A developmental switch of gene expression in the barley seed mediated by HvVP1 (Viviparous-1) and HvGAMYB interactions

Plant Physiology

Volumn 170, Issue 4, 2016, Pages 2146-2158

  Abraham, Zamira ^a   Iglesias Fernández, Raquel ^a   Martínez, Manuel ^a   Rubio Somoza, Ignacio ^a   Díaz, Isabel ^a   Carbonero, Pilar ^a   Vicente Carbajosa, Jesús ^a  

^a ETSI MontesTechnical University of Madrid   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PLANT PROTEIN; PROTEIN BINDING;

AMINO ACID SEQUENCE; ANTIBODY SPECIFICITY; BIOLOGICAL MODEL; CELL NUCLEUS; CHEMISTRY; ENDOSPERM; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HORDEUM; METABOLISM; PHYLOGENY; PLANT SEED; PROMOTER REGION; PROTEIN MOTIF; RNA SPLICING; TRANSCRIPTION INITIATION; TWO HYBRID SYSTEM;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; CELL NUCLEUS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ENDOSPERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GERMINATION; HORDEUM; MODELS, BIOLOGICAL; ORGAN SPECIFICITY; PHYLOGENY; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RNA SPLICING; RNA, MESSENGER; SEEDS; TRANSCRIPTIONAL ACTIVATION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84962076609     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.00092     Document Type: Article

References (67)

1. Alonso R, Oñate-Sánchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Dröge-Laser W (2009) A pivotal role of the basic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based on heterodimerization and protein complex formation. Plant Cell 21: 1747-1761
2. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202-W208
3. Bassel GW, Mullen RT, Bewley JD (2006) ABI3 expression ceases following, but not during, germination of tomato and Arabidopsis seeds. J Exp Bot 57: 1291-1297
4. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30: 276-280
5. Bewley JD (1997) Seed germination and dormancy. Plant Cell 9: 1055-1066
6. Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13: 624-630
7. Casaretto J, Ho TH (2003) The transcription factors HvABI5 and HvVP1 are required for the abscisic acid induction of gene expression in barley aleurone cells. Plant Cell 15: 271-284
8. Diaz I, Martinez M, Isabel-LaMoneda I, Rubio-Somoza I, Carbonero P (2005) The DOF protein, SAD, interacts with GAMYB in plant nuclei and activates transcription of endosperm-specific genes during barley seed development. Plant J 42: 652-662
9. Diaz I, Vicente-Carbajosa J, Abraham Z, Martínez M, Isabel-La Moneda I, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J 29: 453-464
10. Druka A, Muehlbauer G, Druka I, Caldo R, Baumann U, Rostoks N, Schreiber A, Wise R, Close T, Kleinhofs A, et al (2006) An atlas of gene expression from seed to seed through barley development. Funct Integr Genomics 6: 202-211
11. Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171: 501-523
12. Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59: 387-415
13. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, WilkinsMR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In JK Walker, ed, The Proteomics Protocols Handbook. Humana Press, New York, pp 571-607
14. González-Calle V, Barrero-Sicilia C, Carbonero P, Iglesias-Fernández R (2015) Mannans and endo-b-mannanases (MAN) in Brachypodium distachyon: expression profiling and possible role of the BdMAN genes during coleorhiza-limited seed germination. J Exp Bot 66: 3753-3764
15. González-Calle V, Iglesias-Fernández R, Carbonero P, Barrero-Sicilia C (2014) The BdGAMYB protein from Brachypodium distachyon interacts with BdDOF24 and regulates transcription of the BdCathB gene upon seed germination. Planta 240: 539-552
16. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40: D1178-D1186
17. Graeber K, Linkies A, Müller K, Wunchova A, Rott A, Leubner-Metzger G (2010) Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol 73: 67-87
18. Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells: control of SLN1 and GAMYB expression. Plant Physiol 129: 191-200
19. Gubler F, Kalla R, Roberts JK, Jacobsen JV (1995) Gibberellin-regulated expression of a myb gene in barley aleurone cells: evidence for Myb transactivation of a high-pI a-amylase gene promoter. Plant Cell 7: 1879-1891
20. Gubler F, Millar AA, Jacobsen JV (2005) Dormancy release, ABA and preharvest sprouting. Curr Opin Plant Biol 8: 183-187
21. Gubler F, Raventos D, Keys M, Watts R, Mundy J, Jacobsen JV (1999) Target genes and regulatory domains of the GAMYB transcriptional activator in cereal aleurone. Plant J 17: 1-9
22. Hattori T, Vasil V, Rosenkrans L, Hannah LC, McCarty DR, Vasil IK (1992) The Viviparous-1 gene and abscisic acid activate the C1 regulatory gene for anthocyanin biosynthesis during seed maturation in maize. Genes Dev 6: 609-618
23. Hill A, Nantel A, Rock CD, Quatrano RS (1996) A conserved domain of the viviparous-1 gene product enhances the DNA binding activity of the bZIP protein EmBP-1 and other transcription factors. J Biol Chem 271: 3366-3374
24. Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96: 15348-15353
25. Hoecker U, Vasil IK, McCarty DR (1995) Integrated control of seed maturation and germination programs by activator and repressor functions of Viviparous-1 of maize. Genes Dev 9: 2459-2469
26. Hoecker U, Vasil IK, McCarty DR (1999) Signaling from the embryo conditions Vp1-mediated repression of alpha-amylase genes in the aleurone of developing maize seeds. Plant J 19: 371-377
27. Holdsworth MJ, Bentsink L, Soppe WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33-54
28. Iglesias-Fernández R, Rodríguez-Gacio MC, Barrero-Sicilia C, Carbonero P, Matilla A (2011a) Three endo-b-mannanase genes expressed in the micropylar endosperm and in the radicle influence germination of Arabidopsis thaliana seeds. Planta 233: 25-36
29. Iglesias-Fernández R, Rodríguez-Gacio MC, Matilla AJ (2011b) Progress in research on afterripening. Seed Sci Res 21: 69-80
30. Iglesias-Fernández R, Rodríguez-Gacio MdelC, Barrero-Sicilia C, Carbonero P, Matilla AJ (2011c) Molecular analysis of endo-b-mannanase genes upon seed imbibition suggest a cross-talk between radicle and micropylar endosperm during germination of Arabidopsis thaliana. Plant Signal Behav 6: 80-82
31. Iglesias-Fernández R, Wozny D, Iriondo-de Hond M, Oñate-Sánchez L, Carbonero P, Barrero-Sicilia C (2014) The AtCathB3 gene, encoding a cathepsin B-like protease, is expressed during germination of Arabidopsis thaliana and transcriptionally repressed by the basic leucine zipper protein GBF1. J Exp Bot 65: 2009-2021
32. Isabel-LaMoneda I, Diaz I, Martinez M, Mena M, Carbonero P (2003) SAD: a new DOF protein from barley that activates transcription of a cathepsin B-like thiol protease gene in the aleurone of germinating seeds. Plant J 33: 329-340
33. Jones HD, Peters NC, Holdsworth MJ (1997) Genotype and environment interact to control dormancy and differential expression of the VIVIPAROUS 1 homologue in embryos of Avena fatua. Plant J 12: 911-920
34. Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5: 33-36
35. Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Díaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278: 21003-21011
36. Marella HH, Quatrano RS (2007) The B2 domain of VIVIPAROUS1 is bifunctional and regulates nuclear localization and transactivation. Planta 225: 863-872
37. Matsumoto T, Tanaka T, Sakai H, Amano N, Kanamori H, Kurita K, Kikuta A, Kamiya K, Yamamoto M, Ikawa H, et al (2011) Comprehensive sequence analysis of 24, 783 barley full-length cDNAs derived from 12 clone libraries. Plant Physiol 156: 20-28
38. Mayer KF, Waugh R, Brown JW, Schulman A, Langridge P, Platzer M, Fincher GB, Muehlbauer GJ, Sato K, Close TJ, et al (2012) A physical, genetic and functional sequence assembly of the barley genome. Nature 491: 711-716
39. McCarty DR, Carson CB, Stinard PS, Robertson DS (1989) Molecular analysis of viviparous-1: an abscisic acid-insensitive mutant of maize. Plant Cell 1: 523-532
40. McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66: 895-905
41. Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellinresponsive genes in barley aleurone. Plant Physiol 130: 111-119
42. Mena M, Vicente-Carbajosa J, Schmidt RJ, Carbonero P (1998) An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native B-hordein promoter in barley endosperm. Plant J 16: 53-62
43. Moreno-Risueno MA, Díaz I, Carrillo L, Fuentes R, Carbonero P (2007) The HvDOF19 transcription factor mediates the abscisic acid-dependent repression of hydrolase genes in germinating barley aleurone. Plant J 51: 352-365
44. Moreno-Risueno MA, González N, Díaz I, Parcy F, Carbonero P, Vicente-Carbajosa J (2008) FUSCA3 from barley unveils a common transcriptional regulation of seed-specific genes between cereals and Arabidopsis. Plant J 53: 882-894
45. Nakamura S, Toyama T (2001) Isolation of a VP1 homologue from wheat and analysis of its expression in embryos of dormant and non-dormant cultivars. J Exp Bot 52: 875-876
46. Nambara E, Hayama R, Tsuchiya Y, NishimuraM, Kawaide H, Kamiya Y, Naito S (2000) The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 220: 412-423
47. Nonogaki H, Chen F, Bradford KJ (2007) Mechanisms and genes involved in germination sensu stricto. In K Bradford, H Nonogaki, eds, Seed Development, Dormancy and Germination. Blackwell Publishing, Oxford, pp 264-304
48. Oñate L, Vicente-Carbajosa J, Lara P, Díaz I, Carbonero P (1999) Barley BLZ2, a seed-specific bZIP protein that interacts with BLZ1 in vivo and activates transcription from the GCN4-like motif of B-hordein promoters in barley endosperm. J Biol Chem 274: 9175-9182
49. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, Giraudat J (1994) Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell 6: 1567-1582
50. Paz-Ares J, Wienand U, Peterson PA, Saedler H (1986) Molecular cloning of the c locus of Zea mays: a locus regulating the anthocyanin pathway. EMBO J 5: 829-833
51. Pritchard SL, Charlton WL, Baker A, Graham IA (2002) Germination and storage reserve mobilization are regulated independently in Arabidopsis. Plant J 31: 639-647
52. Reidt W, Wohlfarth T, Ellerström M, Czihal A, Tewes A, Ezcurra I, Rask L, Bäumlein H (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21: 401-408
53. Rodríguez MV, Barrero JM, Corbineau F, Gubler F, Benech-Arnold RL (2015) Dormancy in cereals (not too much, not so little): about the mechanisms behind this trait. Seed Sci Res 25: 99-119
54. Rubio-Somoza I, Martinez M, Abraham Z, Diaz I, Carbonero P (2006a) Ternary complex formation between HvMYBS3 and other factors involved in transcriptional control in barley seeds. Plant J 47: 269-281
55. Rubio-Somoza I, Martinez M, Diaz I, Carbonero P (2006b) HvMCB1, a R1MYB transcription factor from barley with antagonistic regulatory functions during seed development and germination. Plant J 45: 17-30
56. Sun TP, Gubler F (2004) Molecular mechanism of gibberellin signaling in plants. Annu Rev Plant Biol 55: 197-223
57. Suzuki M, Kao CY, Cocciolone S, McCarty DR (2001) Maize VP1 complements Arabidopsis abi3 and confers a novel ABA/auxin interaction in roots. Plant J 28: 409-418
58. Swaminathan K, Peterson K, Jack T (2008) The plant B3 superfamily. Trends Plant Sci 13: 647-655
59. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729
60. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680
61. To A, Valon C, Savino G, Guilleminot J, Devic M, Giraudat J, Parcy F (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18: 1642-1651
62. Vasil V, MarcotteWR Jr, Rosenkrans L, Cocciolone SM, Vasil IK, Quatrano RS, McCarty DR (1995) Overlap of Viviparous1 (VP1) and abscisic acid response elements in the Em promoter: G-box elements are sufficient but not necessary for VP1 transactivation. Plant Cell 7: 1511-1518
63. Vicente-Carbajosa J, Carbonero P (2005) Seed maturation: developing an intrusive phase to accomplish a quiescent state. Int J Dev Biol 49: 645-651
64. Vicente-Carbajosa J, Moose SP, Parsons RL, Schmidt RJ (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator Opaque2. Proc Natl Acad Sci USA 94: 7685-7690
65. Vicente-Carbajosa J, Oñate L, Lara P, Diaz I, Carbonero P (1998) Barley BLZ1: a bZIP transcriptional activator that interacts with endospermspecific gene promoters. Plant J 13: 629-640
66. Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55: 1521-1533
67. Zeng Y, Raimondi N, Kermode AR (2003) Role of an ABI3 homologue in dormancy maintenance of yellow-cedar seeds and in the activation of storage protein and Em gene promoters. Plant Mol Biol 51: 39-49