The cuticle is a hydrophobic lipid layer covering the epidermal cells of terrestrial plants. Although many genes involved in Arabidopsis cuticle development have been identified, the transcriptional regulation of these genes is largely unknown. Previously, we demonstrated that AtCFL1 negatively regulates cuticle development by interacting with the HD-ZIP IV transcription factor HDG1. Here, we report that two bHLH transcription factors, AtCFL1 associated protein 1 (CFLAP1) and CFLAP2, are also involved in AtCFL1-mediated regulation of cuticle development. CFLAP1 and CFLAP2 interact with AtCFL1 both in vitro and in vivo. Overexpression of either CFLAP1 or CFLAP2 led to expressional changes of genes involved in fatty acids, cutin and wax biosynthesis pathways and caused multiple cuticle defective phenotypes such as organ fusion, breakage of the cuticle layer and decreased epicuticular wax crystal loading. Functional inactivation of CFLAP1 and CFLAP2 by chimeric repression technology caused opposite phenotypes to the CFLAP1 overexpressor plants. Interestingly, we find that, similar to the transcription factor HDG1, the function of CFLAP1 in cuticle development is dependent on the presence of AtCFL1. Furthermore, both HDG1 and CFLAP1/2 interact with the same C-terminal C4 zinc finger domain of AtCFL1, a domain that is essential for AtCFL1 function. These results suggest that AtCFL1 may serve as a master regulator in the transcriptional regulation of cuticle development, and that CFLAP1 and CFLAP2 are involved in the AtCFL1-mediated regulation pathway, probably through competing with HDG1 to bind to AtCFL1.
References
[1]
Post-Beittenmiller D (1996) Biochemistry and molecular biology of wax production in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 405–430. pmid:15012295 doi: 10.1146/annurev.arplant.47.1.405
[2]
Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42: 51–80. pmid:12467640 doi: 10.1016/s0163-7827(02)00045-0
[3]
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59: 683–707. doi: 10.1146/annurev.arplant.59.103006.093219. pmid:18251711
[4]
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189: 17–39. doi: 10.1111/j.1469-8137.2010.03514.x. pmid:21054411
[5]
Aharoni A, Dixit S, Jetter R, Thoenes E, van Arkel G, et al. (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16: 2463–2480. pmid:15319479 doi: 10.1105/tpc.104.022897
[6]
Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9: 281–287. pmid:16580871 doi: 10.1016/j.pbi.2006.03.001
[7]
Li Y, Beisson F, Koo AJ, Molina I, Pollard M, et al. (2007) Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci USA 104: 18339–18344. pmid:17991776 doi: 10.1073/pnas.0706984104
[8]
Li-Beisson Y, Pollard M, Sauveplane V, Pinot F, Ohlrogge J, et al. (2009) Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci USA 106: 22008–22013. doi: 10.1073/pnas.0909090106. pmid:19959665
[9]
Yang W, Pollard M, Li-Beisson Y, Beisson F, Feig M, et al. (2010) A distinct type of glycerol-3-phosphate acyltransferase with sn-2 preference and phosphatase activity producing 2-monoacylglycerol. Proc Natl Acad Sci USA 107:12040–12045. doi: 10.1073/pnas.0914149107. pmid:20551224
[10]
Yeats TH, Martin LB, Viart HM, Isaacson T, He Y, et al. (2012) The identification of cutin synthase: formation of the plant polyester cutin. Nat Chem Biol. 8: 609–611. doi: 10.1038/nchembio.960. pmid:22610035
[11]
Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, et al. (2012) Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24: 3119–3134. doi: 10.1105/tpc.112.101055. pmid:22805434
[12]
Yeats TH, Huang W, Chatterjee S, Viart HM, Clausen MH, et al. (2014) Tomato Cutin Deficient 1 (CD1) and putative orthologs comprise an ancient family of cutin synthase-like (CUS) proteins that are conserved among land plants. Plant J. 77: 667–675. doi: 10.1111/tpj.12422. pmid:24372802
