant-microbe interactions to probe the regulation of plant carbon metabolism. J. Plant Physiol. 163, 307-318.
4. Bino, R. J., Hall, R. D., Fiehn, O., Kopka, J., Saito, K., Draper, J., Nikolau, B. J., Mendes, P., Roessner-Tunali, U., Beale, M. H., Trethewey, R. N., Lange, B. M., Wurtele, E. S., and Sumner, L.W. (2004). Potential of metabolomics as a functional genomics tool. Trends Plant Sci. 9, 418-425.
5. Bolton, M. D. (2009). Primary metabolism and plant defense - fuel for the fire. Mol. Plant Microbe Interact. 22, 487-497.
6. Bonfg, K. B., Schreiber, U., Gabler, A., Roitsch, T., and Berger, S. (2006). Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225, 1-12.
7. Both, M., Csukai, M., Stumpf, M. P. H., and Spanu, P. D. (2005). Gene expression profiles of Blumeria graminis indicate dynamic changes to primary metabolism during development of an obligate biotrophic pathogen. Plant Cell 17, 2107-2122.
8. Chanda, B., Venugopal, S. C., Kulshrestha, S., Navarre, D. A., Downie, B., Vaillancourt, L., Kachroo, A., and Kachroo, P. (2008). Glycerol-3-phosphate levels are associates with basal resistance to the hemibiotrophic fungus Colletotrichum higginsianum in Arabidopsis. Plant Physiol. 147, 2017-2029.
9. Chaturvedi, R., Krothapalli, K., Makandar, R., Nandi, A., Sparks, A. A., Roth, M. R., Welti, R., and Shah, J. (2008). Plastid omega 3-fatty acid desaturase-dependent accumulation of a systemic acquired resistance inducing activity in petiole exudates of Arabidopsis thaliana is independent of jasmonic acid. Plant J. 54, 106-117.
10. Chen, L.-Q., Hou, B.-H., Lalonde, S., Takanaga, H., Hartung, M. L., Qu, X.-Q., Guo, W.-J., Kim, J.-G., Underwood, W., Chaudhuri, B., Chermak, D., Antony, G., White, F. F., Sommerville, S. C., Mudgett, M. B., and Frommer, W. B. (2010). Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527-532.
11. Chou, H. M., Bundock, N., Rolfe, S. A., and Scholes, J. D. (2000). Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Mol. Plant Pathol. 1, 99-113.
12. de Wit, P. J. G. M., Mehrabi, R., van den Burg, H. A., and Stergiopoulos, I. (2009). Fungal effectors proteins: past, present and future. Mol. Plant Pathol. 10, 735-747.
13. Divon, H. H., and Fluhr, R. (2007). Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol. Lett. 266, 65-74.
14. Doehlemann, G., Wahl, R., Horst, R. J., Voll, L., Usadel, B., Poree, F., Stitt, M., Pons-Kuehnemann, J., Sonnewald, U., Kahmann, R., and Kämper, J. (2008a). Reprogramming a maize plant: tran-scriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J. 56, 181-195.
15. Doehlemann, G., Wahl, R., Vranes, M., de Vries, R. P., Kämper, J., and Kahmann, R. (2008b). Establishment of compatibility in the Ustilago maydis/maize pathosystem. J. Plant Physiol. 165, 29-40.
16. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. PNAS 95, 14863-14868.
17. Essmann, J., Schmitz-Thom, I., Schon, H., Sonnewald, S., Weis, E., and Scharte, J. (2008). RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of to b a cco. Plant Physiol. 147,1288-1299.
18. Gerhardt, R., Stitt, M., and Heldt, H. W. (1987). Subcellular metabolite levels in spinach leaves: regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol. 83, 399-407.
19. Gibon, Y., Blaesing, O. E., Hannemann, J., Carillo, P., Höhne, M., Hendriks, J. H. M., Palacios, N., Cross, J., Selbig, J., and Stitt, M. (2004). A robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell 16, 3304-3325.
20. Hahn, M., Neef, U., Struck, C., Gottfert, M., and Mendgen, K. (1997). A putative amino acid transporter is specifically expressed in haustoria of the rust fungus Uromyces fabae. M o l. Plant Microbe Interact. 10, 438-445.
21. Heineke, D., Wildenberger, K., Sonnewald, U., Willmitzer, L., and Heldt, H.-W. (1994). Accumulation of hexoses in leaf vacuoles - studies with trans-genic tobacco plants expressing yeast-derived invertase in the cytosol, vacuole or appoplasm. Planta 194, 29-33.
22. Herrmann, K. M., and Weaver, L. M. (1999). The shikimate pathway. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 473-503.
23. Horst, R. J., Doehlemann, G., Wahl, R., Kahmann, R., Kämper, J., Sonnewald, U., and Voll, L. M. (2010a). Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.
