A predictive coexpression network identifies novel genes controlling the seed-to-seedling phase transition in arabidopsis Thaliana

Plant Physiology

Volumn 170, Issue 4, 2016, Pages 2218-2231

  Silva, Anderson Tadeu ^a   Ribone, Pamela A ^b   Chan, Raquel L ^b   Ligterink, Wilco ^a   Hilhorst, Henk W M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b UNIVERSIDAD NACIONAL DEL LITORAL   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; MESSENGER RNA; TRANSCRIPTOME;

ARABIDOPSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENE REGULATORY NETWORK; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT GENE; PLANT ROOT; PLANT SEED; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY; SEEDLING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE ONTOLOGY; GENE REGULATORY NETWORKS; GENES, PLANT; GERMINATION; PLANT ROOTS; PRINCIPAL COMPONENT ANALYSIS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SEEDLINGS; SEEDS; TRANSCRIPTOME;

EID: 84962045541     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01704     Document Type: Article

References (57)

1. Allen E, Moing A, Ebbels TM, Maucourt M, Tomos AD, Rolin D, Hooks MA (2010) Correlation network analysis reveals a sequential reorganization of metabolic and transcriptional states during germination and gene-metabolite relationships in developing seedlings of Arabidopsis. BMC Syst Biol 4: 62
2. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61: 1001-1013
3. Aoki K, Ogata Y, Shibata D (2007) Approaches for extracting practical information from gene co-expression networks in plant biology. Plant Cell Physiol 48: 381-390
4. Aryee MJ, Gutiérrez-Pabello JA, Kramnik I, Maiti T, Quackenbush J (2009) An improved empirical Bayes approach to estimating differential gene expression in microarray time-course data: BETR (Bayesian estimation of temporal regulation). BMC Bioinformatics 10: 409
5. Baima S, Forte V, Possenti M, Peñalosa A, Leoni G, Salvi S, Felici B, Ruberti I, Morelli G (2014) Negative feedback regulation of auxin signaling by ATHB8/ACL5-BUD2 transcription module. Mol Plant 7: 1006-1025
6. Baima S, Nobili F, Sessa G, Lucchetti S, Ruberti I, Morelli G (1995) The expression of the Athb-8 homeobox gene is restricted to provascular cells in Arabidopsis thaliana. Development 121: 4171-4182
7. Barrero JM, Millar AA, Griffiths J, Czechowski T, Scheible WR, Udvardi M, Reid JB, Ross JJ, Jacobsen JV, Gubler F (2010) Gene expression profiling identifies two regulatory genes controlling dormancy and ABA sensitivity in Arabidopsis seeds. Plant J 61: 611-622
8. Bassel GW, Fung P, Chow TF, Foong JA, Provart NJ, Cutler SR (2008) Elucidating the germination transcriptional program using small molecules. Plant Physiol 147: 143-155
9. Bassel GW, Lan H, Glaab E, Gibbs DJ, Gerjets T, Krasnogor N, Bonner AJ, Holdsworth MJ, Provart NJ (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108: 9709-9714
10. Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD, et al (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 110: E435-E444
11. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J, Dinneny JR, Mace D, Ohler U, Benfey PN (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318: 801-806
12. Cabello JV, Arce AL, Chan RL (2012) The homologous HD-Zip I transcription factors HaHB1 and AtHB13 confer cold tolerance via the induction of pathogenesis-related and glucanase proteins. Plant J 69: 141-153
13. Cadman CSC, Toorop PE, Hilhorst HWM, Finch-Savage WE (2006) Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J 46: 805-822
14. Carabelli M, Morelli G, Whitelam G, Ruberti I (1996) Twilight-zone and canopy shade induction of the Athb-2 homeobox gene in green plants. Proc Natl Acad Sci USA 93: 3530-3535
