Regulation of cell fate determination by single-repeat R3 MYB transcription factors in Arabidopsis

Frontiers in Plant Science

Volumn 5, Issue APR, 2014, Pages

  Wang, Shucai ^a   Chen, Jin Gui ^b  

^a NORTHEAST NORMAL UNIVERSITY   (China)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

CPC; GL1; GL2; GL3; R3 MYB; Root hair; Trichome; TRY

Indexed keywords

EID: 84901046696     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00133     Document Type: Review

References (82)

1. Bernhardt, C., Zhao, M., Gonzalez, A., Lloyd, A., and 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. doi: 10.1242/dev.01565
2. Bruex, A., Kainkaryam, R. M., Wieckowski, Y., Kang, Y. H., Bernhardt, C., Xia, Y., et al. (2012). A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet. 8:e1002446. doi: 10.1371/journal.pgen.1002446
3. Chen, Y., Yang, X., He, K., Liu, M., Li, J., Gao, Z., et al. (2006). The MYB transcription factor superfamily of Arabidopsis: expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol. Biol. 60, 107-124. doi: 10.1007/s11103-005-2910-y
4. Digiuni, S., Schellmann, S., Geier, F., Greese, B., Pesch, M., Wester, K., et al. (2008). A competitive complex formation mechanism underlies trichome patterning on Arabidopsis leaves. Mol. Syst. Biol. 4, 217. doi: 10.1038/msb.2008.54
5. Dolan, L., and Costa, S. (2001). Evolution and genetics of root hair stripes in the root epidermis. J. Exp. Bot. 52, 413-417. doi: 10.1093/jexbot/52.suppl_1.413
6. Dubos, C., Le Gourrierec, J., Baudry, A., Huep, G., Lanet, E., Debeaujon, I., et al. (2008). MYBL2 is a new regulator of flavonoid biosynthesis in Arabidopsis thaliana. Plant J. 55, 940-953. doi: 10.1111/j.1365-313X.2008.03564.x
7. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., and Lepiniec, L. (2010). MYB transcription factors in Arabidopsis. Trends Plant Sci. 15, 573-581. doi: 10.1016/j.tplants.2010.06.005
8. Eisner, T., Eisner, M., and Hoebeke, E. R. (1998). When defence backfires: detrimental effect of a plant's protective trichomes on an insect beneficial to the plant. Proc. Natl. Acad. Sci. U.S.A. 95, 4410-4414. doi: 10.1073/pnas.95.8.4410
9. Esch, J. J., Chen, M. A., Hillestad, M., and Marks, M. D. (2004). Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J. 40, 860-869. doi: 10.1111/j.1365-313X.2004.02259.x
10. Esch, J. J., Chen, M., Sanders, M., Hillestad, M., Ndkium, S., Idelkope, B., et al. (2003). A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130, 5885-5894 doi: 10.1242/dev.00812
11. Galway, M. E., Masucci, J. D., Lloyd, A. M., Walbot, V., Davis, R. W., and Schiefelbein, J. W. (1994). The TTG gene is required to specify epidermal cell fate and cell patterning in the Arabidopsis root. Dev. Biol. 166, 740-754. doi: 10.1006/dbio.1994.1352
12. Gan, L., Xia, K., Chen, J. G., and 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. doi: 10.1186/1471-2229-11-176
13. Gonzalez, A., Zhao, M., Leavitt, J. M., and Lloyd, A. M. (2008). Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814-827. doi: 10.1111/j.1365-313X.2007.03373.x
14. Grebe, M. (2012). The patterning of epidermal hairs in Arabidopsis-updated. Curr. Opin. Plant Biol. 15, 31-37. doi: 10.1016/j.pbi.2011.10.010
15. Hilscher, J., Schlötterer, C., and Hauser, M. T. (2009). A single amino acid replacement in ETC2 shapes trichome patterning in natural Arabidopsis populations. Curr. Biol. 19, 1747-1751. doi: 10.1016/j.cub.2009.08.057
16. Hülskamp, M., Misra, S., and Jürgens, G. (1994). Genetic dissection of trichome cell development in Arabidopsis. Cell 76, 555-566. doi: 10.1016/0092-8674(94)90118-X
17. Hülskamp, M., and Schnittger, A. (1998). Spatial regulation of trichome formation in Arabidopsis thaliana. Semin. Cell Dev. Biol. 9, 213-220. doi: 10.1006/scdb.1997.0209
18. Ishida, T., Kurata, T., Okada, K., and Wada, T. (2008). A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59, 364-386. doi: 10.1146/annurev.arplant.59.032607.092949
19. Gilroy, S., and Jones, D. L. (2000). Through form to function: root hair development and nutrient uptake. Trends Plant Sci. 5, 56-60. doi: 10.1016/S1360-1385(99)01551-4
20. Kang, Y. H., Kirik, V., Hulskamp, M., Nam, K. H., Hagely, K., Lee, M. M., et al. (2009). The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell 21, 1080-1094. doi: 10.1105/tpc.108.063180
21. Kang, Y. H., Song, S. K., Schiefelbein, J., and Lee, M. M. (2013). Nuclear trapping controls the position-dependent localization of CAPRICE in the root epidermis of Arabidopsis. Plant Physiol. 163, 193-204. doi: 10.1104/pp.113.221028
22. Katiyar, A., Smita, S., Lenka, S. K., Rajwanshi, R., Chinnusamy, V., and Bansal, K. C. (2012). Genome-wide classification and expression analysis of MYB transcription factor families in rice and Arabidopsis. BMC Genomics 13:544. doi: 10.1186/1471-2164-13-544
23. Kim, H. J., and Triplett, B. A. (2001). Cotton fibre growth in planta and in vitro: models for plant cell elongation and cell wall biogenesis. Plant Physiol. 127, 1361-1366. doi: 10.1104/pp.010724
24. Kirik, V., Simon, M., Hülskamp, M., and Schiefelbein, J. (2004a). 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. doi: 10.1016/j.ydbio.2003.12.037
25. Kirik, V., Simon, M., Wester, K., Schiefelbein, J., and Hülskamp, M. (2004b). 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. doi: 10.1007/s11103-004-0893-8
26. Koshino-Kimura, Y., Wada, T., Tachibana, T., Tsugeki, R., Ishiguro, S., and Okada, K. (2005). Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol. 46, 817-826. doi: 10.1093/pcp/pci096
27. Kurata, T., Ishida, T., Kawabata-Awai, C., Noguchi, M., Hattori, S., Sano, R., et al. (2005). Cell-to-cell movement of the CAPRICEprotein in Arabidopsis root epidermal cell differentiation. Development 132, 5387-5398. doi: 10.1242/dev.02139
28. Kwak, S. H., and Schiefelbein, J. (2007). The role of the SCRAMBLED receptor-like kniase in patterning the Arabidopsis root epidermis. Dev. Biol. 302, 118-131. doi: 10.1016/j.ydbio.2006.09.009
29. Kwak, S. H., Shen, R., and Schiefelbein, J. (2005). Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307, 1111-1113. doi: 10.1126/science.1105373
30. Lee, M. M., and Schiefelbein, J. (1999). WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99, 473-483. doi: 10.1016/S0092-8674(00)81536-6
31. Liu, C., Zhao, Y., and Wang, Y. (2006). Artemisinin: current state and perspectives for biotechnological production of an anti malarial drug. Appl. Microbiol. Biotechnol. 72, 11-20. doi: 10.1007/s00253-006-0452-0
32. Lommen, W. J., Schenk, E., Bouwmeester, H. J., and Verstappen, F. W. (2006). Trichome dynamics and artemisinin accumulation during development and senescence of Artemisia annua leaves. Planta Med. 72, 336-345. doi: 10.1055/s-2005-916202
33. Marks, M. D. (1997). Molecular genetic analysis of trichome development in Arabidopsis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 137-163. doi: 10.1146/annurev.arplant.48.1.137
34. Masucci, J. D., Rerie, W. G., Foreman, D. R., Zhang, M., Galway, M. E., Marks, M. D., et al. (1996). The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253-1260.
35. Matsui, K., Umemura, Y., and Ohme-Takagi, M. (2008). AtMYBL2, a protein with a single MYB domain, acts as a negative regulator of anthocyanin biosynthesis in Arabidopsis. Plant J. 55, 954-967. doi: 10.1111/j.1365-313X.2008.03565.x
36. Mauricio, R., and Rausher, M. D. (1997). Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51, 1435-1444. doi: 10.2307/2411196
37. Morohashi, K., Zhao, M., Yang, M., Read, B., Lloyd, A., Lamb, R., et al. (2007). Participation of the Arabidopsis bHLH factor GL3 in trichome initiation regulatory events. Plant Physiol. 145, 736-746. doi: 10.1104/pp.107.104521
38. Nadeau, J. A., and Sack, F. D. (2002). Control of stomatal distribution on the Arabidopsis leaf surface. Science 296, 1697-1700. doi: 10.1126/science.1069596
39. Nemie-Feyissa, D., Olafsdottir, S. M., Heidari, B., and Lillo, C. (2014). Nitrogen depletion and small R3-MYB transcription factors affecting anthocyanin accumulation in Arabidopsis leaves. Phytochemistry 98, 34-40. doi: 10.1016/j.phytochem.2013.12.006
40. Nukumizu, Y., Wada, T., and Tominaga-Wada, R. (2013). Tomato (Solanum lycopersicum) homologs of TRIPTYCHON (SlTRY) and GLABRA3 (SlGL3) are involved in anthocyanin accumulation. Plant Signal. Behav. 8, e24575. doi: 10.4161/psb.24575
41. Oppenheimer, D. G., Herman, P. L., Sivakumaran, S., Esch, J., and Marks, M. D. (1991). A myb gene required for leaf trichome differentiation in Arabidopsis is expressed in stipules. Cell 67, 483-493. doi: 10.1016/0092-8674(91)90523-2
42. Patra, B., Pattanaik, S., and Yuan, L. (2013). Ubiquitin protein ligase 3 mediates the proteasomal degradation of GLABROUS 3 and ENHANCER OF GLABROUS 3, regulators of trichome development and flavonoid biosynthesis in Arabidopsis. Plant J. 74, 435-447. doi: 10.1111/tpj.12132
43. Payne, C. T., Zhang, F., and Lloyd, A. M. (2000). GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156, 1349-1362.
44. Pesch, M., and Hülskamp, M. (2004). Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Curr. Opin. Genet. Dev. 14, 422-427. doi: 10.1016/j.gde.2004.06.007
45. Pesch, M., and Hülskamp, M. (2009). One, two, three. models for trichome patterning in Arabidopsis? Curr. Opin. Plant Biol. 12, 587-592. doi: 10.1016/j.pbi.2009.07.015
46. Pesch, M., and Hülskamp, M. (2011). Role of TRIPTYCHON in trichome patterning in Arabidopsis. BMC Plant Biol. 11:130. doi: 10.1186/1471-2229-11-130
47. Pesch, M., Schultheiß, I., Digiuni, S., Uhrig, J. F., and Hülskamp, M. (2013). Mutual control of intracellular localisation of the patterning proteins AtMYC1, GL1 and TRY/CPC in Arabidopsis. Development 140, 3456-3467. doi: 10.1242/dev.094698
48. Rerie, W. G., Feldmann, K. A., and Marks, M. D. (1994). The GLABRA2 gene encodes a homeo domain protein required for normal trichome development in Arabidopsis. Genes Dev. 8, 1388-1399. doi: 10.1101/gad.8.12.1388
49. Ryu, K. H., Kang, Y. H., Park, Y. H., Hwang, I., Schiefelbein, J., and Lee, M. M. (2005). The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development 132, 4765-4775. doi: 10.1242/dev.02055
50. Ryu, K. H., Zheng, X., Huang, L., and Schiefelbein, J. (2013). Computational modeling of epidermal cell fate determination systems. Curr. Opin. Plant Biol. 16, 5-10. doi: 10.1016/j.pbi.2012.12.003
51. Savage, N. S., Walker, T., Wieckowski, Y., Schiefelbein, J., Dolan, L., and Monk, N. A. (2008). A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol. 6:e235. doi: 10.1371/journal.pbio.0060235
52. Schellmann, S., Hülskamp, M., and Uhrig, J. (2007). Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem. Soc. Trans. 35, 146-148. doi: 10.1042/BST0350146
53. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., et al. (2002). TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J. 21, 5036-5046. doi: 10.1093/emboj/cdf524
54. Schiefelbein, J. (2003). Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74-78. doi: 10.1016/S136952660200002X
55. Schiefelbein, J., Huang, L., and Zheng, X. (2014). Regulation of epidermal cell fate in Arabidopsis roots: the importance of multiple feedback loops. Front. Plant Sci. 5:47. doi: 10.3389/fpls.2014.00047
56. Schiefelbein, J., Kwak, S. H., Wieckowski, Y., Barron, C., and Bruex, A. (2009). The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J. Exp. Bot. 60, 1515-1521. doi: 10.1093/jxb/ern339
57. Schiefelbein, J. W. (2000). Constructing a plant cell. The genetic control of root hair development. Plant Physiol. 124, 1525-1531. doi: 10.1104/pp.124.4.1525
58. Schnittger, A., Folkers, U., Schwab, B., Jürgens, G., and Hülskamp, M. (1999). Generation of a spacing pattern: the role of TRIPTYCHON in trichome patterning in Arabidopsis. Plant Cell 11, 1105-1116.
59. Serna, L. (2005). Epidermal cell patterning and differentiation throughout the apical-basal axis of the seedling. J. Exp. Bot. 56, 1983-1989. doi: 10.1093/jxb/eri213
60. Serna, L. (2008). CAPRICE positively regulates stomatal formation in the Arabidopsis hypocotyl. Plant Signal. Behav. 3, 1077-1082. doi: 10.4161/psb.3.12.6254
61. Simon, M., Lee, M. M., Lin, Y., Gish, L., and Schiefelbein, J. (2007). Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev. Biol. 311, 566-578. doi: 10.1016/j.ydbio.2007.09.001
62. Song, S. K., Ryu, K. H., Kang, Y. H., Song, J. H., Cho, Y. H., Yoo, S. D., et al. (2011). Cell fate in the Arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiol. 157, 1196-1208. doi: 10.1104/pp.111.185785
63. Stracke, R., Werber, M., and Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456. doi: 10.1016/S1369-5266(00)00199-0
64. Tominaga, R., Iwata, M., Sano, R., Inoue, K., Okada, K., and Wada, T. (2008). Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135, 1335-1345. doi: 10.1242/dev.017947
65. Tominaga-Wada, R., Ishida, T., and Wada, T. (2011). New insights into the mechanism of development of Arabidopsis root hairs and trichomes. Int. Rev. Cell Mol. Biol. 286, 67-106. doi: 10.1016/B978-0-12-385859-7.00002-1
66. Tominaga-Wada, R., and 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. doi: 10.3390/ijms13033478
67. Tominaga-Wada, R., Nukumizu, Y., Sato, S., and Wada, T. (2013a). Control of plant trichome and root-hair development by a tomato (Solanum lycopersicum) R3 MYB transcription factor. PLoS ONE 8:e54019. doi: 10.1371/journal.pone.0054019
68. Tominaga-Wada, R., Nukumizu, Y., and Wada, T. (2013b). Flowering is delayed by mutations in homologous genes CAPRICE and TRYPTICHON in the early flowering Arabidopsis cpl3 mutant. J. Plant Physiol. 170, 1466-1468. doi: 10.1016/j.jplph.2013.05.013
69. Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., et al. (2002). Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409-5419. doi: 10.1242/dev.00111
70. Wada, T., Tachibana, T., Shimura, Y., and Okada, K. (1997). Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277, 1113-1116. doi: 10.1126/science.277.5329.1113
71. Wagner, G. J., Wang, E., and Shepherd, R. W. (2004). New approaches for studying and exploiting an old protuberance, the plant trichome. Ann. Bot. 93, 3-11. doi: 10.1093/aob/mch011
72. Walker, A. R., Davison, P. A., Bolognesi-Winfield, A. C., James, C. M., Srinivasan, N., Blundell, T. L., et al. (1999). The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11, 1337-1350.
73. Wang, S., Barron, C., Schiefelbein, J., and Chen, J. G. (2010). Distinct relationships between GLABRA2 and single-repeat R3 MYB transcription factors in the regulation of trichome and root hair patterning in Arabidopsis. New Phytol. 185, 387-400. doi: 10.1111/j.1469-8137.2009.03067.x
74. Wang, S., Hubbard, L., Chang, Y., Guo, J., Schiefelbein, J., and Chen, J. G. (2008). Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. BMC Plant Biol. 8:81. doi: 10.1186/1471-2229-8-81
75. Wang, S., Kwak, S. H., Zeng, Q., Ellis, B. E., Chen, X. Y., Schiefelbein, J., et al. (2007). TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134, 3873-3882. doi: 10.1242/dev.009597
76. Werker, E. (2000). Trichome diversity and development. Adv. Bot. Res. 31, 1-35. doi: 10.1016/S0065-2296(00)31005-9
77. Wester, K., Digiuni, S., Geier, F., Timmer, J., Fleck, C., and Hülskamp, M. (2009). Functional diversity of R3 single-repeat genes in trichome development. Development 136, 1487-1496. doi: 10.1242/dev.021733
78. Yu, N., Cai, W. J., Wang, S., Shan, C. M., Wang, L. J., and Chen, X. Y. (2010). Temporal control of trichome distribution by MicroRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell 22, 2322-2335. doi: 10.1105/tpc.109.072579
79. Zhang, F., Gonzalez, A., Zhao, M., Payne, C. T., and Lloyd, A. (2003). A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130, 4859-4869. doi: 10.1242/dev.00681
80. Zhao, M., Morohashi, K., Hatlestad, G., Grotewold, E., and Lloyd, A. (2008). The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development 135, 1991-1999. doi: 10.1242/dev.016873
81. Zhu, H. F., Fitzsimmons, K., Khandelwal, A., and Kranz, R. G. (2009). CPC, a single-repeat R3 MYB, is a negative regulator of anthocyanin biosynthesis in Arabidopsis. Mol. Plant 2, 790-802. doi: 10.1093/mp/ssp030
82. Zimmermann, I. M., Heim, M. A., Weisshaar, B., and Uhrig, J. F. (2004). Comprehensive identification of Arabidopsis thaliana MYB transcription factors interacting with R/B-like BHLH proteins. Plant J. 40, 22-34. doi: 10.1111/j.1365-313X.2004.02183.x