One, two, three...models for trichome patterning in Arabidopsis?

Current Opinion in Plant Biology

Volumn 12, Issue 5, 2009, Pages 587-592

  Pesch, Marina ^a   Hülskamp, Martin ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; PHYTOHORMONE;

ARABIDOPSIS; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PLANT LEAF; REVIEW;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; MODELS, BIOLOGICAL; PLANT GROWTH REGULATORS; PLANT LEAVES;

ARABIDOPSIS;

EID: 70349556372     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2009.07.015     Document Type: Review

References (51)

1. Schnittger A., Folkers U., Schwab B., Jürgens G., and Hulskamp M. Generation of a spacing pattern: the role of TRIPTYCHON in trichome patterning in Arabidopsis. Plant Cell 11 (1999) 1105-1116
2. Larkin J.C., Young N., Prigge M., and Marks M.D. The control of trichome spacing and number in Arabidopsis. Development 122 (1996) 997-1005
3. Schellmann S., Hulskamp M., and Uhrig J. Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem Soc Trans 35 (2007) 146-148
4. Pesch M., and Hulskamp M. Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Curr Opin Genet Dev 14 (2004) 422-427
5. Larkin J.C., Brown M.L., and Schiefelbein J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu Rev Plant Biol 54 (2003) 403-430
6. Ishida T., Kurata T., Okada K., and Wada T. A genetic regulatory network in the development of trichomes and root hairs. Annu Rev Plant Biol 59 (2008) 364-386
7. Galway M.E., Masucci J.D., Lloyd A.M., Walbot V., Davis R.W., and Schiefelbein J.W. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166 (1994) 740-754
8. Walker A.R., Davison P.A., Bolognesi-Winfield A.C., James C.M., Srinivasan N., Blundell T.L., Esch J.J., Marks M.D., and Gray J.C. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11 (1999) 1337-1349
9. Li S.F., Milliken O.N., Pham H., Seyit R., Napoli R., Preston J., Koltunow A.M., and Parish R.W. The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21 (2009) 72-89
10. Kirik V., Lee M.M., Wester K., Herrmann U., Zheng Z., Oppenheimer D., Schiefelbein J., and Hulskamp M. Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development 132 (2005) 1477-1485
11. Kirik V., Schnittger A., Radchuk V., Adler K., Hulskamp M., and Baumlein H. Ectopic expression of the Arabidopsis AtMYB23 gene induces differentiation of trichome cells. Dev Biol 235 (2001) 366-377
12. Oppenheimer D.G., Herman P.L., Sivakumaran S., Esch J., and Marks M.D. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67 (1991) 483-493
13. Zhang F., Gonzalez A., Zhao M., Payne C.T., and Lloyd A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130 (2003) 4859-4869
14. Bernhardt C., Zhao M., Gonzalez A., Lloyd A., and Schiefelbein J. The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132 (2005) 291-298
15. Payne C.T., Zhang F., and Lloyd A.M. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156 (2000) 1349-1362
16. Kirik V., Simon M., Hulskamp M., and Schiefelbein J. The ENHANCER OF TRY AND CPC1 (ETC1) gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268 (2004) 506-513
17. Kirik V., Simon M., Wester K., Schiefelbein J., and Hulskamp M. ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol Biol 55 (2004) 389-398
18. Wada T., Tachibana T., Shimura Y., and Okada K. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277 (1997) 1113-1116
19. Esch J.J., Chen M.A., Hillestad M., and Marks M.D. Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J 40 (2004) 860-869
20. Wang S., Kwak S.H., Zeng Q., Ellis B.E., Chen X.Y., Schiefelbein J., and Chen J.G. TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134 (2007) 3873-3882
21. Simon M., Lee M.M., Lin Y., Gish L., and Schiefelbein J. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 311 (2007) 566-578
22. Tominaga R., Iwata M., Sano R., Inoue K., Okada K., and Wada T. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135 (2008) 1335-1345
23. Wang S., Hubbard L., Chang Y., Guo J., Schiefelbein J., and Chen J.G. Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biol 8 (2008) 81
24. Wester K., Digiuni S., Geier F., Timmer J., Fleck C., and Hulskamp M. Functional diversity of R3 single-repeat genes in trichome development. Development 136 (2009) 1487-1496. This work provides experimental and theoretical evidence that movement rates of the inhibitors from the trichome cell into neighboring cells depend on the binding strength to GL3, such that strong binding reduces and weak binding increases movement rates.
25. Larkin J.C., Walker J.D., Bolognesi-Winfield A.C., Gray J.C., and Walker A.R. Allele-specific interactions between ttg and gl1 during trichome development in Arabidopsis thaliana. Genetics 151 (1999) 1591-1604
26. Zimmermann I.M., Heim M.A., Weisshaar B., and Uhrig J.F. Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J 40 (2004) 22-34
27. Wang S., and Chen J.G. Arabidopsis transient expression analysis reveals that activation of GLABRA2 may require concurrent binding of GLABRA1 and GLABRA3 to the promoter of GLABRA2. Plant Cell Physiol 49 (2008) 1792-1804
28. Digiuni S., Schellmann S., Geier F., Greese B., Pesch M., Wester K., Dartan B., Mach V., Srinivas B.P., Timmer J., et al. A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves. Mol Syst Biol 4 (2008) 217. This study highlights the power of mathematical modeling to determine the relevant protein interactions for patterning. From three scenarios equally supported by experiments and equally sufficient to simulate a trichome pattern, only one is able to explain the predictions for selected overexpression phenotypes. This indicates that only one interaction scenario is relevant for trichome patterning.
29. Zhao M., Morohashi K., Hatlestad G., Grotewold E., and Lloyd A. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135 (2008) 1991-1999. In vivo binding of GL1, GL3, and TTG1 to the same target promoters provides first evidence that they act in concert to turn on downstream genes. In addition coprecipitation experiments provide evidence for the existence of a trimeric GL1, GL3, and TTG1 complex.
30. Gao Y., Gong X., Cao W., Zhao J., Fu L., Wang X., Schumaker K.S., and Guo Y. SAD2 in Arabidopsis functions in trichome initiation through mediating GL3 function and regulating GL1, TTG1, and GL2 expression. J Integr Plant Biol 50 (2008) 906-917
31. Esch J.J., Chen M., Sanders M., Hillestad M., Ndkium S., Idelkope B., Neizer J., and Marks M.D. A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130 (2003) 5885-5894
32. Bernhardt C., Lee M.M., Gonzalez A., Zhang F., Lloyd A., and Schiefelbein J. The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130 (2003) 6431-6439
33. Hulskamp M., Misera S., and Jürgens G. Genetic dissection of trichome cell development in Arabidopsis. Cell 76 (1994) 555-566
34. Larkin J.C., Oppenheimer D.G., Pollock S., and Marks M.D. Arabidopsis GLABROUS1 gene requires downstream sequences for function. Plant Cell 5 (1993) 1739-1748
35. Bouyer D., Geier F., Kragler F., Schnittger A., Pesch M., Wester K., Balkunde R., Timmer J., Fleck C., and Hulskamp M. Two-dimensional patterning by a trapping/depletion mechanism: the role of TTG1 and GL3 in Arabidopsis trichome formation. PLoS Biol 6 (2008) e141. Several lines of evidence are provided for TTG1 movement. TTG1 protein depletion around trichomes is found in wild-type but not in gl3 mutants, suggesting that binding of TTG1 to GL3 causes the depletion. A novel activator-depletion model is proposed.
36. Schellmann S., Schnittger A., Kirik V., Wada T., Okada K., Beermann A., Thumfahrt J., Jurgens G., and Hulskamp M. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21 (2002) 5036-5046
37. Rerie W.G., Feldmann K.A., and Marks M.D. The glabra 2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Gene Dev 8 (1994) 1388-1399
38. Masucci J.D., Rerie W.G., Foreman D.R., Zhang M., Galway M.E., Marks M.D., and Schiefelbein J.W. The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122 (1996) 1253-1260
39. Cristina M.D., Sessa G., Dolan L., Linstead P., Ruberti S., and Morelli G. The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J 10 (1996) 393-402
40. Johnson C.S., Kolevski B., and Smyth D.R. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14 (2002) 1359-1375
41. Ishida T., Hattori S., Sano R., Inoue K., Shirano Y., Hayashi H., Shibata D., Sato S., Kato T., Tabata S., et al. Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19 (2007) 2531-2543
42. Morohashi K., and Grotewold E. A systems approach reveals regulatory circuitry for Arabidopsis trichome initiation by the GL3 and GL1 selectors. PLoS Genet 5 (2009) e1000396
43. Morohashi K., Zhao M., Yang M., Read B., Lloyd A., Lamb R., and Grotewold E. Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events. Plant Physiol 145 (2007) 736-746. In vivo binding of GL3 and GL1 to downstream promoters provides first evidence for a common role in transcriptional activation. In addition a self-inhibitory effect of GL3 was shown.
44. Jakoby M.J., Falkenhan D., Mader M.T., Brininstool G., Wischnitzki E., Platz N., Hudson A., Hulskamp M., Larkin J., and Schnittger A. Transcriptional profiling of mature Arabidopsis trichomes reveals that NOECK encodes the MIXTA-Like transcriptional regulator MYB106. Plant Physiol 148 (2008) 1583-1602
45. Kurata T., Ishida T., Kawabata-Awai C., Noguchi M., Hattori S., Sano R., Nagasaka R., Tominaga R., Koshino-Kimura Y., Kato T., et al. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132 (2005) 5387-5398
46. Benitez M., Espinosa-Soto C., Padilla-Longoria P., and Alvarez-Buylla E.R. Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis: a dynamic spatial model. BMC Syst Biol 2 (2008) 98. By incorporating all known regulatory interactions between patterning genes, theoretical modeling enabled an evaluation of the redundancy and stability of the interaction network.
47. Benitez M., Espinosa-Soto C., Padilla-Longoria P., Diaz J., and Alvarez-Buylla E.R. Equivalent genetic regulatory networks in different contexts recover contrasting spatial cell patterns that resemble those in Arabidopsis root and leaf epidermis: a dynamic model. Int J Dev Biol 51 (2007) 139-155
48. Meinhardt H., and Gierer A. Applications of a theory of biological pattern formation based on lateral inhibition. J Cell Sci 15 (1974) 321-346
49. Turing A. The chemical basis of morphogenesis. Philos T Roy Soc B 237 (1952) 37-72
50. Hulskamp M. Plant trichomes: a model for cell differentiation. Nat Rev Mol Cell Biol 5 (2004) 471-480
51. Jach G., Pesch M., Richter K., Frings S., and Uhrig J.F. An improved mRFP1 adds red to bimolecular fluorescence complementation. Nat Methods 3 (2006) 597-600