Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2000 Nov;156(3):1349–1362. doi: 10.1093/genetics/156.3.1349

GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1.

C T Payne 1, F Zhang 1, A M Lloyd 1
PMCID: PMC1461316  PMID: 11063707

Abstract

Arabidopsis trichome development and differentiation is a well-studied model for plant cell-fate determination and morphogenesis. Mutations in TRANSPARENT TESTA GLABRA1 (TTG1) result in several pleiotropic defects including an almost complete lack of trichomes. The complex phenotype caused by ttg1 mutations is suppressed by ectopic expression of the maize anthocyanin regulator R. Here it is demonstrated that the Arabidopsis trichome development locus GLABRA3 (GL3) encodes an R homolog. GL3 and GLABRA1 (GL1) interact when overexpressed together in plants. Yeast two-hybrid assays indicate that GL3 participates in physical interactions with GL1, TTG1, and itself, but that GL1 and TTG1 do not interact. These data suggest a reiterated combinatorial model for the differential regulation of such diverse developmental pathways as trichome cell-fate determination, root hair spacing, and anthocyanin secondary metabolism.

Full Text

The Full Text of this article is available as a PDF (620.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abe H., Yamaguchi-Shinozaki K., Urao T., Iwasaki T., Hosokawa D., Shinozaki K. Role of arabidopsis MYC and MYB homologs in drought- and abscisic acid-regulated gene expression. Plant Cell. 1997 Oct;9(10):1859–1868. doi: 10.1105/tpc.9.10.1859. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ang L. H., Chattopadhyay S., Wei N., Oyama T., Okada K., Batschauer A., Deng X. W. Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. Mol Cell. 1998 Jan;1(2):213–222. doi: 10.1016/s1097-2765(00)80022-2. [DOI] [PubMed] [Google Scholar]
  3. Atchley W. R., Fitch W. M. A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A. 1997 May 13;94(10):5172–5176. doi: 10.1073/pnas.94.10.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Campuzano S., Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 1992 Jun;8(6):202–208. doi: 10.1016/0168-9525(92)90234-u. [DOI] [PubMed] [Google Scholar]
  5. Cowling R. J., Kamiya Y., Seto H., Harberd N. P. Gibberellin dose-response regulation of GA4 gene transcript levels in Arabidopsis. Plant Physiol. 1998 Aug;117(4):1195–1203. doi: 10.1104/pp.117.4.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Deng X. W., Matsui M., Wei N., Wagner D., Chu A. M., Feldmann K. A., Quail P. H. COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell. 1992 Nov 27;71(5):791–801. doi: 10.1016/0092-8674(92)90555-q. [DOI] [PubMed] [Google Scholar]
  7. Durfee T., Becherer K., Chen P. L., Yeh S. H., Yang Y., Kilburn A. E., Lee W. H., Elledge S. J. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 1993 Apr;7(4):555–569. doi: 10.1101/gad.7.4.555. [DOI] [PubMed] [Google Scholar]
  8. Fields S., Song O. A novel genetic system to detect protein-protein interactions. Nature. 1989 Jul 20;340(6230):245–246. doi: 10.1038/340245a0. [DOI] [PubMed] [Google Scholar]
  9. Galway M. E., Masucci J. D., Lloyd A. M., Walbot V., Davis R. W., Schiefelbein J. W. The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol. 1994 Dec;166(2):740–754. doi: 10.1006/dbio.1994.1352. [DOI] [PubMed] [Google Scholar]
  10. Goff S. A., Cone K. C., Chandler V. L. Functional analysis of the transcriptional activator encoded by the maize B gene: evidence for a direct functional interaction between two classes of regulatory proteins. Genes Dev. 1992 May;6(5):864–875. doi: 10.1101/gad.6.5.864. [DOI] [PubMed] [Google Scholar]
  11. Goodrich J., Carpenter R., Coen E. S. A common gene regulates pigmentation pattern in diverse plant species. Cell. 1992 Mar 6;68(5):955–964. doi: 10.1016/0092-8674(92)90038-e. [DOI] [PubMed] [Google Scholar]
  12. Herman P. L., Marks M. D. Trichome Development in Arabidopsis thaliana. II. Isolation and Complementation of the GLABROUS1 Gene. Plant Cell. 1989 Nov;1(11):1051–1055. doi: 10.1105/tpc.1.11.1051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hülskamp M., Misŕa S., Jürgens G. Genetic dissection of trichome cell development in Arabidopsis. Cell. 1994 Feb 11;76(3):555–566. doi: 10.1016/0092-8674(94)90118-x. [DOI] [PubMed] [Google Scholar]
  14. Koornneef M., Dellaert L. W., van der Veen J. H. EMS- and radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat Res. 1982 Mar;93(1):109–123. doi: 10.1016/0027-5107(82)90129-4. [DOI] [PubMed] [Google Scholar]
  15. Larkin J. C., Oppenheimer D. G., Lloyd A. M., Paparozzi E. T., Marks M. D. Roles of the GLABROUS1 and TRANSPARENT TESTA GLABRA Genes in Arabidopsis Trichome Development. Plant Cell. 1994 Aug;6(8):1065–1076. doi: 10.1105/tpc.6.8.1065. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Larkin J. C., Young N., Prigge M., Marks M. D. The control of trichome spacing and number in Arabidopsis. Development. 1996 Mar;122(3):997–1005. doi: 10.1242/dev.122.3.997. [DOI] [PubMed] [Google Scholar]
  17. Liu Y., Wang L., Kermicle J. L., Wessler S. R. Molecular consequences of Ds insertion into and excision from the helix-loop-helix domain of the maize R gene. Genetics. 1998 Dec;150(4):1639–1648. doi: 10.1093/genetics/150.4.1639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lloyd A. M., Walbot V., Davis R. W. Arabidopsis and Nicotiana anthocyanin production activated by maize regulators R and C1. Science. 1992 Dec 11;258(5089):1773–1775. doi: 10.1126/science.1465611. [DOI] [PubMed] [Google Scholar]
  19. Ludwig S. R., Habera L. F., Dellaporta S. L., Wessler S. R. Lc, a member of the maize R gene family responsible for tissue-specific anthocyanin production, encodes a protein similar to transcriptional activators and contains the myc-homology region. Proc Natl Acad Sci U S A. 1989 Sep;86(18):7092–7096. doi: 10.1073/pnas.86.18.7092. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miséra S., Müller A. J., Weiland-Heidecker U., Jürgens G. The FUSCA genes of Arabidopsis: negative regulators of light responses. Mol Gen Genet. 1994 Aug 2;244(3):242–252. doi: 10.1007/BF00285451. [DOI] [PubMed] [Google Scholar]
  21. Moffatt B. A., McWhinnie E. A., Agarwal S. K., Schaff D. A. The adenine phosphoribosyltransferase-encoding gene of Arabidopsis thaliana. Gene. 1994 Jun 10;143(2):211–216. doi: 10.1016/0378-1119(94)90098-1. [DOI] [PubMed] [Google Scholar]
  22. Németh K., Salchert K., Putnoky P., Bhalerao R., Koncz-Kálmán Z., Stankovic-Stangeland B., Bakó L., Mathur J., Okrész L., Stabel S. Pleiotropic control of glucose and hormone responses by PRL1, a nuclear WD protein, in Arabidopsis. Genes Dev. 1998 Oct 1;12(19):3059–3073. doi: 10.1101/gad.12.19.3059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Oppenheimer D. G., Herman P. L., Sivakumaran S., Esch J., Marks M. D. A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell. 1991 Nov 1;67(3):483–493. doi: 10.1016/0092-8674(91)90523-2. [DOI] [PubMed] [Google Scholar]
  24. Paz-Ares J., Ghosal D., Wienand U., Peterson P. A., Saedler H. The regulatory c1 locus of Zea mays encodes a protein with homology to myb proto-oncogene products and with structural similarities to transcriptional activators. EMBO J. 1987 Dec 1;6(12):3553–3558. doi: 10.1002/j.1460-2075.1987.tb02684.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Quattrocchio F., Wing J. F., van der Woude K., Mol J. N., Koes R. Analysis of bHLH and MYB domain proteins: species-specific regulatory differences are caused by divergent evolution of target anthocyanin genes. Plant J. 1998 Feb;13(4):475–488. doi: 10.1046/j.1365-313x.1998.00046.x. [DOI] [PubMed] [Google Scholar]