[13]
Kurdyukov S, Faust A, Nawrath C, B？r S, Voisin D, et al. (2006) The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18: 321–339. pmid:16415209 doi: 10.1105/tpc.105.036079
[14]
Xiao F, Goodwin SM, Xiao Y, Sun Z, Baker D, et al. (2004) Arabidopsis CYP86A2 represses Pseudomonas syringae type III genes and is required for cuticle development. EMBO J 23: 2903–2913. pmid:15241470 doi: 10.1038/sj.emboj.7600290
[15]
Greer S, Wen M, Bird D, Wu X, Samuels L, et al. (2007) The cytochrome P450 enzyme CYP96A15 is the midchain alkane hydroxylase responsible for formation of secondary alcohols and ketones in stem cuticular wax of Arabidopsis. Plant Physiol 145: 653–667. pmid:17905869 doi: 10.1104/pp.107.107300
[16]
Sauveplane V, Kandel S, Kastner PE, Ehlting J, Compagnon V, et al. (2009) Arabidopsis thaliana CYP77A4 is the first cytochrome P450 able to catalyze the epoxidation of free fatty acids in plants. FEBS J 276: 719–735. doi: 10.1111/j.1742-4658.2008.06819.x. pmid:19120447
[17]
Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, et al. (2010) Cytochrome P450 family member CYP704B2 catalyzes the {omega}-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22: 173–190. doi: 10.1105/tpc.109.070326. pmid:20086189
[18]
Wellesen K, Durst F, Pinot F, Benveniste I, Nettesheim K, et al. (2001) Functional analysis of the LACERATA gene of Arabidopsis provides evidence for different roles of fatty acid omega-hydroxylation in development. Proc Natl Acad Sci USA 98: 9694–9699. pmid:11493698 doi: 10.1073/pnas.171285998
[19]
Koornneef M, Hanhart CJ, Thiel F (1989) A genetic and phenotypic description of Eceriferum (cer) mutants in Arabidopsis thaliana. J Hered 80: 118–122.
[20]
Bianchi G, Avato P, Salamini F (1979) Glossy mutants of maize. IX. Chemistry of Glossy4, Glossy8, Glossy15 and Glossy18 surface waxes. Heredity 42: 391–395. doi: 10.1038/hdy.1979.42
[21]
Dietrich CR, Perera MA, D Yandeau-Nelson M, Meeley RB, Nikolau BJ, et al. (2005) Characterization of two GL8 paralogs reveals that the 3-ketoacyl reductase component of fatty acid elongase is essential for maize (Zea mays L.) development. Plant J 42: 844–861. pmid:15941398 doi: 10.1111/j.1365-313x.2005.02418.x
[22]
Aarts MG, Keijzer CJ, Stiekema WJ, Pereira A (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7: 2115–2127. pmid:8718622 doi: 10.2307/3870155
[23]
Hannoufa A, Neqruk V, Eisner G, Lemieux B (1996) The CER3 gene of Arabidopsis thaliana is expressed in leaves, stems, roots, flowers and apical meristems. Plant J 10: 459–467. pmid:8811860 doi: 10.1046/j.1365-313x.1996.10030459.x
[24]
Negruk V, Yang P, Subramanian M, McNevin JP, Lemieux B (1996) Molecular cloning and characterization of the CER2 gene of Arabidopsis thaliana. Plant J 9: 137–145. pmid:8820603 doi: 10.1046/j.1365-313x.1996.09020137.x
[25]
Xia Y, Nikolau BJ, Schnable PS (1996) Cloning and characterization of CER2, an Arabidopsis gene that affects cuticular wax accumulation. Plant Cell 8: 1291–1304. pmid:8776898 doi: 10.2307/3870302
[26]
Rowland O, Zheng H, Hepworth SR, Lam P, Jetter R, et al. (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142: 866–877. pmid:16980563 doi: 10.1104/pp.106.086785
[27]
Lü S, Song T, Kosma DK, Parsons EP, Rowland O, et al. (2009) Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 59: 553–564. doi: 10.1111/j.1365-313X.2009.03892.x. pmid:19392700
[28]
Bernard A, Domergue F, Pascal S, Jetter R, Renne C, et al. (2012) Reconstitution of plant alkane biosynthesis in yeast demonstrates that Arabidopsis ECERIFERUM1 and ECERIFERUM3 are core components of a very-long-chain alkane synthesis complex. Plant Cell 24: 3106–3118. doi: 10.1105/tpc.112.099796. pmid:22773744
[29]
Millar AA, Clemens S, Zachgo S, Giblin EM, Taylor DC, et al. (1999) CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell 11: 825–838. pmid:10330468 doi: 10.2307/3870817
[30]
Fiebig A, Mayfield JA, Miley NL, Chau S, Fischer RL, et al. (2000) Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12: 2001–2008. pmid:11041893 doi: 10.2307/3871209
[31]
Hooker TS, Millar AA, Kunst L (2002) Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol 129: 1568–1680. pmid:12177469 doi: 10.1104/pp.003707
[32]
Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter W-D, et al. (1997) Developmental regulation of cell interactions in the Arabidopsis fiddlehead-1 mutant: A role for the epidermal cell wall and cuticle. Dev Biol 189: 311–321. pmid:9299123 doi: 10.1006/dbio.1997.8671
Yephremov A, Wisman E, Huijser P, Huijser C, Wellesen K, et al. (1999) Characterization of the FIDDLEHEAD gene of Arabidopsis reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell 11: 2187–2201. pmid:10559443 doi: 10.2307/3871018
[35]
Pruitt RE, Vielle-Calzada J-P, Ploense SE, Grossniklaus U, Lolle SJ (2000) FIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme. Proc Natl Acad Sci USA 97: 1311–1316. pmid:10655527 doi: 10.1073/pnas.97.3.1311
[36]
Ghanevati M, Jaworski JG (2001) Active-site residues of a plant membrane-bound fatty acid elongase beta-ketoacyl-CoA synthase, FAE1 KCS. Biochim Biophys Acta 1530: 77–85. pmid:11341960 doi: 10.1016/s1388-1981(00)00168-2
[37]
Chen X, Goodwin SM, Boroff VL, Liu X, Jenks MA (2003) Cloning and characterization of the WAX2 gene of Arabidopsis involved in cuticle membrane and wax production. Plant Cell 15: 1170–1185. pmid:12724542 doi: 10.1105/tpc.010926
[38]
Franke R, H？fer R, Briesen I, Emsermann M, Efremova N, et al. (2009) The DAISY gene from Arabidopsis encodes a fatty acid elongase condensing enzyme involved in the biosynthesis of aliphatic suberin in roots and the chalaza-micropyle region of seeds. Plant J 57: 80–95. doi: 10.1111/j.1365-313X.2008.03674.x. pmid:18786002
[39]
Lee SB, Jung SJ, Go YS, Kim HU, Kim JK, et al. (2009) Two Arabidopsis 3-ketoacyl CoA synthase genes, KCS20 and KCS2/DAISY, are functionally redundant in cuticular wax and root suberin biosynthesis, but differentially controlled by osmotic stress. Plant J 60: 462–475. doi: 10.1111/j.1365-313X.2009.03973.x. pmid:19619160
[40]
Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, et al. (2004) Plant cuticular lipid export requires an ABC transporter. Science 306: 702–704. pmid:15499022 doi: 10.1126/science.1102331
[41]
Bird D, Beisson F, Brigham A, Shin J, Greer S, et al. (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52: 485–498. pmid:17727615 doi: 10.1111/j.1365-313x.2007.03252.x
[42]
McFarlane HE, Shin JJ, Bird DA, Samuels AL (2010) Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell 22: 3066–3075. doi: 10.1105/tpc.110.077974. pmid:20870961
[43]
Panikashvili D, Shi JX, Schreiber L, Aharoni A (2011) The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol 190:113–124. doi: 10.1111/j.1469-8137.2010.03608.x. pmid:21232060
[44]
Bessire M, Borel S, Fabre G, Carra？a L, Efremova N, et al. (2011) A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23:1958–1970 doi: 10.1105/tpc.111.083121. pmid:21628525
[45]
Broun P, Poindexter P, Osborne E, Jiang CZ, Riechmann JL (2004) WIN1, a transcriptional activator of epidermal wax accumulation in Arabidopsis. Proc Natl Acad Sci USA 101: 4706–4711. pmid:15070782 doi: 10.1073/pnas.0305574101
[46]
Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, et al. (2007) The transcription factor WIN1/SHN1 regulates cutin biosynthesis in Arabidopsis thaliana. Plant Cell 19: 1278–1294. pmid:17449808 doi: 10.1105/tpc.106.047076
[47]
Shi JX, Malitsky S, De-Oliveira S, Branigan C, Franke RB, et al. (2011) SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 7: e1001388. doi: 10.1371/journal.pgen.1001388. pmid:21637781
[48]
Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, et al. (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42: 689–707. pmid:15918883 doi: 10.1111/j.1365-313x.2005.02405.x
[49]
Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64: 265–278. pmid:17347795 doi: 10.1007/s11103-007-9150-2
[50]
Raffaele S, Vailleau F, Léger A, Joubès J, Miersch O, et al. (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell 20: 752–767. doi: 10.1105/tpc.107.054858. pmid:18326828
[51]
Cominelli E, Sala T, Calvi D, Gusmaroli G, Tonelli C (2008) Over-expression of the Arabidopsis AtMYB41 gene alters cell expansion and leaf surface permeability. Plant J 53:53–64. pmid:17971045 doi: 10.1111/j.1365-313x.2007.03310.x
[52]
Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, et al. (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant Cell 23: 1138–1152. doi: 10.1105/tpc.111.083485. pmid:21398568
[53]
Oshima Y, Shikata M, Koyama T, Ohtsubo N, Mitsuda N, et al. (2013) MIXTA-like transcription factors and WAX INDUCER1/SHINE1 coordinately regulate cuticle development in Arabidopsis and Torenia fournieri. Plant Cell 25: 1609–1624. doi: 10.1105/tpc.113.110783. pmid:23709630
[54]
Kimbara J, Yoshida M, Ito H, Kitagawa M, Takada W, et al. (2013) Inhibition of CUTIN DEFICIENT 2 causes defects in cuticle function and structure and metabolite changes in tomato fruit. Plant Cell Physiol. 54: 1535–1548. doi: 10.1093/pcp/pct100. pmid:23912028
[55]
Javelle M, Vernoud V, Depège-Fargeix N, Arnould C, Oursel D, et al. (2010) Overexpression of the epidermis-specific homeodomain-leucine zipper IV transcription factor Outer Cell Layer1 in maize identifies target genes involved in lipid metabolism and cuticle biosynthesis. Plant Physiol. 154: 273–286. doi: 10.1104/pp.109.150540. pmid:20605912
[56]
Hooker TS, Lam P, Zheng H and Kunst L. (2007) A core subunit of the RNA-processing/degrading exosome specifically influences cuticular wax biosynthesis in Arabidopsis. Plant Cell 19: 904–913. pmid:17351114 doi: 10.1105/tpc.106.049304
[57]
Lü S, Zhao H, Des Marais DL, Parsons EP, Wen X, et al. (2012) Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol. 159: 930–944. doi: 10.1104/pp.112.198697. pmid:22635115
[58]
Wu R, Li S, He S, Wa？mann F, Yu C, et al. (2011) CFL1, a WW domain protein, regulates cuticle development by modulating the function of HDG1, a class IV homeodomain transcription factor, in rice and Arabidopsis. Plant Cell 23: 3392–3411. doi: 10.1105/tpc.111.088625. pmid:21954461
[59]
Ou B, Yin KQ, Liu SN, Yang Y, Gu T, et al. (2011) A high-throughput screening system for Arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol Plant 4: 546–555. doi: 10.1093/mp/ssr002. pmid:21343311
[60]
Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, et al. (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci USA 28: 3582–3587. doi: 10.1073/pnas.1118876109
[61]
Tanaka T, Tanaka H, Machida C, Watanabe M, Machida Y (2004) A new method for rapid visualization of defects in leaf cuticle reveals five intrinsic patterns of surface defects in Arabidopsis. Plant J 37: 139–146. pmid:14675439 doi: 10.1046/j.1365-313x.2003.01946.x
[62]
Sieber P, Schorderet M, Ryser U, Buchala A, Kolattukudy P, et al. (2000) Transgenic Arabidopsis plants expressing a fungal cutinase show alterations in the structure and properties of the cuticle and postgenital organ fusions. Plant Cell 12: 721–738. pmid:10810146 doi: 10.2307/3870997
[63]
Schnurr J, Shockey J, Browse J (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell 16: 629–642. pmid:14973169 doi: 10.1105/tpc.017608
[64]
Voisin D, Nawrath C, Kurdyukov S, Franke RB, Reina-Pinto JJ, et al. (2009) Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLoS Genet 5: e1000703. doi: 10.1371/journal.pgen.1000703. pmid:19876373
[65]
Guo Y, Qin G, Gu H, Qu L.-J. (2009) Dof5.6/HCA2, a Dof transcription factor gene, regulates interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell 21: 3518–3534. doi: 10.1105/tpc.108.064139. pmid:19915089
[66]
Tao Q, Guo D, Wei B, Zhang F, Pang C, et al. (2013) The TIE1 transcriptional repressor links TCP transcription factors with TOPLESS/TOPLESS-RELATED corepressors and modulates leaf development in Arabidopsis. Plant Cell 25: 421–437. doi: 10.1105/tpc.113.109223. pmid:23444332
[67]
Wei B, Zhang J, Pang C, Yu H, Guo D, et al. (2015) The molecular mechanism of SPOROCYTELESS/NOZZLE in controlling Arabidopsis ovule development. Cell Res 25: 121–134. doi: 10.1038/cr.2014.145. pmid:25378179
[68]
Xie C, Mao X, Huang J, Ding Y, Wu J, et al. (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39: W316–322. doi: 10.1093/nar/gkr483. pmid:21715386
[69]
Go YS, Kim H, Kim HJ, Suh MC (2014) Arabidopsis cuticular wax biosynthesis is negatively regulated by the DEWAX gene encoding an AP2/ERF-type transcription factor. Plant Cell 26: 1666–1680. pmid:24692420 doi: 10.1105/tpc.114.123307
[70]
Takahashi Y, Ebisu Y, Kinoshita T, Doi M, Okuma E, et al. (2013) bHLH transcription factors that facilitate K+ uptake during stomatal opening are repressed by abscisic acid through phosphorylation. Sci Signaling 6 (280), ra48. doi: 10.1126/scisignal.2003760
[71]
Sun L, Liu A, Georgopoulos K (1996) Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J 15: 5358–5369. pmid:8895580
[72]
Morgan B, Sun L, Avitahl N, Andrikopoulos K, Ikeda T, et al. (1997) Aiolos, a lymphoid restricted transcription factor that interacts with Ikaros to regulate lymphocyte differentiation. EMBO J 16: 2004–2013. pmid:9155026 doi: 10.1093/emboj/16.8.2004
[73]
Isaacson T, Kosma DK, Matas AJ, Buda GJ, He Y, et al. (2009) Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J 60: 363–377. doi: 10.1111/j.1365-313X.2009.03969.x. pmid:19594708
[74]
Misra S, Hurley JH (1999) Crystal structure of a phosphatidylinositol 3-phosphate-specific membrane-targeting motif, the FYVE domain of Vps27p. Cell 97: 657–666. pmid:10367894 doi: 10.1016/s0092-8674(00)80776-x
[75]
Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Biol 11: 39–46. pmid:11179890 doi: 10.1016/s0959-440x(00)00167-6
[76]
Chen H, Zou Y, Shang Y, Lin H, Wang Y, et al. (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146: 368–376. pmid:18065554 doi: 10.1104/pp.107.111740
[77]
Qin G, Gu H, Zhao Y, Ma Z, Shi G, et al. (2005) An indole-3-acetic acid carboxyl methyltransferase regulates Arabidopsis leaf development. Plant Cell 17: 2693–2704. pmid:16169896 doi: 10.1105/tpc.105.034959
[78]
Guo L, Wang ZY, Lin H, Cui WE, Chen J, et al. (2006) Expression and functional analysis of the rice plasma-membrane intrinsic protein gene family. Cell Res 16: 277–286. pmid:16541126 doi: 10.1038/sj.cr.7310035
[79]
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–ΔΔCt method. Methods 25: 402–408. pmid:11846609 doi: 10.1006/meth.2001.1262
[80]
Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, et al. (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134: 1643–1652. pmid:17376810 doi: 10.1242/dev.003533
[81]
Xia Y, Yu K, Navarre D, Seebold K, Kachroo A, et al. (2010) The glabra1 mutation affects cuticle formation and plant responses to microbes. Plant Physiol 154: 833–846. doi: 10.1104/pp.110.161646. pmid:20699396
[82]
Liu J, Zhong S, Guo X, Hao L, Wei X, et al. (2013) Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr Biol 23: 993–998. doi: 10.1016/j.cub.2013.04.043. pmid:23684977
