C2H2型锌指蛋白基因ZFP5、ZFP6和GIS3通过植物激素调控表皮细胞形成和发育分子机制研究
详细信息    本馆镜像全文|  推荐本文 |  |   获取CNKI官网全文
摘要
拟南芥表皮毛和根毛发育是研究植物表皮细胞发育的模式系统,近年来关于拟南芥表皮毛和根毛发育分子遗传机理的研究已取得很大进展,已克隆到许多调控表皮毛和根毛发育过程的关键功能基因。本实验室以前的研究结果表明GLABROUS INFLORESCENCE STEMS (GIS)基因家族GIS. GLABROUS INFLORESCENCE STEMS2(GIS2)和ZINC FINGER PROTEIN8(ZFPS)通过整合赤霉素和细胞分裂素信号控制拟南芥表皮细胞形成和发育。本研究克隆和分析了3个与GIS基因具有高度同源性的锌指蛋白基因ZINC FINGER PROTEIN5(ZFPS)、ZINC FINGER PROTEIN6(ZFP6)和GLABROUS INFLORESCENCE STEMS3(GIS3),利用遗传学和分子生物学技术对它们调控植物表皮细胞发育的分子机制进行分析。取得主要研究结果如下:
     1.过量表达ZFP5基因显著促进拟南芥表皮毛形成。功能缺失突变体zfp5与野生型相比在花、茎生叶、分枝和主茎花序上形成表皮毛数量显著减少;而且形成根毛数量比野生型显著减少,根毛长度比野生型显著减短。更重要的是,我们发现ZFP5通过赤霉素调控表皮毛形成,通过细胞分裂素调控根毛的生长发育。zfp5突变体根毛短的表型对外施植物激素细胞分裂素,以及营养成分钾和磷饥饿有响应。分子生物学分析显示,ZFP5作用于GIS、GIS2、ZFP8和表皮毛形成重要调控复合体GL1、GL3的上游调控表皮毛发育。利用化学诱导系统和染色体免疫共沉淀CHIP技术,进一步证实ZFP5通过直接作用于ZFP8和CPC分别调控表皮毛和根毛细胞的生长发育。
     2.过量表达ZFP6促进拟南芥花和主茎上表皮毛生长,功能缺失突变体zfp6与野生型相比在花和主茎分枝上形成表皮毛数量显著减少,根毛数量显著减少。分子生物学结果显示,ZFP6作用于表皮毛正向调节因子ZFP5、GIS、GIS2、GL1和GL3的上游,通过赤霉素和细胞分裂素调控表皮毛细胞形成,同时也通过细胞分裂素调控根毛细胞的生长发育。
     3.过量表达GIS3促进拟南芥花和其它组织上产生许多表皮毛,功能缺失突变体gis3与野生型相比在花和分枝上形成表皮毛数量减少。进一步分子生物学分析显示,GIS3作用于表皮毛正向调节因子ZFP5、GIS、GIS2、GL1和GL3的上游,通过赤霉素GA和细胞分裂素调控表皮毛生长发育。
     以上研究结果显示,拟南芥锌指蛋白基因ZFP5、ZFP6和GIS3是调控表皮毛和根毛细胞形成的关键功能基因。这个研究结果进一步证实和补充GIS家族基因通过整合植物激素信号控制表皮毛和根毛细胞形成的作用机制。这些结果为进一步了解和研究拟南芥根毛和表皮毛细胞形成的作用机制提供了坚实的理论基础。同时这个研究结果对于了解植物表皮毛和根毛细胞发育,根系养分吸收,以及与植物激素、环境的互作关系,具有重要的学术意义和实际应用价值。
Arabidopsis (Arabidopsis thaliana) trichome and root hair development is an excellent model system for studying cell development, cell differentiation and cell cycle. Our previous studies have shown that GLABROUS INFLORESCENCE STEMS (GIS) family genes, GIS, GLABROUS INFLORESCENCE STEMS2(GIS2) and ZINC FINGER PROTEIN8(ZFP8), control shoot maturation and epidermal cell fate by integrating gibberellins (GAs) and cytokinin signaling in Arabidopsis. Here, we show that three new C2H2zinc finger proteins, ZINC FINGER PROTEIN5(ZFP5), ZINC FINGER PROTEIN6(ZFP6), GLABROUS INFLORESCENCE STEMS3(GIS3) play important roles in controlling root hair and trichome cell development through cytokinin and GA signalings.
     1. Overexpression of ZFP5resulted in significantly more trichomes on carpels and other inflorescence organs than wild-type plants. zfp5loss-of-function mutant and RNAi lines exhibited reduced numbers of trichomes on sepals, cauline leaves, paraclades and main inflorescence stems in comparison to wild-type plants. Moreover, loss of ZFP5function resulted in shorter and fewer root hairs. More importantly, ZFP5mediated the regulation of trichome initiation by gibberellins. ZFP5gene expression was regulated by different plant hormones and nutrients. The molecular analyses suggested that ZFP5functions upstream of GIS, GIS2, ZFP8, and the key trichome initiation regulators GLABROUS1(GL1) and GLABROUS3(GL3). We further demonstrated that ZFP8was the direct target of ZFP5in controlling trichome cell differentiation, and CPC was the direct target of ZFP5in controlling root hair cell differentiation by using a steroid-inducible activation of ZFP5and ChIP experiment.
     2. Overexpression of ZFP6led to significantly more trichomes on carpels and other inflorescence organs than the control plants. zfp6loss-of-function mutants resulted in fewer trichomes on sepals and lateral branch in comparison to wild-type plants. Moreover, loss of ZFP6function resulted in shorter and less root hairs than their wild type control. ZFP6mediated the regulation of trichome initiation by gibberellins and regulated the development of root hair by cytokinins. The molecular analyses suggested that ZFP6functions upstream of ZFP5, GIS, GIS2, ZFP8, and the key trichome initiation regulators GLABROUS I (GLI) and GLABROUS3(GL3).
     3. Overexpression of GIS3resulted in significantly more trichomes on carpels and other inflorescence organs than the control plants. gis3loss-of-function mutants showed a reduced number of trichomes on sepals, and paraclades in comparison to wild-type plants. It was found that GIS3also mediates the regulation of trichome initiation by gibberellins. The molecular analyses demonstrated that GIS3functioned upstream of ZFP6, ZFP5, GIS, GIS2. ZFP8, the key trichome initiation regulators GLABROUS1(GL1) and GLABROUS3(GL3).
     In summary, ZFP5、ZFP6and GIS3are major genes controlling the development of trichomes and root hairs. This study further supports that GIS family genes control the initiation and development of trichomes and root hairs by integrating hormonal signaling.
引文
1. Abe, T., Hashimoto, T.,2005. Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Ambidopsis plants. Plant J 43,191-204.
    2. Abe, T., Thitamadee, S., Hashimoto, T.,2004. Microtubule defects and cell morphogenesis in the leftyl lefty2 tubulin mutant of Arabidopsis thaliana. Plant Cell Physiol 45,211-220.
    3. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., Harberd, N.P.,2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311,91-94.
    4. Achard, P., Vriezen, W.H., Van Der Straeten, D., Harberd, N.P.,2003. Ethylene regulates Arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15,2816-2825.
    5. Anthony, R.G., Henriques, R., Helfer, A., Meszaros, T., Rios, G., Testerink, C., Munnik, T., Deak, M., Koncz, C.,2004. A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. Embo J.23,572-581.
    6. Baluska, F., Salaj, J., Mathur, J., Braun, M., Jasper, F., Samaj, J., Chua, N.H., Barlow, P.W., Volkmann, D.,2000. Root hair formation:F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Developmental Biology 227,618-632.
    7. Bao, Y.Q., Kost, B., Chua, N.H.,2001. Reduced expression of a-tubulin genes in Arabidopsis thaliana specifically affects root growth and morphology, root hair development and root gravitropism. Plant J.28,145-157.
    8. Barendse, G.W.M., Kepczynski, J., Karssen, C.M., Koomneef, M.,1986. The Role of Endogenous Gibberellins during Fruit and Seed Development-Studies on Gibberellin-Deficient Genotypes of Arabidopsis-Thaliana. Physiol Plantarum 67,315-319.
    9. Basu, D., El-Assal Sel, D., Le, J., Mallery, E.L., Szymanski, D.B.,2004. Interchangeable functions of Arabidopsis PIROGI and the human WAVE complex subunit SRAl during leaf epidermal development. Development 131,4345-4355.
    10. Bates, T.R., Lynch, J.P.,1996. Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19,529-538.
    11. Baumberger, N., Ringli, C., Keller, B.,2001. The chimeric leucine-rich repeat/extensin cell wall protein LRX1 is required for root hair morphogenesis in Arabidopsis thaliana. Genes Dev 15,1128-1139.
    12. Baumberger, N., Steiner, M., Ryser, U., Keller, B., Ringli, C.,2003. Synergistic interaction of the two paralogous Arabidopsis genes LRX1 and LRX2 in cell wall formation during root hair development. Plant J 35,71-81.
    13. Beauclair, Leblanc Antonin, Lemauviel-Lavenant Servane, C.D., and Erwan Le Deunff, 2009. Ethylene modifies architecture of root system in response to stomatal opening and water allocation changes between root and shoot. Plant Signal Behav 4,44-46.
    14. Benitez, M., Espinosa-Soto, C., Padilla-Longoria, P., Alvarez-Buylla, E.R.,2008. Interlinked nonlinear subnetworks underlie the formation of robust cellular patterns in Arabidopsis epidermis:a dynamic spatial model. Bmc Systems Biology 2.
    15. Benitez, M., Espinosa-Soto, C., Padilla-Longoria, P., Diaz, J., Alvarez-Buylla, E.R.,2007. Equivalent genetic regulatory recover contrasting spatial cell networks in different contexts patterns that resemble those in Arabidopsis root and leaf epidermis:a dynamic model. International Journal of Developmental Biology 51,139-155.
    16. Berger, F., Haseloff, J., Schiefelbein, J., Dolan, L.,1998. Positional information in root epidermis is defined during embryogenesis and acts in domains with strict boundaries. Curr Biol 8,421-430.
    17. Bernhardt, C., Lee, M.M., Gonzalez, A., Zhang, F., Lloyd, A., Schiefelbein, J.,2003. The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130,6431-6439.
    18. Bernhardt, C., Zhao, M.Z., Gonzalez, A., Lloyd, A., Schiefelbein, J.,2005. The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132,291-298.
    19. Bibikova, T.N., Blancaflor, E.B., Gilroy, S.,1999. Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J.17,657-665.
    20. Bibikova, T.N., Jacob, T., Dahse, I., Gilroy, S.,1998. Localized changes in apoplastic and cytoplasmic pH are associated with root hair development in Arabidopsis thaliana. Development 125,2925-2934.
    21. Bohme, K., Li, Y., Charlot, F., Grierson, C., Marrocco, K., Okada, K., Laloue, M., Nogue, F.,2004. The Arabidopsis COW1 gene encodes a phosphatidylinositol transfer protein essential for root hair tip growth. Plant J 40,686-698.
    22. Bompard, G., Caron, E.,2004. Regulation of WASP/WAVE proteins:making a long story short. J Cell Biol 166,957-962.
    23. Bouyer, D., Geier, F., Kragler, F., Schnittger, A., Pesch, M., Wester, K., Balkunde, R., Timmer, J., Fleck, C., Huelskamp, M.,2008. Two-dimensional patterning by a trapping/depletion mechanism:The role of TTG1 and GL3 in Arabidopsis trichome formation. Plos Biol 6,1166-1177.
    24. Bowling, S.A., Clarke, J.D., Liu, Y.D., Klessig, D.F., Dong, X.N.,1997. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9,1573-1584.
    25. Bowman, J.L., Sakai, H., Jack, T., Weigel, D., Mayer, U., Meyerowitz, E.M.,1992. SUPERMAN, a regulator of floral homeotic genes in Arabidopsis. Development 114, 599-615.
    26. Buhler, C., Gadelle, D., Forterre, P., Wang, J.C., Bergerat, A.,1998. Reconstitution of DNA topoisomerase Ⅵ of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res 26,5157-5162.
    27. Burk, D.H., Liu, B., Zhong, R., Morrison, W.H., Ye, Z.H.,2001. A katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13,807-827.
    28. Campos, M.L., de Almeida, M., Rossi, M.L., Martinelli, A.P., Litholdo, C.G., Figueira, A., Rampelotti-Ferreira, F.T., Vendramim, J.D., Benedito, V.A., Peres, L.E.P.,2009. Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J Exp Bot 60,4346-4360.
    29. Caro, E., Gutierrez, C., Castellano, M.M.,2007a. A chromatin link that couples cell division to root epidermis patterning in Arabidopsis. Nature 447,213-U216.
    30. Caro et al.,2007b. GEM, a Novel Factor in the Coordination of Cell Division to Cell Fate Decisions in the Arabidopsis Epidermis. Plant Signaling & Behavior 2,494-495.
    31. Cassab, G.I.,1998. Plant Cell Wall Proteins. Annu Rev Plant Physiol Plant Mol Biol 49, 281-309.
    32. Cheng, L., Bucciarelli, B., Liu, J., Zinn, K., Miller, S., Patton-Vogt, J., Allan, D., Shen, J., Vance, C.P.,2011. White Lupin Cluster Root Acclimation to Phosphorus Deficiency and Root Hair Development Involve Unique Glycerophosphodiester Phosphodiesterases. Plant Physiology 156,1131-1148.
    33. Cheong, Y.H., Pandey, G.K., Grant, J.J., Batistic, O., Li, L., Kim, B.-G., Lee, S.-C., Kudla, J., Luan, S.,2007. Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J.52, 223-239.
    34. Chevalier, D., Batoux, M., Fulton, L., Pfister, K., Yadav, R.K., Schellenberg, M., Schneitz, K.,2005. STRUBBELIG defines a receptor kinase-mediated signaling pathway regulating organ development in Arabidopsis. Proc Natl Acad Sci U S A 102,9074-9079.
    35. Chien, J.C., Sussex, I.M.,1996. Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by Gibberellins and photoperiod in Arabidopsis thaliana (L) Heynh. Plant Physiology 111,1321-1328.
    36. Cho, H.T., Cosgrove, D.J.,2002. Regulation of root hair initiation and expansin gene expression in Arabidopsis. Plant Cell 14,3237-3253.
    37. Churchman, M.L., Brown, M.L., Kato, N., Kirik, V., Huelskamp, M., Inze, D., De Veylder, L., Walker, J.D., Zheng, Z., Oppenheimer, D.G., Gwin, T., Churchman, J., Larkin, J.C. 2006. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18,3145-3157.
    38. Ciftci-Yilmaz, S., Mittler, R.,2008. The zinc finger network of plants. Cellular and Molecular Life Sciences 65,1150-1160.
    39. Clough, S.J., Bent, A.F.,1998. Floral dip:a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16,735-743.
    40. Clowes, F.A.L.,2000. Pattern in root meristem development in angiosperms. New Phytol. 146,83-94.
    41. Costa, S., Shaw, P.,2006. Chromatin organization and cell fate switch respond to positional information in Arabidopsis. Nature 439,493-496.
    42. Desbrosses, G., Josefsson, C., Rigas, S., Hatzopoulos, P., Dolan, L.,2003. AKT1 and TRH1 are required during root hair elongation in Arabidopsis. J Exp Bot 54,781-788.
    43. Di Cristina, M., Sessa, G., Dolan, L., Linstead, P., Baima, S., Ruberti, I., 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.
    44. Dolan, L.,2001. The role of ethylene in root hair growth in Arabidopsis. J. Plant Nutr. Soil Sci.-Z. Pflanzenernahr. Bodenkd.164,141-145.
    45. Dolan, L., Costa, S.,2001. Evolution and genetics of root hair stripes in the root epidermis. J Exp Bot 52,413-417.
    46. Dolan, L., Duckett, C.M., Grierson, C., Linstead, P., Schneider, K., Lawson, E., Dean, C., Poethig, S., Roberts, K.,1994. Clonal Relationships and Cell Patterning in the Root Epidermis of Arabidopsis. Development 120,2465-2474.
    47. Downes, B.P., Stupar, R.M., Gingerich, D.J., Vierstra, R.D.,2003. The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis:UPL3 has a specific role in trichome development. Plant J.35,729-742.
    48. Du, W.-j., Yu, D.-y., Fu, S.-x.,2009. Analysis of QTLs for the Trichome Density on the Upper and Downer Surface of Leaf Blade in Soybean Glycine max (L.) Merr. Agricultural Sciences in China 8,529-537.
    49. El Refy, A., Perazza, D., Zekraoui, L., Valay, J.G., Bechtold, N., Brown, S., Hulskamp, M., Herzog, M., Bonneville, J.M.,2003. The Arabidopsis KAKTUS gene encodes a HECT protein and controls the number of endoreduplication cycles. Mol Genet Genomics 270, 403-414.
    50. Esch, J.J., Chen, M., Sanders, M., Hillestad, M., Ndkium, S., Idelkope, B., Neizer, J., Marks, M.D.,2003. A contradictory GLABRA3 allele helps define gene interactions controlling trichome development in Arabidopsis. Development 130,5885-5894.
    51. Esch, J.J., Chen, M.A., Hillestad, M., Marks, M.D.,2004. Comparison of TRY and the closely related At1g01380 gene in controlling Arabidopsis trichome patterning. Plant J.40, 860-869.
    52. Fan, J.-L., Wei, X.-Z., Wan, L.-C., Zhang, L.-Y., Zhao, X.-Q., Liu, W.-Z., Hao, H.-Q., Zhang, H.-Y.,2011. Disarrangement of actin filaments and Ca (2+) gradient by CdCl (2) alters cell wall construction in Arabidopsis thaliana root hairs by inhibiting vesicular trafficking. J Plant Physiol 168,1157-1167.
    53. Favery, B., Ryan, E., Foreman, J., Linstead, P., Boudonck, K., Steer, M., Shaw, P., Dolan, L.,2001. KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidopsis. Genes Dev 15,79-89.
    54. Fu, X.D., Harberd, N.P.,2003. Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421,740-743.
    55. Galway, M.E., Masucci, J.D., Lloyd, A.M., Walbot, V., Davis, R.W., Schiefelbein, J.W., 1994. THE TTG GENE IS REQUIRED TO SPECIFY EPIDERMAL-CELL FATE AND CELL PATTERNING IN THE ARABIDOPSIS ROOT. Developmental Biology 166, 740-754.
    56. Gan, Y., Filleur, S., Rahman, A., Gotensparre, S., Forde, B.G.,2005. Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222, 730-742.
    57. Gan, Y., Yu, H., Peng, J., Broun. P.,2007a. Genetic and molecular regulation by DELLA proteins of trichome development in Arabidopsis. Plant Physiology 145,1031-1042.
    58. Gan, Y.B., Kumimoto, R., Liu, C., Ratcliffe, O., Yu, H., Broun, P.,2006. GLABROUS INFLORESCENCE STEMS modulates the regulation by gibberellins of epidermal differentiation and shoot maturation in Arabidopsis. Plant Cell 18,1383-1395.
    59. Gan, Y.B., Liu, C., Yu, H., Broun, P.,2007b. Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development 134,2073-2081.
    60. Gaymard, F., Pilot, G., Lacombe, B., Bouchez, D., Bruneau, D., Boucherez, J., Michaux-Ferriere, N., Thibaud, J.B., Sentenac, H.,1998. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell 94, 647-655.
    61. Gilding, E.K., Marks, M.D.,2010. Analysis of purified glabra3-shapeshifter trichomes reveals a role for NOECK in regulating early trichome morphogenic events. Plant J.64, 304-317.
    62. Gilroy, S., Jones, D.L.,2000. Through form to function:root hair development and nutrient uptake. Trends Plant Sci.5,56-60.
    63. Gomez-Roldan, V., Fermas, S., Brewer, P.B., Puech-Pages, V., Dun, E.A., Pillot, J.P., Letisse, F., Matusova, R., Danoun, S., Portais, J.C., Bouwmeester, H., Becard, G., Beveridge, C.A., Rameau, C., Rochange, S.F.,2008. Strigolactone inhibition of shoot branching. Nature 455,189-194.
    64. Gourcilleau, D., Lenne, C., Armenise, C., Moulia, B., Julien, J.L., Bronner, G., Leblanc-Fournier, N.,2011. Phylogenetic Study of Plant Q-type C2H2 Zinc Finger Proteins and Expression Analysis of Poplar Genes in Response to Osmotic, Cold and Mechanical Stresses. DNA Research 18,77-92.
    65. Greenboim-Wainberg, Y., Maymon, I., Borochov, R., Alvarez, J., Olszewski, N., Ori, N., Eshed, Y., Weiss, D.,2005. Cross talk between gibberellin and cytokinin:The Arabidopsis GA response inhibitor SPINDLY plays a positive role in cytokinin signaling. Plant Cell 17, 92-102.
    66. Grierson, C.S., Roberts, K., Feldmann, K.A., Dolan, L.,1997. The COW1 locus of Arabidopsis acts after RHD2, and in parallel with RHD3 and TIP1, to determine the shape, rate of elongation, and number of root hairs produced from each site of hair formation. Plant Physiol 115,981-990.
    67. Harada, E., Kim, J.-A., Meyer, A.J., Hell, R., Clemens, S., Choi, Y.-E.,2010. Expression Profiling of Tobacco Leaf Trichomes Identifies Genes for Biotic and Abiotic Stresses. Plant and Cell Physiology 51,1627-1637.
    68. Hartung, F., Angelis, K.J., Meister, A., Schubert, I., Melzer, M., Puchta, H.,2002. An Archaebacterial Topoisomerase Homolog Not Present in Other Eukaryotes Is Indispensable for Cell Proliferation of Plants. Curr Biol 12,1787-1791.
    69. Heim, M.A., Jakoby, M., Werber, M., Martin, C., Weisshaar, B., Bailey, P.C.,2003. The basic helix-loop-helix transcription factor family in plants:a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20,735-747.
    70. Hulskamp, M., Misera, S., Jurgens, G.,1994. GENETIC DISSECTION OF TRICHOME CELL-DEVELOPMENT IN ARABIDOPSIS. Cell 76,555-566.
    71. Hulskamp, M., Schnittger, A., Folkers, U.,1999. Pattern formation and cell differentiation: Trichomes in Arabidopsis as a genetic model system. In:Jeon, K.W. (Ed.), International Review of Cytology-a Survey of Cell Biology, Vol 186, pp.147-178.
    72. Hung, C.Y., Lin, Y., Zhang, M., Pollock, S., Marks, M.D., Schiefelbein, J.,1998. A common position-dependent mechanism controls cell-type patterning and GLABRA2 regulation in the root and hypocotyl epidermis of Arabidopsis. Plant Physiol 117,73-84.
    73. Ishida, T., Kurata, T., Okada, K., Wada, T.,2008. A genetic regulatory network in the development of trichomes and root hairs. Annual Review of Plant Biology 59,365-386.
    74. Jacobsen, S.E., Binkowski, K.A., Olszewski, N.E.,1996. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction Arabidopsis. Proc. Natl. Acad. Sci.U.S. A.93,9292-9296.
    75. Jacobsen, S.E., Olszewski, N.E.,1993. MUTATIONS AT THE SPINDLY LOCUS OF ARABIDOPSIS ALTER GIBBERELLIN SIGNAL-TRANSDUCTION. Plant Cell 5, 887-896.
    76. Johnson, C.S., Kolevski, B., Smyth, D.R.,2002. TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14,1359-1375.
    77. Jones, A.R., Kramer, E.M., Knox, K., Swarup, R., Bennett, M.J., Lazarus, C.M., Leyser, H.M.O., Grierson, C.S.,2009. Auxin transport through non-hair cells sustains root-hair development. Nature Cell Biology 11,78-U156.
    78. Jun, J.H., Ha, C.M., Fletcher, J.C.,2010. BLADE-ON-PETIOLE1 coordinates organ determinacy and axial polarity in Arabidopsis by directly activating ASYMMETRIC LEAVES2. Plant Cell 22,62-76.
    79. Jung, J.-Y., Shin, R., Schachtman, D.P.,2009. Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis. Plant Cell 21,607-621.
    80. Kam, J., Gresshoff, P.M., Shorter. R., Xue, G.P.,2008. The Q-type C2H2 zinc finger subfamily of transcription factors in Triticum aestivum is predominantly expressed in roots and enriched with members containing an EAR repressor motif and responsive to drought stress. Plant Mol.Biol.67,305-322.
    81. Kang, J.-H., Liu, G., Shi, F., Jones, A.D., Beaudry, R.M., Howe, G.A.,2010. The Tomato odorless-2 Mutant Is Defective in Trichome-Based Production of Diverse Specialized Metabolites and Broad-Spectrum Resistance to Insect Herbivores. Plant Physiology 154, 262-272.
    82. Kang, Y.H., Kirik, V., Hulskamp, M., Nam, K.H., Hagely, K., Lee, M.M., Schiefelbeind, J., 2009. The MYB23 Gene Provides a Positive Feedback Loop for Cell Fate Specification in the Arabidopsis Root Epidermis. Plant Cell 21,1080-1094.
    83. Kapoor, S., Kobayashi, A., Takatsuji, H.,2002. Silencing of the tapetum-specific zinc finger gene TAZ1 causes premature degeneration of tapetum and pollen abortion in petunia. Plant Cell 14,2353-2367.
    84. Kazama, H., Dan, H., Imaseki, H., Wasteneys, C.O.,2004. Transient exposure to ethylene stimulates cell division and alters the fate and polarity of hypocotyl epidermal cells. Plant Physiology 134,1614-1623.
    85. Keller, B.,1993. Structural Cell Wall Proteins. Plant Physiol 101,1127-1130.
    86. Kim, H.J., Han, J.H., Kwon, J.K., Park, M., Kim, B.D., Choi, D.,2010. Fine mapping of pepper trichome locus 1 controlling trichome formation in Capsicum annuum L. CM334. Theoretical and Applied Genetics 120,1099-1106.
    87. Kirik, V., Bouyer, D., Schobinger, U., Bechtold, N., Herzog, M., Bonneville, J.M., Hulskamp, M.,2001. CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 11,1891-1895.
    88. Kirik, V., Grini. P.E., Mathur, J., Klinkhammer, I., Adler, K., Bechtold, N., Herzog, M., Bonneville, J.M., Hulskamp, M.,2002a. The Arabidopsis TUBULIN-FOLDING COFACTOR A gene is involved in the control of the alpha/beta-tubulin monomer balance. Plant Cell 14,2265-2276.
    89. Kirik, V., Lee, M.M., Wester, K., Herrmann, U., Zheng, Z.G., Oppenheimer, D., Schiefelbein, J., Hulskamp, M.,2005. Functional diversification of MYB23 and GL1 genes in trichome morphogenesis and initiation. Development 132,1477-1485.
    90. Kirik, V., Mathur, J., Grini, P.E., Klinkhammer, I., Adler, K., Bechtold, N., Herzog, M., Bonneville, J.M., Hulskamp, M.,2002b. Functional analysis of the tubulin-folding cofactor C in Arabidopsis thaliana. Curr Biol 12,1519-1523.
    91. Kirik, V., Simon, M., Huelskamp, M., Schiefelbein, J.,2004a. The ENHANCER OF TRY AND CPCl gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Developmental Biology 268,506-513.
    92. Kirik, V., Simon, M., Wester, K., Schiefelbein, J., Hulskamp, M.,2004b. ENHANCER of TRY and CPC 2 (ETC2) reveals redundancy in the region-specific control of trichome development of Arabidopsis. Plant Mol.Biol.55,389-398.
    93. Kobayashi, H., Yanaka, M., Ikeda, T.M.,2010. Exogenous Methyl Jasmonate Alters Trichome Density on Leaf Surfaces of Rhodes Grass (Chloris gayana Kunth). Journal of Plant Growth Regulation 29,506-511.
    94. Kobayashi, K., Kakihara, F., Kato, M.,1998. Genetic analysis for the production of purple flower zonal Geranium (Pelargonium x hortorum Bailey). Breeding Sci 48,169-176.
    95. Krishna, S.S., Majumdar, I., Grishin, N.V.,2003. Structural classification of zinc fingers. Nucleic Acids Research 31,532-550.
    96. Kubo, K., Sakamoto, A., Kobayashi, A., Rybka, Z., Kanno, Y., Nakagawa, H., Nishino, T., Takatsuji, H.,1998a. Cys (2)/His (2) zinc-finger protein family of petunia:evolution and general mechanism of target-sequence recognition. Nucleic Acids Research 26,608-615.
    97. Kubo, K., Sakamoto, A., Kobayashi, A., Rybka, Z., Kanno, Y., Nakagawa, H., Takatsuji, H.,1998b. Cys2/His2 zinc-finger protein family of petunia:evolution and general mechanism of target-sequence recognition. Nucleic Acids Res 26,608-615.
    98. Kuppusamy, K.T., Chen, A.Y., Nemhauser, J.L.,2009. Steroids are required for epidermal cell fate establishment in Arabidopsis roots. Proc. Natl. Acad. Sci. U. S. A.106.
    99. 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., Wada, T., 2005. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 132,5387-5398.
    100. Kwak, S.-H., Schiefelbein, J.,2007. The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Developmental Biology 302,118-131.
    101. Kwak S.J., a.S.J.,2008. Cellular pattern formation by SCRAMBLED, a leucine-rich repeat receptor-like kinase in Arabidopsis. Plant Signaling & Behavior 3,110-112.
    102. Kwak, S.H., Schiefelbein, J., Shen, R.,2005. Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 307,1111-1113.
    103. Leblanc, A., Renault, H., Lecourt, J., Etienne, P., Deleu, C., Le Deunff, E.,2008. Elongation changes of exploratory and root hair systems induced by aminocyclopropane carboxylic acid and aminoethoxyvinylglycine affect nitrate uptake and BnNrt2.1 and BnNrt1.1 transporter gene expression in oilseed rape. Plant Physiology 146,1928-1940.
    104. Lee, J.J., Woodward, A.W., Chen, Z.J.,2007. Gene expression changes and early events in cotton fibre development. Annals of Botany 100,1391-1401.
    105. Lee, M.M., Schiefelbein, J.,1999. WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 99,473-483.
    106. Li, J., Chory, J.,1997. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90,929-938.
    107. Lin, R.C., Teng, Y.B., Park, H.J., Ding, L., Black, C., Fang, P., Wang, H.Y.,2008. Discrete and essential roles of the multiple domains of Arabidopsis FHY3 in mediating phytochrome A signal transduction. Plant Physiology 148,981-992.
    108. Maes, L., Inze, D., Goossens, A.,2008. Functional Specialization of the TRANSPARENT TESTA GLABRA1 Network Allows Differential Hormonal Control of Laminal and Marginal Trichome Initiation in Arabidopsis Rosette Leaves. Plant Physiology 148, 1453-1464.
    109. Maes, L., Van Nieuwerburgh, F.C.W., Zhang, Y.S., Reed, D.W., Pollier, J., Casteele, S., Inze, D., Covello, P.S., Deforce, D.L.D., Goossens, A.,2010. Dissection of the phytohormonal regulation of trichome formation and biosynthesis of the antimalarial compound artemisinin in Artemisia annua plants. New Phytol.189,176-189.
    110. Marks, M.D., Esch, J J.,2003. Initiating inhibition-Control of epidermal cell patterning in plants. Embo Reports 4,24-25.
    111. Martin, L., Leblanc-Fournier, N., Azri, W., Lenne, C., Henry, C., Coutand, C., Julien, J.L. 2009. Characterization and expression analysis under bending and other abiotic factors of PtaZFP2, a poplar gene encoding a Cys2/His2 zinc finger protein. Tree Physiology 29, 125-136.
    112. Masucci, J.D., Rerie, W.G., Foreman, D.R., Zhang, M., Galway, M.E., Marks, M.D., Schiefelbein, J.W.,1996. The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122,1253-1260.
    113. Masucci, J.D., Schiefelbein, J.W.,1994. The rhd6 Mutation of Arabidopsis thaliana Alters Root-Hair Initiation through an Auxin- and Ethylene-Associated Process. Plant Physiol 106,1335-1346.
    114. Masucci, J.D., Schiefelbein, J.W.,1996. Hormones act downstream of TTG and GL2 to promote root hair outgrowth during epidermis development in the Arabidopsis root. Plant Cell 8,1505-1517.
    115. Mathur, J., Chua, N.H.,2000. Microtubule stabilization leads to growth reorientation in Arabidopsis trichomes. Plant Cell 12,465-477.
    116. Mathur, J., Mathur, N., Kernebeck, B., Hulskamp, M.,2003a. Mutations in actin-related proteins 2 and 3 affect cell shape development in Arabidopsis. Plant Cell 15,1632-1645.
    117. Mathur, J., Mathur, N., Kirik, V., Kemebeck, B., Srinivas, B.P., Hulskamp, M.,2003b. Arabidopsis CROOKED encodes for the smallest subunit of the ARP2/3 complex and controls cell shape by region specific fine F-actin formation. Development 130, 3137-3146.
    118. Mathur, J., Spielhofer, P., Kost, B., Chua, N.H.,1999. The actin cytoskeleton is required to elaborate and maintain spatial patterning during trichome cell morphogenesis in Arabidopsis thaliana. Development 126,5559-5568.
    119. Meissner, R., Michael, A.J.,1997. Isolation and characterisation of a diverse family of Arabidopsis two and three-fingered C2H2 zinc finger protein genes and cDNAs. Plant Mol.Biol.33,615-624.
    120. Michael, G.,2001. The control of root hair formation:suggested mechanisms.. Journal of Plant Nutrition and Soil Science 164,111-119.
    121. Miedema, H., Demidchik, V., Very, A.-A., Bothwell, J.H.F., Brownlee, C., Davies, J.M., 2008. Two voltage-dependent calcium channels co-exist in the apical plasma membrane of Arabidopsis thaliana root hairs. New Phytol.179,378-385.
    122. Miller, J., McLachlan, A.D., Klug, A.,1985. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J 4,1609-1614.
    123. Mitsuya, Y., Takahashi, Y., Uehara, Y., Berberich, T., Miyazaki, A., Takahashi, H., Kusano, T.,2007. Identification of a novel Cys2/His2-type zinc-finger protein as a component of a spermine-signaling pathway in tobacco. J Plant Physiol 164,785-793.
    124. Molendijk, A.J., Bischoff, F., Rajendrakumar, C.S., Friml, J., Braun, M., Gilroy, S., Palme, K.,2001. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20,2779-2788.
    125. Monshausen, G.B., Messerli, M.A., Gilroy, S.,2008. Imaging of the Yellow Cameleon 3.6 indicator reveals that elevations in cytosolic Ca2+ follow oscillating increases in growth in root hairs of Arabidopsis. Plant Physiology 147,1690-1698.
    126. Morohashi, K., Grotewold, E.,2009. A Systems Approach Reveals Regulatory Circuitry for Arabidopsis Trichome Initiation by the GL3 and GL1 Selectors. Plos Genetics 5.
    127. Muller, M., Schmidt, W.,2004. Environmentally induced plasticity of root hair development in Arabidopsis. Plant Physiol 134,409-419.
    128. Mussig, C.,2005. Brassinosteroid-promoted growth. Plant Biol (Stuttg) 7,110-117.
    129. Mussig, C., Shin, G.H., Altmann, T.,2003. Brassinosteroids promote root growth in Arabidopsis. Plant Physiology 133,1261-1271.
    130. Nagarajan, V.K., Jain, A., Poling, M.D., Lewis. A.J., Raghothama, K.G., Smith, A.P.,2011. Arabidopsis Phtl;5 Mobilizes Phosphate between Source and Sink Organs and Influences the Interaction between Phosphate Homeostasis and Ethylene Signaling. Plant Physiology 156,1149-1163.
    131. Nagpal, P., Walker, L.M., Young, J.C., Sonawala, A., Timpte, C., Estelle, M., Reed, J.W., 2000. AXR2 encodes a member of the Aux/IAA protein family. Plant Physiol 123, 563-574.
    132. Nemhauser, Chory, J., Mockler, T.C.,2004. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. Plos Biol 2,1460-1471.
    133. Nesi, N., Debeaujon, I., Jond, C., Pelletier, G., Caboche, M., Lepiniec, L.,2000. The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. Plant Cell 12,1863-1878.
    134. Niu, Y., Jin, C., Jin, G., Zhou, Q., Lin, X., Tang, C., Zhang, Y.,2011. Auxin modulates the enhanced development of root hairs in Arabidopsis thaliana (L.) Heynh. under elevated CO (2). Plant, cell & environment 34,1304-1317.
    135. Ohashi, Y., Oka, A., Rodrigues-Pousada, R., Possenti, M., Ruberti, I., Morelli, G., Aoyama, T.,2003. Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300,1427-1430.
    136. Oppenheimer, D.G., Herman, P.L., Sivakumaran, S., Esch, J., Marks, M.D.,1991. A MYB GENE REQUIRED FOR LEAF TRICHOME DIFFERENTIATION IN ARABIDOPSIS IS EXPRESSED IN STIPULES. Cell 67,483-493.
    137. Oppenheimer, D.G., Pollock, M.A., Vacik, J., Szymanski, D.B., Ericson, B., Feldmann, K., Marks, M.D.,1997. Essential role of a kinesin-like protein in Arabidopsis trichome morphogenesis. Proc. Natl. Acad. Sci. U. S. A.94,6261-6266.
    138. Parenicova, L., de Folter, S., Kieffer, M., Homer, D.S., Favalli, C., Busscher, J., Cook, H.E., Ingram, R.M., Kater, M.M., Davies, B., Angenent, G.C.,2003. Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis:New openings to the MADS world. Plant Cell 15,1538-1551.
    139. Payne, C.T., Zhang, F., Lloyd, A.M.,2000. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 156,1349-1362.
    140. Payne, T., Johnson, S.D., Koltunow, A.M.,2004. KNUCKLES (KNU) encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium. Development 131,3737-3749.
    141. Perazza, D., Herzog, M., Hulskamp, M., Brown, S., Dome, A.M., Bonneville, J.M.,1999. Trichome cell growth in Arabidopsis thaliana can be derepressed by mutations in at least five genes. Genetics 152,461-476.
    142. Perazza, D., Vachon, G., Herzog, M.,1998. Gibberellins promote trichome formation by up-regulating GLABROUS1 in Arabidopsis. Plant Physiology 117,375-383.
    143. Pesch, M., Huelskamp, M.,2009. One, two, three... models for trichome patterning in Arabidopsis? Current Opinion in Plant Biology 12,587-592.
    144. Pesch, M., Hulskamp, M.,2004. Creating a two-dimensional pattern de novo during Arabidopsis trichome and root hair initiation. Current Opinion in Genetics & Development 14,422-427.
    145. Plett, J.M., Mathur, J., Regan, S.,2009. Ethylene receptor ETR2 controls trichome branching by regulating microtubule assembly in Arabidopsis thaliana. J Exp Bot 60, 3923-3933.
    146. Qi, T.C., Song, S.S., Ren, Q.C., Wu, D.W., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C.M., Xie, D.X.,2011. The Jasmonate-ZIM-Domain Proteins Interact with the WD-Repeat/bHLH/MYB Complexes to Regulate Jasmonate-Mediated Anthocyanin Accumulation and Trichome Initiation in Arabidopsis thaliana. Plant Cell 23,1795-1814.
    147. Qiu, J.L., Jilk, R., Marks, M.D., Szymanski, D.B.,2002. The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14,101-118.
    148. Rahman, A., Hosokawa, S., Oono, Y., Amakawa, T., Goto, N., Tsurumi, S.,2002. Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130,1908-1917.
    149. Ramachandran, S., Christensen, H.E., Ishimaru, Y., Dong, C.H., Chao-Ming, W., Cleary, A.L., Chua, N.H.,2000. Profilin plays a role in cell elongation, cell shape maintenance, and flowering in Arabidopsis. Plant Physiol 124,1637-1647.
    150. Rerie. W.G., Feldmann, K.A., Marks, M.D.,1994. THE GLABRA2 GENE ENCODES A HOMEO DOMAIN PROTEIN REQUIRED FOR NORMAL TRICHOME DEVELOPMENT IN ARABIDOPSIS. Genes & Development 8,1388-1399.
    151. Riely, B.K., He, H., Venkateshwaran, M., Sarma. B., Schraiber, J., Ane, J.-M., Cook, D.R., 2011. Identification of legume RopGEF gene families and characterization of a Medicago truncatula RopGEF mediating polar growth of root hairs. Plant J.65,230-243.
    152. Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K.A., Grabov, A., Dolan, L., Hatzopoulos, P.,2001. TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13,139-151.
    153. Roberts, K., Sugimoto-Shirasu, K., Stacey, N.J., Corsar, J., McCann, M.C.,2002. DNA topoisomerase Ⅵ is essential for endoreduplication in Arabidopsis. Curr Biol 12, 1782-1786.
    154. Rugkong, A., McQuinn, R., Giovannoni, J.J., Rose, J.K.C., Watkins, C.B.,2011. Expression of ripening-related genes in cold-stored tomato fruit. Postharvest Biology and Technology 61,1-14.
    155. Sakai, H., Medrano, L.J., Meyerowitz, E.M.,1995. ROLE OF SUPERMAN IN MAINTAINING ARABIDOPSIS FLORAL WHORL BOUNDARIES. Nature 378, 199-203.
    156. Sakamoto, T., Kamiya, N., Ueguchi-Tanaka, M., Iwahori, S.,2001. KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes & Development 15,581-590.
    157. Sako, K., Maki, Y., Imai, K.K., Aoyama, T., Goto, D.B., Yamaguchi, J.,2010. Control of endoreduplication of trichome by RPT2a, a subunit of the 19S proteasome in Arabidopsis. Journal of Plant Research 123,701-706.
    158. Samaj, J., Baluska, F., Menzel, D.,2004. New signalling molecules regulating root hair tip growth. Trends Plant Sci.9,217-220.
    159. Samaj, J., Ovecka, M., Hlavacka, A., Lecourieux, F., Meskiene, I., Lichtscheidl, I., Lenart, P., Salaj, J., Volkmann, D., Bogre, L., Baluska, F., Hirt, H.,2002. Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. Embo J.21, 3296-3306.
    160. Savage, N.S., Walker, T., Wieckowski, Y. Schiefelbein, J., Dolan, L., Monk, N.A.M., 2008. A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. Plos Biol 6,1899-1909.
    161. Schellmann, S., Huelskamp, M., Uhrig, J.,2007. Epidermal pattern formation in the root and shoot of Arabidopsis. Biochemical Society Transactions 35,146-148.
    162. Schellmann, S., Schnittger, A., Kirik, V., Wada, T., Okada, K., Beermann, A., Thumfahrt, J., Jurgens, G., Hulskamp, M.,2002. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. Embo J.21,5036-5046.
    163. Schiefelbein, J.,2003. Cell-fate specification in the epidermis:a common patterning mechanism in the root and shoot. Current Opinion in Plant Biology 6,74-78.
    164. Schiefelbein, J., Kwak, S.H., Wieckowski, Y., Ban-on, C., Bruex, A.,2009. The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot60,1515-1521.
    165. Schiefelbein, J.W., Shipley, A., Rowse, P.,1992. CALCIUM INFLUX AT THE TIP OF GROWING ROOT-HAIR CELLS OF ARABIDOPSIS-THALIANA. Planta 187,455-459.
    166. Schiefelbein, J.W., Somerville, C.,1990. Genetic Control of Root Hair Development in Arabidopsis thaliana. Plant Cell 2,235-243.
    167. Schnepf, E., Deichgraber, G., Bopp, M.,1986. Growth, Cell-Wall Formation and Differentiation in the Protonema of the Moss, Funaria-Hygrometrica-Effects of Plasmolysis on the Developmental Program and Its Expression. Protoplasma 133,50-65.
    168. Schnittger, A., Folkers, U., Schwab, B., Jurgens, G., Hulskamp, M.,1999. Generation of a spacing pattern:The role of TRIPTYCHON in trichome patterning in Arabidopsis. Plant Cell 11,1105-1116.
    169. Schnittger, A., Hulskamp, M.,2002. Trichome morphogenesis:a cell-cycle perspective. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 357,823-826.
    170. Schnittger, A., Schobinger, U., Bouyer, D., Weinl, C., Stierhof, Y.D., Hulskamp, M., 2002a. Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci U S A 99,6410-6415.
    171. Schnittger, A., Schobinger, U., Stierhof, Y.D., Hulskamp, M.,2002b. Ectopic B-Type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12,415-420.
    172. Schnittger, A., Weinl, C., Bouyer, D., Schobinger, U., Hulskamp, M.,2003. Misexpression of the cyclin-dependent kinase inhibitor ICK1/KRP1 in single-celled Arabidopsis trichomes reduces endoreduplication and cell size and induces cell death. Plant Cell 15, 303-315.
    173. Schwab, B., Mathur, J., Saedler, R., Schwarz. H., Frey, B., Scheidegger, C., Hulskamp, M., 2003. Regulation of cell expansion by the DISTORTED genes in Arabidopsis thaliana: actin controls the spatial organization of microtubules. Mol Genet Genomics 269,350-360.
    174. Seifert, G.J., Barber, C., Wells, B., Dolan, L., Roberts, K.,2002. Galactose biosynthesis in Arabidopsis:genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Curr Biol 12,1840-1845.
    175. Seifert, G.J., Barber. C., Wells, B., Roberts, K.,2004. Growth regulators and the control of nucleotide sugar flux. Plant Cell 16,723-730.
    176. Sentenac, H., Bonneaud, N., Minet, M., Lacroute, F., Salmon. J.M., Gaymard, F., Grignon, C.,1992. CLONING AND EXPRESSION IN YEAST OF A PLANT POTASSIUM-ION TRANSPORT-SYSTEM. Science 256,663-665.
    177. Simon, M., Lee, M.M., Lin, Y., Gish, L., Schiefelbein, J., 2007. Distinct and overlapping roles of single-repeat MYB genes in root epidennal patterning. Developmental Biology 311.566-578.
    178. Singh, S.K., Fischer, U., Singh, M., Grebe, M., Marchant, A.,2008. Insight into the early steps of root hair formation revealed by the procustel cellulose synthase mutant of Arabidopsis thaliana. Bmc Plant Biology 8.
    179. Song et al.,2011. Cell Fate in the Arabidopsis Root Epidermis Is Determined by Competition between WEREWOLF and CAPRICE. Plant Physiology in press.
    180. Strader, L.C., Chen, G.L., Bartel, B.,2010. Ethylene directs auxin to control root cell expansion. Plant J.64,874-884.
    181. Sugano, S., Kaminaka, H., Rybka, Z., Catala, R., Salinas, J., Matsui, K., Ohme-Takagi, M., Takatsuji, H.,2003. Stress-responsive zinc finger gene ZPT2-3 plays a role in drought tolerance in petunia. Plant J.36,830-841.
    182. Sun, S.J., Guo, S.Q., Yang, X., Bao, Y.M., Tang, H.J., Sun, H., Huang, J., Zhang, H.S., 2010a. Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61,2807-2818.
    183. Sun, Y., Yang, Y., Yuan, Z., Muller, J.L., Yu, C., Xu, Y.F., Shao, X.H., Li, X.F., Decker, E.L., Reski, R., Huang, H.,2010b. Overexpression of the Arabidopsis Gene UPRIGHT ROSETTE Reveals a Homeostatic Control for Indole-3-Acetic Acid. Plant Physiology 153,1311-1320.
    184. Symonds, V.V., Hatlestad, G., Lloyd, A.M.,2011. Natural Allelic Variation Defines a Role for ATMYCl:Trichome Cell Fate Determination. Plos Genetics 7.
    185. Szumlanski, A.L., Nielsen, E.,2009. The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21,526-544.
    186. Szymanski, D.B.,2005. Breaking the WAVE complex:the point of Arabidopsis trichomes. Current Opinion in Plant Biology 8,103-112.
    187. Szymanski, D.B., Jilk, R.A., Pollock, S.M., Marks, M.D.,1998. Control of GL2 expression in Arabidopsis leaves and trichomes. Development 125,1161-1171.
    188. Szymanski, D.B., Lloyd, A.M., Marks, M.D.,2000. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends Plant Sci.5, 214-219.
    189. Szymanski, D.B., Marks, M.D.,1998. GLABROUS 1 overexpression and TRIPTYCHON alter the cell cycle and trichome cell fate in Arabidopsis. Plant Cell 10,2047-2062.
    190. Szymanski, D.B., Marks, M.D., Wick, S.M.,1999. Organized F-actin is essential for normal trichome morphogenesis in Arabidopsis. Plant Cell 11,2331-2347.
    191. Takatsuji, H.,1998. Zinc-finger transcription factors in plants. Cellular and Molecular Life Sciences 54,582-596.
    192. Takatsuji, H.,1999. Zinc-finger proteins:the classical zinc finger emerges in contemporary plant science. Plant Mol Biol 39,1073-1078.
    193. Takatsuji, H., Mori, M., Benfey, P.N., Ren, L., Chua, N.H.,1992. Characterization of a zinc finger DNA-binding protein expressed specifically in Petunia petals and seedlings. EMBOJ 11,241-249.
    194. Takeda, S., Gapper, C., Kaya, H., Bell, E., Kuchitsu, K., Dolan, L.,2008. Local positive feedback regulation determines cell shape in root hair cells. Science 319,1241-1244.
    195. Tanimoto, M., Roberts, K., Dolan, L.,1995. Ethylene is a positive regulator of root hair development in Arabidopsis thaliana. Plant J 8.943-948.
    196. Tian, Z.D., Zhang, Y., Liu, J., Xie, C.H.,2010. Novel potato C2H2-type zinc finger protein gene, StZFP1, which responds to biotic and abiotic stress, plays a role in salt tolerance. Plant Biology 12,689-697.
    197. Tominaga-Wada, R., Ishida, T., Wada, T.,2011. NEW INSIGHTS INTO THE MECHANISM OF DEVELOPMENT OF ARABIDOPSIS ROOT HAIRS AND TRICHOMES. In:Jeon, K.W. (Ed.), International Review of Cell and Molecular Biology, Vol286, pp.67-106.
    198. Tominaga, R., Iwata, M., Okada, K., Wada, T.,2007. Functional analysis of the epidermal-specific MYB genes CAPRICE and WEREWOLF in Arabidopsis. Plant Cell 19,2264-2277.
    199. Tominaga, R., Iwata, M., Sano, R., Inoue, K., Okada, K., Wada, T.,2008. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development 135,1335-1345.
    200. Traw, M.B., Bergelson, J.,2003. Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiology 133,1367-1375.
    201. Tsutsui, T., Yamaji, N., Ma, J.F.,2011. Identification of a Cis-Acting Element of ART1, a C2H2-Type Zinc-Finger Transcription Factor for Aluminum Tolerance in Rice. Plant Physiology 156,925-931.
    202. Uhrig, J.F., Mutondo. M., Zimmermann, I., Deeks, M.J., Machesky, L.M., Thomas, P.. Uhrig, S., Rambke, C., Hussey. P.J., Huelskamp, M.,2007. The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis. Development 134,967-977.
    203. Umehara, M., Hanada, A., Yoshida, S., Akiyama. K., Arite, T., Takeda-Kamiya, N., Magome, H., Kamiya, Y., Shirasu. K., Yoneyama, K., Kyozuka, J., Yamaguchi, S.,2008. Inhibition of shoot branching by new terpenoid plant hormones. Nature 455,195-200.
    204. Urao, T., YamaguchiShinozaki. K., Mitsukawa, N., Shibata, D., Shinozaki, K.,1996. Molecular cloning and characterization of a gene that encodes a MYC-related protein in Arabidopsis. Plant Mol.Biol.32,571-576.
    205. van Der Krol, A.R., van Poecke, R.M., Vorst, O.F., Voogt, C., van Leeuwen, W., Borst-Vrensen, T.W., Takatsuji, H., van Der Plas, L.H.,1999. Developmental and wound-, cold-, desiccation-, ultraviolet-B-stress-induced modulations in the expression of the petunia zinc finger transcription factor gene ZPT2-2. Plant Physiol 121,1153-1162.
    206. Vincent, P., Chua, M., Nogue, F., Fairbrother, A., Mekeel, H., Xu, Y., Allen, N., Bibikova, T.N., Gilroy, S., Bankaitis, V.A.,2005. A Secl4p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J Cell Biol 168,801-812.
    207. Vissenberg, K., Fry, S.C.,2001. Root hair initiation is coupled to a highly localized increase of xyloglucan endotransglycosylase action in Arabidopsis roots. Plant Physiology 127,1125-1135.
    208. Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., Marks, M.D., Shimura, Y., Okada, K.,2002. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409-5419.
    209. Wada, T., Okada, K.,2002. Development of root-hair and trichome in Arabidopsis. Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme 47,1599-1604.
    210. Wada, T., Tachibana, T., Shimura, Y., Okada, K.,1997. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 277,1113-1116.
    211. Wagner, D., Sablowski, R.W.M., Meyerowitz, E.M.,1999. Transcriptional activation of APETALA1 by LEAFY. Science 285,582-584.
    212. Wagner, G.J., Wang, E., Shepherd, R.W.,2004. New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93,3-11.
    213. Walker, A.R., Davison, P.A., Bolognesi-Winfield, A.C., James, C.M., Srinivasan, N., Blundell, T.L., Esch, J.J., Marks, M.D., Gray, J.C.,1999. The TRANSPARENT TESTA GLABRA1 locus, which regulates trichome differentiation and anthocyanin biosynthesis in Arabidopsis, encodes a WD40 repeat protein. Plant Cell 11,1337-1349.
    214. Walker, J.D., Oppenheimer, D.G., Concienne, J., Larkin, J.C.,2000. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127,3931-3940.
    215. Wang, S., Hubbard, L., Chang, Y, Guo, J., Schiefelbein, J., Chen, J.-G.,2008. Comprehensive analysis of single-repeat R3 MYB proteins in epidermal cell patterning and their transcriptional regulation in Arabidopsis. Bmc Plant Biology 8.
    216. Wang, S., Kwak, S.-H., Zeng, Q., Ellis, B.E., Chen, X.-Y., Schiefelbein, J., Chen, J.-G., 2007. TRICHOMELESS1 regulates trichome patterning by suppressing GLABRA1 in Arabidopsis. Development 134,3873-3882.
    217. Webb, M., Jouannic, S., Foreman, J., Linstead, P., Dolan, L.,2002. Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3--a katanin-p60 protein. Development 129,123-131.
    218. Weinl, C., Marquardt, S., Kuijt, S.J.H., Nowack, M.K., Jakoby, M.J., Hulskamp, M., Schnittger, A.,2005. Novel functions of plant cyclin-dependent kinase inhibitors, ICK1/KRP1, can act non-cell-autonomously and inhibit entry into mitosis. Plant Cell 17, 1704-1722.
    219. Wymer, C.L., Bibikova, T.N., Gilroy, S.,1997. Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. Plant J.12,427-439.
    220. Xu, C.R., Liu, C., Wang, Y.L., Li, L.C., Chen, W.Q., Xu, Z.H., Bai, S.N.,2005. Histone acetylation affects expression of cellular patterning genes in the Arabidopsis root epidermis. Proc Natl Acad Sci U S A 102,14469-14474.
    221. Yang, Z.,2002. Small GTPases:versatile signaling switches in plants. Plant Cell 14 Suppl, S375-388.
    222. Yi, K., Menand, B., Bell, E., Dolan, L.,2010. A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nature Genetics 42,264-U108.
    223. Yoshida, Y., Sano, R., Wada, T., Takabayashi, J., Okada, K.,2009. Jasmonic acid control of GLABRA3 links inducible defense and trichome patterning in Arabidopsis. Development 136,1039-1048.
    224. Yoshioka, K., Fukushima, S., Yamazaki, T., Yoshida, M., Takatsuji, H.,2001. The plant zinc finger protein ZPT2-2 has a unique mode of DNA interaction. J Biol Chem 276, 35802-35807.
    225. Yu, H., Ito, T., Zhao, Y.X., Peng, J.R., Kumar, P.P., Meyerowitz, E.M.,2004. Floral homeotic genes are targets of gibberellin signaling in flower development. Proc. Natl. Acad. Sci. U. S. A.101,7827-7832.
    226. Yu, N., Cai, W.J., Wang, S.C., Shan, C.M., Wang, L.J., Chen, X.Y.,2010. Temporal Control of Trichome Distribution by MicroRNA156-Targeted SPL Genes in Arabidopsis thaliana. Plant Cell 22,2322-2335.
    227. Zhang, F., Gonzalez, A., Zhao, M.Z., Payne, C.T., Lloyd, A.,2003. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 130,4859-4869.
    228. Zhang, H.M., Forde, B.G.,1998. An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279,407-409.
    229. Zhang, X., Guo, X.P., Lei, C.L., Cheng, Z.J., Lin, Q.B., Wang, J.L., Wu, F.Q., Wang, J., Wan, J.M.,2011a. Overexpression of SICZFP1, a Novel TFIIIA-type Zinc Finger Protein from Tomato, Confers Enhanced Cold Tolerance in Transgenic Arabidopsis and Rice. Plant Molecular Biology Reporter 29,185-196.
    230. Zhang, Y., Xiao, Y., Du, F., Cao, L., Dong, H., Ren, H.,2011b. Arabidopsis VILLIN4 is involved in root hair growth through regulating actin organization in a Ca2+-dependent manner. New Phytol.190,667-682.
    231. Zhu, C., Gan, L., Shen, Z., Xia, K.,2006. Interactions between jasmonates and ethylene in the regulation of root hair development in Arabidopsis. Journal of Experimental Botany 57,1299-1308.
    232.黄骥,王建飞,张红生,2004.植物C2H2型锌指蛋白的结构与功能.遗传26,414-418.

© 2004-2018 中国地质图书馆版权所有 京ICP备05064691号 京公网安备11010802017129号

地址:北京市海淀区学院路29号 邮编:100083

电话:办公室:(+86 10)66554848;文献借阅、咨询服务、科技查新:66554700