Inferring transcriptional gene regulation network of starch metabolism in Arabidopsis thaliana leaves using graphical Gaussian model

BMC Systems Biology

Volumn 6, Issue , 2012, Pages

  Ingkasuwan, Papapit ^a   Netrphan, Supatcharee ^b   Prasitwattanaseree, Sukon ^c   Tanticharoen, Morakot ^a   Bhumiratana, Sakarindr ^a   Meechai, Asawin ^a   Chaijaruwanich, Jeerayut ^c   Takahashi, Hideki ^d,e   Cheevadhanarak, Supapon ^a  

^a KING MONGKUT'S UNIVERSITY OF TECHNOLOGY THONBURI   (Thailand)

^b NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^c CHIANG MAI UNIVERSITY   (Thailand)

^d Elements Chemistry Laboratory   (Japan)

^e Michigan State University   (United States)

Author keywords

Arabidopsis thaliana; Constans like; Graphical Gaussian model; Indeterminate domain 5; Starch synthase 4; Transcriptional regulation

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

STARCH; TRANSCRIPTION FACTOR; VEGETABLE PROTEIN;

ANALYSIS OF VARIANCE; ARABIDOPSIS; ARTICLE; BINDING SITE; BIOSYNTHESIS; CIRCADIAN RHYTHM; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; NORMAL DISTRIBUTION; PHYSIOLOGY; PLANT GENE; PLANT LEAF; PROMOTER REGION; REPRODUCIBILITY; STATISTICAL MODEL;

ANALYSIS OF VARIANCE; ARABIDOPSIS; BINDING SITES; CIRCADIAN RHYTHM; CLUSTER ANALYSIS; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENES, PLANT; MODELS, STATISTICAL; NORMAL DISTRIBUTION; PLANT LEAVES; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; REPRODUCIBILITY OF RESULTS; STARCH; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84864931487     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-6-100     Document Type: Article

References (86)

1. Smith AM. Regulation of starch synthesis in storage organs. Regulation of Primary Metabolic Pathways in Plants 1999, 173-193. Kluwer Academic Publishers, Dordrecht, Kruger NJ, Hill SA, Ratcliffe RG, 42, Proceedings of the Phytochemical Society of Europe].
2. Smith AM, Denyer K, Zeeman SC, Edwads A, Martin C. The synthesis of the starch granule. Plant Carbohydrate Biochemistry 1999, 79-89. BIOS Scienctific Publishers Ltd, Oxford.
3. Smith AM, Zeeman SC, Thorneycroft D, Smith SM. Starch mobilization in leaves. J Exp Bot 2003, 54:577-583. 10.1093/jxb/erg036, 12508068.
4. Niittylä T, Messerli G, Trevisan M, Chen J, Smith AM, Zeeman SC. A previously unknown maltose transporter essential for starch degradation in leaves. Science 2004, 303:87-89. 10.1126/science.1091811, 14704427.
5. Sokolov LN, Dominguez-Solis JR, Allary A-L, Buchanan BB, Luan S. A redox-regulated chloroplast protein phosphatase binds to starch diurnally and functions in its accumulation. Proc Natl Acad Sci USA 2006, 103:9732-9737. 10.1073/pnas.0603329103, 1480475, 16772378.
6. Roldán I, Wattebled F, Mercedes Lucas M, Delvallé D, Planchot V, Jiménez S, Pérez R, Ball S, D'Hulst C, Mérida A. The phenotype of soluble starch synthase IV defective mutants of Arabidopsis thaliana suggests a novel function of elongation enzymes in the control of starch granule formation. Plant J 2007, 49:492-504. 10.1111/j.1365-313X.2006.02968.x, 17217470.
7. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, et al. β-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell 2008, 20:1040-1508. 10.1105/tpc.107.056507, 2390740, 18390594.
8. Lohmeier-Vogel E, Kerk D, Nimick M, Wrobel S, Vickerman L, Muench D, Moorhead G. Arabidopsis At5g39790 encodes a chloroplast-localized, carbohydrate-binding, coiled-coil domain-containing putative scaffold protein. BMC Plant Biol 2008, 8:120. 10.1186/1471-2229-8-120, 2653042, 19038037.
9. Kötting O, Santelia D, Edner C, Eicke S, Marthaler T, Gentry MS, Comparot-Moss S, Chen J, Smith AM, Steup M, et al. STARCH-EXCESS4 is a laforin-like phosphoglucan phosphatase required for starch degradation in Arabidopsis thaliana. Plant Cell 2009, 21:334-346. 10.1105/tpc.108.064360, 2648081, 19141707.
10. Li L, Foster CM, Gan Q, Nettleton D, James MG, Myers AM, Wurtele ES. Identification of the novel protein QQS as a component of the starch metabolic network in Arabidopsis leaves. Plant J 2009, 58:485-498. 10.1111/j.1365-313X.2009.03793.x, 19154206.
11. Szydlowski N, Ragel P, Raynaud S, Lucas MM, Roldán I, Montero M, Muñoz FJ, Ovecka M, Bahaji A, Planchot V, et al. Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell 2009, 21:2443-2457. 10.1105/tpc.109.066522, 2751949, 19666739.
12. Tetlow IJ, Morell MK, Emes MJ. Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 2004, 55:2131-2145. 10.1093/jxb/erh248, 15361536.
13. Geigenberger P, Kolbe A, Tiessen A. Redox regulation of carbon storage and partitioning in response to light and sugars. J Exp Bot 2005, 56:1469-1479. 10.1093/jxb/eri178, 15863446.
14. Kötting O, Kossmann J, Zeeman SC, Lloyd JR. Regulation of starch metabolism: the age of enlightenment?. Curr Opin Plant Biol 2010, 13:320-328.
15. Ghosh HP, Preiss J. Adenosine diphosphate glucose pyrophosphorylase: a regulatory enzymein the biosynthesis of starch in spinach leaf chloroplasts. J Biol Chem 1966, 241:4491-4504.
16. Fu Y, Ballicora MA, Leykam JF, Preiss J. Mechanism of reductive activation of potato tuber ADP-glucose pyrophosphorylase. J Biol Chem 1998, 273:25045-25052. 10.1074/jbc.273.39.25045, 9737961.
17. Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P. Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 2002, 14:2191-2213. 10.1105/tpc.003640, 150765, 12215515.
18. Schindler I, Renz A, Schmid FX, Beck E. Activation of spinach pullulanase by reduction results in a decrease in the number of isomeric forms. Biochim Biophys Acta Protein Struct Mol Enzymol 2001, 1548:175-186.
19. Wu C, Colleoni C, Myers AM, James MG. Enzymatic properties and regulation of ZPU1, the maize pullulanase-type starch debranching enzyme. Arch Biochem Biophys 2002, 406:21-32. 10.1016/S0003-9861(02)00412-5, 12234486.
20. Mikkelsen R, Mutenda KE, Mant A, Schürmann P, Blennow A. α-Glucan, water dikinase (GWD): A plastidic enzyme with redox-regulated and coordinated catalytic activity and binding affinity. Proc Natl Acad Sci USA 2005, 102:1785-1790. 10.1073/pnas.0406674102, 547843, 15665090.
21. Sparla F, Costa A, Lo Schiavo F, Pupillo P, Trost P. Redox regulation of a novel plastid-targeted β-amylase of Arabidopsis. Plant Physiol 2006, 141:840-850. 10.1104/pp.106.079186, 1489908, 16698902.
22. Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C. A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar-responsive elements of the iso1 promoter. Plant Cell 2003, 15:2076-2092. 10.1105/tpc.014597, 181332, 12953112.
23. Zhu Y, Cai X-L, Wang Z-Y, Hong M-M. An Interaction between a MYC protein and an EREBP protein is involved in transcriptional regulation of the rice Wx gene. J Biol Chem 2003, 278:47803-47811. 10.1074/jbc.M302806200, 12947109.
24. Tenorio G, Orea A, Romero JM, Mérida T. Oscillation of mRNA level and activity of granule-bound starch synthase I in Arabidopsis leaves during the day/night cycle. Plant Mol Biol 2003, 51:949-958. 10.1023/A:1023053420632, 12777053.
25. Ideker T, Thorsson V, Ranish JA, Christmas R, Buhler J, Eng JK, Bumgarner R, Goodlett DR, Aebersold R, Hood L. Integrated genomic and proteomic analyses of a systematically perturbed metabolic network. Science 2001, 292:929-934. 10.1126/science.292.5518.929, 11340206.
26. Lee TI, Rinaldi NJ, Robert F, Odom DT, Bar-Joseph Z, Gerber GK, Hannett NM, Harbison CT, Thompson CM, Simon I, et al. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 2002, 298:799-804. 10.1126/science.1075090, 12399584.
27. Gardner TS, di Bernardo D, Lorenz D, Collins JJ. Inferring genetic networks and identifying compound mode of action via expression profiling. Science 2003, 301:102-105. 10.1126/science.1081900, 12843395.
28. Wang Y, Joshi T, Zhang X-S, Xu D, Chen L. Inferring gene regulatory networks from multiple microarray datasets. Bioinformatics 2006, 22:2413-2420. 10.1093/bioinformatics/btl396, 16864593.
29. Ma S, Gong Q, Bohnert HJ. An Arabidopsis gene network based on the graphical Gaussian model. Genome Res 2007, 17:1614-1625. 10.1101/gr.6911207, 2045144, 17921353.
30. Carrera J, Rodrigo G, Jaramillo A, Elena S. Reverse-engineering the Arabidopsis thaliana transcriptional network under changing environmental conditions. Genome Biol 2009, 10:R96. 10.1186/gb-2009-10-9-r96, 2768985, 19754933.
31. Needham C, Manfield I, Bulpitt A, Gilmartin P, Westhead D. From gene expression to gene regulatory networks in Arabidopsis thaliana. BMC Syst Biol 2009, 3:85. 10.1186/1752-0509-3-85, 2760521, 19728870.
32. Mao L, Van Hemert J, Dash S, Dickerson J. Arabidopsis gene co-expression network and its functional modules. BMC Bioinformatics 2009, 10:346. 10.1186/1471-2105-10-346, 2772859, 19845953.
33. Schafer J, Strimmer K. An empirical Bayes approach to inferring large-scale gene association networks. Bioinformatics 2005, 21:754-764. 10.1093/bioinformatics/bti062, 15479708.
34. Opgen-Rhein R, Strimmer K. Infering gene dependency networks from genomic longitudinal data: a functional data approach. REVSTAT 2006, 4:53-65.
35. Zeeman SC, Tiessen A, Pilling E, Kato KL, Donald AM, Smith AM. Starch synthesis in Arabidopsis. granule synthesis, composition, and structure. Plant Physiol 2002, 129:516-529. 10.1104/pp.003756, 161669, 12068097.
36. Smith SM, Fulton DC, Chia T, Thorneycroft D, Chapple A, Dunstan H, Hylton C, Zeeman SC, Smith AM. Diurnal changes in the transcriptome encoding enzymes of starch metabolism provide evidence for both transcriptional and posttranscriptional regulation of starch metabolism in Arabidopsis leaves. Plant Physiol 2004, 136:2687-2699. 10.1104/pp.104.044347, 523333, 15347792.
37. Blasing OE, Gibon Y, Gunther M, Hohne M, Morcuende R, Osuna D, Thimm O, Usadel B, Scheible W-R, Stitt M. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell 2005, 17:3257-3281. 10.1105/tpc.105.035261, 1315368, 16299223.
38. Gibon Y, Bläsing OE, Palacios -Rojas N, Pankovic D, Hendriks JHM, Fisahn J, Höhne M, Günther M, Stitt M. Adjustment of diurnal starch turnover to short days: depletion of sugar during the night leads to a temporary inhibition of carbohydrate utilization, accumulation of sugars and post-translational activation of ADP-glucose pyrophosphorylase in the following light period. Plant J 2004, 39:847-862. 10.1111/j.1365-313X.2004.02173.x, 15341628.
39. Storey JD, Xiao W, Leek JT, Tompkins RG, Davis RW. Significance analysis of time course microarray experiments. Proc Natl Acad Sci USA 2005, 102:12837-12842. 10.1073/pnas.0504609102, 1201697, 16141318.
40. Leek JT, Monsen E, Dabney AR, Storey JD. EDGE: extraction and analysis of differential gene expression. Bioinformatics 2006, 22:507-508. 10.1093/bioinformatics/btk005, 16357033.
41. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M. Mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 2004, 37:914-939. 10.1111/j.1365-313X.2004.02016.x, 14996223.
42. Lao NT, Schoneveld O, Mould RM, Hibberd JM, Gray JC, Kavanagh TA. An Arabidopsis gene encoding a chloroplast-targeted β-amylase. Plant J 1999, 20:519-527. 10.1046/j.1365-313X.1999.00625.x, 10652124.
43. Kossmann J, Lloyd J. Understanding and influencing starch biochemistry. Crit Rev Biochem Mol Biol 2000, 35:141-196.
44. Lu Y, Gehan JP, Sharkey TD. Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol 2005, 138:2280-2291. 10.1104/pp.105.061903, 1183414, 16055686.
45. Scheidig A, Fröhlich A, Schulze S, Lloyd JR, Kossmann J. Downregulation of a chloroplast-targeted beta-amylase leads to a starch-excess phenotype in leaves. Plant J 2002, 30:581-591. 10.1046/j.1365-313X.2002.01317.x, 12047632.
46. Kaplan F, Sung DY, Guy CL. Roles of beta-amylase and starch breakdown during temperatures stress. Physiol Plantarum 2006, 126:120-128.
47. Makino S, Kiba T, Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Ueguchi C, Sugiyama T, Mizuno T. Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in Arabidopsis thaliana. Plant Cell Physiol 2000, 41:791-803. 10.1093/pcp/41.6.791, 10945350.
48. Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Más P, Panda S, Kreps JA, Kay SA. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 2000, 289:768-771. 10.1126/science.289.5480.768, 10926537.
49. Ito S, Kawamura H, Niwa Y, Nakamichi N, Yamashino T, Mizuno T. A genetic study of the Arabidopsis circadian clock with reference to the TIMING OF CAB EXPRESSION 1 (TOC1) gene. Plant Cell Physiol 2009, 50:290-303.
50. Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B, Zhu T, Wang X, Kreps JA, Kay SA. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 2000, 290:2110-2113. 10.1126/science.290.5499.2110, 11118138.
51. Kaplan F, Guy CL. RNA interference of Arabidopsis beta-amylase8 prevents maltose accumulation upon cold shock and increases sensitivity of PSII photochemical efficiency to freezing stress. Plant J 2005, 44:730-743. 10.1111/j.1365-313X.2005.02565.x, 16297066.
52. Papuga J, Hoffmann C, Dieterle M, Moes D, Moreau F, Tholl S, Steinmetz A, Thomas C. Arabidopsis LIM proteins: a family of actin bundlers with distinct expression patterns and modes of regulation. Plant Cell 2010, 22:3034-3052. 10.1105/tpc.110.075960, 2965535, 20817848.
53. Dean Rider S, Henderson JT, Jerome RE, Edenberg HJ, Romero-Severson J, Ogas J. Coordinate repression of regulators of embryonic identity by PICKLE during germination in Arabidopsis. Plant J 2003, 35:33-43. 10.1046/j.1365-313X.2003.01783.x, 2515612, 12834400.
54. Steffens NO, Galuschka C, Schindler M, Bulow L, Hehl R. AthaMap: an online resource for in silico transcription factor binding sites in the Arabidopsis thaliana genome. Nucl Acids Res 2004, 32:D368-372. 10.1093/nar/gkh017, 308752, 14681436.
55. Steffens NO, Galuschka C, Schindler M, Bulow L, Hehl R. AthaMap web tools for database-assisted identification of combinatorial cis-regulatory elements and the display of highly conserved transcription factor binding sites in Arabidopsis thaliana. Nucl Acids Res 2005, 33:W397-402. 10.1093/nar/gki395, 1160156, 15980498.
56. Bülow L, Steffens NO, Galuschka C, Schindler M, Hehl R. AthaMap: from in silico data to real transcription factor binding sites. In Silico Biol 2006, 6:243-252. 10.1007/3-540-28185-1_10, 16922688.
57. Galuschka C, Schindler M, Bulow L, Hehl R. AthaMap web tools for the analysis and identification of co-regulated genes. Nucl Acids Res 2007, 35:D857-862. 10.1093/nar/gkl1006, 1761422, 17148485.
58. Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K. ATTED-II provides coexpressed gene networks for Arabidopsis. Nucl Acids Res 2009, 37:D987-D991. 10.1093/nar/gkn807, 2686564, 18953027.
59. Obayashi T, Kinoshita K. Rank of correlation coefficient as a comparable measure for biological significance of gene coexpression. DNA Res 2009, 16:249-260. 10.1093/dnares/dsp016, 2762411, 19767600.
60. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 2003, 301:653-657. 10.1126/science.1086391, 12893945.
61. Tissier AF, Marillonnet S, Klimyuk V, Patel K, Torres MA, Murphy G, Jones JDG. Multiple independent defective suppressor-mutator transposon insertions in Arabidopsis: a tool for functional genomics. Plant Cell 1999, 11:1841-1852. 144107, 10521516.
62. Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR, Görlach J. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 2001, 13:1499-1510. 139543, 11449047.
