Abstract
The roles of multiple GRAS transcription factors (TFs), which play key roles in diverse processes of growth and development, have been characterized in detail. However, the regulatory functions of one third of the GRAS members remain unknown. Here, we characterized the role of SCARECROW-LIKE 28 (SCL28) in the Arabidopsis root; nuclear localization and transcriptional activity indicated that SCL28 likely acts as a TF in the root. SCL28 overexpression (SCL28-OX) promoted cell division and suppressed cell elongation in a zone-specific manner along the root axis. In the presence of the microtubule-destabilizing chemical propyzamide, SCL28-OX exhibited straight root growth, while scl28 roots showed left-handed helical growth similar to the wild type. Under salt and propyzamide treatments, scl28 roots grew straight, while SCL28-OX roots displayed exaggerated right-handed growth. Thus, SCL28 likely plays a role in the root growth response to stressinduced microtubule organization. Additionally, transcriptome analysis revealed that SCL28 regulated the transcription of diverse growth- and development-related genes in plants. In particular, SCL28 regulated the expression of various stressresponse genes. Taken together, our findings provide insight into the regulatory role of SCL28, which orchestrates the linked activity of cell division and elongation under various environmental conditions to achieve root growth plasticity.
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References
Alon U (2007) Network motifs: theory and experimental approaches. Nat Rev Genet 8:450–461
Ban Y, Kobayashi Y, Hara T, Hamada T, Hashimoto T, Takeda S, Hattori T (2013) α-tubulin is rapidly phosphorylated in response to hyperosmotic stress in rice and Arabidopsis. Plant Cell Physiol 54:848–858
Baskin I (2013) Patterns of root growth acclimation: constant processes, changing boundaries. Wiley Interdiscip Rev Dev Biol 2:65–73
Beemster GT, Baskin I (1998) Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. Plant Physiol 116:1515–1526
Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA (1993) Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:57–70
Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692
Bolle C, Koncz C, Chua NH (2000) PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. Genes Dev 14:1269–1278
Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dosedependent root cell fate. Nature 465:316–321
Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin- GUS fusion protein. Plant J 20:503–508
Clough S, Bent A (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Cui H, Hao Y, Kong D (2012) SCARECROW has a SHORT-ROOTindependent role in modulating the sugar response. Plant Physiol 158:1769–1778
Cui H, Hao Y, Kovtun M, Stolc V, Deng XW, Sakakibara H, Kojima M (2011) Genome-wide direct target analysis reveals a role for SHORT-ROOT in root vascular patterning through cytokinin homeostasis. Plant Physiol 157:1221–1231
Cui H, Kong D, Liu X, Hao Y (2014) SCARECROW, SCR-LIKE 23 and SHORT-ROOT control bundle sheath cell fate and function in Arabidopsis thaliana. Plant J 78:319–327
Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425
Curtis M, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469
Dello-Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682
Dello-Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384
Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (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
Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419
Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45:616–629
Fode B, Siemsen T, Thurow C, Weigel R, Gatz C (2008) The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. Plant Cell 20:3122–3135
Fujita S, Pytela J, Hotta T, Kato T, Hamada T, Akamatsu R, Ishida Y, Kutsuna N, Hasezawa S, Nomura Y, Nakagami H, Hashimoto T (2013) An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Curr Biol 23:1969–1978
Fukaki H, Wysocka-Diller J, Kato T, Fujisawa H, Benfey PN, Tasaka M (1998). Genetic evidence that the endodermis is essential for shoot gravitropism in Arabidopsis thaliana. Plant J 14:425–430
Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T (2000) The SPIRAL genes are required for directional control of cell elongation in Aarabidopsis thaliana. Development 127:4443–4453
Gao MJ, Li X, Huang J, Gropp GM, Gjetvaj B, Lindsay DL, Wei S, Coutu C, Chen Z, Wan XC, Hannoufa A, Lydiate DJ, Gruber MY, Chen ZJ, Hegedus DD (2015) SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. Nat Commun 6:7243
Gaudinier A, Brady SM (2016) Mapping transcriptional networks in plants: data-driven discovery of novel biological mechanisms. Annu Rev Plant Biol 67:14.1–14.20
Hashimoto T (2002) Molecular genetic analysis of left-right handedness in plants. Philos Trans R Soc B 357:799–808
Hashimoto T (2015) Microtubules in plants. The Arabidopsis Book 11:e0179
Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567
Heo J-O, Chang KS, Kim IA, Lee M-H, Lee SA, Song SK, Lee MM, 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
Karimi M, Inzé D, Depicker A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195
Kaufmann K, Pajoro A, Angenent GC (2010) Regulation of transcription in plants: mechanisms controlling developmental switches. Nat Rev Genet 11:830–842
Kazda A, Akimcheva S, Watson JM, Riha K (2016) Cell proliferation analysis using EdU labeling in whole plant and histological samples of Arabidopsis. Methods Mol Biol 1370:169–182
Lee M-H, Kim B, Song SK, Heo J-O, Yu N-I, Lee SA, Kim M, Kim DG, Sohn SO, Lim CE, Chang KS, Lee MM, Lim J (2008) Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. Plant Mol Biol 67:659–670
Lee SA, Yoon EK, Heo J-O, Lee M-H, Hwang I, Cheong H, Lee WS, Hwang Y-s, Lim J (2012) Analysis of Arabidopsis glucose insensitive growth mutants reveals the involvement of the plastidial copper transporter PAA1 in glucose-induced intracellular signaling. Plant Physiol 159:1001–1012
Lee SA, Jang S, Yoon EK, Heo J-O, Chang KS, Choi JW, Dhar S, Kim G, Choe, J-E, Heo JB, Kwon C, Ko J-H, Hwang Y-s, Lim J (2016) Interplay between ABA and GA modulates the timing of asymmetric cell divisions in the Arabidopsis root ground tissue. Mol Plant 9:870–884
Levesque MP, Vernoux T, Busch W, Cui H, Wang JY, Blilou I, Hassan H, Nakajima K, Matsumoto N, Lohmann JU, Scheres B, Benfey PN (2006) Whole-genome analysis of the SHORTROOT developmental pathway in Arabidopsis. PLoS Biol 4:e143
Lloyd C, Chan J (2004) Microtubules and the shape of plants to come. Nat Rev Mol Cell Biol 5:13–22
Long Y, Goedhart J, Schneijderberg M, Terpstra I, Shimotohno A, Bouchet BP, Akhmanova A, Gadella TW Jr, Heidstra R, Scheres B, Blilou I (2015) SCARECROW-LIKE23 and SCARECROW jointly specify endodermal cell fate but distinctly control SHORT-ROOT movement. Plant J 84:773–784
Nakamura M, Naoi K, Shoji T, Hashimoto T (2004) Low concentrations of propyzamide and oryzalin alter microtubule dynamics in Arabidopsis epidermal cells. Plant Cell Physiol 45:1330–1334
Naoi K, Hashimoto T (2004) A semi-dominant mutation in an Arabidopsis mitogen-activated protein kinase phosphatase-like gene compromises cortical microtubule organization. Plant Cell 16:1841–1853
Peng J, Carol P, Richards D, King K, Cowling R, Murphy G, Harberd N (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes Dev 11:3194–3205
Perilli S, Sabatini S (2010) Analysis of root meristem size development. Methods Mol Biol 655:177–187
Pysh LD, Wysocka-Diller JW, Camilleri C, Bouchez D, Benfey PN (1999) The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J 18:111–119
Pytela J, Kato T, Hashimoto T (2010) Mitogen-activated protein kinase phosphatase PHS1 is retained in the cytoplasm by nuclear extrusion signal-dependent and independent mechanisms. Planta 231:1311–1322
Scheres B, Di Laurenzio L, Willemsen V, Hauser M-T, Janmaat K, Weisbeek P, Benfey PN (1995) Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the embryonic axis. Development 121:53–62
Shoji T, Suzuki K, Abe T, Kaneko Y, Shi H, Zhu JK, Rus A, Hasegawa PM, Hashimoto T (2006) Salt stress affects cortical microtubule organization and helical growth in Arabidopsis. Plant Cell Physiol 47:1158–1168
Silverstone A, Ciampaglio C, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169
Song SK, Ryu KH, Kang YH, Song JH, Cho YH, Yoo SD, Schiefelbein J, Lee, MM (2011) Cell fate in the Arabidopsis root epidermis is determined by competition between WEREWOLF and CAPRICE. Plant Physiol 157:1196–208
Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JA, Benfey PN (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Naure 466:128–132
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot 65:2633–2643
Thitamadee S, Tuchihara K, Hashimoto T (2002) Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417:193–196
Tian C, Wan P, Sun S, Li J, Chen M (2004) Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol Biol 54:519–532
Torres-Galea P, Hirtreiter B, Bolle C (2013) Two GRAS proteins, SCARECROW-LIKE21 and PHYTOCHROME A SIGNAL TRANSDUCTION1, function cooperatively in phytochrome A signal transduction. Plant Physiol 161:291–304
Torres-Galea P, Huang LF, Chua N-H, Bolle C (2006) The GRAS protein SCL13 is a positive regulator of phytochrome-dependent red light signaling, but can also modulate phytochrome A responses. Mol Genet Genomics 276:13–30
Van Sandt V, Suslov D, Verbelen J-P, Vissenberg K (2007) Xyloglucan endotransglucosylase activity loosens a plant cell wall. Ann Bot 100:1467–1473
Verbelen J-P, De Cnodder T, Le J, Vissenberg K, Baluska F (2006) The root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone and growth terminating zone. Plant Signal Behav 1:296–304
Waki T, Miyashima S, Nakanishi M, Ikeda Y, Hashimoto T, Nakajima K (2012) A GAL4-based targeted activation tagging system in Arabidopsis thaliana. Plant J 73:357–367
Wang C, Li J, Yuan M (2007) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant Cell Physiol 48:1534–1547
Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572
Yoon EK, Dhar S, Lee M-H, Song JH, Lee SA, Kim G, Jang S, Choi JW, Choe, J-E, Kim JH, Lee MM, Lim J (2016) Conservation and diversification of the SHR-SCR-SCL23 regulatory network in the development of the functional endodermis in Arabidopsis shoots. Mol Plant 9:1197–1209
Yu N-I, Lee SA, Lee M-H, Heo J-O, Chang KS, Lim J (2010) Characterization of SHORT-ROOT function in the Arabidopsis root vascular system. Mol Cells 30:113–119
Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo J-O, Lim J, Kamiya Y, Yamaguchi S, Sun T-p (2011) SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. Proc Natl Acad SciUSA 108:2160–2165
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Choe, Je., Kim, B., Yoon, E.K. et al. Characterization of the GRAS transcription factor SCARECROW-LIKE 28’s role in Arabidopsis root growth. J. Plant Biol. 60, 462–471 (2017). https://doi.org/10.1007/s12374-017-0112-1
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DOI: https://doi.org/10.1007/s12374-017-0112-1