and Diversified Expression of the Gene Family Bolster the Floral Stem Cell Network

English version České info

Termination of the stem cells in the floral meristem (also known as floral determinacy) is critical for the reproductive success of plants, and the molecular activities regulating floral determinacy are precisely orchestrated during the course of floral development. In Arabidopsis thaliana, regulators of floral determinacy include several transcription factor genes, such as APETALA2 (AP2), AGAMOUS (AG), SUPERMAN (SUP), and CRABSCLAW (CRC), as well as a microRNA (miRNA), miR172, which targets AP2. How the transcription factor and miRNA genes are coordinately regulated to achieve floral determinacy is unknown. A mutation in POWERDRESS (PWR), a previously uncharacterized gene encoding a SANT-domain-containing protein, was isolated in this study as an enhancer of the weakly indeterminate ag-10 allele. PWR was found to promote the transcription of CRC, MIR172a, b, and c and/or enhance Pol II occupancy at their promoters, without affecting MIR172d or e. A mutation in mature miR172d was additionally found to enhance the determinacy defects of ag-10 in an AP2-dependent manner, providing direct evidence that miR172d is functional in repressing AP2 and thereby contributes to floral determinacy. Thus, while PWR promotes floral determinacy by enhancing the expression of three of the five MIR172 members as well as CRC, MIR172d, whose expression is PWR-independent, also functions in floral stem cell termination. Taken together, these findings demonstrate how transcriptional diversification and functional redundancy of a miRNA family along with PWR-mediated co-regulation of miRNA and transcription factor genes contribute to the robustness of the floral determinacy network.

Vyšlo v časopise: and Diversified Expression of the Gene Family Bolster the Floral Stem Cell Network. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003218
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003218

Souhrn

Zdroje

1. LenhardM, BohnertA, JürgensG, LauxT (2001) Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS. Cell 105: 805–814.

2. SunB, XuY, NgKH, ItoT (2009) A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev 23: 1791–1804.

3. LiuX, KimYJ, MüllerR, YumulRE, LiuC, et al. (2011) AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing WUSCHEL through recruitment of Polycomb Group proteins. Plant Cell 23: 3654–3670.

4. AlvarezJ, SmythDR (1999) CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development 126: 2377–2386.

5. PrunetN, MorelP, ThierryAM, EshedY, BowmanJL, et al. (2008) REBELOTE, SQUINT, and ULTRAPETALA1 function redundantly in the temporal regulation of floral meristem termination in Arabidopsis thaliana. Plant Cell 20: 901–919.

6. Zúñiga-MayoVM, Marsch-MartínezN, de FolterS (2012) JAIBA, a class-II HD-ZIP transcription factor involved in the regulation of meristematic activity, and important for correct gynoecium and fruit development in Arabidopsis. Plant J 71: 314–326.

7. WürschumT, Gross-HardtR, LauxT (2006) APETALA2 regulates the stem cell niche in the Arabidopsis shoot meristem. Plant Cell 18: 295–307.

8. ZhaoL, KimY, DinhTT, ChenX (2007) miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. Plant J 51: 840–849.

9. ChenX (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022–2025.

10. VoinnetO (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669–687.

11. ChenX (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: 21–44.

12. Rubio-SomozaI, WeigelD (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci

13. LeeY, KimM, HanJ, YeomKH, LeeS, et al. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23: 4051–4060.

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

15. FahlgrenN, JogdeoS, KasschauKD, SullivanCM, ChapmanEJ, et al. (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22: 1074–1089.

16. CuperusJT, FahlgrenN, CarringtonJC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23: 431–442.

17. MaherC, SteinL, WareD (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16: 510–519.

18. ZhuQH, HelliwellCA (2011) Regulation of flowering time and floral patterning by miR172. J Exp Bot 62: 487–495.

19. RajagopalanR, VaucheretH, TrejoJ, BartelDP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20: 3407–3425.

20. GrigorovaB, MaraC, HollenderC, SijacicP, ChenX, et al. (2011) LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138: 2451–2456.

21. 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.

22. JiL, LiuX, YanJ, WangW, YumulRE, et al. (2011) ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. PLoS Genet 7: e1001358 doi:10.1371/journal.pgen.1001358.

23. BowmanJL, SmythDR, MeyerowitzEM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1: 37–52.

24. NohYS, AmasinoRM (2003) PIE1, an ISWI family gene, is required for FLC activation and floral repression in Arabidopsis. Plant Cell 15: 1671–1682.

25. BoyerLA, LatekRR, PetersonCL (2004) The SANT domain: a unique histone-tail-binding module? Nat Rev Mol Cell Biol 5: 158–163.

26. AlonsoJM, StepanovaAN, LeisseTJ, KimCJ, ChenH, et al. (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653–657.

27. LiuC, ThongZ, YuH (2009) Coming into bloom: the specification of floral meristems. Development 136: 3379–3391.

28. FornaraF, de MontaiguA, CouplandG (2010) SnapShot: Control of flowering in Arabidopsis. Cell 141: 550, 550.e551–552.

29. DittaG, PinyopichA, RoblesP, PelazS, YanofskyMF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14: 1935–1940.

30. SablowskiRW, MeyerowitzEM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92: 93–103.

31. MaraCD, HuangT, IrishVF (2010) The Arabidopsis floral homeotic proteins APETALA3 and PISTILLATA negatively regulate the BANQUO genes implicated in light signaling. Plant Cell 22: 690–702.

32. ClarkSM, RunningMP, MeyerowitzEM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121: 2057–2067.

33. BowmanJL, SakaiH, JackT, WeigelD, MayerU, et al. (1992) SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114: 599–615.

34. BäurleI, LauxT (2005) Regulation of WUSCHEL transcription in the stem cell niche of the Arabidopsis shoot meristem. Plant Cell 17: 2271–2280.

35. BowmanJL, SmythDR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126: 2387–2396.

36. WinterJ, JungS, KellerS, GregoryRI, DiederichsS (2009) Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 11: 228–234.

37. VolkN, ShomronN (2011) Versatility of MicroRNA biogenesis. PLoS ONE 6: e19391 doi:10.1371/journal.pone.0019391.

38. GuentherMG, BarakO, LazarMA (2001) The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 21: 6091–6101.

39. YuJ, LiY, IshizukaT, GuentherMG, LazarMA (2003) A SANT motif in the SMRT corepressor interprets the histone code and promotes histone deacetylation. EMBO J 22: 3403–3410.

40. AukermanMJ, SakaiH (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15: 2730–2741.

41. SchmidM, UhlenhautNH, GodardF, DemarM, BressanR, et al. (2003) Dissection of floral induction pathways using global expression analysis. Development 130: 6001–6012.

42. BowmanJL, SmythDR, MeyerowitzEM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112: 1–20.

43. LauxT, MayerK, BergerJ, JurgensG (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87–96.

44. CurtisMD, GrossniklausU (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133: 462–469.

45. 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.

46. YuB, BiL, ZhengB, JiL, ChevalierD, et al. (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci U S A 105: 10073–10078.

47. KimYJ, ZhengB, YuY, WonSY, MoB, et al. (2011) The role of Mediator in small and long noncoding RNA production in Arabidopsis thaliana. EMBO J 30: 814–822.

48. HoranK, JangC, Bailey-SerresJ, MittlerR, SheltonC, et al. (2008) Annotating genes of known and unknown function by large-scale coexpression analysis. Plant Physiol 147: 41–57.

49. Rodrigues-PousadaRA, De RyckeR, DedonderA, Van CaeneghemW, EnglerG, et al. (1993) The Arabidopsis 1-Aminocyclopropane-1-Carboxylate Synthase Gene 1 Is Expressed during Early Development. Plant Cell 5: 897–911.

50. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907.

51. ChodavarapuRK, FengS, BernatavichuteYV, ChenPY, StroudH, et al. (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466: 388–392.