  26. Schardl C. L., Byrd A. D., Benzion G., Altschuler M. A., Hildebrand D. F., Hunt A. G. Design and construction of a versatile system for the expression of foreign genes in plants. Gene. 1987;61(1):1–11. doi: 10.1016/0378-1119(87)90359-3. [DOI] [PubMed] [Google Scholar]
  27. Schnittger A., Folkers U., Schwab B., Jürgens G., Hülskamp M. Generation of a spacing pattern: the role of triptychon in trichome patterning in Arabidopsis. Plant Cell. 1999 Jun;11(6):1105–1116. doi: 10.1105/tpc.11.6.1105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shieh M. W., Wessler S. R., Raikhel N. V. Nuclear targeting of the maize R protein requires two nuclear localization sequences. Plant Physiol. 1993 Feb;101(2):353–361. doi: 10.1104/pp.101.2.353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Smith T. F., Gaitatzes C., Saxena K., Neer E. J. The WD repeat: a common architecture for diverse functions. Trends Biochem Sci. 1999 May;24(5):181–185. doi: 10.1016/s0968-0004(99)01384-5. [DOI] [PubMed] [Google Scholar]
  30. Sondek J., Bohm A., Lambright D. G., Hamm H. E., Sigler P. B. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature. 1996 Jan 25;379(6563):369–374. doi: 10.1038/379369a0. [DOI] [PubMed] [Google Scholar]
  31. Szymanski D. B., Jilk R. A., Pollock S. M., Marks M. D. Control of GL2 expression in Arabidopsis leaves and trichomes. Development. 1998 Apr;125(7):1161–1171. doi: 10.1242/dev.125.7.1161. [DOI] [PubMed] [Google Scholar]
  32. Szymanski D. B., Lloyd A. M., Marks M. D. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends Plant Sci. 2000 May;5(5):214–219. doi: 10.1016/s1360-1385(00)01597-1. [DOI] [PubMed] [Google Scholar]
  33. Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K, Martin C. The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco . Plant Cell. 1998 Feb;10(2):135–154. doi: 10.1105/tpc.10.2.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Torii K. U., McNellis T. W., Deng X. W. Functional dissection of Arabidopsis COP1 reveals specific roles of its three structural modules in light control of seedling development. EMBO J. 1998 Oct 1;17(19):5577–5587. doi: 10.1093/emboj/17.19.5577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Urao T., Yamaguchi-Shinozaki K., Mitsukawa N., Shibata D., Shinozaki K. Molecular cloning and characterization of a gene that encodes a MYC-related protein in Arabidopsis. Plant Mol Biol. 1996 Nov;32(3):571–576. doi: 10.1007/BF00019112. [DOI] [PubMed] [Google Scholar]
  36. Walker A. R., Davison P. A., Bolognesi-Winfield A. C., James C. M., Srinivasan N., Blundell T. L., Esch J. J., Marks M. D., Gray J. C. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell. 1999 Jul;11(7):1337–1350. doi: 10.1105/tpc.11.7.1337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. de Pater S., Pham K., Memelink J., Kijne J. RAP-1 is an Arabidopsis MYC-like R protein homologue, that binds to G-box sequence motifs. Plant Mol Biol. 1997 May;34(1):169–174. doi: 10.1023/a:1005898823105. [DOI] [PubMed] [Google Scholar]
  38. de Vetten N., Quattrocchio F., Mol J., Koes R. The an11 locus controlling flower pigmentation in petunia encodes a novel WD-repeat protein conserved in yeast, plants, and animals. Genes Dev. 1997 Jun 1;11(11):1422–1434. doi: 10.1101/gad.11.11.1422. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES