HD-Zip proteins GL2 and HDG11 have redundant functions in Arabidopsis trichomes, and GL2 activates a positive feedback loop via MYB23

Plant Cell

Volumn 26, Issue 5, 2014, Pages 2184-2200

  Khosla, Aashima ^a   Paper, Janet M ^a   Boehler, Allison P ^a,b   Bradley, Amanda M ^a   Neumann, Titus R ^a   Schrick, Kathrin ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b BAYER CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84903640682     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.120360     Document Type: Article

References (45)

1. Balkunde, R., Pesch, M., and Hülskamp, M. (2010). Trichome patterning in Arabidopsis thaliana from genetic to molecular models. Curr. Top. Dev. Biol. 91: 299-321.
2. Baumann, E., Lewald, J., Saedler, H., Schulz, B., and Wisman, E. (1998). Successful PCR-based reverse genetic screens using an En-1-mutagenised Arabidopsis thaliana population generated via single-seed descent. Theor. Appl. Genet. 97: 729-734.
3. Bruex, A., Kainkaryam, R.M., Wieckowski, Y., Kang, Y.H., Bernhardt, C., Xia, Y., Zheng, X., Wang, J.Y., Lee, M.M., Benfey, P., Woolf, P.J., and Schiefelbein, J. (2012). A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet. 8: e1002446.
4. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
5. Di Cristina, M., Sessa, G., Dolan, L., Linstead, P., Baima, S., Ruberti, I., and Morelli, G. (1996). The Arabidopsis Athb-10 (GLABRA2) is an HD-Zip protein required for regulation of root hair development. Plant J. 10: 393-402.
6. 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.
7. Floyd, S.K., Zalewski, C.S., and Bowman, J.L. (2006). Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173: 373-388.
8. Grebe, M. (2012). The patterning of epidermal hairs in Arabidopsis-Updated. Curr. Opin. Plant Biol. 15: 31-37.
9. Guan, X.Y., Li, Q.J., Shan, C.M., Wang, S., Mao, Y.B., Wang, L.J., and Chen, X.Y. (2008). The HD-Zip IV gene GaHOX1 from cotton is a functional homologue of the Arabidopsis GLABRA2. Physiol. Plant. 134: 174-182.
10. Hülskamp, M., Misŕa, S., and Jürgens, G. (1994). Genetic dissection of trichome cell development in Arabidopsis. Cell 76: 555-566.
11. Kamata, N., Okada, H., Komeda, Y., and Takahashi, T. (2013). Mutations in epidermis-specific HD-ZIP IV genes affect floral organ identity in Arabidopsis thaliana. Plant J. 75: 430-440.
12. Kang, Y.H., Kirik, V., Hulskamp, M., Nam, K.H., Hagely, K., Lee, M.M., and Schiefelbein, J. (2009). The MYB23 gene provides a positive feedback loop for cell fate specification in the Arabidopsis root epidermis. Plant Cell 21: 1080-1094.
13. Kirik, V., Lee, M.M., Wester, K., Herrmann, U., Zheng, Z., Oppenheimer, D., Schiefelbein, J., and Hulskamp, M. (2005). Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development 132: 1477-1485.
14. Kirik, V., Schnittger, A., Radchuk, V., Adler, K., Hülskamp, M., and Bäumlein, H. (2001). Ectopic expression of the Arabidopsis AtMYB23 gene induces differentiation of trichome cells. Dev. Biol. 235: 366-377.
15. Koornneef, M., Dellaert, L.W., and van der Veen, J.H. (1982). EMSand radiation-induced mutation frequencies at individual loci in Arabidopsis thaliana (L.) Heynh. Mutat. Res. 93: 109-123.
16. Li, S.F., Milliken, O.N., Pham, H., Seyit, R., Napoli, R., Preston, J., Koltunow, A.M., and Parish, R.W. (2009). The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21: 72-89.
17. Marks, M.D., Wenger, J.P., Gilding, E., Jilk, R., and Dixon, R.A. (2009). Transcriptome analysis of Arabidopsis wild-type and gl3-sst sim trichomes identifies four additional genes required for trichome development. Mol. Plant 2: 803-822.
18. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15: 473-497.
19. Nakamura, M., Katsumata, H., Abe, M., Yabe, N., Komeda, Y., Yamamoto, K.T., and Takahashi, T. (2006). Characterization of the class IV homeodomain-leucine zipper gene family in Arabidopsis. Plant Physiol. 141: 1363-1375.
20. Nordborg, M., et al. (2005). The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3: e196.
21. Ohashi, Y., Oka, A., Rodrigues-Pousada, R., Possenti, M., Ruberti, I., Morelli, G., and Aoyama, T. (2003). Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300: 1427-1430.
22. Peterson, K.M., Shyu, C., Burr, C.A., Horst, R.J., Kanaoka, M.M., Omae, M., Sato, Y., and Torii, K.U. (2013). Arabidopsis homeodomainleucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis. Development 140: 1924-1935.
23. Ponting, C.P., and Aravind, L. (1999). START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24: 130-132.
24. Prigge, M.J., and Clark, S.E. (2006). Evolution of the class III HD-Zip gene family in land plants. Evol. Dev. 8: 350-361.
25. 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.
26. Roeder, A.H., Chickarmane, V., Cunha, A., Obara, B., Manjunath, B.S., and Meyerowitz, E.M. (2010). Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biol. 8: e1000367.
27. Roeder, A.H., Cunha, A., Ohno, C.K., and Meyerowitz, E.M. (2012). Cell cycle regulates cell type in the Arabidopsis sepal. Development 139: 4416-4427.
28. Schrick, K., Nguyen, D., Karlowski, W.M., and Mayer, K.F. (2004). START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 5: R41.
29. Scott, S.P., Teh, A., Peng, C., and Lavin, M.F. (2002). One-step sitedirected mutagenesis of ATM cDNA in large (20kb) plasmid constructs. Hum. Mutat. 20: 323.
30. Shen, B., Sinkevicius, K.W., Selinger, D.A., and Tarczynski, M.C. (2006). The homeobox gene GLABRA2 affects seed oil content in Arabidopsis. Plant Mol. Biol. 60: 377-387.
31. Shi, L., Katavic, V., Yu, Y., Kunst, L., and Haughn, G. (2012). Arabidopsis glabra2 mutant seeds deficient in mucilage biosynthesis produce more oil. Plant J. 69: 37-46.
32. Sparkes, I.A., Runions, J., Kearns, A., and Hawes, C. (2006). Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1: 2019-2025.
33. Stracke, R., Werber, M., and Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4: 447-456.
34. Takada, S., Takada, N., and Yoshida, A. (2013). ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140: 1919-1923.
35. Tominaga-Wada, R., Iwata, M., Sugiyama, J., Kotake, T., Ishida, T., Yokoyama, R., Nishitani, K., Okada, K., and Wada, T. (2009). The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J. 60: 564-574.
36. Vernoud, V., Laigle, G., Rozier, F., Meeley, R.B., Perez, P., and Rogowsky, P.M. (2009). The HD-ZIP IV transcription factor OCL4 is necessary for trichome patterning and anther development in maize. Plant J. 59: 883-894.
37. Wang, S., and Chen, J.G. (2008). 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: 1792-1804.
38. Wang, S., Kwak, S.H., Zeng, Q., Ellis, B.E., Chen, X.Y., Schiefelbein, J., and Chen, J.G. (2007). TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134: 3873-3882.
39. Western, T.L., Burn, J., Tan, W.L., Skinner, D.J., Martin-McCaffrey, L., Moffatt, B.A., and Haughn, G.W. (2001). Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol. 127: 998-1011.
40. Western, T.L., Skinner, D.J., and Haughn, G.W. (2000). Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol. 122: 345-356.
41. Wu, R., Li, S., He, S., Wassmann, F., Yu, C., Qin, G., Schreiber, L., Qu, L.J., and Gu, H. (2011). CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell 23: 3392-3411.
42. Yang, C., Li, H., Zhang, J., Wang, T., and Ye, Z. (2011). Finemapping of the woolly gene controlling multicellular trichome formation and embryonic development in tomato. Theor. Appl. Genet. 123: 625-633.
43. Yang, C.X., and Ye, Z.B. (2013). Trichomes as models for studying plant cell differentiation. Cell. Mol. Life Sci. 70: 1937-1948.
44. Yang, J.Y., Chung, M.C., Tu, C.Y., and Leu, W.M. (2002). OSTF1: a HD-GL2 family homeobox gene is developmentally regulated during early embryogenesis in rice. Plant Cell Physiol. 43: 628-638.
45. Zhu, J.-Y., Sun, Y., and Wang, Z.-Y. (2012). Genome-wide identification of transcription factor-binding sites in plants using chromatin immunoprecipitation followed by microarray (ChIP-chip) or sequencing (ChIP-seq). Methods Mol. Biol. 876: 173-188.