MicroRNA–Mediated Repression of the Seed Maturation Program during Vegetative Development in
The seed maturation program only occurs during late embryogenesis, and repression of the program is pivotal for seedling development. However, the mechanism through which this repression is achieved in vegetative tissues is poorly understood. Here we report a microRNA (miRNA)–mediated repression mechanism operating in leaves. To understand the repression of the embryonic program in seedlings, we have conducted a genetic screen using a seed maturation gene reporter transgenic line in Arabidopsis (Arabidopsis thaliana) for the isolation of mutants that ectopically express seed maturation genes in leaves. One of the mutants identified from the screen is a weak allele of ARGONAUTE1 (AGO1) that encodes an effector protein for small RNAs. We first show that it is the defect in the accumulation of miRNAs rather than other small RNAs that causes the ectopic seed gene expression in ago1. We then demonstrate that overexpression of miR166 suppresses the derepression of the seed gene reporter in ago1 and that, conversely, the specific loss of miR166 causes ectopic expression of seed maturation genes. Further, we show that ectopic expression of miR166 targets, type III homeodomain-leucine zipper (HD-ZIPIII) genes PHABULOSA (PHB) and PHAVOLUTA (PHV), is sufficient to activate seed maturation genes in vegetative tissues. Lastly, we show that PHB binds the promoter of LEAFY COTYLEDON2 (LEC2), which encodes a master regulator of seed maturation. Therefore, this study establishes a core module composed of a miRNA, its target genes (PHB and PHV), and the direct target of PHB (LEC2) as an underlying mechanism that keeps the seed maturation program off during vegetative development.
Vyšlo v časopise:
MicroRNA–Mediated Repression of the Seed Maturation Program during Vegetative Development in. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003091
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003091
Souhrn
The seed maturation program only occurs during late embryogenesis, and repression of the program is pivotal for seedling development. However, the mechanism through which this repression is achieved in vegetative tissues is poorly understood. Here we report a microRNA (miRNA)–mediated repression mechanism operating in leaves. To understand the repression of the embryonic program in seedlings, we have conducted a genetic screen using a seed maturation gene reporter transgenic line in Arabidopsis (Arabidopsis thaliana) for the isolation of mutants that ectopically express seed maturation genes in leaves. One of the mutants identified from the screen is a weak allele of ARGONAUTE1 (AGO1) that encodes an effector protein for small RNAs. We first show that it is the defect in the accumulation of miRNAs rather than other small RNAs that causes the ectopic seed gene expression in ago1. We then demonstrate that overexpression of miR166 suppresses the derepression of the seed gene reporter in ago1 and that, conversely, the specific loss of miR166 causes ectopic expression of seed maturation genes. Further, we show that ectopic expression of miR166 targets, type III homeodomain-leucine zipper (HD-ZIPIII) genes PHABULOSA (PHB) and PHAVOLUTA (PHV), is sufficient to activate seed maturation genes in vegetative tissues. Lastly, we show that PHB binds the promoter of LEAFY COTYLEDON2 (LEC2), which encodes a master regulator of seed maturation. Therefore, this study establishes a core module composed of a miRNA, its target genes (PHB and PHV), and the direct target of PHB (LEC2) as an underlying mechanism that keeps the seed maturation program off during vegetative development.
Zdroje
1. Vicente-CarbajosaJ, CarboneroP (2005) Seed maturation: Developing an intrusive phase to accomplish a quiescent state. Int J Dev Biol 49: 645–651.
2. ZhangH, OgasJ (2009) An epigenetic perspective on developmental regulation of seed genes. Mol Plant 2: 610–627.
3. HendersonJT, LiHC, RiderSD, MordhorstAP, Romero-SeversonJ, 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. LiHC, ChuangK, HendersonJT, RiderSDJr, BaiY, et al. (2005) PICKLE acts during germination to repress expression of embryonic traits. Plant J 44: 1010–1022.
5. TangX, HouA, BabuM, NguyenV, HurtadoL, 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. MoonYH, ChenL, PanRL, ChangHS, ZhuT, et al. (2003) EMF genes maintain vegetative development by repressing the flower program in Arabidopsis. Plant Cell 15: 681–693.
7. ChanvivattanaY, BishoppA, SchubertD, StockC, MoonYH, et al. (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131: 5263–5276.
8. SchubertD, ClarenzO, GoodrichJ (2005) Epigenetic control of plant development by Polycomb-group proteins. Curr Opin Plant Biol 8: 553–561.
9. MakarevichG, LeroyO, AkinciU, SchubertD, ClarenzO, et al. (2006) Different Polycomb group complexes regulate common target genes in Arabidopsis. Embo Rep 7: 947–952.
10. TanakaM, KikuchiA, KamadaH (2008) The Arabidopsis Histone Deacetylases HDA6 and HDA19 Contribute to the Repression of Embryonic Properties after Germination. Plant Physiol 146: 149–161.
11. TsukagoshiH, MorikamiA, NakamuraK (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. SuzukiM, WangHH, McCartyDR (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. GaoMJ, LydiateDJ, LiX, LuiH, GjetvajB, et al. (2009) Repression of seed maturation genes by a trihelix transcriptional repressor in Arabidopsis seedlings. Plant Cell 21: 54–71.
14. GiraudatJ, HaugeBM, ValonC, SmalleJ, ParcyF, et al. (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4: 1251–1261.
15. LotanT, OhtoM, YeeKM, WestMA, LoR, et al. (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93: 1195–1205.
16. LuerssenH, KirikV, HerrmannP, MiseraS (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. StoneSL, KwongLW, YeeKM, PelletierJ, LepiniecL, et al. (2001) LEAFY COTYLEDON2 encodes a B3 domain transcription factor that induces embryo development. Proc Natl Acad Sci USA 98: 11806–11811.
18. KagayaY, ToyoshimaR, OkudaR, UsuiH, YamamotoA, 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. ToA, ValonC, SavinoG, GuilleminotJ, DevicM, et al. (2006) A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell 18: 1642–1651.
20. ParcyF, ValonC, RaynalM, Gaubier-ComellaP, DelsenyM, 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. GazzarriniS, TsuchiyaY, LumbaS, OkamotoM, McCourtP (2004) The transcription factor FUSCA3 controls developmental timing in Arabidopsis through the hormones gibberellin and abscisic acid. Dev Cell 7: 373–385.
22. Santos MendozaM, DubreucqB, MiquelM, CabocheM, LepiniecL (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-RhoadesMW, BartelDP, BartelB (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19–53.
24. RamachandranV, ChenX (2008) Small RNA metabolism in Arabidopsis. Trends Plant Sci 13: 368–374.
25. ChenX (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: 21–44.
26. VoinnetO (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669–687.
27. LuQ, TangX, TianG, WangF, LiuK, et al. (2010) Arabidopsis homolog of the yeast TREX-2 mRNA export complex: components and anchoring nucleoporin. Plant J 61: 259–270.
28. TangX, LimM-H, PelletierJ, TangM, NguyenV, KellerWA, TsangEWT, WangA, RothsteinSJ, HaradaJJ, CuiY (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. VaucheretH (2008) Plant ARGONAUTES. Trends Plant Sci 13: 350–358.
30. BohmertK, CamusI, BelliniC, BouchezD, CabocheM, et al. (1998) AGO1 defines a novel locus of Arabidopsis controlling leaf development. Embo J 17: 170–180.
31. KidnerCA, MartienssenRA (2004) Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428: 81–84.
32. YangL, HuangW, WangH, CaiR, XuY, 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. MorelJB, GodonC, MourrainP, BéclinC, BoutetS, et al. (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14: 629–39.
34. BaumbergerN, BaulcombeDC (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. VaucheretH, VazquezF, CrétéP, BartelDP (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. VaucheretH, MalloryAC, BartelDP (2006) AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Mol Cell 22: 129–136.
37. TelferA, PoethigRS (1998) HASTY: a gene that regulates the timing of shoot maturation in Arabidopsis thaliana. Development 125: 1889–1898.
38. VaucheretH (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20: 759–771.
39. PeragineA, YoshikawaM, WuG, AlbrechtHL, PoethigRS (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. ZhouGK, KuboM, ZhongR, DemuraT, YeZH (2007) Overexpression of miR165 affects apical meristem formation, organ polarity establishment and vascular development in Arabidopsis. Plant Cell Physiol 48: 391–404.
41. YanJ, GuY, JiaX, KangW, PanS, et al. (2012) Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24: 415–427.
42. EmeryJF, FloydSK, AlvarezJ, EshedY, HawkerNP, et al. (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768–1774.
43. MalloryAC, ReinhartBJ, Jones-RhoadesMW, TangG, ZamorePD, et al. (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. Embo J 23: 3356–3364.
44. McConnellJR, EmeryJ, EshedY, BaoN, BowmanJ, et al. (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411: 709–713.
45. JuarezMT, KuiJS, ThomasJ, HellerBA, TimmermansMC (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428: 84–88.
46. PriggeMJ, OtsugaD, AlonsoJM, EckerJR, DrewsGN, 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. McConnellJR, BartonMK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125: 2935–2942.
48. SchenaM, DavisRW (1992) HD-Zip proteins: members of an Arabidopsis homeodomain protein superfamily. Proc Natl Acad Sci USA 89: 3894–3898.
49. SessaG, SteindlerC, MorelliG, RubertiI (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. KidnerCA, TimmermansMC (2007) Mixing and matching pathways in leaf polarity. Curr Opin Plant Biol 10: 13–20.
51. PulidoA, LaufsP (2010) Co-ordination of developmental processes by small RNAs during leaf development. J Exp Bot 61: 1277–1291.
52. BraybrookSA, HaradaJJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13: 624–630.
53. NodineMD, BartelDP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24: 2678–2692.
54. WillmannMR, MehalickAJ, PackerRL, JenikPD (2011) MicroRNAs Regulate the Timing of Embryo Maturation in Arabidopsis. Plant Physiol 155: 1871–1884.
55. GriggSP, GalinhaC, KornetN, CanalesC, ScheresB, TsiantisM (2009) Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr Biol 19: 1485–1490.
56. SmithZR, LongJA (2010) Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464: 423–426.
57. BratzelF, López-TorrejónG, KochM, Del PozoJC, CalonjeM (2010) Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr Biol 20: 1853–1859.
58. PangPP, PruittRE, MeyerowitzEM (1988) Molecular cloning, genomic organization, expression and evolution of 12S seed storage protein genes of Arabidopis thaliana. Plant Mol Biol 11: 805–820.
59. ParkW, LiJ, SongR, MessingJ, ChenX (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12: 1484–1495.
60. PallGS, Codony-ServatC, ByrneJ, RitchieL, HamiltonA (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. EarleyKW, HaagJR, PontesO, OpperK, JuehneT, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616–629.
62. GendrelAV, LippmanZ, MartienssenR, ColotV (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2: 213–218.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 11
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