Joint transcriptomic and metabolomic analyses reveal changes in the primary metabolism and imbalances in the subgenome orchestration in the bread wheat molecular response to Fusarium graminearum

G3: Genes, Genomes, Genetics

Volumn 5, Issue 12, 2015, Pages 2579-2592

  Nussbaumer, Thomas ^a,d   Warth, Benedikt ^b,d   Sharma, Sapna ^a   Amet, Christian ^c   Bueschl, Christoph ^b   Parich, Alexandra ^b   Pfeifer, Matthias ^a   Siegwart, Gerald ^c   Steiner, Barbara ^c   Lemmens, Marc ^c   Schuhmacher, Rainer ^b   Buerstmayr, Hermann ^c   Mayer, Klaus F X ^a   Kugler, Karl G ^a   Schweiger, Wolfgang ^c,e  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^c UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^d UNIVERSITY OF VIENNA   (Austria)

^e UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Deoxynivalenol; Fhb1; Fusarium head blight; Qfhs.ifa 5A; Resistance QTL

Indexed keywords

GLUTAMATE AMMONIA LIGASE; GLUTAMIC ACID; GLYCINE TRANSFER RNA LIGASE; PROTEIN KINASE; TRANSFER RNA; UBIQUITIN PROTEIN LIGASE E3; VOMITOXIN; RNA LIGASE; TRANSCRIPTOME; TRICHOTHECENE DERIVATIVE;

AMINO ACID METABOLISM; ARTICLE; CITRIC ACID CYCLE; CONTROLLED STUDY; FUSARIUM GRAMINEARUM; FUSARIUM HEAD BLIGHT; GENE EXPRESSION; GENE REARRANGEMENT; GLYCOLYSIS; HEXAPLOIDY; METABOLOMICS; NEAR ISOGENIC LINE; NONHUMAN; OXIDATIVE STRESS; PENTOSE PHOSPHATE CYCLE; PLANT DEFENSE; PLANT GENOME; POLYPLOIDY; QUANTITATIVE TRAIT LOCUS; TRITICUM AESTIVUM; TURNOVER TIME; UBIQUITINATION; BASAL METABOLIC RATE; BIOLOGY; DISEASE RESISTANCE; DRUG EFFECTS; FUSARIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; HOST PATHOGEN INTERACTION; METABOLISM; METABOLOME; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PROCEDURES; WHEAT;

BASAL METABOLISM; COMPUTATIONAL BIOLOGY; DISEASE RESISTANCE; FUSARIUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENOMICS; GLUTAMIC ACID; HOST-PATHOGEN INTERACTIONS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; PLANT DISEASES; QUANTITATIVE TRAIT LOCI; RNA LIGASE (ATP); TRANSCRIPTOME; TRICHOTHECENES; TRITICUM; UBIQUITINATION;

EID: 84949994386     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.021550     Document Type: Article

References (80)