63. Englbrecht C, Schoof H, Bohm S. Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome. BMC Genomics 2004, 5:39. 10.1186/1471-2164-5-39, 481060, 15236668.
64. Colasanti J, Tremblay R, Wong A, Coneva V, Kozaki A, Mable B. The maize INDETERMINATE1 flowering time regulator defines a highly conserved zinc finger protein family in higher plants. BMC Genomics 2006, 7:158. 10.1186/1471-2164-7-158, 1586020, 16784536.
65. Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 2007, 21:2196-2204. 10.1101/gad.440307, 1950858, 17785527.
66. Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol 2006, 4:e143. 10.1371/journal.pbio.0040143, 1450008, 16640459.
67. Tanimoto M, Tremblay R, Colasanti J. Altered gravitropic response, amyloplast sedimentation and circumnutation in the Arabidopsis shoot gravitropism 5 mutant are associated with reduced starch levels. Plant Mol Biol 2008, 67:57-69. 10.1007/s11103-008-9301-0, 18259878.
68. Seo PJ, Kim MJ, Ryu J-Y, Jeong E-Y, Park C-M. Two splice variants of the IDD14 transcription factor competitively form nonfunctional heterodimers which may regulate starch metabolism. Nat Commun 2011, 2:303.
69. Seo PJ, Ryu J, Kang SK, Park C-M. Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. Plant J 2011, 65:418-429. 10.1111/j.1365-313X.2010.04432.x, 21265895.
70. Kakizaki T, Matsumura H, Nakayama K, Che F-S, Terauchi R, Inaba T. Coordination of plastid protein import and nuclear gene expression by plastid-to-nucleus retrograde signaling. Plant Physiol 2009, 151:1339-1353. 10.1104/pp.109.145987, 2773054, 19726569.
71. Zentella R, Zhang Z-L, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T-P. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 2007, 19:3037-3057. 10.1105/tpc.107.054999, 2174696, 17933900.
72. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P. Genevestigator V3: a reference expression database for the meta-analysis of transcriptome. Adv Bioinformatics 2008, 5.
73. Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis. Plant Cell 1990, 2:755-767. 159928, 2152125.
74. Nakayama N, Arroyo JM, Simorowski J, May B, Martienssen R, Irish VF. Gene trap lines define domains of gene regulation in Arabidopsis petals and stamens. Plant Cell 2005, 17:2486-2506. 10.1105/tpc.105.033985, 1197429, 16055634.
75. Jaspers P, Blomster T, Brosché M, Salojärvi J, Ahlfors R, Vainonen JP, Reddy RA, Immink R, Angenent G, Turck F, et al. Unequally redundant RCD1 and SRO1 mediate stress and developmental responses and interact with transcription factors. Plant J 2009, 60:268-279. 10.1111/j.1365-313X.2009.03951.x, 19548978.
76. Belles-Boix E, Babiychuk E, Van Montagu M, Inzé D, Kushnir S. CEO1, a new protein from Arabidopsis thaliana, protects yeast against oxidative damage. FEBS Lett 2000, 482:19-24. 10.1016/S0014-5793(00)02016-0, 11018516.
77. Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann H, Kangasjarvi J. Ozone-sensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 2000, 12:1849-1862. 149124, 11041881.
78. Ahlfors R, Lang S, Overmyer K, Jaspers P, Brosche M, Tauriainen A, Kollist H, Tuominen H, Belles-Boix E, Piippo M, et al. Arabidopsis RADICAL-INDUCED CELL DEATH1 belongs to the WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses. Plant Cell 2004, 16:1925-1937. 10.1105/tpc.021832, 514171, 15208394.
79. Yilmaz A, Mejia-Guerra MK, Kurz K, Liang X, Welch L, Grotewold E. AGRIS: the Arabidopsis gene regulatory information server, an update. Nucl Acids Res 2011, 39:D1118-D1122. 10.1093/nar/gkq1120, 3013708, 21059685.
80. Workman C, Jensen LJ, Jarmer H, Berka R, Gautier L, Nielser HB, Saxild H-H, Nielsen C, Brunak S, Knudsen S. A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol 2002, 3:research0048.0041-research0048.0016.
81. Li C, Wong WH. Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 2001, 98:31-36. 10.1073/pnas.98.1.31, 14539, 11134512.
82. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 1995, 57:289-300.
83. Storey JD. A direct approach to false discovery rates. J Royal Stat Soc Ser B 2002, 64:479-498.
84. Fujiwara T, Hirai MY, Chino M, Komeda Y, Naito S. Effects of sulfur nutrition on expression of the soybean seed storage protein genes in transgenic petunia. Plant Physiol 1992, 99:263-268. 10.1104/pp.99.1.263, 1080434, 16668860.
85. Smith AM, Zeeman SC. Quantification of starch in plant tissues. Nat Protoc 2006, 1:1342-1345. 10.1038/nprot.2006.232, 17406420.
86. Sato S, Soga T, Nishioka T, Tomita M. Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection. Plant J 2004, 40:151-163. 10.1111/j.1365-313X.2004.02187.x, 15361149.