A combination of gene expression ranking and co-expression network analysis increases discovery rate in large-scale mutant screens for novel Arabidopsis thaliana abiotic stress genes

Plant Biotechnology Journal

Volumn 13, Issue 4, 2015, Pages 501-513

  Ransbotyn, Vanessa ^a   Yeger Lotem, Esti ^a   Basha, Omer ^a   Acuna, Tania ^a   Verduyn, Christoph ^b   Gordon, Michal ^a   Chalifa Caspi, Vered ^a   Hannah, Matthew A ^b   Barak, Simon ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b Bayer Cropscience Belgium   (Belgium)

Author keywords

Abiotic stress; Arabidopsis thaliana; Co expression network; Mutant screen; Systems biology; Transcriptome

Indexed keywords

ARABIDOPSIS THALIANA;

ARABIDOPSIS; DNA MICROARRAY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; PHYSIOLOGICAL STRESS; PLANT GENE;

ARABIDOPSIS; GENE EXPRESSION; GENE REGULATORY NETWORKS; GENES, PLANT; MUTAGENESIS, INSERTIONAL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; STRESS, PHYSIOLOGICAL;

EID: 84928178134     PISSN: 14677644     EISSN: 14677652     Source Type: Journal    
DOI: 10.1111/pbi.12274     Document Type: Article

References (65)

