Control of Plant Trichome and Root-Hair Development by a Tomato (Solanum lycopersicum) R3 MYB Transcription Factor

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Tominaga Wada, Rumi ^a   Nukumizu, Yuka ^a   Sato, Shusei ^b   Wada, Takuji ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

^b KAZUSA DNA RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; GENE REPRESSION; GENETIC SIMILARITY; GENETIC TRANSFORMATION; GL3 GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLANT DEVELOPMENT; PLANT GENE; PLANT GENOME; ROOT HAIR; TOMATO; TRICHOME; TRY GENE;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; PHYLOGENY; PLANT EPIDERMIS; PLANT ROOTS; PLANTS, GENETICALLY MODIFIED; TRANSCRIPTION FACTORS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; LYCOPERSICON ESCULENTUM;

EID: 84872257161     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054019     Document Type: Article

References (62)

1. Wada T, Tachibana T, Shimura Y, Okada K, (1997) Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277: 1113-1116.
2. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, et al. (2002) TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 21: 5036-5046.
3. Kirik V, Simon M, Huelskamp M, (2004) Schiefelbein J (2004) The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 268: 506-513.
4. Kirik V, Simon M, Wester K, (2004) Schiefelbein J, Hulskamp M (2004) ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol Biol 55: 389-398.
5. Esch JJ, Chen MA, Hillestad M, Marks MD, (2004) Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J 40: 860-869.
6. Simon M, Lee MM, Lin Y, Gish L, (2007) Schiefelbein J (2007) Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 311: 566-578.
7. Tominaga R, Iwata M, Sano R, Inoue K, Okada K, et al. (2008) Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135: 1335-1345.
8. Wang S, Kwak SH, Zeng Q, Ellis BE, Chen XY, et al. (2007) TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873-3882.
9. Gan L, Xia K, Chen JG, Wang S, (2011) Functional Characterization of TRICHOMELESS2, a New Single-Repeat R3 MYB Transcription Factor in the Regulation of Trichome Patterning in Arabidopsis. BMC Plant Biol 11: 176.
10. Tominaga-Wada R, Nukumizu Y, (2012) Expression Analysis of an R3-Type MYB Transcription Factor CPC-LIKE MYB4 (TRICHOMELESS2) and CPL4-Related Transcripts in Arabidopsis. Int J Mol Sci 13: 3478-3491.
11. Hulskamp M, Misra S, Jurgens G, (1994) Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555-566.
12. Payne CT, Zhang F, Lloyd AM, (2000) GL3 encodes a bHLH protein that regulates trichome development in arabidopsis through interaction with GL1 and TTG1. Genetics 156: 1349-1362.
13. Bernhardt C, Lee MM, Gonzalez A, Zhang F, Lloyd A, et al. (2003) The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130: 6431-6439.
14. Galway ME, Masucci JD, Lloyd AM, Walbot V, Davis RW, et al. (1994) The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev Biol 166: 740-754.
15. Rerie WG, Feldmann KA, Marks MD, (1994) The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev 8: 1388-1399.
16. Lee MM, (1999) Schiefelbein J (1999) WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99: 473-483.
17. Bernhardt C, Zhao M, Gonzalez A, Lloyd A, (2005) Schiefelbein J (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132: 291-298.
18. Koshino-Kimura Y, Wada T, Tachibana T, Tsugeki R, Ishiguro S, et al. (2005) Regulation of CAPRICE Transcription by MYB Proteins for Root Epidermis Differentiation in Arabidopsis. Plant Cell Physiol 46: 817-826.
19. Esch JJ, Chen M, Sanders M, Hillestad M, Ndkium S, et al. (2003) A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130: 5885-5894.
20. Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A, (2003) A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130: 4859-4869.
21. Szymanski DB, Jilk RA, Pollock SM, Marks MD, (1998) Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125: 1161-1171.
22. Lee MM, (2001) Schiefelbein J (2001) Developmentally distinct MYB genes encode functionally equivalent proteins in Arabidopsis. Development 128: 1539-1546.
23. Hülskamp M, Kirik V (2000) Trichome differentiation and morphogenesis in Arabidopsis. In: Hallahan DL, Gray JC, editors. Advances in Botanical Research. New York: Academic Press. 37-75.
24. Werker E (2000) Trichome diversity and development. In: Hallahan DL, Gray JC, editors. Advances in Botanical Research. New York: Academic Press. 37-75.
25. Kang JH, Liu G, Shi F, Jones AD, Beaudry RM, et al. (2010) The tomato odorless-2 mutant is defective in trichome-based production of diverse specialized metabolites and broad-spectrum resistance to insect herbivores. Plant Physiol 154: 262-272.
26. Kang JH, Shi F, Jones AD, Marks MD, Howe GA, (2010) Distortion of trichome morphology by the hairless mutation of tomato affects leaf surface chemistry. J Exp Bot 61: 1053-1064.
27. Schilmiller A, Shi F, Kim J, Charbonneau AL, Holmes D, et al. (2010) Mass spectrometry screening reveals widespread diversity in trichome specialized metabolites of tomato chromosomal substitution lines. Plant J 62: 391-403.
28. Luckwill LC, (1943) The genus Lycopersicon: a historical, biological and taxonomic survey of the wild and cultivated tomato. Aberd Univ Stud 120: 1-44.
29. Baur R, Binder S, Benz G, (1991) Non-glandular leaf trichomes as short-term inducible defense of the grey alder, Alnus incana (L.), against the chrysomelid beetle, Agelastica alni L. Oecologia. 87: 219-226.
30. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, et al. (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119: 71-84.
31. Cormack RGH, (1947) A comparative model of developing epidermal cells in white mustard and tomato roots. American Journal of Botany 34: 310-314.
32. Clowes FAL, (2000) Pattern in root meristem development in angiosperms. New Phytologist 146: 83-94.
33. Dolan L, Costa S, (2001) Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot 52: 413-417.
34. Kim DW, Lee SH, Choi SB, Won SK, Heo YK, et al. (2006) Functional conservation of a root hair cell-specific cis-element in angiosperms with different root hair distribution patterns. Plant Cell 18: 2958-2970.
35. Leavitt RG, (1904) Trichomes of the root in vascular cryptograms and angiosperms. Proc Boston Soc Nat Hist 31: 273-313.
36. Cormack RGH, (1937) The development of root hair by Elodea canadensis. New Phytol 36: 19-25.
37. Cutter EG, Hung CY, (1972) Symmetric and asymmetric mitosis and cytokinesis in the root tip of Hydrocharis morsus-ranae L. J Cell Sci. 11: 723-737.
38. Dolan L, (1996) Pattern in the root epidermis: an interplay of diffusible signals and cellular geometry. Annals of Botany 77: 547-553.
39. Pemberton LM, Tsai SL, Lovell PH, Harris PJ, (2001) Epidermal patterning in seedlings roots of eudicotyledons. Annals of Botany 87: 649-654.
40. Murashige T, Skoog F, (1962) A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiologia Plantarum 15: 473-497.
41. Kurata T, Ishida T, Kawabata-Awai C, Noguchi M, Hattori S, et al. (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132: 5387-5398.
42. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, et al. (2007) 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: 2531-2543.
43. Okada K, Shimura Y, (1990) Reversible Root Tip Rotation in Arabidopsis Seedlings Induced by Obstacle-Touching Stimulus. Science 250: 274-276.
44. Yoo SY, Bomblies K, Yoo SK, Yang JW, Choi MS, et al. (2005) The 35S promoter used in a selectable marker gene of a plant transformation vector affects the expression of the transgene. Planta 221: 523-530.
45. Clough SJ, Bent AF, (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
46. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
47. Girardi CL, Bermudez K, Bernadac A, Chavez A, Zouine M, et al. (2006) The mitochondrial elongation factor LeEF-Tsmt is regulated during tomato fruit ripening and upon wounding and ethylene treatment. Postharvest Biology and Technology 42: 1-7.
48. Tominaga-Wada R, Iwata M, Sugiyama J, Kotake T, Ishida T, et al. (2009) The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J 60: 564-574.
49. Yoshizumi T, Tsumoto Y, Takiguchi T, Nagata N, Yamamoto YY, et al. (2006) Increased level of polyploidy1, a conserved repressor of CYCLINA2 transcription, controls endoreduplication in Arabidopsis. Plant Cell 18: 2452-2468.
50. Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, et al. (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20: 735-747.
51. Tominaga-Wada R, Iwata M, Nukumizu Y, Wada T, (2011) Analysis of IIId, IIIe and IVa group basic-helix-loop-helix proteins expressed in Arabidopsis root epidermis. Plant Sci 181: 471-478.
52. Pires N, Dolan L, (2009) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27: 862-874.
53. Tominaga R, Iwata M, Okada K, Wada T, (2007) Functional analysis of the epidermal-specific MYB genes CAPRICE and WEREWOLF in Arabidopsis. Plant Cell 19: 2264-2277.
54. Wada T, Kurata T, Tominaga R, Koshino-Kimura Y, Tachibana T, et al. (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129: 5409-5419.
55. Consortium TTG, (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
56. Zhao M, Morohashi K, Hatlestad G, Grotewold E, Lloyd A, (2008) The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135: 1991-1999.
57. Baudry A, Heim MA, Dubreucq B, Caboche M, Weisshaar B, et al. (2004) TT2, TT8, and TTG1 synergistically specify the expression of BANYULS and proanthocyanidin biosynthesis in Arabidopsis thaliana. Plant J 39: 366-380.
58. Nesi N, Debeaujon I, Jond C, Pelletier G, Caboche M, et al. (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12: 1863-1878.
59. Baudry A, Caboche M, Lepiniec L, (2006) TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana. Plant J 46: 768-779.
60. Marks MD, Esch JJ, (2003) Initiating inhibition. Control of epidermal cell patterning in plants. EMBO Rep 4: 24-25.
61. Zhao H, Wang X, Zhu D, Cui S, Li X, et al. (2012) A single amino acid substitution in IIIf subfamily of basic helix-loop-helix transcription factor AtMYC1 leads to trichome and root hair patterning defects by abolishing its interaction with partner proteins in Arabidopsis. J Biol Chem 287: 14109-14121.
62. Pires N, Dolan L, (2010) Early evolution of bHLH proteins in plants. Plant Signal Behav 5: 911-912.