, Volume 147, Issue 1–2, pp 25–36 | Cite as

Transcriptomic approaches to unravel plant–pathogen interactions in legumes

  • Carine Ameline-Torregrosa
  • Bernard Dumas
  • Franziska Krajinski
  • Marie-Thérèse Esquerre-Tugaye
  • Christophe Jacquet


The use of in silico and in vivo transcriptomic tools have revolutionized the way biological processes are studied. These technologies provide a global approach that is well suited for the analysis of plant–pathogen interactions, in which complex gene networks are regulated. Most of the available studies involving gene arrays were reported in Arabidopsis thaliana, but recent evidence showed that the information gained on this model plant may not always be extrapolated to legumes. Transcriptomic data generated specifically from legume–pathogen pathosystems are therefore needed to improve our understanding of the mechanisms underlying resistance of host plants and pathogenicity of their invaders. This review focuses on the few available studies that describe the characterisation of compatible or incompatible interactions between legumes and parasites through transcriptomic approaches, and summarizes various strategies that can increase our knowledge in this domain.

Key Words

disease EST gene arrays M. truncatula soybean resistance 



day post inoculation


differential gene expression




expressed sequence tag


hour post inoculation


jasmonic acid




salicylic acid


systemic acquired resistance


sudden death symptom


suppression subtractive hybridization


tentative consensus sequence


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  1. Asamizu, E., Y. Nakamura, S. Sato & S. Tabata, 2004. Characteristics of the Lotus Japonicus gene repertoire deduced from large-scale expressed sequence tag (EST) analysis. Plant Mol Biol 54: 405–414.PubMedCrossRefGoogle Scholar
  2. Birch, P.R.J. & S. Kamoun, 2000. Studying interaction transcriptomes: coordinated analyses of gene expression during plant–microorganism interactions. In: E.S.R. Wood (Ed.), New Technologies for Life Sciences: A Trends Guide, pp. 77–82. Elsevier Science, London.Google Scholar
  3. Borevitz, J.O., D. Liang, D. Plouffe, H.S. Chang, T. Zhu, D. Weigel, C.C. Berry, E. Winzeler & J. Chory, 2003. Large-scale identification of single-feature polymorphisms in complex genomes. Genome Res 13: 513–523.PubMedCrossRefGoogle Scholar
  4. Brazma, A., P. Hingamp, J. Quackenbush, G. Sherlock, P. Spellman, C. Stoeckert, J. Aach, W. Ansorge, C.A. Ball, H.C. Causton, T. Gaasterland, P. Glenisson, F.C. Holstege, I.F. Kim, V. Markowitz, J.C. Matese, H. Parkinson, A. Robinson, U. Sarkans, S. Schulze-Kremer, J. Stewart, R. Taylor, J. Vilo & M. Vingron, 2001. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29: 365–371.PubMedCrossRefGoogle Scholar
  5. Broughton, W.J., G. Hernandez, M. Blair, S. Beebe, P. Gepts & J. Vanderleyden, 2003. Beans (Phaseolus spp.); model food legumes. Plant Soil 252: 55–128.CrossRefGoogle Scholar
  6. Buckhout, T.J. & O. Thimm, 2003. Insights into metabolism obtained from microarray analysis. Curr Opin Plant Biol 6: 288–296.PubMedCrossRefGoogle Scholar
  7. Cheong, Y.H., H.S. Chang, R. Gupta, X. Wang, T. Zhu & S. Luan, 2002. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661–677.PubMedCrossRefGoogle Scholar
  8. Cho, S. & F.J. Muehlbauer, 2004. Genetic effect of differentially regulated fungal response genes on resistance to necrotrophic fungal pathogens in chickpea (Cicer arietinum L.). Physiol Mol Plant Pathol 64: 57–66.CrossRefGoogle Scholar
  9. Cluzet, S., C. Torregrosa, C. Jacquet, C. Lafitte, J. Fournier, L. Mercier, S. Salamagne, X. Briand, M.T. Esquerre-Tugaye & B. Dumas, 2004. Gene expression profiling and protection of Medicago truncatula against a fungal infection in response to an elicitor from green algae Ulva spp. Plant Cell Environ 27: 917–928.CrossRefGoogle Scholar
  10. Colebatch, G., S. Kloska, B. Trevaskis, S. Freund, T. Altmann & M.K. Udvardi, 2002. Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant Microbe Interact 15: 411–420.PubMedGoogle Scholar
  11. Constantin, G.D., B.N. Krath, S.A. MacFarlane, M. Nicolaisen, I. Elisabeth Johansen & O.S. Lund, 2004. Virus-induced gene silencing as a tool for functional genomics in a legume species. Plant J 40: 622–631.PubMedCrossRefGoogle Scholar
  12. Cook, D.R., 1999. Medicago truncatula, a model in the making! Curr Opin Plant Biol 2: 301–304.Google Scholar
  13. d’Erfurth, I., V. Cosson, A. Eschstruth, H. Lucas, A. Kondorosi & P. Ratet, 2003. Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant J 34: 95–106.PubMedCrossRefGoogle Scholar
  14. Diatchenko, L., Y.F. Lau, A.P. Campbell, A. Chenchik, F. Moqadam, B. Huang, S. Lukyanov, K. Lukyanov, N. Gurskaya, E.D. Sverdlov & P.D. Siebert, 1996. Suppression subtractive hybridization: A method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93: 6025–6030.PubMedCrossRefGoogle Scholar
  15. Dixon, R.A., L. Achnine, P. Kota, C.-J. Liu, M.S.S. Reddy & L. Wang, 2002. The phenylpropanoid pathway and plant defence – a genomic perspective. Mol Plant Pathol 3: 371–390.CrossRefGoogle Scholar
  16. Donson, J., Y. Fang, G. Espiritu-Santo, W. Xing, A. Salazar, S. Miyamoto, V. Armendarez & W. Volkmuth, 2002. Comprehensive gene expression analysis by transcript profiling. Plant Mol Biol 48: 75–97.PubMedCrossRefGoogle Scholar
  17. El Yahyaoui, F., H. Kuster, B. Ben Amor, N. Hohnjec, A. Puhler, A. Becker, J. Gouzy, T. Vernie, C. Gough, A. Niebel, L. Godiard & P. Gamas, 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.PubMedCrossRefGoogle Scholar
  18. Eulgem, T., V.J. Weigman, H.-S. Chang, J.M. McDowell, E.B. Holub, J. Glazebrook, T. Zhu & J.L. Dangl, 2004. Gene expression signatures from three genetically separable resistance gene signaling pathways for downy mildew resistance. Plant Physiol 135: 1129–1144.PubMedCrossRefGoogle Scholar
  19. Fedorova, M., J. van de Mortel, P.A. Matsumoto, J. Cho, C.D. Town, K.A. VandenBosch, J.S. Gantt & C.P. Vance, 2002. Genome-wide identification of nodule-specific transcripts in the model legume Medicago truncatula. Plant Physiol 130: 519–537.PubMedCrossRefGoogle Scholar
  20. Foster-Hartnett, D., S. Penuela, D. Danesh, K.A. Sharapova, K.A. VandenBosch, N.D. Young & D.A. Samac, 2004. Histochemical and transcriptome analysis of the interactions between Medicago truncatula and the pathogens Colletotrichum trifolii and Erisyphe pisi. Legumes for the benefit of agriculture, nutrition and the environment. In: Proceedings of Second International Conference on Legume Genomics and Genetics, 7–11 June 2004, Dijon, p. 239.Google Scholar
  21. Gamas, P., F. de Billy & G. Truchet, 1998. Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. Mol Plant Microbe Interact 11: 393–403.PubMedGoogle Scholar
  22. Graham, M.A., K.A.T. Silverstein, S.B. Cannon & K.A. VandenBosch, 2004. Computational identification and characterization of novel genes from legumes. Plant Physiol 135: 1179–1197.PubMedCrossRefGoogle Scholar
  23. Green, C.D., J.F. Simons, B.E. Taillon & D.A. Lewin, 2001. Open systems: Panoramic views of gene expression. J Immunol Methods 250: 67–79.PubMedCrossRefGoogle Scholar
  24. Hammond-Kosack, K.E. & J.E. Parker, 2003. Deciphering plant–pathogen communication: Fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14: 177–193.PubMedCrossRefGoogle Scholar
  25. Handberg, K. & J. Stougaard, 1992. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant J 2: 487–492.CrossRefGoogle Scholar
  26. Harmer, S.L. & S.A. Kay, 2000. Microarrays: Determining the balance of cellular transcription. Plant Cell 12: 613–616.PubMedCrossRefGoogle Scholar
  27. Hays, D.B. & D.Z. Skinner, 2001. Development of an expressed sequence tag (EST) library for Medicago sativa. Plant Sci 161: 517–526.CrossRefGoogle Scholar
  28. Hazen, S.P. & S.A. Kay, 2003. Gene arrays are not just for measuring gene expression. Trends Plant Sci 8: 413–416.PubMedCrossRefGoogle Scholar
  29. Hofte, H., T. Desprez, J. Amselem, H. Chiapello, P. Rouze, M. Caboche, A. Moisan, M.F. Jourjon, J.L. Charpenteau, P. Berthomieu, et al., 1993. An inventory of 1152 expressed sequence tags obtained by partial sequencing of cDNAs from Arabidopsis thaliana. Plant J 4: 1051–1061.PubMedCrossRefGoogle Scholar
  30. Huitema, E., V.G.A.A. Vleeshouwers, D.M. Francis & S. Kamoun, 2003. Active defence responses associated with non-host resistance of Arabidopsis thaliana to the oomycete pathogen Phytophthora infestans. Mol Plant Pathol 4: 487–500.CrossRefGoogle Scholar
  31. Iqbal, M., S. Yaegashi, V. Njiti, R. Ahsan, K. Cryder & D. Lightfoot, 2002. Resistance locus pyramids alter transcript abundance in soybean roots inoculated with Fusarium solani f.sp. glycines. Mol Genet Genomics 268: 407–417.PubMedCrossRefGoogle Scholar
  32. Iqbal, M., S. Yaegashi, R. Ahsan, K.L. Shopinski, T.M. Nair & D. Lightfoot, 2004. Root response to Fusarium solani f. sp. glycines: Temporal accumulation of transcripts in partially resistant and susceptible soybean. Legumes for the benefit of agriculture, nutrition and the environment. In: Proceedings of Second International Conference on Legume Genomics and Genetics, 7–11 June 2004, Dijon, p. 234.Google Scholar
  33. Journet, E.-P., D. van Tuinen, J. Gouzy, H. Crespeau, V. Carreau, M.-J. Farmer, A. Niebel, T. Schiex, O. Jaillon, O. Chatagnier, L. Godiard, F. Micheli, D. Kahn, V. Gianinazzi-Pearson & P. Gamas, 2002. Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30: 5579–5592.PubMedCrossRefGoogle Scholar
  34. Kazan, K., P.M. Schenk, I. Wilson & J.M. Manners, 2001. DNA microarrays: New tools in the analysis of plant defence responses. Mol Plant Pathol 2: 177–185.CrossRefGoogle Scholar
  35. Kuester, H., N. Hohnjec, F. Krajinski, Y.F. El, K. Manthey, J. Gouzy, M. Dondrup, F. Meyer, J. Kalinowski, L. Brechenmacher, D. van Tuinen, V. Gianinazzi-Pearson, A. Puhler, P. Gamas & A. Becker, 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.CrossRefGoogle Scholar
  36. Kuester, H. & A. Bendahmane, 2004. New genomics tools and resources. Grain Legumes 40: 15.Google Scholar
  37. Lee, S., S.Y. Kim, E. Chung, Y.H. Joung, H.S. Pai, C.G. Hur & D. Choi, 2004. EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines). Funct Integr Genomics 4: 196–205.PubMedCrossRefGoogle Scholar
  38. Liu, C.J., D. Huhman, L.W. Sumner & R.A. Dixon, 2003. Regiospecific hydroxylation of isoflavones by cytochrome p450 81E enzymes from Medicago truncatula. Plant J 36: 471–484.PubMedCrossRefGoogle Scholar
  39. Maleck, K., A. Levine, T. Eulgem, A. Morgan, J. Schmid, K.A. Lawton, J.L. Dangl & R.A. Dietrich, 2000. The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403–410.PubMedCrossRefGoogle Scholar
  40. Marshall, E., 2004. Getting the noise out of gene arrays. Science 306: 630–631.PubMedCrossRefGoogle Scholar
  41. Moy, P., D. Qutob, B.P. Chapman, I. Atkinson & M. Gijzen, 2004. Patterns of gene expression upon infection of soybean plants by Phytophthora sojae. Mol Plant Microbe Interact 17: 1051–1062.PubMedGoogle Scholar
  42. Narusaka, Y., M. Narusaka, M. Seki, J. Ishida, M. Nakashima, A. Kamiya, A. Enju, T. Sakurai, M. Satoh, M. Kobayashi, Y. Tosa, P. Park & K. Shinozaki, 2003. The cDNA microarray analysis using an Arabidopsis pad3 mutant reveals the expression profiles and classification of genes induced by Alternaria brassicicola attack. Plant Cell Physiol 44: 377–387.PubMedCrossRefGoogle Scholar
  43. Narusaka, Y., M. Narusaka, P. Park, Y. Kubo, T. Hirayama, M. Seki, T. Shiraishi, J. Ishida, M. Nakashima, A. Enju, T. Sakurai, M. Satou, M. Kobayashi & K. Shinozaki, 2004. RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol Plant Microbe Interact 17: 749–762.PubMedGoogle Scholar
  44. Nyamsuren, O., F. Colditz, S. Rosendahl, M. Tamasloukht, T. Bekel, F. Meyer, H. Kuester, P. Franken & F. Krajinski, 2003. Transcriptional profiling of Medicago truncatula roots after infection with Aphanomyces euteiches (oomycota) identifies novel genes upregulated during this pathogenic interaction. Physiol Mol Plant Pathol 63: 17–26.CrossRefGoogle Scholar
  45. Perry, J.A., T.L. Wang, T.J. Welham, S. Gardner, J.M. Pike, S. Yoshida & M. Parniske, 2003. A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol 131: 866–871.PubMedCrossRefGoogle Scholar
  46. Qutob, D., P.T. Hraber, B.W. Sobral & M. Gijzen, 2000. Comparative analysis of expressed sequences in Phytophthora sojae. Plant Physiol 123: 243–254.PubMedCrossRefGoogle Scholar
  47. Sawbridge, T., E.-K. Ong, C. Binnion, M. Emmerling, K. Meath, K. Nunan, M. O’Neill, F. O’Toole, J. Simmonds & K. Wearne, 2003. Generation and analysis of expressed sequence tags in white clover (Trifolium repens L.). Plant Sci 165: 1077–1087.CrossRefGoogle Scholar
  48. Scheideler, M., N.L. Schlaich, K. Fellenberg, T. Beissbarth, N.C. Hauser, M. Vingron, A.J. Slusarenko & J.D. Hoheisel, 2002. Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277: 10555–10561.PubMedCrossRefGoogle Scholar
  49. Schenk, P.M., K. Kazan, I. Wilson, J.P. Anderson, T. Richmond, S.C. Somerville & J.M. Manners, 2000. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97: 11655–11660.PubMedCrossRefGoogle Scholar
  50. Schenk, P.M., K. Kazan, J.M. Manners, J.P. Anderson, R.S. Simpson, I.W. Wilson, S.C. Somerville & D.J. Maclean, 2003. Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiol 132: 999–1010.PubMedCrossRefGoogle Scholar
  51. Schoor, S. & B.A. Moffatt, 2004. Applying high throughput techniques in the study of adenosine kinase in plant metabolism and development. Front Biosci 9: 1771–1781.PubMedGoogle Scholar
  52. Shoemaker, R., P. Keim, L. Vodkin, E. Retzel, S.W. Clifton, R. Waterston, D. Smoller, V. Coryell, A. Khanna, J. Erpelding, X. Gai, V. Brendel, C. Raph-Schmidt, E.G. Shoop, C.J. Vielweber, M. Schmatz, D. Pape, Y. Bowers, B. Theising, J. Martin, M. Dante, T. Wylie & C. Granger, 2002. A compilation of soybean ESTs: generation and analysis. Genome 45: 329–338.PubMedCrossRefGoogle Scholar
  53. Suzuki, H., L. Achnine, R. Xu, S.P. Matsuda & R.A. Dixon, 2002. A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula. Plant J 32: 1033–1048.PubMedCrossRefGoogle Scholar
