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Coordination of Flower Maturation by a Regulatory Circuit of Three MicroRNAs


The development of multicellular organisms relies on interconnected genetic programs that control progression through their life cycle. MicroRNAs (miRNAs) and transcription factors (TFs) play key roles in such regulatory circuits. Here, we describe how three evolutionary conserved miRNA-TF pairs interact to form multiple checkpoints during reproductive development of Arabidopsis thaliana. Genetic, cellular, and physiological experiments show that miR159- and miR319-regulated MYB and TCP transcription factors pattern the expression of miR167 family members and their ARF6/8 targets. Coordinated action of these miRNA-TF pairs is crucial for the execution of consecutive hormone-dependent transitions during flower maturation. Cross-regulation includes both cis- and trans-regulatory interactions between these miRNAs and their targets. Our observations reveal how different miRNA-TF pairs can be organized into modules that coordinate successive steps in the plant life cycle.


Vyšlo v časopise: Coordination of Flower Maturation by a Regulatory Circuit of Three MicroRNAs. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003374
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003374

Souhrn

The development of multicellular organisms relies on interconnected genetic programs that control progression through their life cycle. MicroRNAs (miRNAs) and transcription factors (TFs) play key roles in such regulatory circuits. Here, we describe how three evolutionary conserved miRNA-TF pairs interact to form multiple checkpoints during reproductive development of Arabidopsis thaliana. Genetic, cellular, and physiological experiments show that miR159- and miR319-regulated MYB and TCP transcription factors pattern the expression of miR167 family members and their ARF6/8 targets. Coordinated action of these miRNA-TF pairs is crucial for the execution of consecutive hormone-dependent transitions during flower maturation. Cross-regulation includes both cis- and trans-regulatory interactions between these miRNAs and their targets. Our observations reveal how different miRNA-TF pairs can be organized into modules that coordinate successive steps in the plant life cycle.


Zdroje

1. WuMF, TianQ, ReedJW (2006) Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211–4218.

2. TabataR, IkezakiM, FujibeT, AidaM, TianCE, et al. (2010) Arabidopsis AUXIN RESPONSE FACTOR6 and 8 regulate jasmonic acid biosynthesis and floral organ development via repression of class 1 KNOX genes. Plant Cell Physiol 51: 164–175.

3. RuP, XuL, MaH, HuangH (2006) Plant fertility defects induced by the enhanced expression of microRNA167. Cell Res 16: 457–465.

4. NagpalP, EllisCM, WeberH, PloenseSE, BarkawiLS, et al. (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132: 4107–4118.

5. TodescoM, Rubio-SomozaI, Paz-AresJ, WeigelD (2010) A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet 6: e1001031 doi:10.1371/journal.pgen.1001031.

6. ReevesPH, EllisCM, PloenseSE, WuMF, YadavV, et al. (2012) A regulatory network for coordinated flower maturation. PLoS Genet 8: e1002506 doi:10.1371/journal.pgen.1002506.

7. WenCK, ChangC (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14: 87–100.

8. 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.

9. ChengY, DaiX, ZhaoY (2006) Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes Dev 20: 1790–1799.

10. FengXL, NiWM, ElgeS, Mueller-RoeberB, XuZH, et al. (2006) Auxin flow in anther filaments is critical for pollen grain development through regulating pollen mitosis. Plant Mol Biol 61: 215–226.

11. CecchettiV, AltamuraMM, FalascaG, CostantinoP, CardarelliM (2008) Auxin regulates Arabidopsis anther dehiscence, pollen maturation, and filament elongation. Plant Cell 20: 1760–1774.

12. ScofieldS, DewitteW, MurrayJA (2007) The KNOX gene SHOOT MERISTEMLESS is required for the development of reproductive meristematic tissues in Arabidopsis. Plant J 50: 767–781.

13. OriN, EshedY, ChuckG, BowmanJL, HakeS (2000) Mechanisms that control KNOX gene expression in the Arabidopsis shoot. Development 127: 5523–5532.

14. PautotV, DockxJ, HamantO, KronenbergerJ, GrandjeanO, et al. (2001) KNAT2: evidence for a link between knotted-like genes and carpel development. Plant Cell 13: 1719–1734.

15. AchardP, HerrA, BaulcombeDC, HarberdNP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131: 3357–3365.

16. MillarAA, GublerF (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17: 705–721.

17. PalatnikJF, AllenE, WuX, SchommerC, SchwabR, et al. (2003) Control of leaf morphogenesis by microRNAs. Nature 425: 257–263.

18. RhoadesMW, ReinhartBJ, LimLP, BurgeCB, BartelB, et al. (2002) Prediction of plant microRNA targets. Cell 110: 513–520.

19. AllenRS, LiJ, StahleMI, DubroueA, GublerF, et al. (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci USA 104: 16371–16376.

20. AllenRS, LiJ, Alonso-PeralMM, WhiteRG, GublerF, et al. (2010) MicroR159 regulation of most conserved targets in Arabidopsis has negligible phenotypic effects. Silence 1: 18.

21. LiuQ, ZhangYC, WangCY, LuoYC, HuangQJ, et al. (2009) Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett 583: 723–728.

22. WarthmannN, DasS, LanzC, WeigelD (2008) Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae. Mol Biol Evol 25: 892–902.

23. NagA, KingS, JackT (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106: 22534–22539.

24. SawchukMG, HeadP, DonnerTJ, ScarpellaE (2007) Time-lapse imaging of Arabidopsis leaf development shows dynamic patterns of procambium formation. New Phytol 176: 560–571.

25. PalatnikJF, WollmannH, SchommerC, SchwabR, BoisbouvierJ, et al. (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13: 115–125.

26. JackT, FoxGL, MeyerowitzEM (1994) Arabidopsis homeotic gene APETALA3 ectopic expression: transcriptional and posttranscriptional regulation determine floral organ identity. Cell 76: 703–716.

27. WolbangCM, ChandlerPM, SmithJJ, RossJJ (2004) Auxin from the developing inflorescence is required for the biosynthesis of active gibberellins in barley stems. Plant Physiol 134: 769–776.

28. ChengH, SongS, XiaoL, SooHM, ChengZ, et al. (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet 5: e1000440 doi:10.1371/journal.pgen.1000440.

29. LiXG, SuYH, ZhaoXY, LiW, GaoXQ, et al. (2010) Cytokinin overproduction-caused alteration of flower development is partially mediated by CUC2 and CUC3 in Arabidopsis. Gene 450: 109–120.

30. BartrinaI, OttoE, StrnadM, WernerT, SchmüllingT (2011) Cytokinin regulates the activity of reproductive meristems, flower organ size, ovule formation, and, thus, seed yield in Arabidopsis thaliana. Plant Cell tpc.110.079079.

31. SchommerC, PalatnikJF, AggarwalP, ChetelatA, CubasP, et al. (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biol 6: e230 doi:10.1371/journal.pbio.0060230.

32. FeysB, BenedettiCE, PenfoldCN, TurnerJG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6: 751–759.

33. StintziA, BrowseJ (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97: 10625–10630.

34. CaldelariD, WangG, FarmerEE, DongX (2010) Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol Biol 75: 25–33.

35. BrioudesF, JolyC, SzécsiJ, VaraudE, LerouxJ, et al. (2009) Jasmonate controls late development stages of petal growth in Arabidopsis thaliana. Plant J 60: 1070–1080.

36. SehrEM, AgustiJ, LehnerR, FarmerEE, SchwarzM, et al. (2010) Analysis of secondary growth in the Arabidopsis shoot reveals a positive role of jasmonate signalling in cambium formation. Plant J 63: 811–822.

37. BellE, CreelmanRA, MulletJE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci USA 92: 8675–8679.

38. JensenAB, RaventosD, MundyJ (2002) Fusion genetic analysis of jasmonate-signalling mutants in Arabidopsis. Plant J 29: 595–606.

39. SchmidM, DavisonTS, HenzSR, PapeUJ, DemarM, et al. (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37: 501–506.

40. BrodersenP, Sakvarelidze-AchardL, Bruun-RasmussenM, DunoyerP, YamamotoYY, et al. (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185–1190.

41. SmaczniakC, ImminkRG, MuinoJM, BlanvillainR, BusscherM, et al. (2012) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A 109: 1560–1565.

42. ValocziA, VarallyayE, KauppinenS, BurgyanJ, HaveldaZ (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47: 140–151.

43. CubasP, LauterN, DoebleyJ, CoenE (1999) The TCP domain: a motif found in proteins regulating plant growth and development. Plant J 18: 215–222.

44. KosugiS, OhashiY (2002) DNA binding and dimerization specificity and potential targets for the TCP protein family. Plant J 30: 337–348.

45. AggarwalP, Das GuptaM, JosephAP, ChatterjeeN, SrinivasanN, et al. (2010) Identification of specific DNA binding residues in the TCP family of transcription factors in Arabidopsis. Plant Cell 22: 1174–1189.

46. Martin-TrilloM, CubasP (2010) TCP genes: a family snapshot ten years later. Trends Plant Sci 15: 31–39.

47. Rubio-SomozaI, CuperusJT, WeigelD, CarringtonJC (2009) Regulation and functional specialization of small RNA-target nodes during plant development. Curr Opin Plant Biol 12: 622–627.

48. Rubio-SomozaI, WeigelD (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16: 258–264.

49. TaoY, FerrerJL, LjungK, PojerF, HongF, et al. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133: 164–176.

50. StepanovaAN, Robertson-HoytJ, YunJ, BenaventeLM, XieDY, et al. (2008) TAA1-mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133: 177–191.

51. ZhaoZ, AndersenSU, LjungK, DolezalK, MiotkA, et al. (2010) Hormonal control of the shoot stem-cell niche. Nature 465: 1089–1092.

52. JasinskiS, PiazzaP, CraftJ, HayA, WoolleyL, et al. (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 15: 1560–1565.

53. FleishonS, ShaniE, OriN, WeissD (2011) Negative reciprocal interactions between gibberellin and cytokinin in tomato. New Phytol 190: 609–617.

54. PengJ (2009) Gibberellin and jasmonate crosstalk during stamen development. J Integr Plant Biol 51: 1064–1070.

55. HardtkeCS, BerlethT (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17: 1405–1411.

56. DonnerTJ, SherrI, ScarpellaE (2010) Auxin signal transduction in Arabidopsis vein formation. Plant Signal Behav 5: 70–72.

57. DettmerJ, EloA, HelariuttaY (2009) Hormone interactions during vascular development. Plant Mol Biol 69: 347–360.

58. ChenKY, CongB, WingR, VrebalovJ, TanksleySD (2007) Changes in regulation of a transcription factor lead to autogamy in cultivated tomatoes. Science 318: 643–645.

59. PengP, ChanSW, ShahGA, JacobsenSE (2006) Plant genetics: increased outcrossing in hothead mutants. Nature 443: E8 discussion E8-9.

60. TantikanjanaT, NasrallahJB (2012) Non-cell-autonomous regulation of crucifer self-incompatibility by Auxin Response Factor ARF3. Proc Natl Acad Sci U S A 109: 19468–19473.

61. VenglatSP, DumonceauxT, RozwadowskiK, ParnellL, BabicV, et al. (2002) The homeobox gene BREVIPEDICELLUS is a key regulator of inflorescence architecture in Arabidopsis. Proc Natl Acad Sci USA 99: 4730–4735.

62. OdellJT, NagyF, ChuaN-H (1985) Identification of DNA-sequences required for activity of the cauliflower mosaic virus-35S promoter. Nature 313: 810–812.

63. Weigel D, Glazebrook J (2002) Arabidopsis: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. 354 p.

64. WollmannH, MicaE, TodescoM, LongJA, WeigelD (2010) On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development. Development 137: 3633–3642.

65. WangJW, CzechB, WeigelD (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138: 738–749.

66. BlázquezMA, SoowalLN, LeeI, WeigelD (1997) LEAFY expression and flower initiation in Arabidopsis. Development 124: 3835–3844.

67. Gomez-MeñaC, de FolterS, CostaMM, AngenentGC, SablowskiR (2005) Transcriptional program controlled by the floral homeotic gene AGAMOUS during early organogenesis. Development 132: 429–438.

68. MathieuJ, YantLJ, MürdterF, KüttnerF, SchmidM (2009) Repression of flowering by the miR172 target SMZ. PLoS Biol 7: e1000148 doi:10.1371/journal.pbio.1000148.

69. ChenH, ZouY, ShangY, LinH, WangY, et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368–376.

70. XieZ, AllenE, FahlgrenN, CalamarA, GivanSA, et al. (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138: 2145–2154.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


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