Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

The AP2-type transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE promote G1/S transition

Abstract

The paralogous genes DORNRÖSCHEN (DRN) and DORNRÖSCHEN-LIKE (DRNL) encode AP2-type transcription factors that are expressed and act cell-autonomously in the central stem-cell zone or lateral organ founder cells (LOFCs) in the peripheral zone of the Arabidopsis shoot meristem (SAM), but their molecular contribution is unknown. Here, we show using the Arabidopsis thaliana MERISTEM LAYER 1 promoter that DRN and DRNL share a common function in cell cycle progression and potentially provide local competence for G1-S transitions in the SAM. Analysis of double transgenic DRN::erGFP and DRNL::erCERULEAN promoter fusion lines suggests that the trajectory of this cellular competence starts with DRN activity in the central stem-cell zone and extends locally via DRNL activity into groups of founder cells at the IM or FM periphery. Our data support the scenario that after gene duplication, DRN and DRNL acquired different transcription domains within the shoot meristem, but retained protein function that affects cell cycle progression, either centrally in stem cells or peripherally in primordial founder cells, a finding that is of general relevance for meristem function.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adrian J, Chang J, Ballenger CE, Bargmann BOR, Alassimone J, Davies KA, Lau OS, Matos JL, Hachez C, Lanctot A, Vaten A, Birnbaum KD, Bergmann DC (2015) Transcriptome dynamics of the stomatal lineage: birth, amplification, and termination of a self-renewing population. Dev Cell 33:107–118

  2. Banno H, Ikeda Y, Niu QW, Chua NH (2001) Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. Plant Cell 13:2609–2618

  3. Banno H, Mase H, Maekawa K (2006) Analysis of functional domains and binding sequences of Arabidopsis transcription factor ESR1. Plant Biotechnol 23:3003–3008

  4. Barroco RM, Van Poucke K, Bergervoet JH, De Veylder L, Groot SP, Inze D, Engler G (2005) The role of the cell cycle machinery in resumption of postembryonic development. Plant Physiol 137:127–140

  5. Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

  6. Berger F, Linstead P, Dolan L, Haseloff J (1998) Stomata patterning on the hypocotyl of Arabidopsis thaliana is controlled by genes involved in the control of root epidermis patterning. Dev Biol 194:226–234

  7. Besnard F, Refahi Y, Morin V, Marteaux B, Brunoud G, Chambrier P, Rozier F, Mirabet V, Legrand J, Laine S, Thevenon E, Farcot E, Cellier C, Das P, Bishopp A, Dumas R, Parcy F, Helariutta Y, Boudaoud A, Godin C, Traas J, Guedon Y, Vernoux T (2014) Cytokinin signalling inhibitory fields provide robustness to phyllotaxis. Nature 505:417–421

  8. Beveridge CA, Mathesius U, Rose RJ, Gresshoff PM (2007) Common regulatory themes in meristem development and whole-plant homeostasis. Curr Opin Plant Biol 10:44–51

  9. Borghi L, Gutzat R, Futterer J, Laizet Y, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811

  10. Bossinger G, Smyth DR (1996) Initiation patterns of flower and floral organ development in Arabidopsis thaliana. Development 122:1093–1102

  11. Bouyer D, Roudier F, Heese M, Andersen ED, Gey D, Nowack MK, Goodrich J, Renou JP, Grini PE, Colot V, Schnittger A (2011) Polycomb repressive complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7:e1002014

  12. Breuer C, Ishida T, Sugimoto K (2010) Developmental control of endocycles and cell growth in plants. Curr Opin Plant Biol 13:654–660

  13. Chandler JW, Werr W (2014) Arabidopsis floral phytomer development: auxin response relative to biphasic modes of organ initiation. J Exp Bot 65:3097–3110

  14. Chandler JW, Cole M, Flier A, Grewe B, Werr W (2007) The AP2 transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development 134:1653–1662

  15. Chandler JW, Cole M, Werr W (2008) The role of DORNRÖSCHEN (DRN) and DRN-LIKE (DRNL) in Arabidopsis embryonic patterning. Plant Signal Behav 3:49–51

  16. Chandler JW, Cole M, Jacobs B, Comelli P, Werr W (2011a) Genetic integration of DORNRÖSCHEN and DORNRÖSCHEN-LIKE reveals hierarchical interactions in auxin signalling and patterning of the Arabidopsis apical embryo. Plant Mol Biol 75:223–236

  17. Chandler JW, Jacobs B, Cole M, Comelli P, Werr W (2011b) DORNRÖSCHEN-LIKE expression marks Arabidopsis floral organ founder cells and precedes auxin response maxima. Plant Mol Biol 76:171–185

  18. Cole M, Jacobs B, Soubigou-Taconnat L, Balzergue S, Renou JP, Chandler JW, Werr W (2013) Live imaging of DORNRÖSCHEN and DORNRÖSCHEN-LIKE promoter activity reveals dynamic changes in cell identity at the microcallus surface of Arabidopsis embryonic suspensions. Plant Cell Rep 32:45–59

  19. Craft J, Samalova M, Baroux C, Townley H, Martinez A, Jepson I, Tsiantis M, Moore I (2005) New pOp/LhG4 vectors for stringent glucocorticoid-dependent transgene expression in Arabidopsis. Plant J 41:899–918

  20. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92

  21. Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JA (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104:14537–14542

  22. Dinneny JR, Weigel D, Yanofsky MF (2006) NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis. Development 133:1645–1655

  23. Eklund DM, Cierlik I, Staldal V, Claes AR, Vestman D, Chandler J, Sundberg E (2011) Expression of Arabidopsis SHORT INTERNODES/STYLISH family genes in auxin biosynthesis zones of aerial organs is dependent on a GCC box-like regulatory element. Plant Physiol 157:2069–2080

  24. Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Hofte H (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol 114:295–305

  25. Gendreau E, Hofte H, Grandjean O, Brown S, Traas J (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J 13:221–230

  26. Guo J, Wei J, Xu J, Sun MX (2014) Inducible knock-down of GNOM during root formation reveals tissue-specific response to auxin transport and its modulation of local auxin biosynthesis. J Exp Bot 65:1165–1179

  27. Gutzat R, Borghi L, Futterer J, Bischof S, Laizet Y, Hennig L, Feil R, Lunn J, Gruissem W (2011) RETINOBLASTOMA-RELATED PROTEIN controls the transition to autotrophic plant development. Development 138:2977–2986

  28. Hirano H, Harashima H, Shinmyo A, Sekine M (2008) Arabidopsis RETINOBLASTOMA-RELATED PROTEIN 1 is involved in G1 phase cell cycle arrest caused by sucrose starvation. Plant Mol Biol 66:259–275

  29. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168

  30. Hung CY, Lin Y, Zhang M, Pollock S, Marks MD, Schiefelbein J (1998) A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol 117:73–84

  31. Ikeda Y, Banno H, Niu QW, Howell SH, Chua NH (2006) The ENHANCER OF SHOOT REGENERATION 2 gene in Arabidopsis regulates CUP-SHAPED COTYLEDON 1 at the transcriptional level and controls cotyledon development. Plant Cell Physiol 47:1443–1456

  32. Jakoby M, Schnittger A (2004) Cell cycle and differentiation. Curr Opin Plant Biol 7:661–669

  33. Karim MR, Hirota A, Kwiatkowska D, Tasaka M, Aida M (2009) A role for Arabidopsis PUCHI in floral meristem identity and bract suppression. Plant Cell 21:1360–1372

  34. Kirch T, Simon R, Grunewald M, Werr W (2003) The DORNRÖSCHEN/ENHANCER OF SHOOT REGENERATION1 gene of Arabidopsis acts in the control of meristem cell fate and lateral organ development. Plant Cell 15:694–705

  35. Kono A, Umeda-Hara C, Adachi S, Nagata N, Konomi M, Nakagawa T, Uchimiya H, Umeda M (2007) The Arabidopsis D-type cyclin CYCD4 controls cell division in the stomatal lineage of the hypocotyl epidermis. Plant Cell 19:1265–1277

  36. Kuwabara A, Gruissem W (2014) Arabidopsis Retinoblastoma-related and Polycomb group proteins: cooperation during plant cell differentiation and development. J Exp Bot 65:2667–2676

  37. Kwiatkowska D, Dumais J (2003) Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis L. J Exp Bot 54:1585–1595

  38. Liu Y, Zhao TJ, Liu JM, Liu WQ, Liu Q, Yan YB, Zhou HM (2006) The conserved Ala37 in the ERF/AP2 domain is essential for binding with the DRE element and the GCC box. FEBS Lett 580:1303–1308

  39. Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311:94–98

  40. Marsch-Martinez N, Greco R, Becker JD, Dixit S, Bergervoet JHW, Karaba A, de Folter S, Pereira A (2006) BOLITA, an Arabidopsis AP2/ERF-like transcription factor that affects cell expansion and proliferation/differentiation pathways. Plant Mol Biol 62:825–843

  41. Matsuo N, Banno H (2008) The Arabidopsis transcription factor ESR1 induces in vitro shoot regeneration through transcriptional activation. Plant Physiol Biochem 46:1045–1050

  42. Matsuo N, Mase H, Makino M, Takahashi H, Banno H (2009) Identification of ENHANCER OF SHOOT REGENERATION 1-upregulated genes during in vitro shoot regeneration. Plant Biotechnol 26:385–393

  43. Melaragno JE, Mehrotra B, Coleman AW (1993) Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5:1661–1668

  44. Nadeau JA, Sack FD (2002) Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:1697–1700

  45. Nag A, Yang Y, Jack T (2007) DORNRÖSCHEN-LIKE, an AP2 gene, is necessary for stamen emergence in Arabidopsis. Plant Mol Biol 65:219–232

  46. Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709

  47. Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

  48. Nieuwland J, Scofield S, Murray JA (2009) Control of division and differentiation of plant stem cells and their derivatives. Semin Cell Dev Biol 20:1134–1142

  49. Nomura Y, Matsuo N, Banno H (2009) A domain containing the ESR motif in ENHANCER OF SHOOT REGENERATION 1 functions as a transactivation domain. Plant Biotechnol 26:395–401

  50. Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614

  51. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU (2007) Termination of asymmetric cell division and differentiation of stomata. Nature 445:501–505

  52. Reddy GV (2008) Live-imaging stem-cell homeostasis in the Arabidopsis shoot apex. Curr Opin Plant Biol 11:88–93

  53. Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237

  54. Saibo NJ, Vriezen WH, Beemster GT, Van Der Straeten D (2003) Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 33:989–1000

  55. Schiessl K, Kausika S, Southam P, Bush M, Sablowski R (2012) JAGGED controls growth anisotropy and coordination between cell size and cell cycle during plant organogenesis. Curr Biol 22:1739–1746

  56. Schiessl K, Muino JM, Sablowski R (2014) Arabidopsis JAGGED links floral organ patterning to tissue growth by repressing Kip-related cell cycle inhibitors. Proc Natl Acad Sci USA 111:2830–2835

  57. Scofield S, Dewitte W, Nieuwland J, Murray JA (2013) The Arabidopsis homeobox gene SHOOT MERISTEMLESS has cellular and meristem-organisational roles with differential requirements for cytokinin and CYCD3 activity. Plant J 75:53–66

  58. Sessions A, Weigel D, Yanofsky MF (1999) The Arabidopsis thaliana MERISTEM LAYER 1 promoter specifies epidermal expression in meristems and young primordia. Plant J 20:259–263

  59. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

  60. Stahl Y, Simon R (2005) Plant stem cell niches. Int J Dev Biol 49:479–489

  61. Takada S, Jürgens G (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134:1141–1150

  62. Takahashi N, Kajihara T, Okamura C, Kim Y, Katagiri Y, Okushima Y, Matsunaga S, Hwang I, Umeda M (2013) Cytokinins control endocycle onset by promoting the expression of an APC/C activator in Arabidopsis roots. Curr Biol 23:1812–1817

  63. Überlacker B, Werr W (1996) Vectors with rare-cutter restriction enzyme sites for expression of open reading frames in transgenic plants. Mol Breed 2:293–295

  64. van der Graaff E, Dulk-Ras AD, Hooykaas PJ, Keller B (2000) Activation tagging of the LEAFY PETIOLE gene affects leaf petiole development in Arabidopsis thaliana. Development 127:4971–4980

  65. Vandenbussche F, Verbelen JP, Van Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27:275–284

  66. Weimer AK, Nowack MK, Bouyer D, Zhao X, Harashima H, Naseer S, De Winter F, Dissmeyer N, Geldner N, Schnittger A (2012) Retinoblastoma related1 regulates asymmetric cell divisions in Arabidopsis. Plant Cell 24:4083–4095

Download references

Acknowledgements

This work was funded by the Deutsche Forschungsgemeinschaft through SFB 572 and through Normalverfahren WE 1262/10-1. The TMM::TMM-GFP and MUTE::nGFP marker lines and spch, mute and tmm mutant lines were kindly provided by Dr. Dominique Bergmann (Stanford). The GL2::GFP line and gl2 seeds were obtained from Dr. Martin Hülskamp (University of Cologne).

Author information

Correspondence to Wolfgang Werr.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Seeliger, I., Frerichs, A., Glowa, D. et al. The AP2-type transcription factors DORNRÖSCHEN and DORNRÖSCHEN-LIKE promote G1/S transition. Mol Genet Genomics 291, 1835–1849 (2016). https://doi.org/10.1007/s00438-016-1224-x

Download citation

Keywords

  • Arabidopsis
  • Shoot apical meristem
  • Lateral organ founder cell
  • Cell cycle