Lignin, mitochondrial family, and photorespiratory transporter classification as case studies in using co-expression, co-response, and protein locations to aid in identifying transport functions

Frontiers in Plant Science

Volumn 5, Issue MAR, 2014, Pages

  Tohge, Takayuki ^a   Fernie, Alisdair R ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Co expression network; Informatic identification; Plant metabolism; Transporters

Indexed keywords

EID: 84901056358     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00075     Document Type: Review

References (75)

1. Alejandro, S., Lee, Y., Tohge, T., Sudre, D., Osorio, S., Park, J., et al. (2012). AtABCG29 is a monolignol transporter involved in lignin biosynthesis. Curr. Biol. 10, 1207-1212. doi: 10.1016/j.cub.2012.04.064
2. Altman, R. B., and Raychaudhuri, S. (2001). Whole-genome expression analysis: challenges beyond clustering. Curr. Opin. Struct. Biol. 11, 340-347. doi: 10.1016/s0959-440x(00)00212-8
3. Aoki, N., Ohnishi, J., and Kanai, R. (1992). Two different mechanisms for transport of pyruvate into mesophyll chloroplasts of c-4 plants-a comparative-study. Plant Cell Physiol. 33, 805-809.
4. Araújo, W. L., Ishizaki, K., Nunes-Nesi, A., Larson, T. R., Tohge, T., Krahnert, I., et al. (2010). Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22, 1549-1563. doi: 10.1105/tpc.110.075630
5. Araújo, W. L., Tohge, T., Ishizaki, K., Leaver, C. J., and Fernie, A. R. (2011). Protein degradation-an alternative respiratory substrate for stressed plants. Trends Plant Sci. 16, 489-498. doi: 10.1016/j.tplants.2011.05.008
6. Bordych, C., Eisenhut, M., Pick, T. R., Kuelahoglu, C., and Weber, A. P. M. (2013). Co-expression analysis as tool for the discovery of transport proteins in photorespiration. Plant Biol. 15, 686-693. doi: 10.1111/plb.12027
7. Bringmann, M., Li, E., Sampathkumar, A., Kocabek, T., Hauser, M.-T., and Persson, S. (2012). POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell 24, 163-177. doi: 10.1105/tpc.111.093575
8. Brown, D. M., Zeef, L. A. H., Ellis, J., Goodacre, R., and Turner, S. R. (2005). Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17, 2281-2295. doi: 10.1105/tpc.105.031542
9. Cocuron, J.-C., Lerouxel, O., Drakakaki, G., Alonso, A. P., Liepman, A. H., Keegstra, K., et al. (2007). A gene from the cellulose synthase-like C family encodes a beta-1,4 glucan synthase. Proc. Natl. Acad. Sci. U.S.A. 104, 8550-8555. doi: 10.1073/pnas.0703133104
10. De Michele, R., Ast, C., Loqué, D., Ho, C.-H., Andrade, S. L., Lanquar, V., et al. (2013). Fluorescent sensors reporting the activity of ammonium transceptors in live cells. eLIFE 2:e00800. doi: 10.7554/eLife.00800
11. Ehlting, J., Mattheus, N., Aeschliman, D. S., Li, E. Y., Hamberger, B., Cullis, I. F., et al. (2005). Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J. 42, 618-640. doi: 10.1111/j.1365-313X.2005.02403.x
12. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U. S. A. 95, 14863-14868. doi: 10.1073/pnas.95.25.14863
13. Eisenhut, M., Planchais, S., Cabassa, C., Guivarc'h, A., Justin, A.-M., Taconnat, L., et al. (2013). Arabidopsis A BOUT DE SOUFFLE is a putative mitochondrial transporter involved in photorespiratory metabolism and is required for meristem growth at ambient CO2 levels. Plant J. 73, 836-849. doi: 10.1111/tpj.12082
14. Fribourg, S., Romier, C., Werten, S., Gangloff, Y. G., Poterszman, A., and Moras, D. (2001). Dissecting the interaction network of multiprotein complexes by pairwise coexpression of subunits in E. coli. J. Mol. Biol. 306, 363-373. doi: 10.1006/jmbi.2000.4376
15. Furumoto, T., Yamaguchi, T., Ohshima-Ichie, Y., Nakamura, M., Tsuchida-Iwata, Y., Shimamura, M., et al. (2011). A plastidial sodium-dependent pyruvate transporter. Nature 476, 472-475. doi: 10.1038/nature10250
16. Gasch, A. P., and Eisen, M. B. (2002). Exploring the conditional coregulation of yeast gene expression through fuzzy k-means clustering. Genome Biol. 3, 1-22. doi: 10.1186/gb-2002-3-11-research0059
17. Getz, G., Levine, E., and Domany, E. (2000). Coupled two-way clustering analysis of gene microarray data. Proc. Natl. Acad. Sci. U.S.A. 97, 12079-12084. doi: 10.1073/pnas.210134797
18. Gigolashvili, T., Yatusevich, R., Rollwitz, I., Humphry, M., Gershenzon, J., and Flugge, U. I. (2009). The Plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21 1813-1829. doi: 10.1105/tpc.109.066399
19. Goda, H., Sasaki, E., Akiyama, K., Maruyama-Nakashita, A., Nakabayashi, K., Li, W., et al. (2008). The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 55, 526-542. doi: 10.1111/j.1365-313X.2008.03510.x
20. Hirai, M. Y., Sugiyama, K., Sawada, Y., Tohge, T., Obayashi, T., Suzuki, A., et al. (2007). Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 6478-6483. doi: 10.1073/pnas.0611629104
21. Hoffmann, C., Plocharski, B., Haferkamp, I., Leroch, M., Ewald, R., Bauwe, H., et al. (2013). From endoplasmic reticulum to mitochondria: absence of the Arabidopsis ATP antiporter endoplasmic reticulum adenylate transporter1 perturbs photorespiration. Plant Cell 25, 2647-2660. doi: 10.1105/tpc.113.113605
22. Holt K. E., Millar A. H., and Whelan J. (2006) ModuleFinder and CoReg: alternative tools for linking gene expression modules with promoter sequences motifs to uncover gene regulation mechanisms in plants. Plant Methods. 2:8. doi: 10.1186/1746-4811-2-8
23. Hwang, S., Rhee, S. Y., Marcotte, E. M., and Lee, I. (2011). Systematic prediction of gene function in Arabidopsis thaliana using a probabilistic functional gene network. Nat. Protoc. 6, 1429-1442. doi: 10.1038/nprot.2011.372
24. Katari, M. S., Nowicki, S. D., Aceituno, F. F., Nero, D., Kelfer, J., Thompson, L. P., et al. (2010). VirtualPlant: a software platform to support systems biology research. Plant Physiol. 152, 500-515. doi: 10.1104/pp.109.147025
25. Kinoshita, H., Nagasaki, J., Yoshikawa, N., Yamamoto, A., Takito, S., Kawasaki, M., et al. (2010). The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. Plant J. 65, 15-26. doi: 10.1111/j.1365-313X.2010.04397.x
26. Kinoshita H., Nagasaki J., Yoshikawa N., Yamamoto A., Takito S., Kawasaki M., et al. (2011). The chloroplastic 2-oxoglutarate/malate transporter has dual function as the malate valve and in carbon/nitrogen metabolism. Plant J. 65. 15-26. doi: 10.1111/j.1365-313X.2010.04397.x
27. Lawand, S., Dorne, A. J., Long, D., Coupland, G., Mache, R., and Carol, P. (2002). Arabidopsis a bout de souffle, which is homologous with mammalian carnitine acyl carrier, is required for postembryonic growth in the light. Plant Cell 14, 2161-2173. doi: 10.1105/Tpc.002485
28. Le Hir, R., Sorin, C., Chakraborti, D., Moritz, T., Schaller, H., Tellier, F., et al. (2013). ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. Plant J. 76, 811-24. doi: 10.1111/tpj.12334
29. Lee, H. K., Hsu, A. K., Sajdak, J., Qin, J., and Pavlidis, P. (2004). Coexpression analysis of human genes across many microarray data sets. Genome Res. 14, 1085-1094. doi: 10.1101/gr.1910904
30. Li, K. C., Liu, C. T., Sun, W., Yuan, S. S., and Yu, T. W. (2004). A system for enhancing genome-wide coexpression dynamics study. Proc. Natl. Acad. Sci. U.S.A. 101, 15561-15566. doi: 10.1073/pnas.0402962101
31. Liu, X., and Bush, D. R. (2006). Expression and transcriptional regulation of amino acid transporters in plants. Amino Acids 30, 113-120. doi: 10.1007/s00726-005-0248-z
32. Maleck, K., Levine, A., Eulgem, T., Morgan, A., Schmid, J., Lawton, K. A., et al. (2000). The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat. Genet. 26, 403-410. doi: 10.1038/82521
33. Mao, D. Q., Luo, Y., Zhang, J. H., and Zhu, J. (2005). A new strategy of cooperativity of biclustering and hierarchical clustering: A case of analyzing yeast genomic microarray datasets. Front. Biosci. 10:1619-1627.
34. Marinova, K., Pourcel, L., Weder, B., Schwarz, M., Barron, D., Routaboul, J. M., et al. (2007). The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19, 2023-2038. doi: 10.1105/tpc.106.046029
35. Martinoia, E., Meyer, S., De Angeli, A., and Nagy, R. (2012). Vacuolar transporters in their physiological context. Annu. Rev. Plant Biol. 63, 183-213. doi: 10.1146/annurev-arplant-042811-105608
36. Mintz-Oron, S., Meir, S., Malitsky, S., Ruppin, E., Aharoni, A., and Shlomi, T. (2012). Reconstruction of Arabidopsis metabolic network models accounting for subcellular compartmentalization and tissue-specificity. Proc. Natl. Acad. Sci. U.S.A. 109, 339-344. doi: 10.1073/pnas.1100358109
37. Mutwil, M., Obro, J., Willats, W. G. T., and Persson, S. (2008). GeneCAT-novel webtools that combine BLAST and co-expression analyses. Nucleic Acids Res. 36, W320-W326. doi: 10.1093/nar/gkn292
38. Nour-Eldin, H. H., and Halkier, B. A. (2013). The emerging field of transport engineering of plant specialized metabolites. Curr. Opin. Biotechnol. 24, 263-270. doi: 10.1016/j.copbio.2012.09.006
39. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H., and Kinoshita, K. (2009). ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987-D991. doi: 10.1093/nar/gkn807
40. Obayashi, T., Nishida, K., Kasahara, K., and Kinoshita, K. (2011). ATTED-II Updates: condition-specific gene coexpression to extend coexpression analyses and applications to a broad range of flowering plants. Plant Cell Physiol. 52, 213-219. doi: 10.1093/pcp/pcq203
41. Okazaki, Y., Shimojima, M., Sawada, Y., Toyooka, K., Narisawa, T., Mochida, K., et al. (2009). A chloroplastic UDP-glucose pyrophosphorylase from Arabidopsis is the committed enzyme for the first step of sulfolipid biosynthesis. Plant Cell 21, 892-909. doi: 10.1105/tpc.108.063925
42. Palmieri, F., Pierri, C. L., De Grassi, A., Nunes-Nesi, A., and Fernie, A. R. (2011). Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J. 66, 161-181. doi: 10.1111/j.1365-313X.2011.04516.x
43. Persson, S., Wei, H. R., Milne, J., Page, G. P., and Somerville, C. R. (2005). Identification of genes required for cellulose synthesis by regression analysis of public microarray data sets. Proc. Natl. Acad. Sci. U.S.A. 102, 8633-8638. doi: 10.1073/pnas.0503392102
44. Pick, T. R., Braeutigam, A., Schulz, M. A., Obata, T., Fernie, A. R., and Weber, A. P. M. (2013). PLGG1, a plastidic glycolate glycerate transporter, is required for photorespiration and defines a unique class of metabolite transporters. Proc. Natl. Acad. Sci. U.S.A. 110, 3185-3190. doi: 10.1073/pnas.1215142110
45. Prieto, C., Risueno, A., Fontanillo, C., and De Las Rivas, J. (2008). Human gene coexpression landscape: confident network derived from tissue transcriptomic profiles. PLoS ONE 3:e3911. doi: 10.1371/journal.pone.0003911
46. Raychaudhuri, S., Sutphin, P. D., Chang, J. T., and Altman, R. B. (2001). Basic microarray analysis: grouping and feature reduction. Trends Biotechnol. 19, 189-193. doi: 10.1016/s0167-7799(01)01599-2
47. Renné, P., Dressen, U., Hebbeker, U., Hille, D., Flügge, U. I., Westhoff, P. et al. (2003). The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J. 35, 316-331. doi: 10.1046/j.1365-313X.2003.01806.x