15. Carrera E, Holman T, Medhurst A, Peer W, Schmuths H, Footitt S, Theodoulou FL, Holdsworth MJ (2007) Gene expression profiling reveals defined functions of the ATP-binding cassette transporter COMATOSE late in phase II of germination. Plant Physiol 143: 1669-1679
16. Choi H, Jeong S, Kim DS, Na HJ, Ryu JS, Lee SS, Nam HG, Lim PO, Woo HR (2014) The homeodomain-leucine zipper ATHB23, a phytochrome B-interacting protein, is important for phytochrome B-mediated red light signaling. Physiol Plant 150: 308-320
17. Dekkers BJW, Pearce S, van Bolderen-Veldkamp RP, Marshall A, Widera P, Gilbert J, Drost HG, Bassel GW, Müller K, King JR, et al (2013) Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol 163: 205-215
18. Ding YH, Liu NY, Tang ZS, Liu J, Yang WC (2006) Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18: 815-830
19. Fait A, Angelovici R, Less H, Ohad I, Urbanczyk-Wochniak E, Fernie AR, Galili G (2006) Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol 142: 839-854
20. Feng CZ, Chen Y, Wang C, Kong YH, WuWH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80: 654-668
21. Finch-Savage WE, Cadman CSC, Toorop PE, Lynn JR, Hilhorst HWM (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J 51: 60-78
22. Finkelstein R, Gampala SS, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE (ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol Biol 59: 253-267
23. Freeman TC, Goldovsky L, Brosch M, van Dongen S, Mazière P, Grocock RJ, Freilich S, Thornton J, Enright AJ (2007) Construction, visualisation, and clustering of transcription networks from microarray expression data. PLoS Comput Biol 3: 2032-2042
24. Fulda M, Schnurr J, Abbadi A, Heinz E, Browse J (2004) Peroxisomal acyl-CoA synthetase activity is essential for seedling development in Arabidopsis thaliana. Plant Cell 16: 394-405
25. Gadbury G, Garrett K, Allison D (2009) Challenges and approaches to statistical design and inference in high-dimensional investigations. In DA Belostotsky, ed, Plant Systems Biology. Humana Press, Totowa, NJ, pp 181-206
26. Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S, Smyth GK (2005) Limma linear models for microarray data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Springer, New York, pp 397-420
27. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80
28. Gutierrez L, VanWuytswinkel O, Castelain M, Bellini C (2007) Combined networks regulating seed maturation. Trends Plant Sci 12: 294-300
29. Hammani K, Gobert A, Small I, Giegé P (2011) A PPR protein involved in regulating nuclear genes encoding mitochondrial proteins? Plant Signal Behav 6: 748-750
30. Henriksson E, Olsson ASB, Johannesson H, Johansson H, Hanson J, Engström P, Söderman E (2005) Homeodomain leucine zipper class I genes in Arabidopsis: expression patterns and phylogenetic relationships. Plant Physiol 139: 509-518
31. Holdsworth MJ, Bentsink L, Soppe WJJ (2008a) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33-54
32. Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008b) Postgenomics dissection of seed dormancy and germination. Trends Plant Sci 13: 7-13
33. Hu W, Franklin KA, Sharrock RA, Jones MA, Harmer SL, Lagarias JC (2013) Unanticipated regulatory roles for Arabidopsis phytochromes revealed by null mutant analysis. Proc Natl Acad Sci USA 110: 1542-1547
34. Huijser P, Schmid M(2011) The control of developmental phase transitions in plants. Development 138: 4117-4129
35. Huq E, Al-Sady B, Hudson M, Kim C, Apel K, Quail PH (2004) Phytochrome-interacting factor 1 is a critical bHLH regulator of chlorophyll biosynthesis. Science 305: 1937-1941
36. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15
37. Jiang L, Liu Y, Sun H, Han Y, Li J, Li C, Guo W, Meng H, Li S, Fan Y, et al (2013) The mitochondrial folylpolyglutamate synthetase gene is required for nitrogen utilization during early seedling development in Arabidopsis. Plant Physiol 161: 971-989
