1,048
Views
16
CrossRef citations to date
0
Altmetric
Research Paper

Auxin as an inducer of asymmetrical division generating the subsidiary cells in stomatal complexes of Zea mays

, , &
Article: e984531 | Received 08 Aug 2014, Accepted 23 Sep 2014, Published online: 01 Apr 2015

References

  • Stebbins LG, Shah SS. Developmental studies of cell differentiation in the epidermis of monocotyledons. II. Cytological features of stomatal development in the Graminae. Dev Biol 1960; 2:477-500; http://dx.doi.org/10.1016/0012-1606(60)90050-6
  • Galatis B, Apostolakos P. The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol 2004; 161:613-39; http://dx.doi.org/10.1046/j.1469-8137.2003.00986.x
  • Facette MR, Smith LG. Division polarity in developing stomata. Curr Opin Plant Biol 2012; 15:585-92; PMID:23044038; http://dx.doi.org/10.1016/j.pbi.2012.09.013
  • Pillitteri LJ, Torii KU. Mechanisms of stomatal development. Annu Rev Plant Biol 2012; 63:591-614; PMID:22404473
  • Wick SM. The preprophase band. In: Lloyd CW. ed. The cytoskeletal basis of plant growth and form. Academic Press London 1991; 231-44.
  • Bünning E. Polarität und inäquale teilung pflanzlichen protoplasten. Protoplasmatologia 1957; 8:1-86.
  • Stebbins LG, Jain SK. Developmental studies of cell differentation in the epidermis of monocotyledons. I. Allium, Rhoeo, and Commelina. Dev Biol 1960; 2:409-26; http://dx.doi.org/10.1016/0012-1606(60)90025-7
  • Pickett-Heaps JD, Northcote DH. Cell division in the formation of the stomatal complex of the young leaves of wheat. J Cell Sci 1966; 1:121-8; PMID:5929805
  • Apostolakos P, Galatis B. Induction, polarity and spatial control of cytokinesis in some abnormal subsidiary cell mother cells of Zea mays. Protoplasma 1987; 140:26-42; http://dx.doi.org/10.1007/BF01273253
  • Green PB, Erickson RO, Richmond PA. On the physical basis of cell morphogenesis. Ann N Y Acad Sci. 1970; 175:712-31; http://dx.doi.org/10.1111/j.1749-6632.1970.tb45187.x
  • Pickett-Heaps JD, Gunning BES, Brown RC, Lemmon BE, Cleary AL. The cytoplast concept in plant cells: cytoplasmic domains and the evolution of spatially organised cell division. Am J Bot 1999; 86:153-72; PMID:21680355; http://dx.doi.org/10.2307/2656933
  • Apostolakos P, Panteris E, Galatis B. The involvement of phospholipases C and D in the asymmetric division of subsidiary cell mother cells of Zea mays. Cell Motil Cytoskel 2008; 65:863-75; http://dx.doi.org/10.1002/cm.20308
  • Giannoutsou E, Apostolakos P, Galatis B. Actin filament-organized local cortical endoplasmic reticulum aggregations in developing stomatal complexes of grasses. Protoplasma 2011; 248:373-90; PMID:20644970; http://dx.doi.org/10.1007/s00709-010-0180-2
  • Dhonukshe P, Kleine-Vehn J, Friml J. Cell polarity, auxin transport, and cytoskeleton-mediated division planes: who comes first? Protoplasma 2005; 226:67-73; PMID:16231102; http://dx.doi.org/10.1007/s00709-005-0104-8
  • Oliva M, Vernoux T, Traas J. From auxin transport to patterning. In: Chen R, Baluška F. eds. Polar auxin transport. Springer-Verlag Heidelberg 2013; 259-79.
  • Prasad K, Dhonukshe P. Polar auxin transport: cell polarity to patterning. In: Chen R, Baluška F. eds. Polar auxin transport. Springer-Verlag Heidelberg 2013; 25-44.
  • Forestan C, Varotto S. The role of PIN auxin efflux carriers in polar auxin transport and accumulation and their effect on shaping maize development. Mol Plant 2012; 5:787-98; PMID:22186966; http://dx.doi.org/10.1093/mp/ssr103
  • Zgurski JM, Sharma R, Bolokoski DA, Schultz EA. Asymmetric auxin response precedes asymmetric growth and differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis leaves. Plant Cell 2005; 17:77-91; PMID:15608337; http://dx.doi.org/10.1105/tpc.104.026898
  • Le J, Liu X-G, Yang K-Z, Chen X-L, Zou J-J, Wang H-Z, Wang M, Vanneste S, Morita M, Tasaka M, et al. Auxin transport and activity regulate stomatal patterning and development. Nature Commun 2014; 5:3090; http://dx.doi.org/10.1038/ncomms4090
  • Tsiantis M, Brown MIN, Skibinski G, Langdale JA. Disruption of auxin transport is associated with aberrant leaf development in maize. Plant Physiol 1999; 121:1163-8; PMID:10594103; http://dx.doi.org/10.1104/pp.121.4.1163
  • Nelissen H, Rymen B, Jikumaru Y, Demuynck K, Van Lijsebettens M, Kamiya Y, Inzé D, Beemster GTS. A local maximum in gibberellin levels regulates maize leaf growth by spatial control of cell division. Curr Biol 2012; 22:1183-7; PMID:22683264; http://dx.doi.org/10.1016/j.cub.2012.04.065
  • Balzan S, Gurmukh SJ, Carraro N. The role of auxin transporters in monocots development. Front Plant Sci 2014; 5:393; PMID:25177324; http://dx.doi.org/10.3389/fpls.2014.00393
  • Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jurgens G, Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003; 115:591-602; http://dx.doi.org/10.1016/S0092-8674(03)00924-3
  • Nick P. Probing the actin-auxin oscillator. Plant Signal Behav 2010; 5:94-8; PMID:20023411; http://dx.doi.org/10.4161/psb.5.2.10337
  • Tsuda E, Yang H, Nishimura T, Uehara Y, Sakai T, Furutani M, Koshiba T, Hirose M, Nozaki H, Murphy AS, et al. Alkoxy-auxins are selective inhibitors of auxin transport mediated by PIN, ABCB, and AUX1 transporters. J Biol Chem 2011; 286:2354-64; PMID:21084292; http://dx.doi.org/10.1074/jbc.M110.171165
  • Geldner N, Friml J, Stierhof Y-D, Jürgens G, Palme K. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 2001; 413:425-8; PMID:11574889; http://dx.doi.org/10.1038/35096571
  • Wiśniewska J, Xu J, Seifertová D, Brewer PB, Růžička K, Blilou I, Rouquie D, Benková E, Scheres B, Friml J. Polar PIN localization directs auxin flow in plants. Science 2006; 312:883; PMID:16601151; http://dx.doi.org/10.1126/science.1121356
  • Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H, Heilmann M, van Wijk R, Vermeer JEM, Heilmann I, Munnik T, et al. Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 2014; 26:2114-28; PMID:24876254; http://dx.doi.org/10.1105/tpc.114.126185
  • Joo JH, Yoo HJ, Hwang I, Lee JS, Nam KH, Bae YS. Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 2005; 579:1243-8; PMID:15710420; http://dx.doi.org/10.1016/j.febslet.2005.01.018
  • Li L, Saga N, Mikami K. Phosphatidylinositol 3-kinase activity and asymmetrical accumulation of F-actin are necessary for establishment of cell polarity in the early development of monospores from the marine red alga Porphyra yezoensis. J Exp Bot 2008; 59:3575-86; PMID:18703492; http://dx.doi.org/10.1093/jxb/ern207
  • Vlahos CJ, Matter WF, Hui KY, Brown RF. A specific inhibitor of phosphatidylinositol 3-kinase, 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one (LY294002). J Biol Chem 1994; 269:5241-48; PMID:8106507