48. Rieder, B., and Neuhaus, H. E. (2011). Identification of an Arabidopsis plasma membrane-located ATP transporter important for anther development. Plant Cell 23, 1932-1944. doi: 10.1105/tpc.111.084574
49. Rolland, N., Curien, G., Finazzi, G., Kuntz, M., Marechal, E., Matringe, M., et al. (2012). The Biosynthetic capacities of the plastids and integration between cytoplasmic and chloroplast processes. Annu. Rev. Genet. 46, 233-264. doi: 10.1146/annurev-genet-110410-132544
50. Ruprecht, C., and Persson, S. (2012). Co-expression of cell-wall related genes: new tools and insights. Front. Plant Sci. 3:1-7. doi: 10.3389/fpls.2012.00083
51. Saito, K., Yonekura-Sakakibara, K., Nakabayashi, R., Higashi, Y., Yamazaki, M., Tohge, T., et al. (2013). The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiol. Biochem. 72, 21-34. doi: 10.1016/j.plaphy.2013.02.001
52. Sakurai, N., Ara, T., Ogata, Y., Sano, R., Ohno, T., Sugiyama, K., et al. (2011). KaPPA-View4: a metabolic pathway database for representation and analysis of correlation networks of gene co-expression and metabolite co-accumulation and omics data. Nucleic Acids Res. 39, D677-D684. doi: 10.1093/nar/gkq989
53. Sanchez-Rodriguez, C., Bauer, S., Hematy, K., Saxe, F., Ibanez, A. B., Vodermaier, V., et al. (2012). Chitinase-like1/pom-pom1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell 24, 589-607. doi: 10.1105/tpc.111.094672
54. Sawada, Y., Toyooka, K., Kuwahara, A., Sakata, A., Nagano, M., Saito, K., et al. (2009). Arabidopsis bile acid: sodium symporter family protein 5 is involved in methionine-derived glucosinolate biosynthesis. Plant Cell Physiol. 50, 1579-1586. doi: 10.1093/pcp/pcp110
55. Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M., and Wisman, E. (2001). Microarray analysis of diurnal and circadian-regulated genes in Arabidopsis. Plant Cell 13, 113-123. doi: 10.1105/tpc.13.1.113
56. Schneidereit, J., Hausler, R. E., Fiene, G., Kaiser, W. M., and Weber, A. P. M. (2006). Antisense repression reveals a crucial role of the plastidic 2-oxoglutarate/malate translocator DiT1 at the interface between carbon and nitrogen metabolism. Plant J. 45, 206-224. doi: 10.1111/j.1365-313X.2005.02594.x
57. Schroeder, J. I., Delhaize, E., Frommer, W. B., Guerinot, M. L., Harrison, M. J., Herrera-Estrella, L., et al. (2013). Using membrane transporters to improve crops for sustainable food production. Nature 497, 60-66. doi: 10.1038/nature11909
58. Schwacke, R., Schneider, A., van der Graaff, E., Fischer, K., Catoni, E., Desimone, M., et al. (2003). ARAMEMNON, a novel database for Arabidopsis integral membrane proteins. Plant Physiol. 131, 16-26. doi: 10.1104/pp.011577
59. Stitt, M. (2013). Systems-integration of plant metabolism: means, motive and opportunity. Curr. Opin. Plant Biol. 16, 381-388. doi: 10.1016/j.pbi.2013.02.012
60. Sweetlove, L. J., and Fernie, A. R. (2013). Spatial organization of metabolism within the plant cell. Annu. Rev. Plant Biol. 64, 723-746. doi: 10.1146/annurev-arplant-050312-120233
61. Taniguchi, M., Taniguchi, Y., Kawasaki, M., Takeda, S., Kato, T., Sato, S., et al. (2002). Identifying and characterizing plastidic 2-oxoglutarate/malate and dicarboxylate transporters in Arabidopsis thaliana. Plant Cell Physiol. 43, 706-717. doi: 10.1093/pcp/pcf109
