Epidermal cell differentiation

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T. Kurata, M. Iwata, T. Murata, T. Maruyama, T. Nishiyama tekurata@nibb.ac.jp, tomoakin@kenroku.kanazawa-u.ac.jp

The transition of green plants to land from an aqueous environment resulted in evolutionary pressure for epidermal tissue differentiation (Raven et al., 2005). In A. thaliana, proper initiation of a surface layer from a shoot meristem requires ATML1 and PDF2, which are members of the HD-Zip IV gene family (Abe et al., 2003). In addition to these genes, the angiosperm HD-Zip IV family includes ANL2 (Kubo et al., 1999) and GL2 (Masucci et al., 1996), both of which are involved in epidermal cell differentiation. All four genes together with 11 other uncharacterised genes form the HD-Zip IV group. Land plant orthologues of these genes were expanded in each of angiosperms, S. moellendorffii and P. patens lineages, suggesting that the molecular mechanism of epidermal cell-type determination in angiosperms differentiated after the divergence of P. patens and S. moellendorffii.

The patterning of cell fate in epidermal cells by the induction of GL2 is determined by intra- and inter-cellular regulatory circuits of transcription factors (Larkin et al., 2003). A complex containing WD40 (TTG1), R2-R3 MYB (GL1 and WER), and bHLH (EGL3 and GL3) is involved in trichome and root hair patterning in A. thaliana (Larkin et al., 2003). Putative orthologues of the genes encoding bHLH were found in all land plant lineages, but putative orthologues of TTG1 were only found in angiosperms. The genes encoding R2-R3 MYB genes, which belong to subgroup 15 of the MYB family and carry the signature amino acid sequence WVxxDxFELSxL (Kranz et al., 1998; Stracke et al., 2001), were found only in eudicots. CPC, a member of the R3-small MYB family that includes ETC1, ETC2, and TRY, moves between cells to regulate the protein cassette, resulting in the determination of cell fate in neighbouring cells(Wada et al., 2002; Kurata et al., 2005). The R3-small MYB genes were found only in angiosperms. The lack of R3-small MYB suggests that the molecular mechanism of epidermal cell patterning is different in S. moellendorffii and P. patens from that in A. thaliana. Genes encoding proteins involved in the basal machinery of epidermal cell differentiation such as the putative GTP-binding protein RHD3 (Wang et al., 1997) and the serine/threonine protein kinase IRE (Oyama et al., 2002) were conserved in all land plants.

Flavonoids function as a protectant from ultraviolet radiation and pathogens, and as a pigment for attracting insects in angiosperms. The WD40/R2-R3 MYB/bHLH protein cassette is also used in flavonoid biosynthesis (Zhang et al., 2003). Expansion of the bHLH genes in angiosperms is likely related to their subfunctionalization into root hair and trichome differentiation and flavonoid biosynthesis.


References

Abe, M., Katsumata, H., Komeda, Y., and Takahashi, T. (2003). Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development 130, 635-643.

Kranz, H.D., Denekamp, M., Greco, R., Jin, H., Leyva, A., Meissner, R.C., Petroni, K., Urzainqui, A., Bevan, M., Martin, C., Smeekens, S., Tonelli, C., Paz-Ares, J., and Weisshaar, B. (1998). Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J. 16, 263-276.

Kubo, H., Peeters, A.J.M., Aarts, M.G.M., Pereira, A., and Koornneef, M. (1999). ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plan Cell 11, 1217-1226.

Kurata, T., Ishida, T., Kawabata-Awai, C., Noguchi, M., Hattori, S., Sano, R., Nagasaka, R., Tominaga, R., Koshino-Kimura, Y., Kato, T., Sato, S., Tabata, S., Okada, K., and Wada, T. (2005). Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132, 5387-5398.

Larkin, J.C., Brown, M.L., and Schiefelbein, J. (2003). How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu. Rev. Plant Biol. 54, 403-430.

Masucci, J.D., Rerie, W.G., Foreman, D.R., Zhang, M., Galway, M.E., Marks, M.D., and Schiefelbein, J.W. (1996). The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122, 1253-1260.

Oyama, T., Shimura, Y., and Okada, K. (2002). The IRE gene encodes a protein kinase homologue and modulates root hair growth in Arabidopsis. Plant J. 30, 289-299.

Raven, P.H., Evert, R.F., and Eichhorn, S.E. (2005). Biology of Plants. (New York: W. H. Freeman and Company).

Stracke, R., Werber, M., and Weisshaar, B. (2001). The R2R3-MYB gene family in Arabidopsis thaliana. Curr. Opin. Plant Biol. 4, 447-456.

Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., Marks, M.D., Shimura, Y., and Okada, K. (2002). Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409-5419.

Wang, H.Y., Lockwood, S.K., Hoeltzel, M.F., and Schiefelbein, J.W. (1997). The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Genes Dev. 11, 799-811.

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.

Table of gene numbers

Gene functions Gene Gene used as a query The number of putative orthologs
Arabidopsis thaliana Oryza sativa Selaginalla moellendorffii Physcomitrella patens
Epidermal cell differentiation ANL2, AtML1, GL2, and PDF2 1), 4) GL2 17 10 5 (9) 4
Epidermal cell differentiation TTG1 TTG1 1 1 0 0
Epidermal cell differentiation ATAN11 TTG1 2 1 1 (2) 4
Epidermal cell differentiation MYB23, GL1, and WER 1) MYB23 3 0 0 0
Epidermal cell differentiation EGL3, GL3, and TT8 4) GL3 4 7 1 (2) 1
Epidermal cell differentiation CPC, ETC1, ETC2, and TRY CPC 6 1 0 0
Epidermal cell differentiation RHD3 4) RHD3 3 3 1 (1) 3
Epidermal cell differentiation IRE 2), 4) IRE 4 2 2 (4) 5
Epidermal cell differentiation AKT1 and SPIK AKT1 7 9 0 4
Epidermal cell differentiation RHD2 2), 4) RHD2 10 9 11 (20) 4
Epidermal cell differentiation RIC1 to RIC10 2) RIC1 10 10 1 (2) 1
Epidermal cell differentiation SUB SUB 3 4 0 0

Table of gene models in the assembly

protein id gene name
450557 HDZ41-1
450555 HDZ41-2
146759 HDZ42-1
234698 HDZ42-2
230527 HDZ43-1
140884 HDZ43-2
270223 AN11-1
146202 AN11-2
73360 GL3-1
87033 GL3-2
73603 RHD3-1
439743 RHD3-2
89070 IRE1-1
451604 IRE1-2
97417 RHD2L1-1
135543 RHD2L1-2
101139 RHD2L2-1
122844 RHD2L2-2
451605 RHD2L3-1
81185 RHD2L4-1
128789 RHD2L4-2
451607 RHD2L5-1
451606 RHD2L5-2
451608 RHD2L6-2
110111 RHD2L7-1
127954 RHD2L7-2
168047 RHD2L8-1
115913 RHD2L8-2
92462 RHD2L9-1
121926 RHD2L9-2
74260 RHD2L10-1
86677 RHD2L10-2
183259 RHD2L11-1
183352 RHD2L11-2
451613 RIC1-1
451130 RIC1-2
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