MicroRNA-Mediated Repression of the Seed Maturation Program during Vegetative Development in Arabidopsis

PLoS Genetics

Volumn 8, Issue 11, 2012, Pages

  Tang, Xurong ^a,b,c   Bian, Shaomin ^a,d   Tang, Mingjuan ^a   Lu, Qing ^a   Li, Shengben ^e   Liu, Xigang ^e   Tian, Gang ^a,d   Nguyen, Vi ^a   Tsang, Edward W T ^b   Wang, Aiming ^a   Rothstein, Steven J ^c   Chen, Xuemei ^e   Cui, Yuhai ^a,d  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 1 PROTEIN; MICRORNA; MICRORNA 166; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ALLELE; ARABIDOPSIS; ARGONAUTE 1 GENE; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; GENE FUNCTION; GENE INTERACTION; GENE ISOLATION; GENE LOSS; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC CODE; GENETIC SCREENING; PHABULOSA GENE; PHAVOLUTA GENE; PLANT GENE; PLANT LEAF; REPORTER GENE; SEED DEVELOPMENT; TRANSGENIC PLANT; VEGETATIVE GROWTH;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ARGONAUTE PROTEINS; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; HOMEODOMAIN PROTEINS; MICRORNAS; PLANT LEAVES; SEEDS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; PROSPECT HILL VIRUS;

EID: 84870664436     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003091     Document Type: Article

References (62)