  • Galatis B. The organization of microtubules in guard cell mother cells of Zea mays. Can J Bot 1982; 60:1148-66; http://dx.doi.org/10.1139/b82-145
  • Panteris E, Apostolakos P, Galatis B. Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucleus to its polar position. Cell Motil Cytoskel 2006; 63:696-709; http://dx.doi.org/10.1002/cm.20155
  • Panteris E, Galatis B, Quader H, Apostolakos P. Cortical actin filament organization in developing and functioning stomatal complexes of Zea mays and Triticum turgidum. Cell Motil Cytoskel 2007; 64:531-48; http://dx.doi.org/10.1002/cm.20203
  • Galatis B, Apostolakos P, Katsaros C. Synchronous organization of two preprophase microtubule bands and final cell plate arrangement in subsidiary cell mother cells of some Triticum species. Protoplasma 1983; 117:24-39; http://dx.doi.org/10.1007/BF01281781
  • Galatis B, Apostolakos P, Katsaros C. Positional inconsistency between preprophase microtubule band and final cell plate arrangement during triangular subsidiary cell and atypical hair cell formation in two Triticum species. Can J Bot 1984; 62:343-59; http://dx.doi.org/10.1139/b84-053
  • Galatis B. Differentiation of stomatal meristemoids and guard cell mother cells into guard-like cells in Vigna sinensis leaves after colchicine treatment. An ultrastructural and experimental approach. Planta 1977; 136:103-14; PMID:24420314; http://dx.doi.org/10.1007/BF00396185
  • Bünning E. General processes of differentiation. In: Milthorpe F.L. ed. The growth of leaves. Butterworths Scientific Publications London 1956; 18-30.
  • Facette MR, Shen Z, Björnsdóttir FR, Briggs SP, Smith LG. Parallel proteomic and phosphoproteomic analyses of successive stages of maize leaf development. Plant Cell 2013; 25:2798-812; PMID:23933881; http://dx.doi.org/10.1105/tpc.113.112227
  • Wabnick K, Kleine-Vehn J, Balla J, Sauer M, Naramoto S, Reinöhl V, Merks RMH, Govaerts W, Friml J. Emergence of tissue polarization from synergy of intracellular and extracellular auxin signaling. Mol Syst Biol 2010; 6:447; PMID:21179019
  • De Smet I, Beeckman T. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat Rev Mol Cell Biol 2011; 12:177-88; PMID:21346731; http://dx.doi.org/10.1038/nrm3064
  • Saibo NJM, Vriezen WH, Beemster GTS, Van Der Straeten D. Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 2003; 33:989-1000; PMID:12631324; http://dx.doi.org/10.1046/j.1365-313X.2003.01684.x
  • Zhang J-Y, He S-B, Li L, Yang H-Q. Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll. Proc Nat Acad Sci U S A 2014; 111:E3015-23; http://dx.doi.org/10.1073/pnas.1400542111
  • Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T. Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 2002; 14:2339-51; PMID:12368490; http://dx.doi.org/10.1105/tpc.004960
  • De Veylder L, Beeckman T, Inzé D. The ins and outs of the plant cell cycle. Nat Rev Mol Cell Biol 2007; 8:655-65; PMID:17643126; http://dx.doi.org/10.1038/nrm2227
  • Wang L, Ruan Y-L. Regulation of cell division and expansion by sugar and auxin signalling. Front Plant Sci 2013; 4:163; PMID:23755057
  • Lee Y, Munnik T, Lee Y. Plant Phosphatidylinositol 3-Kinase. In: Munnik T. ed. Lipid Signaling in Plants. Plant Cell Monographs, Springer-Verlag Heidelberg 2010; 16:95-106.
  • Cleary AL. Actin in formation of stomatal complexes. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW. eds. Actin: a dynamic framework for multiple plant cell functions. Kluwer Academic Publishers Dordrecht 2000; 411-26.
