Interaction between Two Timing MicroRNAs Controls Trichome Distribution in
MicroRNAs are important aging regulators in many organisms. In Arabidopsis the miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) transcription factors play important roles as an endogenous age cue in programming phase transition and phase-dependent morphogenesis, including trichome patterning. However, how the timely increasing SPL output is modulated remains elusive. By dissecting the regulatory network controlling trichome formation on stem, we show that a group of GRAS family members, LOST MERISTEMS 1 (LOM1), LOM2 and LOM3, targeted by timing miR171, function in modulating the SPL activity through direct protein-protein interaction. LOMs promote trichome formation through attenuating the SPL (such as SPL9) activity of trichome repression. The LOM-SPL interaction affects many aspects of plant growth and development, including flowering, aging and chlorophyll biosynthesis. Interestingly, MIR171A gene expression is regulated by its own targets (LOMs), forming a feedback loop to program plant life. Our study establishes an age-dependent regulatory network composed of two timing miRNAs which act oppositely through direct interaction of their target proteins.
Vyšlo v časopise:
Interaction between Two Timing MicroRNAs Controls Trichome Distribution in. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004266
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004266
Souhrn
MicroRNAs are important aging regulators in many organisms. In Arabidopsis the miR156-targeted SQUAMOSA PROMOTER BINDING PROTEIN LIKE (SPL) transcription factors play important roles as an endogenous age cue in programming phase transition and phase-dependent morphogenesis, including trichome patterning. However, how the timely increasing SPL output is modulated remains elusive. By dissecting the regulatory network controlling trichome formation on stem, we show that a group of GRAS family members, LOST MERISTEMS 1 (LOM1), LOM2 and LOM3, targeted by timing miR171, function in modulating the SPL activity through direct protein-protein interaction. LOMs promote trichome formation through attenuating the SPL (such as SPL9) activity of trichome repression. The LOM-SPL interaction affects many aspects of plant growth and development, including flowering, aging and chlorophyll biosynthesis. Interestingly, MIR171A gene expression is regulated by its own targets (LOMs), forming a feedback loop to program plant life. Our study establishes an age-dependent regulatory network composed of two timing miRNAs which act oppositely through direct interaction of their target proteins.
Zdroje
1. LeeRC, FeinbaumRL, AmbrosV (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843–854.
2. WangJW, CzechB, WeigelD (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738–749.
3. WuG, ParkMY, ConwaySR, WangJW, WeigelD, et al. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750–759.
4. WuG, PoethigRS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539–3547.
5. YuS, GalvaoVC, ZhangYC, HorrerD, ZhangTQ, et al. (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24: 3320–3332.
6. LawsonEJ, PoethigRS (1995) Shoot development in plants: time for a change. Trends Genet 11: 263–268.
7. TelferA, BollmanKM, PoethigRS (1997) Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development 124: 645–654.
8. PayneCT, ZhangF, LloydAM (2000) GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156: 1349–1362.
9. PeschM, HulskampM (2004) Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Curr Opin Genet Dev 14: 422–427.
10. RamsayNA, GloverBJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10: 63–70.
11. RerieWG, FeldmannKA, MarksMD (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8: 1388–1399.
12. IshidaT, KurataT, OkadaK, WadaT (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59: 365–386.
13. EschJJ, ChenMA, HillestadM, MarksMD (2004) Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J 40: 860–869.
14. WadaT, TachibanaT, ShimuraY, OkadaK (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113–1116.
15. SchellmannS, SchnittgerA, KirikV, WadaT, OkadaK, et al. (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21: 5036–5046.
16. KirikV, SimonM, HuelskampM (2004) Schiefelbein J (2004) The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268: 506–513.
17. KirikV, SimonM, WesterK, SchiefelbeinJ, HulskampM (2004) ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol Biol 55: 389–398.
18. SimonM, LeeMM, LinY, GishL, SchiefelbeinJ (2007) Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 311: 566–578.
19. WangS, KwakSH, ZengQ, EllisBE, ChenXY, et al. (2007) TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873–3882.
20. GanL, XiaK, ChenJG, WangS (2011) Functional characterization of TRICHOMELESS2, a new single-repeat R3 MYB transcription factor in the regulation of trichome patterning in Arabidopsis. BMC Plant Biol 11: 176.
21. Tominaga-WadaR, NukumizuY (2012) Expression Analysis of an R3-Type MYB Transcription Factor CPC-LIKE MYB4 (TRICHOMELESS2) and CPL4-Related Transcripts in Arabidopsis. Int J Mol Sci 13: 3478–3491.
22. QiT, SongS, RenQ, WuD, HuangH, et al. (2011) The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23: 1795–1814.
23. YuN, CaiWJ, WangS, ShanCM, WangLJ, et al. (2010) Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22: 2322–2335.
24. StuurmanJ, JaggiF, KuhlemeierC (2002) Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes Dev 16: 2213–2218.
25. EngstromEM, AndersenCM, Gumulak-SmithJ, HuJ, OrlovaE, et al. (2011) Arabidopsis homologs of the Petunia HAIRY MERISTEM gene are required for maintenance of shoot and root indeterminacy. Plant Physiol 155: 735–750.
26. WangL, MaiYX, ZhangYC, LuoQ, YangHQ (2010) MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol Plant 3: 794–806.
27. LlaveC, XieZ, KasschauKD, CarringtonJC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297: 2053–2056.
28. RhoadesMW, ReinhartBJ, LimLP, BurgeCB, BartelB, et al. (2002) Prediction of plant microRNA targets. Cell 110: 513–520.
29. SchulzeS, SchaferBN, ParizottoEA, VoinnetO, TheresK (2010) LOST MERISTEMS genes regulate cell differentiation of central zone descendants in Arabidopsis shoot meristems. Plant J 64: 668–678.
30. GanY, KumimotoR, LiuC, RatcliffeO, YuH, et al. (2006) GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18: 1383–1395.
31. ZhouZ, AnL, SunL, GanY (2012) ZFP5 encodes a functionally equivalent GIS protein to control trichome initiation. Plant Signal Behav 7: 28–30.
32. ZhouZ, SunL, ZhaoY, AnL, YanA, et al. (2013) Zinc Finger Protein 6 (ZFP6) regulates trichome initiation by integrating gibberellin and cytokinin signaling in Arabidopsis thaliana. New Phytol 198: 699–708.
33. EngstromEM (2011) Phylogenetic analysis of GRAS proteins from moss, lycophyte and vascular plant lineages reveals that GRAS genes arose and underwent substantial diversification in the ancestral lineage common to bryophytes and vascular plants. Plant Signal Behav 6: 850–854.
34. ShikataM, KoyamaT, MitsudaN, Ohme-TakagiM (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50: 2133–2145.
35. Smith-VikosT, SlackFJ (2012) MicroRNAs and their roles in aging. Journal of Cell Science 125: 7–17.
36. de LencastreA, PincusZ, ZhouK, KatoM, LeeSS, et al. (2010) MicroRNAs both promote and antagonize longevity in C. elegans. Curr Biol 20: 2159–2168.
37. MuraseK, HiranoY, SunTP, HakoshimaT (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459–463.
38. GriffithsJ, MuraseK, RieuI, ZentellaR, ZhangZL, et al. (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399–3414.
39. SunTP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21: R338–345.
40. LiuHH, TianX, LiYJ, WuCA, ZhengCC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14: 836–843.
41. ZhouL, LiuY, LiuZ, KongD, DuanM, et al. (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61: 4157–4168.
42. ZhaoM, TaiH, SunS, ZhangF, XuY, et al. (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS One 7: e29669.
43. LiangG, HeH, YuD (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7: e48951.
44. ManavellaPA, KoenigD, Rubio-SomozaI, BurbanoHA, BeckerC, et al. (2013) Tissue-specific silencing of Arabidopsis SU(VAR)3-9 HOMOLOG8 by miR171a. Plant Physiol 161: 805–812.
45. AxtellMJ, SnyderJA, BartelDP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19: 1750–1769.
46. MiuraK, IkedaM, MatsubaraA, SongXJ, ItoM, et al. (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42: 545–549.
47. JiaoY, WangY, XueD, WangJ, YanM, et al. (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42: 541–544.
48. WangK, WangZ, LiF, YeW, WangJ, et al. (2012) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44: 1098–1103.
49. CurabaJ, TalbotM, LiZ, HelliwellC (2013) Over-expression of microRNA171 affects phase transitions and floral meristem determinancy in barley. BMC Plant Biol 13: 6.
50. WangJW, SchwabR, CzechB, MicaE, WeigelD (2008) Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20: 1231–1243.
51. GouJY, FelippesFF, LiuCJ, WeigelD, WangJW (2011) Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell 23: 1512–1522.
52. ChenH, ZouY, ShangY, LinH, WangY, et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368–376.
53. PappI, MetteMF, AufsatzW, DaxingerL, SchauerSE, et al. (2003) Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol 132: 1382–1390.
54. HongGJ, XueXY, MaoYB, WangLJ, ChenXY (2012) Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635–2648.
55. BanerjeeR, SchleicherE, MeierS, VianaRM, PokornyR, et al. (2007) The signaling state of Arabidopsis cryptochrome 2 contains flavin semiquinone. J Biol Chem 282: 14916–14922.
56. ArnonDI (1949) Copper enzymes in isolated chloroplasts: Polyphenol oxidase in Beta vulgaris. Plant Physiol 24: 1–15.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 4
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- The Sequence-Specific Transcription Factor c-Jun Targets Cockayne Syndrome Protein B to Regulate Transcription and Chromatin Structure
- Genetic Predisposition to In Situ and Invasive Lobular Carcinoma of the Breast
- Widespread Use of Non-productive Alternative Splice Sites in
- RNA Editome in Rhesus Macaque Shaped by Purifying Selection