1. Aharoni, A., and G. Galili, 2011 Metabolic engineering of the plant primary-secondary metabolism interface. Curr. Opin. Biotechnol. 22: 239-244.
2. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman, 1990 Basic local alignment search tool. J. Mol. Biol. 215: 403-410.
3. Anders, S., P. T. Pyl, and W. Huber, 2015 HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31: 166-169.
4. Anderson, J. A., R. Stack, S. Liu, B. Waldron, A. Fjeld et al., 2001 DNA markers for Fusarium head blight resistance QTLs in two wheat populations. Theor. Appl. Genet. 102: 1164-1168.
5. Araújo, W. L., T. Tohge, K. Ishizaki, C. J. Leaver, and A. R. Fernie, 2011 Protein degradation-an alternative respiratory substrate for stressed plants. Trends Plant Sci. 16: 489-498.
6. Audenaert, K., A. Vanheule, M. Höfte, and G. Haesaert, 2013 Deoxynivalenol: a major player in the multifaceted response of Fusarium to its environment. Toxins (Basel) 6: 1-19.
7. Bennetzen, J. L., and W. Ramakrishna, 2002 Numerous small rearrangements of gene content, order and orientation differentiate grass genomes. Plant Mol. Biol. 48: 821-827.
8. Bolton, M. D., 2009 Primary metabolism and plant defense-fuel for the fire. Mol. Plant Microbe Interact. 22: 487-497.
9. Brenchley, R., M. Spannagl, M. Pfeifer, G. L. Barker, R. D'Amore et al., 2012 Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491: 705-710.
10. Brugière, N., F. Dubois, A. M. Limami, M. Lelandais, Y. Roux et al., 1999 Glutamine synthetase in the phloem plays a major role in controlling proline production. The Plant Cell Online 11: 1995-2011.
11. Buerstmayr, H., M. Lemmens, L. Hartl, L. Doldi, B. Steiner et al., 2002 Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat. I. Resistance to fungal spread (Type II resistance). Theor. Appl. Genet. 104: 84-91.
12. Buerstmayr, H., B. Steiner, L. Hartl, M. Griesser, N. Angerer et al., 2003 Molecular mapping of QTLs for Fusarium head blight resistance in spring wheat. II. Resistance to fungal penetration and spread. Theor. Appl. Genet. 107: 503-508.
13. Buerstmayr, H., T. Ban, and J. A. Anderson, 2009 QTL mapping and marker-assisted selection for Fusarium head blight resistance in wheat: a review. Plant Breed. 128: 1-26.
14. Choulet, F., T. Wicker, C. Rustenholz, E. Paux, J. Salse et al., 2010 Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. The Plant Cell Online 22: 1686-1701.
15. Choulet, F., A. Alberti, S. Theil, N. Glover, V. Barbe et al., 2014 Structural and functional partitioning of bread wheat chromosome 3B. Science 345: 1249721.
16. Diethelm, M., M. Rhiel, C. Wagner, S. Mikolajewski, J. Groth et al., 2012 Gene expression analysis of four WIR1-like genes in floret tissues of European winter wheat after challenge with G. zeae. Euphytica 186: 103-114.
17. Fabro, G., I. Kovács, V. Pavet, L. Szabados, and M. E. Alvarez, 2004 Proline accumulation and AtP5CS2 gene activation are induced by plantpathogen incompatible interactions in Arabidopsis. Mol. Plant Microbe Interact. 17: 343-350.
18. Fahima, T., J. Cheng, J. Peng, E. Nevo, and A. Korol, 2006 Asymmetry distribution of disease resistance genes and domestication synrome QTLs in tetraploid wheat genome in 8th International Congress of Plant Molecular Biology, Adelaide, Australia, August 20-25, 2006.
19. Falcon, S., and R. Gentleman, 2007 Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258.
20. Feldman, M., and A. A. Levy, 2012 Genome evolution due to allopolyploidization in wheat. Genetics 192: 763-774.
21. Feldman, M., A. A. Levy, T. Fahima, and A. Korol, 2012 Genomic asymmetry in allopolyploid plants: wheat as a model. J. Exp. Bot. 63: 5045-5059.
22. Feuillet, C., and J. Salse, 2009 Comparative genomics in the triticae, p. 451 in Genetics and Genomics of the Triticeae, edited by Feuillet, C., and G. J. Muehlbauer. Springer Science + Business Media, New York, NY.
23. Finley, D., B. Bartel, and A. Varshavsky, 1989 The tails of ubiquitin precursors are ribosomal proteins whose fusion to ubiquitin facilitates ribosome biogenesis. Nature 338: 394-401.
24. Forde, B. G., and P. J. Lea, 2007 Glutamate in plants: metabolism, regulation, and signalling. J. Exp. Bot. 58: 2339-2358.
25. Foroud, N., T. Ouellet, A. Laroche, B. Oosterveen, M. Jordan et al., 2012 Differential transcriptome analyses of three wheat genotypes reveal different host response pathways associated with Fusarium head blight and trichothecene resistance. Plant Pathol. 61: 296-314.
26. Gunnaiah, R., A. C. Kushalappa, R. Duggavathi, S. Fox, and D. J. Somers, 2012 Integrated metabolo-proteomic approach to decipher the mechanisms by which wheat QTL (Fhb1) contributes to resistance against Fusarium graminearum. PLoS One 7: e40695.
27. Hiller, K., J. Hangebrauk, C. Jäger, J. Spura, K. Schreiber et al., 2009 MetaboliteDetector: comprehensive analysis tool for targeted and nontargeted GC/MS based metabolome analysis. Anal. Chem. 81: 3429-3439.
28. Huhn, M. R., E. M. Elias, F. Ghavami, S. F. Kianian, S. Chao et al., 2012 Tetraploid Tunisian wheat germplasm as a new source of Fusarium head blight resistance. Crop Sci. 52: 136-145.
29. Hunt, E., S. Gattolin, H. J. Newbury, J. S. Bale, H.-M. Tseng et al., 2010 A mutation in amino acid permease AAP6 reduces the amino acid content of the Arabidopsis sieve elements but leaves aphid herbivores unaffected. J. Exp. Bot. 61: 55-64.
30. Jansen, C., D. Von Wettstein, W. Schäfer, K.-H. Kogel, A. Felk et al., 2005 Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc. Natl. Acad. Sci. USA 102: 16892-16897.
31. Jia, H., S. Cho, and G. J. Muehlbauer, 2009 Transcriptome analysis of a wheat near-isogenic line pair carrying Fusarium head blight-resistant and-susceptible alleles. Mol. Plant Microbe Interact. 22: 1366-1378.
32. Jin, F., D. Zhang, W. Bockus, P. S. Baenziger, B. Carver et al., 2013 Fusarium head blight resistance in US winter wheat cultivars and elite breeding lines. Crop Sci. 53: 2006-2013.
33. Gottwald, S., B. Samans, S. Lück, and W. Friedt, 2012 Jasmonate and ethylene dependent defence gene expression and suppression of fungal virulence factors: two essential mechanisms of Fusarium head blight resistance in wheat? BMC Genomics 13: 369.
34. Kazan, K., D. M. Gardiner, and J. M. Manners, 2012 On the trail of a cereal killer: recent advances in Fusarium graminearum pathogenomics and host resistance. Mol. Plant Pathol. 13: 399-413.
35. Kim, M., J.-H. Lim, C. S. Ahn, K. Park, G. T. Kim et al., 2006 Mitochondria-associated hexokinases play a role in the control of programmed cell death in Nicotiana benthamiana. Plant Cell 18: 2341-2355.
36. Kolesnikov, N., E. Hastings, M. Keays, O. Melnichuk, Y. A. Tang et al., 2014 ArrayExpress update-simplifying data submissions. Nucleic Acids Res. 43(Database Issue): D1113-1116.
37. Kugler, K. G., G. Siegwart, T. Nussbaumer, C. Ametz, M. Spannagl et al., 2013 Quantitative trait loci-dependent analysis of a gene co-expression network associated with Fusarium head blight resistance in bread wheat (Triticum aestivum L.). BMC Genomics 14: 728.
38. Langfelder, P., and S. Horvath, 2007 Eigengene networks for studying the relationships between co-expression modules. BMC Syst. Biol. 1: 54.
39. Langfelder, P., and S. Horvath, 2008 WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9: 559.
40. Langfelder, P., B. Zhang, and S. Horvath, 2008 Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24: 719-720.
41. Langmead, B., and S. L. Salzberg, 2012 Fast gapped-read alignment with Bowtie 2. Nat. Methods 9: 357-359.
42. Lemmens, M., U. Scholz, F. Berthiller, C. Dall'Asta, A. Koutnik et al., 2005 The ability to detoxify the mycotoxin deoxynivalenol colocalizes with a major quantitative trait locus for Fusarium head blight resistance in wheat. Mol. Plant Microbe Interact. 18: 1318-1324.
43. Liu, S., X. Zhang, M. O. Pumphrey, R. W. Stack, B. S. Gill et al., 2006 Complex microcolinearity among wheat, rice, and barley revealed by fine mapping of the genomic region harboring a major QTL for resistance to Fusarium head blight in wheat. Funct. Integr. Genomics 6: 83-89.
44. Marcussen, T., S. R. Sandve, L. Heier, M. Spannagl, M. Pfeifer et al., 2014 Ancient hybridizations among the ancestral genomes of bread wheat. Science 345: 1250092.
45. Masclaux-Daubresse, C., M. Reisdorf-Cren, K. Pageau, M. Lelandais, O. Grandjean et al., 2006 Glutamine synthetase-glutamate synthase pathway and glutamate dehydrogenase play distinct roles in the sink-source nitrogen cycle in tobacco. Plant Physiol. 140: 444-456.
46. Masclaux-Daubresse, C., F. Daniel-Vedele, J. Dechorgnat, F. Chardon, L. Gaufichon et al., 2010 Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Ann. Bot. 105: 1141-1157.
47. Mayer, K. F., S. Taudien, M. Martis, H., Šimková, P. Suchánková et al., 2009 Gene content and virtual gene order of barley chromosome 1H. Plant Physiol. 151: 496-505.
48. Mayer, K. F., J. Rogers, J. Dolezel, C. Pozniak, K. Eversole et al., 2014 A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345: 1251788.
49. McMullen, M., S. Halley, B. Schatz, S. Meyer, J. Jordahl et al., 2008 Integrated strategies for Fusarium head blight management in the United States. Cereal Res. Commun. 36: 563-568.
50. Miflin, B. J., and D. Z. Habash, 2002 The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. J. Exp. Bot. 53: 979-987.
51. Mujeeb-Kazi, A., A. Gul, M. Farooq, S. Rizwan, and I. Ahmad, 2008 Rebirth of synthetic hexaploids with global implications for wheat improvement. Crop Pasture Sci. 59: 391-398.
52. Nussbaumer, T., K. G. Kugler, K. C. Bader, S. Sharma, M. Seidel et al., 2014a RNASeqExpressionBrowser-a web interface to browse and visualize high-throughput expression data. Bioinformatics 30: 2519-2520.
53. Nussbaumer, T., K. G. Kugler, W. Schweiger, K. C. Bader, H. Gundlach et al., 2014b chromoWIZ: a web tool to query and visualize chromosomeanchored genes from cereal and model genomes. BMC Plant Biol. 14: 348.
54. Peng, J., Y. Ronin, T. Fahima, M. S. Röder, Y. Li et al., 2003 Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat. Proc. Natl. Acad. Sci. USA 100: 2489-2494.
55. Pestka, J. J., 2010 Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 84: 663-679.
56. Pfeifer, M., K. G. Kugler, S. R. Sandve, B. Zhan, H. Rudi et al., 2014 Genome interplay in the grain transcriptome of hexaploid bread wheat. Science 345: 1250091.
57. Pirgozliev, S. R., S. G. Edwards, M. C. Hare, and P. Jenkinson, 2003 Strategies for the control of Fusarium head blight in cereals. Eur. J. Plant Pathol. 109: 731-742.
58. Prat, N., M. Buerstmayr, B. Steiner, O. Robert, and H. Buerstmayr, 2014 Current knowledge on resistance to Fusarium head blight in tetraploid wheat. Mol. Breed. 34: 1689-1699.
59. Pritsch, C., G. J. Muehlbauer, W. R. Bushnell, D. A. Somers, and C. P. Vance, 2000 Fungal development and induction of defense response genes during early infection of wheat spikes by Fusarium graminearum. Mol. Plant Microbe Interact. 13: 159-169.
60. Robinson, M. D., D. J. McCarthy, and G. K. Smyth, 2010 edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
61. Rojas, C. M., M. Senthil-Kumar, V. Tzin, and K. S. Mysore, 2014 Regulation of primary plant metabolism during plant-pathogen interactions and its contribution to plant defense. Front. Plant Sci. 5: 17.
62. Salek, R. M., K. Haug, P. Conesa, J. Hastings, M. Williams et al., 2013 The MetaboLights repository: curation challenges in metabolomics. Database 2013: bat029.
63. Schmidt, R., H. Stransky, and W. Koch, 2007 The amino acid permease AAP8 is important for early seed development in Arabidopsis thaliana. Planta 226: 805-813.
64. Schwachtje, J., and I. T. Baldwin, 2008 Why does herbivore attack reconfigure primary metabolism? Plant Physiol. 146: 845-851.
65. Schweiger, W., B. Steiner, C. Ametz, G. Siegwart, G. Wiesenberger et al., 2013 Transcriptomic characterization of two major Fusarium resistance quantitative trait loci (QTLs), Fhb1 and Qfhs. ifa-5A, identifies novel candidate genes. Mol. Plant Pathol. 14: 772-785.
66. Seifi, H. S., J. Van Bockhaven, G. Angenon, and M. Höfte, 2013 Glutamate metabolism in plant disease and defense: friend or foe? Mol. Plant Microbe Interact. 26: 475-485.
67. Sharma, S. S., and K.-J. Dietz, 2006 The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J. Exp. Bot. 57: 711-726.
68. Stegle, O., K. J. Denby, E. J. Cooke, D. L. Wild, Z. Ghahramani et al., 2010 A robust Bayesian two-sample test for detecting intervals of differential gene expression in microarray time series. J. Comput. Biol. 17: 355-367.
69. Steiner, B., H. Kurz, M. Lemmens, and H. Buerstmayr, 2009 Differential gene expression of related wheat lines with contrasting levels of head blight resistance after Fusarium graminearum inoculation. Theor. Appl. Genet. 118: 753-764.
70. Sumner, L. W., A. Amberg, D. Barrett, M. H. Beale, R. Beger et al., 2007 Proposed minimum reporting standards for chemical analysis Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3: 211-221.
71. Sweetlove, L. J., K. F. Beard, A. Nunes-Nesi, A. R. Fernie, and R. G. Ratcliffe, 2010 Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15: 462-470.
72. Tegeder, M., and D. Rentsch, 2010 Uptake and partitioning of amino acids and peptides. Mol. Plant 3: 997-1011.
73. Trapnell, C., A. Roberts, L. Goff, G. Pertea, D. Kim et al., 2012 Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7: 562-578.
74. Walter, S., P. Nicholson, and F. M. Doohan, 2010 Action and reaction of host and pathogen during Fusarium head blight disease. New Phytol. 185: 54-66.
75. Walter, S., J. M. Brennan, C. Arunachalam, K. I. Ansari, X. Hu et al., 2008 Components of the gene network associated with genotypedependent response of wheat to the Fusarium mycotoxin deoxynivalenol. Funct. Integr. Genomics 8: 421-427.
76. Warth, B., A. Parich, C. Bueschl, D. Schoefbeck, N. K. N. Neumann et al., 2015 GC-MS based targeted metabolic profiling identifies changes in the wheat metabolome following deoxynivalenol treatment. Metabolomics 11: 722-738.
77. Wendel, J. F., 2000 Genome evolution in polyploids, pp. 225-249 in Plant Molecular Evolution, edited by Goyle, J. J., and B. S. Gaut. Springer, The Netherlands.
78. Xiao, J., X. Jin, X. Jia, H. Wang, A. Cao et al., 2013 Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics 14: 197.
79. Xiao, W., J. Sheen, and J.-C. Jang, 2000 The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44: 451-461.
80. Zhuang, Y., A. Gala, and Y. Yen, 2013 Identification of functional genic components of major Fusarium head blight resistance quantitative trait loci in wheat cultivar Sumai 3. Mol. Plant Microbe Interact. 26: 442-450.