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. 1999 Apr;151(4):1591–1604. doi: 10.1093/genetics/151.4.1591

Allele-specific interactions between ttg and gl1 during trichome development in Arabidopsis thaliana.

J C Larkin 1, J D Walker 1, A C Bolognesi-Winfield 1, J C Gray 1, A R Walker 1
PMCID: PMC1460562  PMID: 10101180

Abstract

Trichome development in Arabidopsis thaliana is a well-characterized model for the study of plant cell differentiation. Two genes that play an essential role in the initiation of trichome development are GL1 and TTG. Mutations in either gene prevent the initiation of most trichomes. The GL1 gene encodes a myb-related transcription factor. Mutations in TTG are pleiotropic, affecting anthocyanins, root hairs, and seed coat mucilage in addition to trichomes. Six ttg alleles were examined and shown to form a hypomorphic series. The severity of all aspects of the ttg phenotype varied in parallel in this allelic series. The weakest allele, ttg-10, causes frequent clusters of adjacent trichomes, suggesting a role for TTG in inhibiting neighboring cells from choosing the trichome fate. This allele results from a mutation in the 5'-untranslated region of ttg and creates an out-of-frame upstream AUG codon. The ttg-10 allele shows several unusual genetic interactions with the weak hypomorphic gl1-2 allele, including intergenic noncomplementation and a synthetic glabrous phenotype. These interactions are specific for the gl1-2 allele. The implication of these results for current models of trichome development is discussed.

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Selected References

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  1. Akada R., Kallal L., Johnson D. I., Kurjan J. Genetic relationships between the G protein beta gamma complex, Ste5p, Ste20p and Cdc42p: investigation of effector roles in the yeast pheromone response pathway. Genetics. 1996 May;143(1):103–117. doi: 10.1093/genetics/143.1.103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artavanis-Tsakonas S., Matsuno K., Fortini M. E. Notch signaling. Science. 1995 Apr 14;268(5208):225–232. doi: 10.1126/science.7716513. [DOI] [PubMed] [Google Scholar]
  3. Benezra R., Davis R. L., Lockshon D., Turner D. L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 1990 Apr 6;61(1):49–59. doi: 10.1016/0092-8674(90)90214-y. [DOI] [PubMed] [Google Scholar]
  4. Brennan K., Tateson R., Lewis K., Arias A. M. A functional analysis of Notch mutations in Drosophila. Genetics. 1997 Sep;147(1):177–188. doi: 10.1093/genetics/147.1.177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burke D., Gasdaska P., Hartwell L. Dominant effects of tubulin overexpression in Saccharomyces cerevisiae. Mol Cell Biol. 1989 Mar;9(3):1049–1059. doi: 10.1128/mcb.9.3.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chandler V. L., Radicella J. P., Robbins T. P., Chen J., Turks D. Two regulatory genes of the maize anthocyanin pathway are homologous: isolation of B utilizing R genomic sequences. Plant Cell. 1989 Dec;1(12):1175–1183. doi: 10.1105/tpc.1.12.1175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cone K. C., Burr F. A., Burr B. Molecular analysis of the maize anthocyanin regulatory locus C1. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9631–9635. doi: 10.1073/pnas.83.24.9631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cone K. C., Cocciolone S. M., Burr F. A., Burr B. Maize anthocyanin regulatory gene pl is a duplicate of c1 that functions in the plant. Plant Cell. 1993 Dec;5(12):1795–1805. doi: 10.1105/tpc.5.12.1795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Esch J. J., Oppenheimer D. G., Marks M. D. Characterization of a weak allele of the GL1 gene of Arabidopsis thaliana. Plant Mol Biol. 1994 Jan;24(1):203–207. doi: 10.1007/BF00040586. [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. Grotewold E., Drummond B. J., Bowen B., Peterson T. The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell. 1994 Feb 11;76(3):543–553. doi: 10.1016/0092-8674(94)90117-1. [DOI] [PubMed] [Google Scholar]
  12. Hays T. S., Deuring R., Robertson B., Prout M., Fuller M. T. Interacting proteins identified by genetic interactions: a missense mutation in alpha-tubulin fails to complement alleles of the testis-specific beta-tubulin gene of Drosophila melanogaster. Mol Cell Biol. 1989 Mar;9(3):875–884. doi: 10.1128/mcb.9.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huffaker T. C., Hoyt M. A., Botstein D. Genetic analysis of the yeast cytoskeleton. Annu Rev Genet. 1987;21:259–284. doi: 10.1146/annurev.ge.21.120187.001355. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hülskamp M., Schnittger A. Spatial regulation of trichome formation in Arabidopsis thaliana. Semin Cell Dev Biol. 1998 Apr;9(2):213–220. doi: 10.1006/scdb.1997.0209. [DOI] [PubMed] [Google Scholar]
  16. Irish V. F., Sussex I. M. Function of the apetala-1 gene during Arabidopsis floral development. Plant Cell. 1990 Aug;2(8):741–753. doi: 10.1105/tpc.2.8.741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jacobson A., Peltz S. W. Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu Rev Biochem. 1996;65:693–739. doi: 10.1146/annurev.bi.65.070196.003401. [DOI] [PubMed] [Google Scholar]
  18. Joshi C. P., Zhou H., Huang X., Chiang V. L. Context sequences of translation initiation codon in plants. Plant Mol Biol. 1997 Dec;35(6):993–1001. doi: 10.1023/a:1005816823636. [DOI] [PubMed] [Google Scholar]
  19. Keegan L., Gill G., Ptashne M. Separation of DNA binding from the transcription-activating function of a eukaryotic regulatory protein. Science. 1986 Feb 14;231(4739):699–704. doi: 10.1126/science.3080805. [DOI] [PubMed] [Google Scholar]
  20. Klein T. M., Roth B. A., Fromm M. E. Regulation of anthocyanin biosynthetic genes introduced into intact maize tissues by microprojectiles. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6681–6685. doi: 10.1073/pnas.86.17.6681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Larkin J. C., Marks M. D., Nadeau J., Sack F. Epidermal cell fate and patterning in leaves. Plant Cell. 1997 Jul;9(7):1109–1120. doi: 10.1105/tpc.9.7.1109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Larkin J. C., Oppenheimer D. G., Pollock S., Marks M. D. Arabidopsis GLABROUS1 Gene Requires Downstream Sequences for Function. Plant Cell. 1993 Dec;5(12):1739–1748. doi: 10.1105/tpc.5.12.1739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. 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]
  28. Marks M. David. MOLECULAR GENETIC ANALYSIS OF TRICHOME DEVELOPMENT IN ARABIDOPSIS. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):137–163. doi: 10.1146/annurev.arplant.48.1.137. [DOI] [PubMed] [Google Scholar]
  29. Neer E. J., Schmidt C. J., Nambudripad R., Smith T. F. The ancient regulatory-protein family of WD-repeat proteins. Nature. 1994 Sep 22;371(6495):297–300. doi: 10.1038/371297a0. [DOI] [PubMed] [Google Scholar]
  30. 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]
  32. 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]
  33. 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]
  34. Rerie W. G., Feldmann K. A., Marks M. D. The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 1994 Jun 15;8(12):1388–1399. doi: 10.1101/gad.8.12.1388. [DOI] [PubMed] [Google Scholar]
  35. Rieping M., Fritz M., Prat S., Gatz C. A dominant negative mutant of PG13 suppresses transcription from a cauliflower mosaic virus 35S truncated promoter in transgenic tobacco plants. Plant Cell. 1994 Aug;6(8):1087–1098. doi: 10.1105/tpc.6.8.1087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schnittger A., Jürgens G., Hülskamp M. Tissue layer and organ specificity of trichome formation are regulated by GLABRA1 and TRIPTYCHON in Arabidopsis. Development. 1998 Jun;125(12):2283–2289. doi: 10.1242/dev.125.12.2283. [DOI] [PubMed] [Google Scholar]
  37. Simon M. A., Bowtell D. D., Dodson G. S., Laverty T. R., Rubin G. M. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signaling by the sevenless protein tyrosine kinase. Cell. 1991 Nov 15;67(4):701–716. doi: 10.1016/0092-8674(91)90065-7. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Theisen H., Purcell J., Bennett M., Kansagara D., Syed A., Marsh J. L. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development. 1994 Feb;120(2):347–360. doi: 10.1242/dev.120.2.347. [DOI] [PubMed] [Google Scholar]
  40. Wada T., Tachibana T., Shimura Y., Okada K. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science. 1997 Aug 22;277(5329):1113–1116. doi: 10.1126/science.277.5329.1113. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. van Hoof A., Green P. J. Premature nonsense codons decrease the stability of phytohemagglutinin mRNA in a position-dependent manner. Plant J. 1996 Sep;10(3):415–424. doi: 10.1046/j.1365-313x.1996.10030415.x. [DOI] [PubMed] [Google Scholar]

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