Abstract
Key message
The semidominant EMS-induced mutant w5 affects epicuticular wax deposition and mapped to an approximately 194-kb region on chromosome 7DL.
Abstract
Epicuticular wax is responsible for the glaucous appearance of plants and protects against many biotic and abiotic stresses. In wheat (Triticum aestivum L.), β-diketone is a major component of epicuticular wax in adult plants and contributes to the glaucousness of the aerial organs. In the present study, we identified an ethyl methanesulfonate-induced epicuticular wax-deficient mutant from the elite wheat cultivar Jimai22. Compared to wild-type Jimai22, the mutant lacked β-diketone and failed to form the glaucous coating on all aerial organs. The mutant also had significantly increased in cuticle permeability, based on water loss and chlorophyll efflux. Genetic analysis indicated that the mutant phenotype is controlled by a single, semidominant gene on the long arm of chromosome 7D, which was not allelic to the known wax gene loci W1–W4, and was therefore designated W5. W5 was finely mapped to an ~ 194-kb region (flanked by the molecular markers SSR2 and STARP11) that harbored four annotated genes according to the reference genome of Chinese Spring (RefSeq v1.0). Collectively, these data will broaden the knowledge of the genetic basis underlying epicuticular wax deposition in wheat.
Similar content being viewed by others
References
Adamski NM, Bush MS, Simmonds J, Turner AS, Mugford SG, Jones A, Findlay K, Pedentchouk N, von Wettstein-Knowles P, Uauy C (2013) The inhibitor of wax 1 locus (Iw1) prevents formation of beta- and OH-beta-diketones in wheat cuticular waxes and maps to a sub-cM interval on chromosome arm 2BS. Plant J Cell Mol Biol 74:989–1002. https://doi.org/10.1111/tpj.12185
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. https://doi.org/10.1105/tpc.104.022897
Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292. https://doi.org/10.1146/annurev.ecolsys.29.1.263
Bennett D, Izanloo A, Edwards J, Kuchel H, Chalmers K, Tester M, Reynolds M, Schnurbusch T, Langridge P (2012) Identification of novel quantitative trait loci for days to ear emergence and flag leaf glaucousness in a bread wheat (Triticum aestivum L.) population adapted to southern Australian conditions. Theor Appl Genet 124:697–711. https://doi.org/10.1007/s00122-011-1740-3
Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52:110–129. https://doi.org/10.1016/j.plipres.2012.10.002
Bessire M, Chassot C, Jacquat A-C, Humphry M, Borel S, Petétot JM-C, Métraux J-P, Nawrath C (2007) A permeable cuticle in Arabidopsis leads to a strong resistance to Botrytis cinerea. EMBO J 26:2158–2168. https://doi.org/10.1038/sj.emboj.7601658
Bi H, Luang S, Li Y, Bazanova N, Morran S, Song Z, Perera MA, Hrmova M, Borisjuk N, Lopato S (2016) Identification and characterization of wheat drought-responsive MYB transcription factors involved in the regulation of cuticle biosynthesis. J Exp Bot 67:5363–5380. https://doi.org/10.1093/jxb/erw298
Bi H, Luang S, Li Y, Bazanova N, Borisjuk N, Hrmova M, Lopato S (2017) Wheat drought-responsive WXPL transcription factors regulate cuticle biosynthesis genes. Plant Mol Biol 94:15–32. https://doi.org/10.1007/s11103-017-0585-9
Börner A, Schumann E, Fürste A, Cöster H, Leithold B, Röder M, Weber W (2002) Mapping of quantitative trait loci determining agronomic important characters in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 105:921–936. https://doi.org/10.1007/s00122-002-0994-1
Chai G, Li C, Xu F, Li Y, Shi X, Wang Y, Wang Z (2018) Three endoplasmic reticulum-associated fatty acyl-coenzyme a reductases were involved in the production of primary alcohols in hexaploid wheat (Triticum aestivum L.). BMC Plant Biol 18:41. https://doi.org/10.1186/s12870-018-1256-y
Chai L, Chen Z, Bian R, Zhai H, Cheng X, Peng H, Yao Y, Hu Z, Xin M, Guo W, Sun Q, Zhao A, Ni Z (2019) Dissection of two quantitative trait loci with pleiotropic effects on plant height and spike length linked in coupling phase on the short arm of chromosome 2D of common wheat (Triticum aestivum L.). Theor Appl Genet 132:1815–1831. https://doi.org/10.1007/s00122-019-03318-z
Clavijo BJ, Venturini L, Schudoma C, Accinelli GG, Kaithakottil G, Wright J, Borrill P, Kettleborough G, Heavens D, Chapman H, Lipscombe J, Barker T, Lu F-H, McKenzie N, Raats D, Ramirez-Gonzalez RH, Coince A, Peel N, Percival-Alwyn L, Duncan O, Trösch J, Yu G, Bolser DM, Namaati G, Kerhornou A, Spannagl M, Gundlach H, Haberer G, Davey RP, Fosker C, Palma FD, Phillips AL, Millar AH, Kersey PJ, Uauy C, Krasileva KV, Swarbreck D, Bevan MW, Clark MD (2017) An improved assembly and annotation of the allohexaploid wheat genome identifies complete families of agronomic genes and provides genomic evidence for chromosomal translocations. Genome Res 27:885–896. https://doi.org/10.1101/gr.217117.116
Devi KD, Punyarani K, Singh NS, Devi HS (2013) An efficient protocol for total DNA extraction from the members of order Zingiberales-suitable for diverse PCR based downstream applications. Springerplus 2:669. https://doi.org/10.1186/2193-1801-2-669
Dubcovsky J, Echaide M, Giancola S, Rousset M, Luo MC, Joppa LR, Dvorak J (1997) Seed-storage-protein loci in RFLP maps of diploid, tetraploid, and hexaploid wheat. Theor Appl Genet 95:1169–1180. https://doi.org/10.1007/s001220050678
Fay JC, McCullough HL, Sniegowski PD, Eisen MB (2004) Population genetic variation in gene expression is associated with phenotypic variation in Saccharomyces cerevisiae. Genome Biol 5:R26. https://doi.org/10.1186/gb-2004-5-4-r26
Gadaleta A, Giancaspro A, Giove SL, Zacheo S, Mangini G, Simeone R, Signorile A, Blanco A (2009) Genetic and physical mapping of new EST-derived SSRs on the A and B genome chromosomes of wheat. Theor Appl Genet 118:1015. https://doi.org/10.1007/s00122-008-0958-1
Gao L, Yang G, Li Y, Fan N, Li H, Zhang M, Xu R, Zhang M, Zhao A, Ni Z, Zhang Y (2019) Fine mapping and candidate gene analysis of a QTL associated with leaf rolling index on chromosome 4 of maize (Zea mays L.). Theor Appl Genet 132:3047–3062. https://doi.org/10.1007/s00122-019-03405-1
Gaume L, Perret P, Gorb E, Gorb S, Labat JJ, Rowe N (2004) How do plant waxes cause flies to slide? Experimental tests of wax-based trapping mechanisms in three pitfall carnivorous plants. Arthropod Struct Dev 33:103–111. https://doi.org/10.1016/j.asd.2003.11.005
Guo J, Xu W, Yu X, Shen H, Li H, Cheng D, Liu A, Liu J, Liu C, Zhao S, Song J (2016) Cuticular wax accumulation is associated with drought tolerance in wheat near-isogenic lines. Front Plant Sci 7:1809. https://doi.org/10.3389/fpls.2016.01809
Hen-Avivi S, Savin O, Racovita RC, Lee WS, Adamski NM, