Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage

English version České info

Generation of self-organized, functional tissue patterns is critical for development and regeneration in multicellular organisms. Small valves on the epidermis of land plants, called stomata, mediate gas-exchange while minimizing water loss. Density and spacing of stomata are regulated by transcription factors that drive differentiation as well as by cell-cell signaling components that regulate entry and spacing of stomatal lineage cells. To unravel how interaction of these components translates into two-dimensional patterning of stomata, we have taken an integrative approach employing molecular genetics, imaging, and mathematical modeling. In this paper we have identified a regulatory circuit controlling the initiation of the stomatal cell lineage. The key elements of the circuit are a positive feedback loop constituting self-activation of the transcription factors SCREAM / SCREAM2 (SCRMs) that requires SPEECHLESS (SPCH), and a negative feedback loop involving the signaling ligand EPF2, the receptor modifier TOO MANY MOUTHS, and the SPCH•SCRMs module. The receptor ERECTA, on the other hand, lies outside of the regulatory loop. Our mathematical modeling recapitulated all known stomatal phenotypes with the addition of two regulatory nodes. This work highlights the molecular framework of a self-organizing patterning system in plants.

Vyšlo v časopise: Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005374
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005374

Souhrn

Zdroje

1. MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445: 537–540. 17183265

2. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU (2007) Termination of asymmetric cell division and differentiation of stomata. Nature 445: 501–505. 17183267

3. Ohashi-Ito K, Bergmann DC (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell 18: 2493–2505. 17088607

4. Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, et al. (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation. Plant Cell 20: 1775–1785. doi: 10.1105/tpc.108.060848 18641265

5. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309: 290–293. 16002616

6. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T (2007) The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21: 1720–1725. 17639078

7. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, et al. (2009) Epidermal cell density is auto-regulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR2 in Arabidopsis leaves. Plant Cell Physiol 50: 1019–1031. doi: 10.1093/pcp/pcp068 19435754

8. Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19: 864–869. doi: 10.1016/j.cub.2009.03.069 19398336

9. Lee JS, Kuroha T, Hnilova M, Khatayevich D, Kanaoka MM, et al. (2012) Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev 26: 126–136. doi: 10.1101/gad.179895.111 22241782

10. Bergmann DC, Lukowitz W, Somerville CR (2004) Stomatal development and pattern controlled by a MAPKK kinase. Science 304: 1494–1497. 15178800

11. Wang H, Ngwenyama N, Liu Y, Walker J, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63–73. 17259259

12. Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322: 1113–1116. doi: 10.1126/science.1162263 19008449

13. Pillitteri LJ, Peterson KM, Horst RJ, Torii KU (2011) Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23: 3260–3275. doi: 10.1105/tpc.111.088583 21963668

14. Robinson S, Barbier de Reuille P, Chan J, Bergmann D, Prusinkiewicz P, et al. (2011) Generation of spatial patterns through cell polarity switching. Science 333: 1436–1440. doi: 10.1126/science.1202185 21903812

15. Peterson KM, Rychel AL, Torii KU (2010) Out of the mouths of plants: the molecular basis of the evolution and diversity of stomatal development. Plant Cell 22: 296–306. doi: 10.1105/tpc.109.072777 20179138

16. Rowe MH, Bergmann DC (2010) Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development. Curr Opin Plant Biol 13: 548–555. doi: 10.1016/j.pbi.2010.06.002 20638894

17. Rychel AL, Peterson KM, Torii KU (2010) Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J Plant Res 123: 275–280. doi: 10.1007/s10265-010-0330-9 20336477

18. Nadeau JA, Sack FD (2002) Control of stomatal distribution on the Arabidopsis leaf surface. Science 296: 1697–1700. 12040198

19. Torii KU (2012) Two-dimensional spatial patterning in developmental systems. Trends Cell Biol 22: 438–446. doi: 10.1016/j.tcb.2012.06.002 22789547

20. Kondo S, Miura T (2010) Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329: 1616–1620. doi: 10.1126/science.1179047 20929839

21. Gierer A, Meinhardt H (1972) A theory of biological patten formation. Kybernetik 12: 30–39. 4663624

22. Kim TW, Michniewicz M, Bergmann DC, Wang ZY (2012) Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482: 419–422. doi: 10.1038/nature10794 22307275

23. Gudesblat GE, Schneider-Pizon J, Betti C, Mayerhofer J, Vanhoutte I, et al. (2012) SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat Cell Biol 14: 548–554. doi: 10.1038/ncb2471 22466366

24. Khan M, Rozhon W, Bigeard J, Pflieger D, Husar S, et al. (2013) Brassinosteroid-regulated GSK3/Shaggy-like kinases phosphorylate mitogen-activated protein (MAP) kinase kinases, which control stomata development in Arabidopsis thaliana. J Biol Chem 288: 7519–7527. doi: 10.1074/jbc.M112.384453 23341468

25. De Rybel B, Audenaert D, Vert G, Rozhon W, Mayerhofer J, et al. (2009) Chemical inhibition of a subset of Arabidopsis thaliana GSK3-like kinases activates brassinosteroid signaling. Chem Biol 16: 594–604. doi: 10.1016/j.chembiol.2009.04.008 19549598

26. Lu P, Porat R, Nadeau JA, O'Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8: 2155–2168. 8989876

27. Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, et al. (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463: 241–244. doi: 10.1038/nature08682 20010603

28. Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, et al. (2010) Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol 51: 1–8. doi: 10.1093/pcp/pcp180 20007289

29. Ohki S, Takeuchi M, Mori M (2011) The NMR structure of stomagen reveals the basis of stomatal density regulation by plant peptide hormones. Nat Commun 2: 512. doi: 10.1038/ncomms1520 22027592

30. Meinhardt H (1982) Models of biological pattern formation. London, UK: Academic Press.

31. Turing AM (1952) The chemical basis of morphogenesis. Philos Trans R Soc London B 237: 37–72.

32. Lee JS, Hnilova M, Maes M, Lin YCL, Putarjunan A, et al. (2015) Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:439–43 doi: 10.1038/nature14561 26083750

33. Abrash EB, Davies KA, Bergmann DC (2011) Generation of Signaling Specificity in Arabidopsis by Spatially Restricted Buffering of Ligand-Receptor Interactions. Plant Cell 23: 2864–2879. doi: 10.1105/tpc.111.086637 21862708

34. Torii KU (2012) Mix-and-match: ligand-receptor pairs in stomatal development and beyond. Trends Plant Sci 17: 711–719. doi: 10.1016/j.tplants.2012.06.013 22819466

35. Uchida N, Lee JS, Horst RJ, Lai H-H, Kajita R, et al. (2012) Regulation of inflorescence architecture by intertissue layer ligand-receptor communication between Proc Natl Acad Sci U S A 109: 6337–6342. doi: 10.1073/pnas.1117537109 22474391

36. Lau OS, Davies KA, Chang J, Adrian J, Rowe MH, et al. (2014) Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells. Science 345: 1605–1609. doi: 10.1126/science.1256888 25190717

37. Ayer DE, Kretzner L, Eisenman RN (1993) Mad: a heterodimeric partner for Max that antagonizes Myc transcriptional activity. Cell 72: 211–222. 8425218

38. Sloan SR, Shen CP, McCarrick-Walmsley R, Kadesch T (1996) Phosphorylation of E47 as a potential determinant of B-cell-specific activity. Mol Cell Biol 16: 6900–6908. 8943345

39. Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61: 681–704. doi: 10.1146/annurev.arplant.043008.092057 20192752

40. Engineer CB, Ghassemian M, Anderson JC, Peck SC, Hu H, et al. (2014) Carbonic anhydrases, EPF2 and a novel protease mediate CO control of stomatal development. Nature 513: 246–250. doi: 10.1038/nature13452 25043023

41. Hulskamp M (2004) Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5: 471–480. 15173826

42. Serna L, Martin C (2006) Trichomes: different regulatory networks lead to convergent structures. Trends Plant Sci 11: 274–280. 16697247

43. Schnittger A, Folkers U, Schwab B, Jurgens G, Hulskamp M (1999) Generation of a spacing pattern: the role of triptychon in trichome patterning in Arabidopsis. Plant Cell 11: 1105–1116. 10368181

44. Bouyer D, Geier F, Kragler F, Schnittger A, Pesch M, et al. (2008) Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol 6: e141. doi: 10.1371/journal.pbio.0060141 18547143

45. Yan L, Cheng X, Jia R, Qin Q, Guan L, et al. (2014) New phenotypic characteristics of three tmm alleles in Arabidopsis thaliana. Plant Cell Rep 33: 719–731. doi: 10.1007/s00299-014-1571-1 24553751

46. Adrian J, Chang J, Ballenger CE, Bargmann BO, Alassimone J, et al. (2015) Transcriptome dynamics of the stomatal lineage: birth, amplification, and termination of a self-renewing population. Dev Cell 33: 107–118. doi: 10.1016/j.devcel.2015.01.025 25850675

47. Kondo S, Asai R (1995) A reaction-diffusion wave on the skin of the marine angelfish Pomacanthus. Nature 376: 765–768. 24547605

48. Inaba M, Yamanaka H, Kondo S (2012) Pigment pattern formation by contact-dependent depolarization. Science 335: 677. doi: 10.1126/science.1212821 22323812

49. Muller P, Rogers KW, Jordan BM, Lee JS, Robson D, et al. (2012) Differential diffusivity of Nodal and Lefty underlies a reaction-diffusion patterning system. Science 336: 721–724. doi: 10.1126/science.1221920 22499809

50. Sheth R, Marcon L, Bastida MF, Junco M, Quintana L, et al. (2012) Hox genes regulate digit patterning by controlling the wavelength of a Turing-type mechanism. Science 338: 1476–1480. doi: 10.1126/science.1226804 23239739

51. Takada S, Jurgens G (2007) Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development 134: 1141–1150. 17301085

52. Peterson KM, Shyu C, Burr CA, Horst RJ, Kanaoka MM, et al. (2013) Arabidopsis homeodomain-leucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis. Development 140: 1924–1935. doi: 10.1242/dev.090209 23515473

53. Bowler C, Benvenuto G, Laflamme P, Molino D, Probst AV, et al. (2004) Chromatin techniques for plant cells. Plant J 39: 776–789. 15315638

54. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. 11328886