1932

Abstract

Deciphering the networks that underpin complex biological processes using experimental data remains a significant, but promising, challenge, a task made all the harder by the added complexity of host-pathogen interactions. The aim of this article is to review the progress in understanding plant immunity made so far by applying network modeling algorithms and to show how this computational/mathematical strategy is facilitating a systems view of plant defense. We review the different types of network modeling that have been used, the data required, and the type of insight that such modeling can provide. We discuss the current challenges in modeling the regulatory networks that underlie plant defense and the future developments that may help address these challenges.

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2014-08-04
2024-04-19
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Literature Cited

  1. Albert R, Jeong H, Barabasi A. 1.  2000. Error and attack tolerance of complex networks. Nature 406:6794378–82 [Google Scholar]
  2. 2. Arabidopsis Interactome Mapping Consortium 2011. Evidence for network evolution in an Arabidopsis interactome map. Science 333:6042601–7 [Google Scholar]
  3. Argueso CT, Ferreira FJ, Epple P, To JPC, Hutchison CE. 3.  et al. 2012. Two-component elements mediate interactions between cytokinin and salicylic acid in plant immunity. PLoS Genet. 8:1e1002448 [Google Scholar]
  4. Barabási A-L, Oltvai ZN. 4.  2004. Network biology: understanding the cell's functional organization. Nat. Rev. Genet. 5:2101–13 [Google Scholar]
  5. Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T. 5.  et al. 2011. Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl. Acad. Sci. USA 108:239709–14 [Google Scholar]
  6. Baxter L, Jironkin A, Hickman R, Moore J, Barrington C. 6.  et al. 2012. Conserved noncoding sequences highlight shared components of regulatory networks in dicotyledonous plants. Plant Cell 24:103949–65 [Google Scholar]
  7. Beal MJ, Falciani F, Ghahramani Z, Rangel C, Wild DL. 7.  2005. A Bayesian approach to reconstructing genetic regulatory networks with hidden factors. Bioinformatics 21:3349–56 [Google Scholar]
  8. Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC. 8.  2012. Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol. 196:2596–605 [Google Scholar]
  9. Bhosale R, Jewell JB, Hollunder J, Koo AJK, Vuylsteke M. 9.  et al. 2013. Predicting gene function from uncontrolled expression variation among individual wild-type Arabidopsis plants. Plant Cell 25:2865–77 [Google Scholar]
  10. Carrera J, Rodrigo G, Jaramillo A, Elena SF. 10.  2009. Reverse-engineering the Arabidopsis thaliana transcriptional network under changing environmental conditions. Genome Biol. 10:9R96 [Google Scholar]
  11. Cheng YT, Li X. 11.  2012. Ubiquitination in NB-LRR-mediated immunity. Curr. Opin. Plant Biol. 15:4392–99 [Google Scholar]
  12. Cheval C, Aldon D, Galaud J-P, Ranty B. 12.  2013. Calcium/calmodulin-mediated regulation of plant immunity. Biochim. Biophys. Acta 1833:71766–71 [Google Scholar]
  13. de Oliveira Dal'Molin CG, Quek L-E, Palfreyman RW, Brumbley SM, Nielsen LK. 13.  2010. AraGEM, a genome-scale reconstruction of the primary metabolic network in Arabidopsis. Plant Physiol. 152:2579–89 [Google Scholar]
  14. De Smet R, Marchal K. 14.  2010. Advantages and limitations of current network inference methods. Nat. Rev. Microbiol. 8:10717–29 [Google Scholar]
  15. Dixon RA. 15.  2001. Natural products and plant disease resistance. Nature 411:6839843–47 [Google Scholar]
  16. Elmore JM, Liu J, Smith B, Phinney B, Coaker G. 16.  2012. Quantitative proteomics reveals dynamic changes in the plasma membrane during Arabidopsis immune signaling. Mol. Cell Proteomics 11:4M111.014555 [Google Scholar]
  17. Galagan JE, Minch K, Peterson M, Lyubetskaya A, Azizi E. 17.  et al. 2013. The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 499:7457178–83 [Google Scholar]
  18. Geisler-Lee J, O'Toole N, Ammar R, Provart NJ, Millar AH, Geisler M. 18.  2007. A predicted interactome for Arabidopsis. Plant Physiol. 145:2317–29 [Google Scholar]
  19. 19. Gene Ontology Consortium 2000. Gene ontology: tool for the unification of biology. Nat. Genet 25:125–29 [Google Scholar]
  20. Hickman R, Hill C, Penfold CA, Breeze E, Bowden L. 20.  et al. 2013. A local regulatory network around three NAC transcription factors in stress responses and senescence in Arabidopsis leaves. Plant J. 75:126–39 [Google Scholar]
  21. Higo K, Ugawa Y, Iwamoto M, Korenaga T. 21.  1999. Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res. 27:1297–300 [Google Scholar]
  22. Jones JDG, Dangl JL. 22.  2006. The plant immune system. Nature 444:7117323–29 [Google Scholar]
  23. Kesarwani M, Yoo J, Dong X. 23.  2007. Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol. 144:1336–46 [Google Scholar]
  24. Kim Y, Han S, Choi S, Hwang D. 24.  2013. Inference of dynamic networks using time-course data. Brief. Bioinforma doi:10.1093-bib-bbt028
  25. Kliebenstein DJ, Rowe HC, Denby KJ. 25.  2005. Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J. 44:125–36 [Google Scholar]
  26. Krouk G, Lingeman J, Colon AM, Coruzzi G, Shasha D. 26.  2013. Gene regulatory networks in plants: learning causality from time and perturbation. Genome Biol. 14:6123 [Google Scholar]
  27. Lalonde S, Sero A, Pratelli R, Pilot G, Chen J. 27.  et al. 2010. A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2. Front. Physiol. 1:24 [Google Scholar]
  28. Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C. 28.  et al. 2012. The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40:D1202–10 [Google Scholar]
  29. Le D-H, Kwon Y-K. 29.  2013. A coherent feedforward loop design principle to sustain robustness of biological networks. Bioinformatics 29:5630–37 [Google Scholar]
  30. Lee I, Ambaru B, Thakkar P, Marcotte EM, Rhee SY. 30.  2010. Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat. Biotechnol. 28:2149–56 [Google Scholar]
  31. Lee I, Lehner B, Crombie C, Wong W, Fraser AG, Marcotte EM. 31.  2008. A single gene network accurately predicts phenotypic effects of gene perturbation in Caenorhabditis elegans. Nat. Genet. 40:2181–88 [Google Scholar]
  32. Lee I, Li Z, Marcotte EM. 32.  2007. An improved, bias-reduced probabilistic functional gene network of baker's yeast, Saccharomyces cerevisiae. PLoS ONE 2:10e988 [Google Scholar]
  33. Lee I, Seo Y-S, Coltrane D, Hwang S, Oh T. 33.  et al. 2011. Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc. Natl. Acad. Sci. USA 108:4518548–53 [Google Scholar]
  34. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y. 34.  et al. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30:1325–27 [Google Scholar]
  35. Li Z-G, He F, Zhang Z, Peng Y-L. 35.  2011. Prediction of protein-protein interactions between Ralstonia solanacearum and Arabidopsis thaliana. Amino Acids 42:62363–71 [Google Scholar]
  36. Locke JCW, Southern MM, Kozma-Bognár L, Hibberd V, Brown PE. 36.  et al. 2005. Extension of a genetic network model by iterative experimentation and mathematical analysis. Mol. Syst. Biol. 1:2005.0013 [Google Scholar]
  37. Ma S, Gong Q, Bohnert HJ. 37.  2007. An Arabidopsis gene network based on the graphical Gaussian model. Genome Res. 17:111614–25 [Google Scholar]
  38. Ma S, Shah S, Bohnert HJ, Snyder M, Dinesh-Kumar SP. 38.  2013. Incorporating motif analysis into gene co-expression networks reveals novel modular expression pattern and new signaling pathways. PLoS Genet. 9:10e1003840 [Google Scholar]
  39. Maere S, Van Dijck P, Kuiper M. 39.  2008. Extracting expression modules from perturbational gene expression compendia. BMC Syst. Biol. 2:33 [Google Scholar]
  40. Marbach D, Prill RJ, Schaffter T, Mattiussi C, Floreano D, Stolovitzky G. 40.  2010. Revealing strengths and weaknesses of methods for gene network inference. Proc. Natl. Acad. Sci. USA 107:146286–91 [Google Scholar]
  41. Margolin AA, Nemenman I, Basso K, Wiggins C, Stolovitzky G. 41.  et al. 2006. ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinforma. 7:Suppl. 1S7 [Google Scholar]
  42. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R. 42.  et al. 2013. JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res. 42:1D142–47 [Google Scholar]
  43. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S. 43.  et al. 2006. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34:D108–10 [Google Scholar]
  44. Meng X, Zhang S. 44.  2013. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51:245–66 [Google Scholar]
  45. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J. 45.  et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:6042596–601 [Google Scholar]
  46. Naseem M, Philippi N, Hussain A, Wangorsch G, Ahmed N, Dandekar T. 46.  2012. Integrated systems view on networking by hormones in Arabidopsis immunity reveals multiple crosstalk for cytokinin. Plant Cell 24:51793–814 [Google Scholar]
