Antagonistic Gene Activities Determine the Formation of Pattern Elements along the Mediolateral Axis of the Fruit

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The Arabidopsis fruit mainly consists of a mature ovary that shows three well defined territories that are pattern elements along the mediolateral axis: the replum, located at the medial plane of the flower, and the valve and the valve margin, both of lateral nature. JAG/FIL activity, which includes the combined functions of JAGGED (JAG), FILAMENTOUS FLOWER (FIL), and YABBY3 (YAB3), contributes to the formation of the two lateral pattern elements, whereas the cooperating genes BREVIPEDICELLUS (BP) and REPLUMLESS (RPL) promote replum development. A recent model to explain pattern formation along the mediolateral axis hypothesizes that JAG/FIL activity and BP/RPL function as antagonistic lateral and medial factors, respectively, which tend to repress each other. In this work, we demonstrate the existence of mutual exclusion mechanisms between both kinds of factors, and how this determines the formation and size of the three territories. Medial factors autonomously constrain lateral factors so that they only express outside the replum, and lateral factors negatively regulate the medially expressed BP gene in a non-autonomous fashion to ensure correct replum development. We also have found that ASYMMETRIC LEAVES1 (AS1), previously shown to repress BP both in leaves and ovaries, collaborates with JAG/FIL activity, preventing its repression by BP and showing synergistic interactions with JAG/FIL activity genes. Therefore AS gene function (the function of the interacting genes AS1 and AS2) has been incorporated in the model as a new lateral factor. Our model of antagonistic factors provides explanation for mutant fruit phenotypes in Arabidopsis and also may help to understand natural variation of fruit shape in Brassicaceae and other species, since subtle changes in gene expression may cause conspicuous changes in the size of the different tissue types.

Vyšlo v časopise: Antagonistic Gene Activities Determine the Formation of Pattern Elements along the Mediolateral Axis of the Fruit. PLoS Genet 8(11): e32767. doi:10.1371/journal.pgen.1003020
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003020

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Zdroje

1. BowmanJL, BaumSF, EshedY, PutterillJ, AlvarezJ (1999) Molecular genetics of gynoecium development in Arabidopsis. Curr Top Dev Biol 45: 155–205.

2. FerrandizC, PelazS, YanofskyMF (1999) Control of carpel and fruit development in Arabidopsis. Annu Rev Biochem 68: 321–354.

3. DinnenyJR, YanofskyMF (2005) Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. Bioessays 27: 42–49.

4. BalanzaV, NavarreteM, TriguerosM, FerrandizC (2006) Patterning the female side of Arabidopsis: the importance of hormones. J Exp Bot 57: 3457–3469.

5. RoederAH, YanofskyMF (2006) Fruit development in Arabidopsis. Arabidopsis Book 4: e0075.

6. OstergaardL (2009) Don't ‘leaf’ now. The making of a fruit. Curr Opin Plant Biol 12: 36–41.

7. Martinez-Laborda A, Vera A (2009) Arabidopsis fruit development. In: Ostergaard L, editor. Fruit Development and Seed Dispresal Annual Plant Reviews, Volume 38. Oxford, UK: Wiley-Blackwell.

8. Vivian-SmithA, KoltunowAM (1999) Genetic analysis of growth-regulator-induced parthenocarpy in Arabidopsis. Plant Physiol 121: 437–451.

9. FerrandizC (2002) Regulation of fruit dehiscence in Arabidopsis. J Exp Bot 53: 2031–2038.

10. GuQ, FerrandizC, YanofskyMF, MartienssenR (1998) The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development. Development 125: 1509–1517.

11. ByrneME, GrooverAT, FontanaJR, MartienssenRA (2003) Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development 130: 3941–3950.

12. SmithHM, HakeS (2003) The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell 15: 1717–1727.

13. RoederAH, FerrandizC, YanofskyMF (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr Biol 13: 1630–1635.

14. BhattAM, EtchellsJP, CanalesC, LagodienkoA, DickinsonH (2004) VAAMANA–a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene 328: 103–111.

15. LiljegrenSJ, DittaGS, EshedY, SavidgeB, BowmanJL, et al. (2000) SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis. Nature 404: 766–770.

16. LiljegrenSJ, RoederAH, KempinSA, GremskiK, OstergaardL, et al. (2004) Control of fruit patterning in Arabidopsis by INDEHISCENT. Cell 116: 843–853.

17. RajaniS, SundaresanV (2001) The Arabidopsis myc/bHLH gene ALCATRAZ enables cell separation in fruit dehiscence. Curr Biol 11: 1914–1922.

18. FerrandizC, LiljegrenSJ, YanofskyMF (2000) Negative regulation of the SHATTERPROOF genes by FRUITFULL during Arabidopsis fruit development. Science 289: 436–438.

19. Alonso-CantabranaH, RipollJJ, OchandoI, VeraA, FerrandizC, et al. (2007) Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene. Development 134: 2663–2671.

20. GirinT, SorefanK, OstergaardL (2009) Meristematic sculpting in fruit development. J Exp Bot 60: 1493–1502.

21. LincolnC, LongJ, YamaguchiJ, SerikawaK, HakeS (1994) A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. Plant Cell 6: 1859–1876.

22. ChuckG, LincolnC, HakeS (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8: 1277–1289.

23. DouglasSJ, ChuckG, DenglerRE, PelecandaL, RiggsCD (2002) KNAT1 and ERECTA regulate inflorescence architecture in Arabidopsis. Plant Cell 14: 547–558.

24. 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 U S A 99: 4730–4735.

25. LongJA, MoanEI, MedfordJI, BartonMK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature 379: 66–69.

26. ChenQ, AtkinsonA, OtsugaD, ChristensenT, ReynoldsL, et al. (1999) The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formation. Development 126: 2715–2726.

27. SawaS, ItoT, ShimuraY, OkadaK (1999) FILAMENTOUS FLOWER controls the formation and development of arabidopsis inflorescences and floral meristems. Plant Cell 11: 69–86.

28. SawaS, WatanabeK, GotoK, LiuYG, ShibataD, et al. (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev 13: 1079–1088.

29. SiegfriedKR, EshedY, BaumSF, OtsugaD, DrewsGN, et al. (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117–4128.

30. WatanabeK, OkadaK (2003) Two discrete cis elements control the abaxial side-specific expression of the FILAMENTOUS FLOWER gene in Arabidopsis. Plant Cell 15: 2592–2602.

31. DinnenyJR, YadegariR, FischerRL, YanofskyMF, WeigelD (2004) The role of JAGGED in shaping lateral organs. Development 131: 1101–1110.

32. OhnoCK, ReddyGV, HeislerMG, MeyerowitzEM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131: 1111–1122.

33. ByrneME, BarleyR, CurtisM, ArroyoJM, DunhamM, et al. (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967–971.

34. ByrneME, SimorowskiJ, MartienssenRA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129: 1957–1965.

35. DinnenyJR, WeigelD, YanofskyMF (2005) A genetic framework for fruit patterning in Arabidopsis thaliana. Development 132: 4687–4696.

36. RipollJJ, RoederAH, DittaGS, YanofskyMF (2011) A novel role for the floral homeotic gene APETALA2 during Arabidopsis fruit development. Development 138: 5167–5176.

37. BellaouiM, PidkowichMS, SamachA, KushalappaK, KohalmiSE, et al. (2001) The Arabidopsis BELL1 and KNOX TALE homeodomain proteins interact through a domain conserved between plants and animals. Plant Cell 13: 2455–2470.