38. Johannesson H, Wang Y, Hanson J, Engström P (2003) The Arabidopsis thaliana homeobox gene ATHB5 is a potential regulator of abscisic acid responsiveness in developing seedlings. Plant Mol Biol 51: 719-729
39. Law SR, Narsai R, Taylor NL, Delannoy E, Carrie C, Giraud E, Millar AH, Small I, Whelan J (2012) Nucleotide and RNA metabolism prime translational initiation in the earliest events of mitochondrial biogenesis during Arabidopsis germination. Plant Physiol 158: 1610-1627
40. Maia J, Dekkers BJW, Provart NJ, Ligterink W, Hilhorst HWM (2011) The re-establishment of desiccation tolerance in germinated Arabidopsis thaliana seeds and its associated transcriptome. PLoS ONE 6: e29123
41. Mansfield SG, Briarty LG (1996) The dynamics of seedling and cotyledon cell development in Arabidopsis thaliana during reserve mobilization. Int J Plant Sci 157: 280-295
42. Mazzella MA, Arana MV, Staneloni RJ, Perelman S, Rodriguez Batiller MJ, Muschietti J, Cerdán PD, Chen K, Sánchez RA, Zhu T, et al (2005) Phytochrome control of the Arabidopsis transcriptome anticipates seedling exposure to light. Plant Cell 17: 2507-2516
43. Moon J, Zhu L, Shen H, Huq E (2008) PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci USA 105: 9433-9438
44. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497
45. Nakashima K, Fujita Y, Katsura K, Maruyama K, Narusaka Y, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006) Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol Biol 60: 51-68
46. Narsai R, Law SR, Carrie C, Xu L, Whelan J (2011) In-depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiol 157: 1342-1362
47. Orlando D, Brady S, Koch J, Dinneny J, Benfey P (2009b) Manipulating large-scale Arabidopsis microarray expression data: identifying dominant expression patterns and biological process enrichment. In DA Belostotsky, ed, Plant Systems Biology. Humana Press, Totowa, NJ, pp 57-77
48. R Development Core Team (2011) R: A Language and Environment for Statistical Computing. Vienna, Austria: the R Foundation for Statistical Computing. http://www.R-project.org/.
49. Rajjou L, Gallardo K, Debeaujon I, Vandekerckhove J, Job C, Job D (2004) The effect of a-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol 134: 1598-1613
50. Ribone PA, Capella M, Chan RL (2015) Functional characterization of the homeodomain leucine zipper I transcription factor AtHB13 reveals a crucial role in Arabidopsis development. J Exp Bot 66: 5929-5943
51. Rougvie AE (2005) Intrinsic and extrinsic regulators of developmental timing: from miRNAs to nutritional cues. Development 132: 3787-3798
52. Tepperman JM, Hwang YS, Quail PH (2006) phyA dominates in transduction of red-light signals to rapidly responding genes at the initiation of Arabidopsis seedling de-etiolation. Plant J 48: 728-742
53. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M, Chow A, Steinhauser D, Persson S, Provart NJ (2009) Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ 32: 1633-1651
54. Vanstraelen M, Van Damme D, De Rycke R, Mylle E, Inze D, Geelen D (2006) Cell cycle-dependent targeting of a kinesin at the plasma membrane demarcates the division site in plant cells. Curr Biol 16: 308-314
55. Verdier J, Lalanne D, Pelletier S, Torres-Jerez I, Righetti K, Bandyopadhyay K, Leprince O, Chatelain E, Vu BL, Gouzy J, et al (2013) A regulatory network-based approach dissects late maturation processes related to the acquisition of desiccation tolerance and longevity of Medicago truncatula seeds. Plant Physiol 163: 757-774
56. Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223: 7-12
57. Wang J, Wang Y, Wang Z, Liu L, Zhu XG, Ma X (2011) Synchronization of cytoplasmic and transferred mitochondrial ribosomal protein gene expression in land plants is linked to Telo-box motif enrichment. BMC Evol Biol 11: 161