1. Vicente-Carbajosa J, Carbonero P, (2005) Seed maturation: Developing an intrusive phase to accomplish a quiescent state. Int J Dev Biol 49: 645-651.
2. Zhang H, Ogas J, (2009) An epigenetic perspective on developmental regulation of seed genes. Mol Plant 2: 610-627.
3. Henderson JT, Li HC, Rider SD, Mordhorst AP, Romero-Severson J, et al. (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134: 995-1005.
4. Li HC, Chuang K, Henderson JT, Rider SD Jr, Bai Y, et al. (2005) PICKLE acts during germination to repress expression of embryonic traits. Plant J 44: 1010-1022.
5. Tang X, Hou A, Babu M, Nguyen V, Hurtado L, et al. (2008) The Arabidopsis BRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves. Plant Physiol 147: 1143-1157.
6. Moon YH, Chen L, Pan RL, Chang HS, Zhu T, et al. (2003) EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15: 681-693.
7. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, et al. (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263-5276.
8. Schubert D, Clarenz O, Goodrich J, (2005) Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8: 553-561.
9. Makarevich G, Leroy O, Akinci U, Schubert D, Clarenz O, et al. (2006) Different Polycomb group complexes regulate common target genes in Arabidopsis. Embo Rep 7: 947-952.
10. Tanaka M, Kikuchi A, Kamada H, (2008) The Arabidopsis Histone Deacetylases HDA6 and HDA19 Contribute to the Repression of Embryonic Properties after Germination. Plant Physiol 146: 149-161.
11. Tsukagoshi H, Morikami A, Nakamura K, (2007) Two B3 domain transcriptional repressors prevent sugar-inducible expression of seed maturation genes in Arabidopsis seedlings. Proc Natl Acad Sci USA 104: 2543-2547.
12. Suzuki M, Wang HH, McCarty DR, (2007) Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes. Plant Physiol 143: 902-911.
13. Gao MJ, Lydiate DJ, Li X, Lui H, Gjetvaj B, et al. (2009) Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell 21: 54-71.
14. Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, et al. (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251-1261.
15. Lotan T, Ohto M, Yee KM, West MA, Lo R, et al. (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195-1205.
16. Luerssen H, Kirik V, Herrmann P, Misera S, (1998) FUSCA3 encodes a protein with a conserved VP1/AB13-like B3 domain which is of functional importance for the regulation of seed maturation in Arabidopsis thaliana. Plant J 15: 755-764.
17. Stone SL, Kwong LW, Yee KM, Pelletier J, Lepiniec L, et al. (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98: 11806-11811.
18. Kagaya Y, Toyoshima R, Okuda R, Usui H, Yamamoto A, et al. (2005) LEAFY COTYLEDON1 controls seed storage protein genes through its regulation of FUSCA3 and ABSCISIC ACID INSENSITIVE3. Plant Cell Physiol 46: 399-406.
19. To A, Valon C, Savino G, Guilleminot J, Devic M, et al. (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18: 1642-1651.
20. Parcy F, Valon C, Raynal M, Gaubier-Comella P, Delseny M, et al. (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.
21. Gazzarrini S, Tsuchiya Y, Lumba S, Okamoto M, McCourt P, (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7: 373-385.
22. Santos Mendoza M, Dubreucq B, Miquel M, Caboche M, Lepiniec L, (2005) LEAFY COTYLEDON 2 activation is sufficient to trigger the accumulation of oil and seed specific mRNAs in Arabidopsis leaves. FEBS Lett 579: 4666-4670.
23. Jones-Rhoades MW, Bartel DP, Bartel B, (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53.
24. Ramachandran V, Chen X, (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci 13: 368-374.
25. Chen X, (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: 21-44.
26. Voinnet O, (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
27. Lu Q, Tang X, Tian G, Wang F, Liu K, et al. (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61: 259-270.
28. Tang X, Lim M-H, Pelletier J, Tang M, Nguyen V, Keller WA, Tsang EWT, Wang A, Rothstein SJ, Harada JJ, Cui Y, (2012) Synergistic Repression of the Embryonic Program by SET DOMAIN GROUP 8 and EMBRYONIC FLOWER 2 in Arabidopsis Seedlings. J Exp Bot 63: 1391-1404.
29. Vaucheret H, (2008) Plant ARGONAUTES. Trends Plant Sci 13: 350-358.
30. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, et al. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. Embo J 17: 170-180.
31. Kidner CA, Martienssen RA, (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428: 81-84.
32. Yang L, Huang W, Wang H, Cai R, Xu Y, et al. (2006) Characterizations of a hypomorphic argonaute1 mutant reveal novel AGO1 functions in Arabidopsis lateral organ development. Plant Mol Biol 61: 63-78.
33. Morel JB, Godon C, Mourrain P, Béclin C, Boutet S, et al. (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629-39.
34. Baumberger N, Baulcombe DC, (2005) Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci U S A 102: 11928-11933.
35. Vaucheret H, Vazquez F, Crété P, Bartel DP, (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18: 1187-1197.
36. Vaucheret H, Mallory AC, Bartel DP, (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22: 129-136.
37. Telfer A, Poethig RS, (1998) HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development 125: 1889-1898.
38. Vaucheret H, (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20: 759-771.
39. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS, (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18: 2368-2379.
40. Zhou GK, Kubo M, Zhong R, Demura T, Ye ZH, (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48: 391-404.
41. Yan J, Gu Y, Jia X, Kang W, Pan S, et al. (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24: 415-427.
42. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, et al. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768-1774.
43. Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. Embo J 23: 3356-3364.
44. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, et al. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709-713.
45. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC, (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428: 84-88.
46. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, et al. (2005) Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17: 61-76.
47. McConnell JR, Barton MK, (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935-2942.
48. Schena M, Davis RW, (1992) HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89: 3894-3898.
49. Sessa G, Steindler C, Morelli G, Ruberti I, (1998) The Arabidopsis Athb-8,-9 and-14 genes are members of a small gene family coding for highly related HD-ZIP proteins. Plant Mol Biol 38: 609-622.
50. Kidner CA, Timmermans MC, (2007) Mixing and matching pathways in leaf polarity. Curr Opin Plant Biol 10: 13-20.
51. Pulido A, Laufs P, (2010) Co-ordination of developmental processes by small RNAs during leaf development. J Exp Bot 61: 1277-1291.
52. Braybrook SA, Harada JJ, (2008) LECs go crazy in embryo development. Trends Plant Sci 13: 624-630.
53. Nodine MD, Bartel DP, (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24: 2678-2692.
54. Willmann MR, Mehalick AJ, Packer RL, Jenik PD, (2011) MicroRNAs Regulate the Timing of Embryo Maturation in Arabidopsis. Plant Physiol 155: 1871-1884.
55. Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, Tsiantis M, (2009) Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr Biol 19: 1485-1490.
56. Smith ZR, Long JA, (2010) Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464: 423-426.
57. Bratzel F, López-Torrejón G, Koch M, Del Pozo JC, Calonje M, (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20: 1853-1859.
58. Pang PP, Pruitt RE, Meyerowitz EM, (1988) Molecular cloning, genomic organization, expression and evolution of 12S seed storage protein genes of Arabidopis thaliana. Plant Mol Biol 11: 805-820.
59. Park W, Li J, Song R, Messing J, Chen X, (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12: 1484-1495.
60. Pall GS, Codony-Servat C, Byrne J, Ritchie L, Hamilton A, (2007) Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res 35: e60.
61. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629.
62. Gendrel AV, Lippman Z, Martienssen R, Colot V, (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2: 213-218.