Abstract
The aerial surface of land plants is protected by a cuticle against abiotic and biotic stresses. A better understanding of the determinants of cuticle formation and function has the potential to contribute to the breeding of more drought tolerant and disease resistant crop varieties. Two doubled haploid (DH) mapping populations, Steptoe × Morex populations and OWB-dominant × recessive populations were exploited to genetically position homologs of a set of known cuticle-associated genes. These genes were also placed on a consensus map, BinMap2005, which includes 27 eceriferum (cer) loci. Of the 49 known cuticle-associated genes, 21 identified a homolog in barley, and of these, 14 were mapped. There was a complete linkage between HvCER6 and cer-zg, suggesting the possibility that HvCER6 is the candidate gene of CER-ZG. Positioning known cuticle-associated genes on a consensus map containing cuticle mutant loci may guide the selection of candidate genes for cuticle mutants, and thus facilitate the isolation of cuticle-associated genes in barley.
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Aarts, M.G., Keijzer, C.J., Stiekema, W.J., Pereira, A. 1995. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7:2115–2127.
Aharoni, A., Dixit, S., Jetter, R., Thoenes, E., van Arkel, G., Pereira, A. 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.
Ambavaram, M.M.R., Krishnan, A., Trijatmiko, K.R., Pereira, A. 2011. Coordinated activation of cellulose and repression of lignin biosynthesis pathways in rice. Plant Physiol. 155:916–931.
Barthlott, W., Neinhuis, C. 1997. Purity of the sacred lotus, or escape from contamination in biological surfaces. Planta 202:1–8.
Baud, S., Bellec, Y., Miquel, M., Bellini, C., Caboche, M., Lepiniec, L., Faure, J.D., Rochat, C. 2004. Gurke and pasticcino3 mutants affected in embryo development are impaired in acetyl-CoA carboxylase. Eur. Mol. Biol. Organ. Rep. 5:515–520.
Becraft, P.W., Kang, S.H., Suh, S.G. 2001. The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol. 127:486–496.
Bessire, M., Borel, S., Fabre, G., Carraça, L., Efremova, N., Yephremov, A., Cao, Y., Jetter, R., Jacquat, A.C., Métraux, J.P., Nawrath, C. 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.
Bourdenx, B., Bernard, A., Domergue, F., Pascal, S., Léger, A., Roby, D., Pervent, M., Vile, D., Haslam, R.P., Napier, J.A., Lessire, R., Joubès, J. 2011. Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol. 156:29–45.
Chen, G.X., Sagi, M., Weining, S., Krugman, T., Fahima, T., Korol, A.B., Nevo, E. 2004. Wild barley eibi1 mutation identifies a gene essential for leaf water conservation. Planta 219:684–693.
Chen, G.X., Komatsuda, T., Ma, J.F., Nawrath, C., Pourkheirandish, M., Tagiri, A., Hu, Y.G., Sameri, M., Li, X., Zhao, X., Liu, Y., Li, C., Ma, X., Wang, A., Nair, S., Wang, N., Miyao, A., Sakuma, S., Yamaji, N., Zheng, X., Nevo, E. 2011. An ATP-binding cassette subfamily Gfull transporter is essential for the retention of leaf water in both wild barley and rice. Proc. Natl. Acad. Sci. USA 108:12354–12359.
Costa, J.M., Corey, A., Hayes, P.M., Jobet, C., Kleinhofs, A., Kopisch-Obusch, A., Kramer, S.F., Kudrna, D., Li, M., Riera-Lizarazu, O., Sato, K., Szucs, P., Toojinda, T., Vales, M.I., Wolfe, R.I. 2001. Molecular mapping of the Oregon Wolfe Barleys: an exceptionally polymorphic doubled-haploid population. Theor. Appl. Genet. 103:415–424.
Dietrich, C.R., Perera, M.A, Yandeau-Nelson, M.D., Meeley, R.B., Nikolau, B.J., Schnable, P.S. 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.
Fiebig, A., Mayfield, J.A., Miley, N.L., Chau, S., Fischer, R.L., Preuss, D. 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.
Franckowiak, J.D. 1997. Revised linkage maps for morphological markers in barley, Hordeum vulgare. Barley Genet. Newsl. 26:9–21.
Franke, R., Höfer, R., Briesen, I., Emsermann, M., Efremova, N., Yephremov, A., Schreiber, L. 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.
Hooker, T.S., Millar, A.A., Kunst, L. 2002. Significance of the expression of the CER6 condensing enzyme for cuticular wax production in Arabidopsis. Plant Physiol. 129:1568–1580.
Islam, M.A., Du, H., Ning, J., Ye, H., Xiong, L. 2009. Characterization of Glossy1 -homologous genes in rice involved in leaf wax accumulation and drought resistance. Plant Mol. Biol. 70:443–456.
Ito, Y., Kimura, F., Hirakata, K., Tsuda, K., Takasugi, T., Eiguchi, M., Nakagawa, K., Kurata, N. 2011. Fatty acid elongase is required for shoot development in rice. Plant J. 66:680–688.
Javelle, M., Vernoud, V., Depège-Fargeix, N., Arnould, C., Oursel, D., Domergue, F., Sarda, X., Rogowsky, P.M. 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.
Jenks, M.A., Ashworth, E.N. 1999. Plant epicuticular waxes: function, production, and genetics. In: Janick, J. (ed.), Horticulture Reviews. John Wiley and Sons, New York, pp. 1–68.
Jenks, M.A., Tuttle, H.A., Eigenbrode, S.D., Feldmann, K.A. 1995. Leaf epicuticular waxes of the eceriferum mutants in Arabidopsis. Plant Physiol. 108:369–377.
Jetter, R., Kunst, L., Samuels, A.L. 2006. Composition of plant cuticular waxes. In: Riederer, M., Müller, C. (eds), Biology of the Plant Cuticle. Blackwell, London, UK, pp. 145–181.
Kamigaki, A., Kondo, M., Mano, S., Hayashi, M., Nishimura, M. 2009. Suppression of peroxisome biogenesis factor 10 reduces cuticular wax accumulation by disrupting the ER network in Arabidopsis thaliana. Plant Cell Physiol. 50:2034–2046.
Kim, K.S., Park, S.H., Kim, D.K., Jenks, M.A. 2007. Influence of water deficit on leaf cuticular waxes of soybean (Glycine max (L.) Merr.). Int. Plant. Sci. 168:307–316.
Komatsuda, T., Nakamura, I., Takaiwa, F., Oka, S. 1998. Development of STS markers closely linked to the vrs1 locus in barley, Hordeum vulgare. Genome 41:680–685.
Kosma, D.K., Bourdenx, B., Bernard, A., Parsons, E.P., Lü, S., Joubès, J., Jenks, M.A. 2009. The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol. 151:1918–1929.
Larsson, S., Svenningsson, M. 1986. Cuticular transpiration and epicuticular lipids of primary leaves of barley (Hordeum vulgare). Physiol. Plant. 68:13–19.
Lee, S.B., Go, Y.S., Bae, H.J., Park, J.H., Cho, S.H., Cho, H.J., Lee, D.S., Park, O.K., Hwang, I., Suh, M.C. 2009. Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol. 150:42–54.
Li-Beisson, Y., Pollard, M., Sauveplane, V., Pinot, F., Ohlrogge, J., Beisson, F. 2009. Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc. Natl. Acad. Sci. USA 106:22008–22013.
Li, C., Wang, A., Ma, X., Nevo, E., Chen, G. 2010. Consensus maps of cloned plant cuticle genes. Sci. Cold Arid Regi. 2:465–476.
Lü, S., Zhao, H., Parsons, E.P., Xu, C., Kosma, D.K., Xu, X., Chao, D., Lohrey, G., Bangarusamy, D.K., Wang, G., Bressan, R.A., Jenks, M.A. 2011. The glossyhead1 (gsd1) allele of ACC1 reveals a principal role for multi-domain ACETYL-COA CARBOXYLASE in the biosynthesis of cuticular waxes by Arabidopsis thaliana. Plant Physiol. 157:1079–1092.
Lundqvist, U., von Wettstein-Knowles, P., von Wettstein, D. 1968. Induction of eceriferum mutants in barley by ionizing radiations and chemical mutagens. II. Hereditas 59:473–504.
Lundqvist, U., Lundqvist, A. 1988. Mutagen specificity in barley for 1580 eceriferum mutants localized to 79 loci. Hereditas 108:1–12.
Lundqvist, V., von Wettstein, D. 1988. Stock list for eceriferum mutants. Barley Genet. Newsl. 15:89–93.
Millar, A.A., Clemens, S., Zachgo, S., Giblin, E.M., Taylor, D.C., Kunst, L. 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.
Moose, S.P., Sisco, P.H. 1996. Glossy15, an APETALA2 -like gene from maize that regulates leaf epidermal cell identity. Genes Dev. 10:3018–3027.
Nawrath, C. 2002. The biopolymers cutin and suberin. In: Somerville, C.R., Meyerowitz, E.M. (eds), The Arabidopsis Book. American Society of Plant Biologists, Rockville, MD, USA. Doi:https://doi.org/10.1199/tab.0021, https://doi.org/www.aspb.org/publications/arabidopsis/
Nawrath, C. 2006. Unraveling the complex network of cuticular structure and function. Curr. Opin. Plant Biol. 9:281–287.
Panikashvili, D., Shi, J.X., Schreiber, L., Aharoni, A. 2011. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 90:113–124.
Park, J.J., Jin, P., Yoon, J., Yang, J.I., Jeong, H.J., Ranathunge, K., Schreiber, L., Franke, R., Lee, I.J., An, G. 2010. Mutation in Wilted Dwarf and lethal 1 (WDL1) cause abnornal cuticle formation and rapid water loss in rice. Plant Mol. Biol. 74:91–103.
Pruitt, R.E., Vielle-Calzada, J.P., Ploense, S.E., Grossniklaus, U., Lolle, S.J. 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.
Richardson, A., Boscari, A., Schreiber, L., Kerstiens, G., Jarvis, M., Herzyk, P., Fricke, W. 2007. Cloning and expression analysis of candidate genes involved in wax deposition along the growing barley (Hordeum vulgare) leaf. Planta 226:1459–1473.
Riederer, M., Schreiber, L. 2001. Protecting against water loss: analysis of the barrier properties of plant cuticles. J. Exp. Bot. 52:2023–2032.
Ristic, Z., Jenks, M.A. 2002. Leaf cuticle and water loss in maize lines differing in dehydration avoidance. J. Plant Physiol. 159:645–651.
Rozen, S., Skaletsky, H. 2000. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132:365–386.
Sánchez, F.J., Manzanares, M., de Andrés, E.F., Tenorio, J.L., Ayerbe, L. 2001. Residual transpiration rate, epicuticular wax load and leaf colour of pea plants in drought conditions. Influence on harvest index and canopy temperature. Eur. J. Agron. 15:57–70.
Shepherd, T., Griffiths, W.D. 2006. The effects of stress on plant cuticular waxes. New Phytol. 171:469–499.
Stein, N., Prasad, M., Scholz, U., Thiel, T., Zhang, H., Wolf, M., Kota, R., Varshney, R.K., Perovic, D., Grosse, I., Graner, A. 2007. A 1,000-loci transcript map of the barley genome: New anchoring points for integrative grass genomics. Theor. Appl. Genet. 114:823–839.
Sturaro, M., Hartings, H., Schmelzer, E., Velasco, R., Salamini, F., Motto, M. 2005. Cloning and characterization of GLOSSY1, a maize gene involved in cuticle membrane and wax production. Plant Physiol. 138:478–489.
Tacke, E., Korfhage, C., Michel, D., Maddaloni, M., Motto, M., Lanzini, S., Salamini, F., Döring, H.P. 1995. Transposon tagging of the maize Glossy2 locus with the transposable element En/Spm. Plant J. 8:907–917.
Trijatmiko, K.R., van Arkel, G., Pereira, A. 2005. Expression of the Arabidopsis SHINE gene in rice for drought resistance. In: Trijatmiko, K.R. (ed.), Comparative analysis of drought resistance genes in Arabidopsis and rice. PhD Thesis, Wageningen University, The Netherlands, pp. 87–101.
Voisin, D., Nawrath, C., Kurdyukov, S., Franke, R.B., Reina-Pinto, J.J., Efremova, N., Will, I., Schreiber, L., Yephremov, A. 2009. Dissection of the complex phenotype in cuticular mutants of Arabidopsis reveals a role of SERRATE as a mediator. PLoS Genet. 5:e1000703
von Wettstein-Knowles, P. 1972. Genetic control of b-diketone and hydro-b-diketone synthesis in epicuticular waxes of barley. Planta 106:113–130.
von Wettstein-Knowles, P. 1992. Molecular genetics of the lipid synthesis in barley. In: Munck, L., Kirkegaard, K., Jensen, B. (eds), Barley Genetics VI, Vol. 2. Munksgaard International Publishers, Copenhagen, Denmark, pp. 753–771.
Voorrips, R.E. 2002. MapChart: Software for the graphical presentation of linkage maps and QTLs. J. Hered. 93:77–78.
Wang, Y., Wan, L., Zhang, L., Zhang, Z., Zhang, H., Quan, R., Zhou, S., Huang, R. 2012. An ethylene response factor OsWR1 responsive to drought stress transcriptionally activates wax synthesis related genes and increases wax production in rice. Plant Mol. Biol. 8:275–288.
Wu, R., Li, S., He, S., Wassmann, F., Yu, C., Qin, G., Schreiber, L., Qu, L.J., Gu, H. 2010. 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 74:91–103.
Xia, Y., Nikolau, B.J., Schnable, P.S. 1996. Cloning and characterization of CER2, an Arabidopsis gene that affects cuticular wax accumulation. Plant Cell 8:1291–1304.
Xu, X., Dietrich, C.R., Delledonne, M., Xia, Y., Wen, T.J., Robertson, D.S., Nikolau, B.J., Schnable, P.S. 1997. Sequence analysis of the cloned glossy8 gene of maize suggests that it may code for a beta-ketoacyl reductase required for the biosynthesis of cuticular waxes. Plant Physiol. 115:501–510.
Yang, J., Isabel Ordiz, M., Jaworski, J.G., Beachy, R.N. 2011. Induced accumulation of cuticular waxes enhances drought tolerance in Arabidopsis by changes in development of stomata. Plant Physiol. Biochem. 49:1448–1455.
Yu, D., Ranathunge, K., Huang, H., Pei, Z., Franke, R., Schreiber, L., He, C. 2008. Wax crystal-sparse leaf1 encodes a, b-ketoacyl CoA synthase involved in biosynthesis of cuticular waxes on rice leaf. Planta 228:675–685.
Zhang, J.Y., Broeckling, C.D., Blancaflor, E.B., Sledge, M.K., Sumner, L.W., Wang, Z.Y. 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.
Zhang, J., Broeckling, C.D., Sumner, L.W., Wang, Z. 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.
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Li, C., Ma, X., Wang, A. et al. Genetic Mapping of Cuticle-Associated Genes in Barley. CEREAL RESEARCH COMMUNICATIONS 41, 23–34 (2013). https://doi.org/10.1556/CRC.2012.0020
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DOI: https://doi.org/10.1556/CRC.2012.0020