38. SmithHM, BoschkeI, HakeS (2002) Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci U S A 99: 9579–9584.

39. ColeM, NolteC, WerrW (2006) Nuclear import of the transcription factor SHOOT MERISTEMLESS depends on heterodimerization with BLH proteins expressed in discrete sub-domains of the shoot apical meristem of Arabidopsis thaliana. Nucleic Acids Res 34: 1281–1292.

40. KanrarS, OngukaO, SmithHM (2006) Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta 224: 1163–1173.

41. 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.

42. RutjensB, BaoD, van Eck-StoutenE, BrandM, SmeekensS, et al. (2009) Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J 58: 641–654.

43. RagniL, Belles-BoixE, GunlM, PautotV (2008) Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell 20: 888–900.

44. KumaranMK, BowmanJL, SundaresanV (2002) YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis. Plant Cell 14: 2761–2770.

45. XuB, LiZ, ZhuY, WangH, MaH, et al. (2008) Arabidopsis genes AS1, AS2, and JAG negatively regulate boundary-specifying genes to promote sepal and petal development. Plant Physiol 146: 566–575.

46. LeeDK, GeislerM, SpringerPS (2009) LATERAL ORGAN FUSION1 and LATERAL ORGAN FUSION2 function in lateral organ separation and axillary meristem formation in Arabidopsis. Development 136: 2423–2432.

47. GomezMD, UrbezC, Perez-AmadorMA, CarbonellJ (2011) Characterization of constricted fruit (ctf) mutant uncovers a role for AtMYB117/LOF1 in ovule and fruit development in Arabidopsis thaliana. PLoS ONE 6: e18760 doi:10.1371/journal.pone.0018760.

48. BrewerPB, HowlesPA, DorianK, GriffithME, IshidaT, et al. (2004) PETAL LOSS, a trihelix transcription factor gene, regulates perianth architecture in the Arabidopsis flower. Development 131: 4035–4045.

49. IshidaT, AidaM, TakadaS, TasakaM (2000) Involvement of CUP-SHAPED COTYLEDON genes in gynoecium and ovule development in Arabidopsis thaliana. Plant Cell Physiol 41: 60–67.

50. LarueCT, WenJ, WalkerJC (2009) A microRNA-transcription factor module regulates lateral organ size and patterning in Arabidopsis. Plant J 58: 450–463.

51. EshedY, IzhakiA, BaumSF, FloydSK, BowmanJL (2004) Asymmetric leaf development and blade expansion in Arabidopsis are mediated by KANADI and YABBY activities. Development 131: 2997–3006.

52. GoldshmidtA, AlvarezJP, BowmanJL, EshedY (2008) Signals derived from YABBY gene activities in organ primordia regulate growth and partitioning of Arabidopsis shoot apical meristems. Plant Cell 20: 1217–1230.

53. KanayaE, NakajimaN, OkadaK (2002) Non-sequence-specific DNA binding by the FILAMENTOUS FLOWER protein from Arabidopsis thaliana is reduced by EDTA. J Biol Chem 277: 11957–11964.

54. StahleMI, KuehlichJ, StaronL, von ArnimAG, GolzJF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21: 3105–3118.

55. DinnenyJR, WeigelD, YanofskyMF (2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133: 1645–1655.

56. OhtaM, MatsuiK, HiratsuK, ShinshiH, Ohme-TakagiM (2001) Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13: 1959–1968.

57. KagaleS, LinksMG, RozwadowskiK (2010) Genome-wide analysis of ethylene-responsive element binding factor-associated amphiphilic repression motif-containing transcriptional regulators in Arabidopsis. Plant Physiol 152: 1109–1134.

58. HiratsuK, OhtaM, MatsuiK, Ohme-TakagiM (2002) The SUPERMAN protein is an active repressor whose carboxy-terminal repression domain is required for the development of normal flowers. FEBS Lett 514: 351–354.

59. HiratsuK, MitsudaN, MatsuiK, Ohme-TakagiM (2004) Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem Biophys Res Commun 321: 172–178.

60. TiwariSB, HagenG, GuilfoyleTJ (2004) Aux/IAA proteins contain a potent transcriptional repression domain. Plant Cell 16: 533–543.

61. LiuZ, KarmarkarV (2008) Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci 13: 137–144.

62. SzemenyeiH, HannonM, LongJA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319: 1384–1386.

63. GallavottiA, LongJA, StanfieldS, YangX, JacksonD, et al. (2010) The control of axillary meristem fate in the maize ramosa pathway. Development 137: 2849–2856.

64. PauwelsL, BarberoGF, GeerinckJ, TillemanS, GrunewaldW, et al. (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464: 788–791.

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

66. SemiartiE, UenoY, TsukayaH, IwakawaH, MachidaC, et al. (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128: 1771–1783.

67. XuL, XuY, DongA, SunY, PiL, et al. (2003) Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity. Development 130: 4097–4107.

68. GuoM, ThomasJ, CollinsG, TimmermansMC (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20: 48–58.

69. BowmanJL, EshedY, BaumSF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18: 134–141.

70. KidnerCA, TimmermansMC (2007) Mixing and matching pathways in leaf polarity. Curr Opin Plant Biol 10: 13–20.

71. SmithZR, LongJA (2010) Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 464: 423–426.

72. NemhauserJL, FeldmanLJ, ZambryskiPC (2000) Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. Development 127: 3877–3888.

73. GarciaD, CollierSA, ByrneME, MartienssenRA (2006) Specification of leaf polarity in Arabidopsis via the trans-acting siRNA pathway. Curr Biol 16: 933–938.

74. SorefanK, GirinT, LiljegrenSJ, LjungK, RoblesP, et al. (2009) A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459: 583–586.

75. ArnaudN, LawrensonT, OstergaardL, SablowskiR (2011) The same regulatory point mutation changed seed-dispersal structures in evolution and domestication. Curr Biol 21: 1215–1219.

76. KoornneefM, van EdenJ, HanhartCJ, StamP, BraaksmaFJ, et al. (1983) Linkage map of Arabidopsis thaliana. J Hered 74: 265–272.

77. HayA, TsiantisM (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38: 942–947.

78. SavidgeB, RounsleySD, YanofskyMF (1995) Temporal relationship between the transcription of two Arabidopsis MADS box genes and the floral organ identity genes. Plant Cell 7: 721–733.

79. RipollJJ, FerrandizC, Martinez-LabordaA, VeraA (2006) PEPPER, a novel K-homology domain gene, regulates vegetative and gynoecium development in Arabidopsis. Dev Biol 289: 346–359.

80. RipollJJ, Rodriguez-CazorlaE, Gonzalez-ReigS, AndujarA, Alonso-CantabranaH, et al. (2009) Antagonistic interactions between Arabidopsis K-homology domain genes uncover PEPPER as a positive regulator of the central floral repressor FLOWERING LOCUS C. Dev Biol 333: 251–262.

81. QuesadaV, PonceMR, MicolJL (1999) OTC and AUL1, two convergent and overlapping genes in the nuclear genome of Arabidopsis thaliana. FEBS Lett 461: 101–106.

82. PfafflMW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.

83. OchandoI, Jover-GilS, RipollJJ, CandelaH, VeraA, et al. (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in Arabidopsis. Plant Physiol 141: 607–619.

84. KoyamaT, FurutaniM, TasakaM, Ohme-TakagiM (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. Plant Cell 19: 473–484.

85. LaufsP, PeaucelleA, MorinH, TraasJ (2004) MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development 131: 4311–4322.

86. YantL, MathieuJ, DinhTT, OttF, LanzC, et al. (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22: 2156–2170.

87. HayA, BarkoulasM, TsiantisM (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133: 3955–3961.

88. GirinT, StephensonP, GoldsackCM, KempinSA, PerezA, et al. (2010) Brassicaceae INDEHISCENT genes specify valve margin cell fate and repress replum formation. Plant J 63: 329–338.