24. Horst, R. J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kämper, J., and Voll, L. M. (2010b). A model of Ustilago maydis leaf tumor metabolism. Plant Signal. Behav. 5, 1446-1449.
25. Horst, R. J., Engelsdorf, T., Sonnewald, U., and Voll, L. M. (2008). Infection of maize leaves with Ustilago maydis prevents establishment of C-4 photosynthesis. J. Plant Physiol. 165, 19-28.
26. Hückelhoven, R., Fodor, J., Preis, C., and Kogel, K. H. (1999). Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with h2o2 accu -mulation but are not accompanied by enhanced concentrations of salicylic acid. Plant Physiol. 119, 1251-1260.
27. Jain, S. K., Langen, G., Hess, W., Borner, T., Huckelhoven, R., and Kogel, K.-H. (2004). The white barley mutant albos-trians shows enhanced resistance to the biotroph Blumeria graminis f. sp. hordei. Mol. Plant Microbe Interact. 17, 374-382.
28. Kachroo, A., Lapchyk, L., Fukushige, H., Hildebrand, D., Klessig, D., and Kachroo, P. (2003). Plastidial fatty acid signaling modulates salicylic acid- and jasmonic acid-mediated defense pathways in the Arabidopsis ssi2 mutant. Plant Cell 15, 2952-2965.
29. Kahmann, R., and Kämper, J. (2004). Ustilago maydis: how its biology relates to pathogenic development. New Phytol. 164, 31-42.
30. Kämper, J., Kahmann, R., Bolker, M., Ma, L.-J., Brefort, T., Saville, B. J., Banuett, F., Kronstad, J. W., Gold, S. E., Muller, O., Perlin, M. H., Wosten, H. A. B., de Vries, R., Ruiz-Herrera, J., Reynaga-Pena, C. G., Snetselaar, K., McCann, M., Perez-Martin, J., Feldbrugge, M., Basse, C. W., Steinberg, G., Ibeas, J. I., Holloman, W., Guzman, P., Farman, M., Stajich, J. E., Sentandreu, R., Gonzalez-Prieto, J. M., Kennell, J. C., Molina, L., Schirawski, J., Mendoza-Mendoza, A., Greilinger, D., Munch, K., Rossel, N., Scherer, M., Vranes, M., Ladendorf, O., Vincon, V., Fuchs, U., Sandrock, B., Meng, S., Ho, E. C. H., Cahill, M. J., Boyce, K. J., Klose, J., Klosterman, S. J., Deelstra, H. J., Ortiz-Castellanos, L., Li, W., Sanchez-Alonso, P., Schreier, P. H., Hauser-Hahn, I., Vaupel, M., Koopmann, E., Friedrich, G., Voss, H., Schluter, T., Margolis, J., Platt, D., Swimmer, C., Gnirke, A., Chen, F., Vysotskaia, V., Mannhaupt, G., Guldener, U., Munsterkotter, M., Haase, D., Oesterheld, M., Mewes, H.-W., Mauceli, E. W., DeCaprio, D., Wade, C. M., Butler, J., Young, S., Jaffe, D. B., Calvo, S., Nusbaum, C., Galagan, J., and Birren, B. W. (2006). Insights from the genome of the biotrophic fungal plant pathogen Ustilago may-dis. Nature 444, 97-101.
31. Kocal, N., Sonnewald, U., and Sonnewald, S. (2008). Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesica-toria. Plant Physiol. 148, 1523-1536.
32. Leidreiter, K., Kruse, A., Heineke, D., Robinson, D. G., and Heldt, H.-W. (1995). Subcellular volumes and metabolite concentrations in potato (Solanum tuberosum cv. Désirée) leaves. Bot. Acta 108, 439-444.
33. Mendgen, K., and Hahn, M. (2002). Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7, 352-356.
34. Molitor, A., Zajic, D., Voll, L. M., Pons-Kühnemann, J., Kogel, K. H., and Waller, F. (2011). Transcriptome and metabolite analysis of the barley-powdery mildew interaction reveals priming as a mechanism of P. indica-induced systemic resistance. Mol. Plant Microbe Interact. [Epub ahead of print].
35. Münch, S., Lingner, U., Floss, D. S., Ludwig, N., Sauer, N., and Deising, H. (2008). The hemibiotrophic lifestyle of Colletotrichum sp ecies. J. Plant Physiol. 165, 41-51.
36. Münch, S., Ludwig, N., Floß, D. S., Sugui, J. A., Koszucka, A. M., Voll, L. M., Sonnewald, U., and Deising, H. B. (2011). Identification of virulence genes in the corn pathogen Colletotrichum graminicola by Agrobacterium tumefaciens-mediated transformation. Mol. Plant Pathol. 12, 43-55.
37. Olea, F., Perez-Garcia, A., Canton, F. R., Rivera, M. E., Canas, R., Avila, C., Cazorla, F. M., Canovas, F. M., and de Vicente, A. (2004). Up-regulation and localization of asparagine synthetase in tomato leaves infected by the bacterial pathogen Pseudomonas syringae. Plant Cell Physiol. 45, 770-780.
38. Parker, D., Beckmann, M., Zubair, H., Enot, D. P., Caracuel-Rios, Z., Overy, D. P., Snowdon, S., Talbot, N. J., and Draper, J. (2009). Metabolomic analysis reveals a common pattern of metabolic re-programming during invasion of three host plant species by Magnaporthe grisea. Plant J. 59, 723-737.
39. Raffaele, S., Vailleau, F., Léger, A., Joubès, J., Miersch, O., Huard, C., Blée, E., Mongrand, S., Domergue, F., and Roby, D. (2008). A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20, 752-767.
40. Sana, T. R., Fischer, S., Wohlgemuth, G., Katrekar, A., Jung, K. H., Ronald, P. C., and Fiehn, O. (2010). Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. Metabolomics 6,451-465.
41. Scharte, J., Schön, H., Tjaden, Z., Weis, E., and von Schaewen, A. (2009). Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants. Proc. Natl. Acad. Sci. U.S.A. 106, 8061-8066.
42. Schulze-Siebert, D., Heineke, D., Scharf, H., and Schulz, G. (1984). Pyruvate-der ived amino acids in spinach chloro-plasts: synthesis and regulation during photosynthetic carbon metabolism. Plant Physiol. 76, 465-471.
43. Siemens, J., González, M. C., Wolf, S., Hofmann, C., Greiner, S., Du, Y., Rausch, T., Roitsch, T., and Ludwig-Müller, J. (2011). Extracellular invertase is involved in the r egulation of clubroot disease in Arabidopsis thaliana. Mol. Plant Pathol. 12, 247-262.
44. Struck, C., Ernst, M., and Hahn, M. (2002). Characterization of a devel-opmentally regulated amino acid transporter (AAT1p) of the rust fungus Uromyces fabae. Mol. Plant Pathol. 3, 23-30.
45. Struck, C., Mueller, E., Martin, H., and Lohaus, G. (2004). The Uromyces fab ae UfAAT3 gene encodes a general amino acid permease that prefers uptake of in planta scarce amino acids. Mol. Plant Pathol. 5, 183-189.
46. Swarbrick, P. J., Schulze-Lefert, P., and Scholes, J. D. (2006). Metabolic consequences of susceptibility and resistance (race-specifc and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ. 29, 1061-1076.
47. Tavernier, V., Cadiou, S., Pageau, K., Lauge, R., Reisdorf-Cren, M., Langin, T., and Masclaux-Daubresse, C. (2007). The plant nitrogen mobilization promoted by Colletotrichum lindemuthi-anum in Phaseolus leaves depends on fungus pathogenicity. J. Exp. Bot. 58, 3351-3360.
48. Thimm, O., Bläsing, O., Gibon, Y., Nagel, A., Meyer, S., Krüger, P., Selbig, J., Müller, L. A., Rhee, S. Y., and 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.
49. Truman, W., de Zabala, M. T., and Grant, M. (2006). Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J. 46, 14-33.
50. van Kan, J. A. L. (2006). Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11, 247-253.
51. Voegele, R. T., Struck, C., Hahn, M., and Mendgen, K. (2001). The role of haus-toria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc. Natl. Acad. Sci. U.S.A. 98, 8133-8138.
52. Voegele, R. T., Wirsel, S., Möll, U., Lechner, M., and Mendgen, K. (2006). Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol. Plant Microbe Interact. 19, 625-634.
53. Wahl, R., Wippel, K., Goos, S., and Kämper, J. (2010). Norbert Sauer a novel high-affnity sucrose transporter is required for virulence of the plant pathogen Ustilago maydis. PLoS Biol. 8, e1000303. doi: 10.1371/journal. pbio.1000303
54. Ward, J. L., Forcat, S., Beckmann, M., Bennett, M., Miller, S. J., Baker, J. M., Hawkins, N. D., Vermeer, C. P., Lu, C., Lin, W., Truman, W. M., Beale, M. H., Draper, J., Mansfield, J. W., and Grant, M (2010). The metabolic transition during disease following infection of Arabidopsis thaliana by Pseudomonas syringae pv. tomato. Plant J. 63, 443-457.
55. Wiberg, A. (1974). Genetical studies of spontaneous sources of resistance to powdery mildew in barley. Hereditas 77, 89-148.
56. Widarto, H. T., Van Der Meijden, E., Lefeber, A. W., Erkelens, C., Kim, H. K., Choi, Y. H., and Verpoorte, R. (2006). Metabolomic differentiation of Brassica rapa following herbivory by different insect instars using two-dimensional nuclear magnetic resonance spectros-copy. J. Chem. Ecol. 32, 2417-2428.s