  • Smith LG. Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2001; 2:33-9; PMID:11413463; http://dx.doi.org/10.1038/35048050
  • Xu T, Wen M, Nagawa S, Fu Y, Chen J-G, Wu M-J, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z. Cell surface- and Rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 2010; 143:99-110; PMID:20887895; http://dx.doi.org/10.1016/j.cell.2010.09.003
  • Yang Z, Lavagi I. Spatial control of plasma membrane domains: ROP GTPase-based symmetry breaking. Curr Opin Plant Biol 2012; 15:601-7; PMID:23177207; http://dx.doi.org/10.1016/j.pbi.2012.10.004
  • Nakamura M, Kiefer CS, Grebe M. Planar polarity, tissue polarity and planar morphogenesis in plants. Curr Opin Plant Biol 2012; 15:593-600; PMID:22906885; http://dx.doi.org/10.1016/j.pbi.2012.07.006
  • Wu H-m, Hazak O, Cheung AY, Yalovsky S. RAC/ROP GTPases and auxin signaling. Plant Cell 2011; 23:1208-18; PMID:21478442; http://dx.doi.org/10.1105/tpc.111.083907
  • Humphries JA, Vejlupkova Z, Luo A, Meeley RB, Sylvester AW, Fowler JE, Smith LG. ROP GTPases act with the receptor-like protein PAN1 to polarize asymmetric cell division in maize. Plant Cell 2011; 23:2273-84; PMID:21653193; http://dx.doi.org/10.1105/tpc.111.085597
  • Cartwright HN, Humphries JA, Smith LG. PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 2009; 323:649-51; PMID:19179535; http://dx.doi.org/10.1126/science.1161686
  • Zhang X, Facette M, Humphries JA, Shen Z, Park Y, Sutimantanapi D, Sylvester AW, Briggs SP, Smith LG. Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor-like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell 2012; 24:4577-89; PMID:23175742; http://dx.doi.org/10.1105/tpc.112.104125
  • Panteris E, Galatis B, Apostolakos P. Examination of the possible role of PAN1 protein in the ontogenesis of Zea mays stomatal complexes. In: Gkelis S, Karousou R, Kokkini S, Panteris E. eds. Program and Abstracts. 13th Panhellenic Scientific Conference, Hellenic Botanical Society, Thessaloniki 3–6 October, 2013; p. 118.
  • Sutimantanapi D, Pater D, Smith LG. Divergent roles for maize PAN1 and PAN2 receptor-like proteins in cytokinesis and cell morphogenesis. Plant Physiol 2014; 164:1905-17; PMID:24578508; http://dx.doi.org/10.1104/pp.113.232660
  • Kennard JL, Cleary AL. Pre-mitotic nuclear migration in subsidiary mother cells of Tradescantia occurs in G1 of the cell cycle and requires F-actin. Cell Motil Cytoskel 1997; 36:55-67; http://dx.doi.org/10.1002/(SICI)1097-0169(1997)36:1%3c55::AID-CM5%3e3.0.CO;2-G
  • Zegzouti H, Anthony RG, Jahchan N, Bögre L, Christensen SK. Phosphorylation and activation of PINOID by the phospholipid signaling kinase 3-phosphoinositide-dependent protein kinase 1 (PDK1) in Arabidopsis. Proc Nat Acad Sci U S A 2006; 103:6404-9; http://dx.doi.org/10.1073/pnas.0510283103
  • Li G, Xue H-W. Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 2007; 19:281-95; PMID:17259265; http://dx.doi.org/10.1105/tpc.106.041426
  • Testerink C, Munnik T. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 2011; 62:2349-61; PMID:21430291; http://dx.doi.org/10.1093/jxb/err079
  • O'Brien TP, McCully ME. The study of plant structure. Principles and selected methods. Termarcarphi Pty, Melbourne 1981; 352p.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.