  54. Tao, Y., Z. Xie, W. Chen, J. Glazebrook, H.S. Chang, B. Han, T. Zhu, G. Zou & F. Katagiri, 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317–330.PubMedCrossRefGoogle Scholar
  55. Thomma, B., K. Eggermont, I. Penninckx, B. Mauch-Mani, R. Vogelsang, B.P.A. Cammue & W.F. Broekaert, 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95: 15107–15111.CrossRefGoogle Scholar
  56. Tian, A.-G., J. Wang, P. Cui, Y.-J. Han, H. Xu, L.-J. Cong, X.-G. Huang, X.-L. Wang, Y.-Z. Jiao, B.-J. Wang, Y.-J. Wang, J.-S. Zhang & S.-Y. Chen, 2004. Characterization of soybean genomic features by analysis of its expressed sequence tags. Theor Appl Genet 108: 903–913.PubMedCrossRefGoogle Scholar
  57. Torregrosa, C., S. Cluzet, J. Fournier, T. Huguet, P. Gamas, J.M. Prosperi, M.T. Esquerre-Tugaye, B. Dumas & C. Jacquet, 2004. Cytological, genetic, and molecular analysis to characterize compatible and incompatible interactions between Medicago truncatula and Colletotrichum trifolii. Mol Plant Microbe Interact 17: 909–920.PubMedGoogle Scholar
  58. Tuteja, J.H., S.J. Clough, W.C. Chan & L.O. Vodkin, 2004. Tissue-specific gene silencing mediated by a naturally occurring chalcone synthase gene cluster in Glycine max. Plant Cell 16: 819–835.PubMedCrossRefGoogle Scholar
  59. van Wees, S.C., H.S. Chang, T. Zhu & J. Glazebrook, 2003. Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132: 606–617.PubMedCrossRefGoogle Scholar
  60. VandenBosch, K.A. & G. Stacey, 2003. Summaries of legume genomics projects from around the globe. Community resources for crops and models. Plant Physiol 131: 840–865.CrossRefGoogle Scholar
  61. Vodkin, L.O., A. Khanna, R. Shealy, S.J. Clough, D.O. Gonzalez, R. Philip, G. Zabala, F. Thibaud-Nissen, M. Sidarous, M.V. Stromvik, E. Shoop, C. Schmidt, E. Retzel, J. Erpelding, R.C. Shoemaker, A.M. Rodriguez-Huete, J.C. Polacco, V. Coryell, P. Keim, G. Gong, L. Liu, J. Pardinas & P. Schweitzer, 2004. Microarrays for global expression constructed with a low redundancy set of 27,500 sequenced cDNAs representing an array of developmental stages and physiological conditions of the soybean plant. BMC Genomics 5: 73.PubMedCrossRefGoogle Scholar
  62. Wan, J., F.M. Dunning & A.F. Bent, 2002. Probing plant–pathogen interactions and downstream defense signaling using DNA microarrays. Funct Integr Genomics 2: 259–273.PubMedCrossRefGoogle Scholar
  63. Zhu, H., D.J. Kim, J.M. Baek, H.K. Choi, L.C. Ellis, H. Kuester, W.R. McCombie, H.M. Peng & D.R. Cook, 2003. Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organization. Plant Physiol 131: 1018–1026.PubMedCrossRefGoogle Scholar
  64. Zou, J., S. Rodriguez-Zas, D.O. Gonzales, L. Vodkin & S.J. Clough, 2004. Gene expression profiling of soybean response during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Legumes for the benefit of agriculture, nutrition and the environment In: Proceedings of Second International Conference on Legume Genomics and Genetics, 7–11 June 2004, Dijon, p. 245.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Carine Ameline-Torregrosa
    • 1
    • 3
  • Bernard Dumas
    • 1
  • Franziska Krajinski
    • 2
  • Marie-Thérèse Esquerre-Tugaye
    • 1
  • Christophe Jacquet
    • 1
  1. 1.Pôle de Biotechnologie VégétaleUMR 5546 CNRS – Université Paul SabatierCastanet-Tolosan CedexFrance
  2. 2.Lehrgebiet MolekulargenetikUniversität HannoverHannoverGermany
  3. 3.Department of Plant PathologyUniversity of MinnesotaSaint PaulU.S.A.

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