Browse > Article
http://dx.doi.org/10.14348/molcells.2016.0105

Control of Asymmetric Cell Divisions during Root Ground Tissue Maturation  

Choi, Ji Won (Department of Systems Biotechnology, Konkuk University)
Lim, Jun (Department of Systems Biotechnology, Konkuk University)
Publication Information
Molecules and Cells / v.39, no.7, 2016 , pp. 524-529 More about this Journal
Abstract
Controlling the production of diverse cell/tissue types is essential for the development of multicellular organisms such as animals and plants. The Arabidopsis thaliana root, which contains distinct cells/tissues along longitudinal and radial axes, has served as an elegant model to investigate how genetic programs and environmental signals interact to produce different cell/tissue types. In the root, a series of asymmetric cell divisions (ACDs) give rise to three ground tissue layers at maturity (endodermis, middle cortex, and cortex). Because the middle cortex is formed by a periclinal (parallel to the axis) ACD of the endodermis around 7 to 14 days post-germination, middle cortex formation is used as a parameter to assess maturation of the root ground tissue. Molecular, genetic, and physiological studies have revealed that the control of the timing and extent of middle cortex formation during root maturation relies on the interaction of plant hormones and transcription factors. In particular, abscisic acid and gibberellin act synergistically to regulate the timing and extent of middle cortex formation, unlike their typical antagonism. The SHORT-ROOT, SCARECROW, SCARECROW-LIKE 3, and DELLA transcription factors, all of which belong to the plant-specific GRAS family, play key roles in the regulation of middle cortex formation. Recently, two additional transcription factors, SEUSS and GA- AND ABA-RESPONSIVE ZINC FINGER, have also been characterized during ground tissue maturation. In this review, we provide a detailed account of the regulatory networks that control the timing and extent of middle cortex formation during post-embryonic root development.
Keywords
asymmetric cell division; ground tissue; plant hormone; root development; transcription factor;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Lee, S.A., Jang, S., Yoon, E.K., Heo, J.-O., Chang, K.S., Choi, J.W., Dhar, S., Kim, G., Choe, J.E., Heo, J.B., et al. (2016). Interplay between ABA and GA modulates the timing of asymmetric cell divisions in the Arabidopsis root ground tissue. Mol. Plant 9, 870-884.   DOI
2 Levesque, M.P., Vernoux, T., Busch, W., Cui, H., Wang, J.Y., Blilou, I., Hassan, H., Nakajima, K., Matsumoto, N., Lohmann, J.U., et al. (2006). Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4, e143.   DOI
3 Miyashima, S., and Nakajima, K. (2011). The root endodermis: a hub of developmental signals and nutrient flow. Plant Signal. Behav. 6, 1954-1958.   DOI
4 Paquette, A.J., and Benfey, P.N. (2005). Maturation of the ground tissue of the root is regulated by gibberellin and SCARECROW and requires SHORT-ROOT. Plant Physiol. 138, 636-640.   DOI
5 Pauluzzi, G., Divol, F., Puig, J., Guiderdoni, E., Dievart, A., and Perin, C. (2012). Surfing along the root ground tissue gene network. Dev. Biol. 365, 14-22.   DOI
6 Peng, J., Carol, P., Richards, D., King, K., Cowling, R., Murphy, G., and Harberd, N. (1997). The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev. 11, 3194-3205.   DOI
7 Pysh, L.D., Wysocka-Diller, J.W., Camilleri, C., Bouchez, D., and Benfey, P.N. (1999). The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18, 111-119.   DOI
8 Rebouillat, J., Dievart, A., Verdeil, J., Escoute, J., Giese, G., Breitler, J., Gantet, P., Espeout, S., Guiderdoni, E., and Perin, C. (2009). Molecular genetics of rice root development. Rice 2, 15-34.   DOI
9 Rohde, A., Kurup, S., and Holdsworth, M. (2000). ABI3 emerges from the seed. Trends Plant Sci. 5, 418-419.   DOI
10 Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C., and Weisbeek, P. (1994). Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 120, 2475-2487.
11 Scheres, B., Di Laurenzio, L., Willemsen, V., Hauser, M.T., Janmaat, K., Weisbeek, P., and Benfey, P.N. (1995). Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121, 53-62.
12 Shani, E., Weinstain, R., Zhang, Y., Castillejo, C., Kaiserli, E., Chory, J., Tsien, R.Y., and Estelle, M. (2013). Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc. Natl. Acad. Sci. USA 110, 4834-4839.   DOI
13 Silverstone, A., Ciampaglio, C., and Sun, T. (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10, 155-169.   DOI
14 Smolarkiewicz, M., and Dhonukshe, P. (2013). Formative cell divisions: principal determinants of plant morphogenesis. Plant Cell Physiol. 54, 333-342.   DOI
15 Sridhar VV, Surendrarao A, and Liu Z (2006) APETALA1 and SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development. Development 133, 3159-3166.   DOI
16 Sun, T.P., and Gubler, F. (2004). Molecular mechanism of gibberellin signaling in plants. Ann. Rev. Plant Biol. 55, 197-223.   DOI
17 Ten Hove, C.A., and Heidstra, R. (2008). Who begets whom? Plant cell fate determination by asymmetric cell division. Curr. Opin. Plant Biol. 11, 34-41.   DOI
18 Ubeda-Tomas, S., Federici, F., Casimiro, I., Beemster, G.T., Bhalerao, R., Swarup, R., Doerner, P., Haseloff, J., and Bennett, M.J. (2009). Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr. Biol. 19, 1194-1199.   DOI
19 Tian, C., Wan, P., Sun, S., Li, J., and Chen, M. (2004). Genomewide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol. Biol. 54, 519-532.   DOI
20 Ubeda-Tomas, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G.T., Hedden, P., Bhalerao, R., and Bennett, M.J. (2008). Root growth in Arabidopsis requires gibberellin/DELLA signaling in the endodermis. Nat. Cell Biol. 10, 625-628.   DOI
21 Weiss, D., and Ori, N. (2007). Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol. 144, 1240-1246.   DOI
22 Wu, S., Lee, C.M., Hayashi, T., Price, S., Divol, F., Henry, S., Pauluzzi, G., Perin, C., and Gallagher, K.L. (2014). A plausible mechanism, based upon SHORT-ROOT movement, for regulating the number of cortex cell layers in roots. Proc. Natl. Acad. Sci. USA 111, 16184-16189.   DOI
23 Zentella, R., Zhang, Z.L., Park, M., Thomas, S.G., Endo, A., Murase, K., Fleet, C.M., Jikumaru, Y., Nambara, E., Kamiya, Y., et al. (2007). Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19, 3037-3057.   DOI
24 Zhang, Z.L., Ogawa, M., Fleet, C.M., Zentella, R., Hu, J., Heo, J.-O., Lim, J., Kamiya, Y., Yamaguchi, S., and Sun, T.P. (2011). SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc. Natl. Acad. Sci. USA 108, 2160-2165.   DOI
25 Baum, S.F., Dubrovsky, Joseph G., and Rost, Thomas L. (2002). Apical organization and maturation of the cortex and vascular cylinder in Arabidopsis thaliana (Brassicaceae) roots. Am. J. Bot. 89, 908-920.   DOI
26 Abrash, E.B., and Bergmann, D.C. (2009). Asymmetric cell divisions: a view from plant development. Dev. Cell 16, 783-796.   DOI
27 Azhakanandam, S., Nole-Wilson, S., Bao, F., and Franks, R.G. (2008). SEUSS and AINTEGUMENTA mediate patterning and ovule initiation during gynoecium medial domain development. Plant Physiol. 146, 1165-1181.   DOI
28 Bao, F., Azhakanandam, S., and Franks, R.G. (2010). SEUSS and SEUSS-LIKE transcriptional adaptors regulate floral and embryonic development in Arabidopsis. Plant Physiol. 152, 821-836.   DOI
29 Benfey, P.N., Linstead, P.J., Roberts, K., Schiefelbein, J.W., Hauser, M.T., and Aeschbacher, R.A. (1993). Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119, 57-70.
30 Bolle, C. (2004). The role of GRAS proteins in plant signal transduction and development. Planta 218, 683-692.   DOI
31 Coudert, Y., Perin, C., Courtois, B., Khong, N.G., and Gantet, P. (2010). Genetic control of root development in rice, the model cereal. Trends Plant Sci. 15, 219-226.   DOI
32 Cui, H., and Benfey, P.N. (2009b). Cortex proliferation: simple phenotype, complex regulatory mechanisms. Plant Signal. Behav. 4, 551-553.   DOI
33 Cruz-Ramirez, A., Diaz-Trivino, S., Blilou, I., Grieneisen, V.A., Sozzani, R., Zamioudis, C., Miskolczi, P., Nieuwland, J., Benjamins, R., Dhonukshe, P., et al. (2012). A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150, 1002-1015.   DOI
34 Cui, H. (2015). Cortex proliferation in the root is a protective mechanism against abiotic stress. Plant Signal. Behav. 10, e1011949.   DOI
35 Cui, H., and Benfey, P.N. (2009a). Interplay between SCARECROW, GA and LIKE HETEROCHROMATIN PROTEIN 1 in ground tissue patterning in the Arabidopsis root. Plant J. 58, 1016-1027.   DOI
36 Cui, H., Levesque, M.P., Vernoux, T., Jung, J.W., Paquette, A.J., Gallagher, K.L., Wang, J.Y., Blilou, I., Scheres, B., and Benfey, P.N. (2007). An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316, 421-425.   DOI
37 Cui, H., Kong, D., Wei, P., Hao, Y., Torii, K.U., Lee, J.S., and Li, J. (2014). SPINDLY, ERECTA and its ligand STOMAGEN have a role in redox-mediated cortex proliferation in the Arabidopsis root. Mol. Plant 7, 1727-1739.   DOI
38 De Smet, I., and Beeckman, T. (2011). Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat. Rev. Mol. Cell Biol. 12, 177-188.   DOI
39 Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.N. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86, 423-433.   DOI
40 Dinneny, J.R. (2014). A gateway with a guard: how the endodermis regulates growth through hormone signaling. Plant Sci. 214, 14-19.   DOI
41 Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K., and Scheres, B. (1993). Cellular organization of the Arabidopsis thaliana root. Development 119, 71-84.
42 Duan, L., Dietrich, D., Ng, C.H., Chan, P.M., Bhalerao, R., Bennett, M.J., and Dinneny, J.R. (2013). Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25, 324-341.   DOI
43 Esau, K. (1953). Plant anatomy. Wiley & Sons, New York.
44 Esau, K. (1977). Anatomy of seed plants, 2nd edition. Wiley & Sons, New York.
45 Finkelstein, R.R. (2013). Abscisic acid biosynthesis and response. In The Arabidopsis book 11, e0166.
46 Finkelstein, R.R., Gampala, S.S., and Rock, C.D. (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell 14 Suppl, S15-45.   DOI
47 Finkelstein, R.R., Reeves, W., Ariizumi, T., and Steber, C. (2008). Molecular aspects of seed dormancy. Ann. Rev. Plant Biol. 59, 387-415.   DOI
48 Franks, R.G., Wang, C., Levin, J.Z., and Liu, Z. (2002). SEUSS, a member of a novel family of plant regulatory proteins, represses floral homeotic gene expression with LEUNIG. Development 129, 253-263.
49 Gong, X., Flores-Vergara, M.A., Hong, J.H., Chu, H., Lim, J., Franks, R.G., Liu, Z., and Xu, J. (2016). SEUSS integrates gibberellin signaling with transcriptional inputs from the SHR-SCR-SCL3 module to regulate middle cortex formation in the Arabidopsis root. Plant Physiol. 170, 1675-1683.
50 Grigorova B, Mara C, Hollender C, Sijacic P, Chen X, and Liu Z (2011) LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138, 2451-2456.   DOI
51 Harberd, N.P., Belfield, E., and Yasumura, Y. (2009). The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an "inhibitor of an inhibitor" enables flexible response to fluctuating environments. Plant Cell 21, 1328-1339.   DOI
52 He, C.J., Drew, M.C., and Morgan, P.W. (1994). Induction of enzymes associated with Lysigenous aerenchyma formation in roots of Zea mays during hypoxia or nitrogen starvation. Plant Physiol. 105, 861-865.   DOI
53 Heidstra, R., Welch, D., and Scheres, B. (2004). Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 18, 1964-1969.   DOI
54 Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.T., and Benfey, P.N. (2000). The SHORTROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101, 555-567.   DOI
55 Heo, J.-O., Chang, K.S., Kim, I.A., Lee, M.-H., Lee, S.A., Song, S.K., Lee, M.M., and Lim, J. (2011). Funneling of gibberellin signaling by the GRAS transcription regulator SCARECROW-LIKE 3 in the Arabidopsis root. Proc. Natl. Acad. Sci. USA 108, 2166-2171.   DOI
56 Hiratsu, K., Matsui, K., Koyama, T., and Ohme-Takagi, M. (2003). Dominant repression of target genes by chimeric repressors that include the EAR motif, a repression domain, in Arabidopsis. Plant J. 34, 733-739.   DOI
57 Jiang, C., and Fu, X. (2007). GA action: turning on de-DELLA repressing signaling. Curr. Opin. Plant Biol. 10, 461-465.   DOI
58 Hiratsu, K., Mitsuda, N., Matsui, K., and Ohme-Takagi, M. (2004). Identification of the minimal repression domain of SUPERMAN shows that the DLELRL hexapeptide is both necessary and sufficient for repression of transcription in Arabidopsis. Biochem. Biophys. Res. Commun. 321, 172-178.   DOI
59 Hoffmann-Benning, S., and Kende, H. (1992). On the role of abscisic acid and gibberellin in the regulation of growth in rice. Plant Physiol. 99, 1156-1161.   DOI
60 Horvitz, H.R., and Herskowitz, I. (1992). Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell 68, 237-255.   DOI
61 Knoblich, J.A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.   DOI
62 Ko, J.H., Yang, S.H., and Han, K.H. (2006). Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J. 47, 343-355.   DOI
63 Koizumi, K., Hayashi, T., and Gallagher, K.L. (2012a). SCARECROW reinforces SHORT-ROOT signaling and inhibits periclinal cell divisions in the ground tissue by maintaining SHR at high levels in the endodermis. Plant Signal. Behav. 7, 1573-1577.   DOI
64 Koizumi, K., Hayashi, T., Wu, S., and Gallagher, K.L. (2012b). The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue. Proc. Natl. Acad. Sci. USA 109, 13010-13015.   DOI
65 Lee, M.-H., Kim, B., Song, S.K., Heo, J.O., Yu, N.I., Lee, S.A., Kim, M., Kim, D.G., Sohn, S.O., Lim, C.E., et al. (2008). Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol. Biol. 67, 659-670.   DOI