1. Alonso, J.M., Stepanova, A.N., Leisse, T.J., Kim, C.J., Chen, H., Shinn, P., Stevenson, D.K., Zimmerman, J., Barajas, P., Cheuk, R., Gadrinab, C., Heller, C., Jeske, A., Koesema, E., Meyers, C.C., Parker, H., Prednis, L., Ansari, Y., Choy, N., Deen, H., Geralt, M., Hazari, N., Hom, E., Karnes, M., Mulholland, C., Ndubaku, R., Schmidt, I., Guzman, P., Aguilar-Henonin, L., Schmid, M., Weigel, D., Carter, D.E., Marchand, T., Risseeuw, E., Brogden, D., Zeko, A., Crosby, W.L., Berry, C.C. and Ecker, J.R. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science, 301, 653-657.
2. Andronis, C., Barak, S., Knowles, S.M., Sugano, S. and Tobin, E.M. (2008) The clock protein CCA1 and the bZIP transcription factor HY5 physically interact to regulate gene expression in Arabidopsis. Mol. Plant. 1, 58-67.
3. Aoki, K., Ogata, Y. and Shibata, D. (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol. 48, 381-390.
4. Aubert, Y., Vile, D., Pervent, M., Aldon, D., Ranty, B., Simonneau, T., Vavasseur, A. and Galaud, J.P. (2010) RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol. 51, 1975-1987.
5. Bassel, G.W., Lanc, H., Glaab, E., Gibbs, D.J., Gerjets, T., Krasnogor, N., Bonner, A.J., Holdsworth, M.J. and Provart, N.J. (2011a) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc. Natl Acad. Sci. USA, 108, 9709-9714.
6. Bassel, G.W., Glaab, E., Marquez, J., Holdsworth, M.J. and Bacardit, J. (2011b) Functional network construction in Arabidopsis using rule-based machine learning on large-scale data sets. Plant Cell, 23, 3101-3116.
7. Bassel, G.W., Gaudinier, A., Brady, S.M., Hennig, L. and Rhee, S.Y. (2012) Systems analysis of plant functional, transcriptional, physical interaction, and metabolic networks. Plant Cell, 24, 3859-3875.
8. Bhaskara, G.B., Nguyen, T.T. and Verslues, P.E. (2012) Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol. 160, 379-395.
9. Bolle, C. (2009) Phenotyping of abiotic responses and hormone treatment in Arabidopsis. Methods Mol. Biol. 479, 35-59.
10. Budziszewski, G.J., Lewis, S.P., Glover, L.W., Reineke, J., Jones, G., Ziemnik, L.S., Lonowski, J., Nyfeler, B., Aux, G., Zhou, Q., McElver, J., Patton, D.A., Martienssen, R., Grossniklaus, U., Ma, H., Law, M. and Levin, J.Z. (2001) Arabidopsis genes essential for seedling viability: isolation of insertional mutants and molecular cloning. Genetics, 159, 1765-1778.
11. Cai, B., Li, C.H. and Huang, J. (2014) Systematic identification of cell-wall related genes in Populus based on analysis of functional modules in co-expression network. PLoS One, 9, e95176.
12. Chiapusio, G., Sanchez, A.M., Reigosa, M.J., Gonzalez, L. and Pellissier, F. (1997) Do germination indices adequately reflect allelochemical effects on the germination process? J. Chem. Ecol. 23, 2445-2453.
13. Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K. and Mittler, R. (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell, 17, 268-281.
14. Dobritsa, A.A., Geanconteri, A., Shrestha, J., Carlson, A., Kooyers, N., Coerper, D., Urbanczyk-Wochniak, E., Bench, B.J., Sumner, L.W., Swanson, R. and Preuss, D. (2011) A large-scale genetic screen in Arabidopsis to identify genes involved in pollen exine production. Plant Physiol. 157, 947-970.
15. d'Erfurth, I., Jolivet, S., Froger, N., Catrice, O., Novatchkova, M., Simon, M., Jenczewski, E. and Mercier, R. (2008) Mutations in AtPS1 (Arabidopsis thaliana Parallel Spindle 1) lead to the production of diploid pollen grains. PLoS Genet. 4, e1000274.
16. Feller, A., Machemer, K., Braun, E.L. and Grotewold, E. (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 66, 94-116.
17. Ficklin, S.P., Luo, F. and Feltus, F.A. (2010) The association of multiple interacting genes with specific phenotypes in rice using gene coexpression networks. Plant Physiol. 154, 13-24.
18. Friedel, S., Usadel, B., von Wirén, N. and Sreenivasulu, N. (2012) Reverse engineering: a key component of systems biology to unravel global abiotic stress cross-talk. Front. Plant Sci. 3, 294.
19. Fu, F.F. and Xue, H.W. (2010) Coexpression analysis identifies Rice Starch Regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol. 154, 927-938.
20. Gillis, J. and Pavlidis, P. (2011) The impact of multifunctional genes on "guilt by association" analysis. PLoS One, 6, e17258.
21. Guo, W.J. and Ho, T.H.D. (2008) An abscisic acid-induced protein, HVA22, inhibits gibberellin-mediated programmed cell death in cereal aleurone cells. Plant Physiol. 147, 1710-1722.
22. Gutierrez, R.A., Stokes, T.L., Thum, K., Xu, X., Obertello, M., Katari, M.S., Tanurdzic, M., Dean, A., Nero, D.C., McClung, C.R. and Coruzzi, G.M. (2001) Systems approach identifies an organic nitrogen-responsive gene network that is regulated by the master clock control gene CCA1. Proc. Natl Acad. Sci. USA, 105, 4939-4944.
23. Heyndrickx, K.S. and Vandepoele, K. (2012) Systematic identification of functional plant modules through the integration of complementary data sources. Plant Physiol. 159, 884-901.
24. Joshi-Saha, A., Valon, C. and Leung, J. (2011) Abscisic acid signal off the STARTing block. Mol. Plant, 4, 562-580.
25. Kant, P., Kant, S., Gordon, M., Shaked, R. and Barak, S. (2007) STRESS RESPONSE SUPPRESSOR1 and STRESS RESPONSE SUPPRESSOR2, two DEAD-box RNA helicases that attenuate Arabidopsis responses to multiple abiotic stresses. Plant Physiol. 145, 814-830.
26. Kant, P., Gordon, M., Kant, S., Zolla, G., Davydov, O., Heimer, Y.M., Chalifa-Caspi, V., Shaked, R. and Barak, S. (2008) Functional-genomics-based identification of genes that regulate Arabidopsis responses to multiple abiotic stresses. Plant Cell Environ. 31, 697-714.
27. Kevei, E., Gyula, P., Hal, l.A., Kozma-Bognar, L., Kim, W.Y., Eriksson, M.E., Toth, R., Hanano, S., Feher, B., Southern, M.M., Bastow, R.M., Viczian, A., Hibberd, V., Davis, S.J., Somers, D.E., Nagy, F. and Millar, A.J. (2006) Forward genetic analysis of the circadian clock separates the multiple functions of ZEITLUPE1. Plant Physiol. 140, 933-945.
28. Kim, E., Shin, J. and Lee, I. (2010) Assessment of effectiveness of the network-guided genetic screen. Mol. BioSyst. 6, 1803-1806.
29. Kim, Y.S., Park, S., Gilmour, S.J. and Thomashow, M.F. (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 75, 364-376.
30. Koiwa, H., Bressan, R.A. and Hasegawa, P.M. (2006) Identification of plant stress-responsive determinants in Arabidopsis by large-scale forward genetic screens. J. Exp. Bot. 57, 1119-1128.
31. Koornneef, M., Hanhart, C., Hilhorst, H.W.M. and Karssen, C.M. (1989) In vivo inhibition of seed development and reserve protein accumulation in recombinants of abscisic acid biosynthesis and responsiveness mutants in Arabidopsis thaliana. Plant Physiol. 90, 463-469.
32. Lan, H., Carson, R., Provart, N.J. and Bonner, A.J. (2007) Combining classifiers to predict gene function in Arabidopsis thaliana using large-scale gene expression measurements. BMC Bioinformatics, 8, 358.
33. Lau, O.S., Huang, X., Charron, J.B., Lee, J.H., Li, G. and Deng, X.W. (2011) Interaction of Arabidopsis DET1 with CCA1 and LHY in mediating transcriptional repression in the plant circadian clock. Mol. Cell, 43, 703-712.
34. Lee, H., Hsu, A., Sajdak, J., Qin, J. and Pavlidis, P. (2004) Coexpression analysis of human genes across many microarray data sets. Genome Res. 14, 1085-1094.
35. Lee, I., Ambaru, B., Thakkar, P., Marcotte, E. and Rhee, S.Y. (2010) Rational association of genes with traits using a genome-scale gene network for Arabidopsis thaliana. Nat. Biotechnol. 28, 149-156.
36. Lee, I., Seob, Y.S., Coltrane, D., Hwanga, S., Oh, T., Marcotte, E.M. and Ronald, P.C. (2011) Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc. Natl Acad. Sci. USA, 108, 18548-18553.
37. Li, S., Pandey, S., Gookin, T.E., Zhao, Z., Wilson, L. and Assmann, S.M. (2012) Gene-sharing networks reveal organizing principles of transcriptomes in Arabidopsis and other multicellular organisms. Plant Cell, 24, 1362-1378.
38. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K. and Shinozaki, K. (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell, 10, 1391-1406.
39. Lu, Y., Savage, L.J., Larson, M.D., Wilkerson, C.G. and Las, R.L. (2011) Chloroplast 2010: a database for large-scale phenotypic screening of Arabidopsis mutants. Plant Physiol. 155, 1589-1600.
40. Ma, C., Xin, M., Feldmann, K.A. and Wang, X. (2014) Machine learning-based differential network analysis: a study of stress-responsive transcriptomes in Arabidopsis. Plant Cell, 26, 520-537.
41. Mao, L., Van Hemert, J.L., Dash, S. and Dickerson, J.A. (2009) Arabidopsis gene co-expression network and its functional modules. BMC Bioinformatics, 10, 346.
42. McElver, J., Tzafrir, I., Aux, G., Rogers, R., Ashby, C., Smith, K., Thomas, C., Schetter, A., Zhou, Q., Cushman, M.A., Tossberg, J., Nickle, T., Levin, J.Z., Law, M., Meinke, D. and Patton, D. (2001) Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics, 159, 1751-1763.
43. Miller, G. and Mittler, R. (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann. Bot. 98, 279-288.
44. Mutwil, M., Usadel, B., Schutte, M., Loraine, A., Ebenhoh, O. and Persson, S. (2010) Assembly of an interactive correlation network for the Arabidopsis genome using a novel heuristic clustering algorithm. Plant Physiol. 152, 29-43.
45. Nakashima, K., Shinwari, Z.K., Sakuma, Y., Seki, M., Miura, S., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol. Biol. 42, 657-665.
46. Nakashima, K., Takasaki, H., Mizoi, J., Shinozaki, K. and Yamaguchi-Shinozaki, K. (2012) NAC transcription factors in plant abiotic stress responses. Biochim. Biophys. Acta, 1819, 97-103.
47. Pagnussat, G.C., Yu, H.J., Ngo, Q.A., Rajani, S., Mayalagu, S., Johnson, C.S., Capron, A., Xie, L.F., Ye, D. and Sundaresan, V. (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development, 132, 603-614.
48. Rama Devi, S., Chen, X., Oliver, D.J. and Xiang, C. (2006) A novel high-throughput genetic screen for stress-responsive mutants of Arabidopsis thaliana reveals new loci involving stress responses. Plant J. 47, 652-663.
49. Ravasz, E. (2009) Detecting hierarchical modularity in biological networks. Methods Mol. Biol. 541, 145-160.
50. Rhee, S.Y. and Mutwil, M. (2014) Towards revealing the functions of all genes in plants. Trends Plant Sci. 19, 212-221.
51. Ruan, J., Dean, A.K. and Zhang, W. (2010) A general co-expression network-based approach to gene expression analysis: comparison and applications. BMC Syst. Biol. 4, 8.
52. Saeed, A.I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., Sturn, A., Snuffin, M., Rezantsev, A., Popov, D., Ryltsov, A., Kostukovich, E., Borisovsky, I., Liu, Z., Vinsavich, A., Trush, V. and Quackenbush, J. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques, 34, 374-378.
53. Scarpeci, T.E., Zanor, M.I. and Valle, E.M. (2008) Investigating the role of plant heat shock proteins during oxidative stress. Plant Signal. Behav. 3, 856-857.
54. Schneitz, K., Hulskamp, M., Kopczak, S.D. and Pruitt, R.E. (1997) Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development, 124, 1367-1376.
55. Seo, Y.J., Park, J.B., Cho, Y.J., Jung, C., Seo, H.S., Park, S.K., Nahm, B.H. and Song, J.T. (2010) Overexpression of the ethylene-responsive factor gene BrERF4 from Brassica rapa increases tolerance to salt and drought in Arabidopsis plants. Mol. Cells, 30, 271-277.
56. Singh, K.B. (1998) Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol. 118, 1111-1120.
57. Stockinger, E.J., Gilmour, S.J. and Thomashow, M.F. (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc. Natl Acad. Sci. USA, 94, 1035-1040.
58. Stuart, J., Segal, E., Koller, D. and Kim, S. (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science, 302, 249-255.
59. Takenaka, M., Verbitskiy, D., Zehrmann, A. and Brennicke, A. (2010) Reverse genetic screening identifies five E-class PPR proteins involved in RNA editing in mitochondria of Arabidopsis thaliana. J. Biol. Chem. 285, 27122-27129.
60. Tzfadia, O., Amar, D., Bradbury, L.M.T., Wurtzel, E.T. and Shamir, R. (2012) The MORPH algorithm: ranking candidate genes for membership in Arabidopsis and tomato pathways. Plant Cell, 24, 4389-4406.
61. Ulitsky, I., Maron-Katz, A., Shavit, S., Sagir, D., Linhart, C., Elkon, R., Tanay, A., Sharan, R., Shiloh, Y. and Shamir, R. (2010) Expander: from expression microarrays to networks and functions. Nat. Protoc. 5, 303-322.
62. Usadel, B., Obayashi, T., Mutwil, M., Giorgi, F.M., Bassel, G.W., Tanimoto, M., Chow, A., Steinhauser, D., Persson, S. and Provart, N.J. (2009) Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant, Cell Environ. 32, 1633-1651.
63. Wang, J., Chen, L., Wang, Y., Zhang, J., Liang, Y. and Xu, D. (2013) A computational systems biology study for understanding salt tolerance mechanism in rice. PLoS One, 8, e64929.
64. Wolfe, C.J., Kohane, I.S. and Butte, A.J. (2005) Systematic survey reveals general applicability of "guilt-by-association" within gene coexpression networks. BMC Bioinformatics, 6, 227.
65. Yang, Z., Tian, L., Latoszek-Green, M., Brown, D. and Wu, K. (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol. Biol. 58, 585-596.