  47. Penfold CA, Buchanan-Wollaston V, Denby KJ, Wild DL. 47.  2012. Nonparametric Bayesian inference for perturbed and orthologous gene regulatory networks. Bioinformatics 28:12i233–41 [Google Scholar]
  48. Penfold CA, Wild DL. 48.  2011. How to infer gene networks from expression profiles, revisited. Interface Focus 1:6857–70 [Google Scholar]
  49. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM. 49.  2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:5308–16 [Google Scholar]
  50. Pokhilko A, Fernández AP, Edwards KD, Southern MM, Halliday KJ, Millar AJ. 50.  2012. The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops. Mol. Syst. Biol. 8:574 [Google Scholar]
  51. Polanski K, Rhodes J, Hill CL, Zhang P, Jenkins D. 51.  et al. 2014. Wigwams: identifying gene modules co-regulated across multiple biological conditions. Bioinformatics 30:962–70 [Google Scholar]
  52. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M. 52.  et al. 2009. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev. 23:180–92 [Google Scholar]
  53. Popescu SC, Popescu GV, Bachan S, Zhang Z, Seay M. 53.  et al. 2007. Differential binding of calmodulin-related proteins to their targets revealed through high-density Arabidopsis protein microarrays. Proc. Natl. Acad. Sci. USA 104:114730–35 [Google Scholar]
  54. Sato M, Tsuda K, Wang L, Coller J, Watanabe Y. 54.  et al. 2010. Network modeling reveals prevalent negative regulatory relationships between signaling sectors in Arabidopsis immune signaling. PLoS Pathog. 6:7e1001011 [Google Scholar]
  55. Seo Y-S, Chern M, Bartley LE, Han M, Jung K-H. 55.  et al. 2011. Towards establishment of a rice stress response interactome. PLoS Genet. 7:4e1002020 [Google Scholar]
  56. Supper J, Strauch M, Wanke D, Harter K, Zell A. 56.  2007. EDISA: extracting biclusters from multiple time-series of gene expression profiles. BMC Bioinforma. 8:334 [Google Scholar]
  57. Sweetlove LJ, Fell D, Fernie AR. 57.  2008. Getting to grips with the plant metabolic network. Biochem. J. 409:127–41 [Google Scholar]
  58. Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S. 58.  et al. 2003. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:2317–30 [Google Scholar]
  59. Tierney L, Linde J, Müller S, Brunke S, Molina JC. 59.  et al. 2012. An interspecies regulatory network inferred from simultaneous RNA-seq of Candida albicans invading innate immune cells. Front. Microbiol. 3:85 [Google Scholar]
  60. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW. 60.  et al. 2009. Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ. 32:121633–51 [Google Scholar]
  61. Vermeirssen V, Deplancke B, Barrasa MI, Reece-Hoyes JS, Arda HE. 61.  et al. 2007. Matrix and Steiner-triple-system smart pooling assays for high-performance transcription regulatory network mapping. Nat. Methods 4:8659–64 [Google Scholar]
  62. Werhli AV, Grzegorczyk M, Husmeier D. 62.  2006. Comparative evaluation of reverse engineering gene regulatory networks with relevance networks, graphical Gaussian models and Bayesian networks. Bioinformatics 22:202523–31 [Google Scholar]
  63. Williams TCR, Poolman MG, Howden AJM, Schwarzlander M, Fell DA. 63.  et al. 2010. A genome-scale metabolic model accurately predicts fluxes in central carbon metabolism under stress conditions. Plant Physiol. 154:1311–23 [Google Scholar]
  64. Windram O, Madhou P, McHattie S, Hill C, Hickman R. 64.  et al. 2012. Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:93530–57 [Google Scholar]
  65. Yang J, Osman K, Iqbal M, Stekel DJ, Luo Z. 65.  et al. 2012. Inferring the Brassica rapa interactome using protein-protein interaction data from Arabidopsis thaliana. Front. Plant Sci. 3:297 [Google Scholar]
  66. Yu H, Kim PM, Sprecher E, Trifonov V, Gerstein M. 66.  2007. The importance of bottlenecks in protein networks: correlation with gene essentiality and expression dynamics. PLoS Comput. Biol. 3:4e59 [Google Scholar]
  67. Zhang H, Jin J, Tang L, Zhao Y, Gu X. 67.  et al. 2011. PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res. 39:D1114–17 [Google Scholar]
  68. Zheng Z-L, Zhao Y. 68.  2013. Transcriptome comparison and gene coexpression network analysis provide a systems view of citrus response to “Candidatus Liberibacter asiaticus” infection. BMC Genomics 14:27 [Google Scholar]
  69. Zhu P, Gu H, Jiao Y, Huang D, Chen M. 69.  2011. Computational identification of protein-protein interactions in rice based on the predicted rice interactome network. Genomics Proteomics Bioinforma. 9:4–5128–37 [Google Scholar]
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