62. Tohge, T., and Fernie, A. R. (2012). Co-expression and co-responses: within and beyond transcription. Front. Plant Sci. 3:248-248. doi: 10.3389/fpls.2012.00248
63. Tohge, T., Kusano, M., Fukushima, A., Saito, K., and Fernie, A. (2011). Transcriptional and metabolic programs following exposure of plants to UV-B irradiation. Plant Signal. Behav. 6, 1987-1992. doi: 10.4161/psb.6.12.18240
64. Tohge, T., Ramos, M. S., Nunes-Nesi, A., Mutwil, M., Giavalisco, P., Steinhauser, D., et al. (2011). Toward the storage metabolome: profiling the barley vacuole. Plant Physiol. 157, 1469-1482. doi: 10.1104/pp.111.185710
65. Tohge, T., Yonekura-Sakakibara, K., Niida, R., Watanabe-Takahashi, A., and Saito, K. (2007). Phytochemical genomics in Arabidopsis thaliana: A case study for functional identification of flavonoid biosynthesis genes. Pure Appl. Chem. 79, 811-823. doi: 10.1351/pac200779040811
66. Toufighi, K., Brady, S. M., Austin, R., Ly, E., and Provart, N. J. (2005). The botany array resource: e-Northerns, expression angling, and promoter analyses. Plant J. 43, 153-163. doi: 10.1111/j.1365-313X.2005.02437.x
67. Usadel, B., Obayashi, T., Mutwil, M., Giorgi, F. M., Bassel, G. W., Tanimoto, M., et al. (2009). Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ. 32, 1633-1651. doi: 10.1111/j.1365-3040.2009.02040.x
68. Vanholme, R., Cesarino, I., Rataj, K., Xiao, Y., Sundin, L., Goeminne, G., et al. (2013). Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341, 1103-1106. doi: 10.1126/science.1241602
69. Voehringer, D. W., Hirschberg, D. L., Xiao, J., Lu, Q., Roederer, M., Lock, C., et al. (2000). Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc. Natl. Acad. Sci. U.S.A. 97, 2680-2685. doi: 10.1073/pnas.97.6.2680
70. Weber, A. P. M., and Linka, N. (2011). Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu. Rev. Plant Biol. 62, 53-77. doi: 10.1146/annurev-arplant-042110-103903
71. Yonekura-Sakakibara, K., Fukushima, A., Nakabayashi, R., Hanada, K., Matsuda, F., Sugawara, S., et al. (2012). Two glycosyltransferases involved in anthocyanin modification delineated by transcriptome independent component analysis in Arabidopsis thaliana. Plant J. 69, 154-167. doi: 10.1111/j.1365-313X.2011.04779.x
72. Yonekura-Sakakibara, K., Tohge, T., Matsuda, F., Nakabayashi, R., Takayama, H., Niida, R., et al. (2008). Comprehensive flavonol profiling and transcriptome coexpression analysis leading to decoding gene-metabolite correlations in Arabidopsis. Plant Cell 20, 2160-2176. doi: 10.1105/tpc.108.058040
73. Yonekura-Sakakibara, K., Tohge, T., Niida, R., and Saito, K. (2007). Identification of a flavonol 7-O-rhamnosyltransferase gene determining flavonoid pattern in Arabidopsis by transcriptome coexpression analysis and reverse genetics. J. Biol. Chem. 282, 14932-14941. doi: 10.1074/jbc.M611498200
74. Zhang, L., King, O., Wong, S., Goldberg, D., Tong, A., Lesage, G., et al. (2005). Motifs, themes and thematic maps of an integrated Saccharomyces cerevisiae interaction network. J. Biol. 4, 6. doi: 10.1186/jbiol23
75. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632. doi: 10.1104/pp.104.046367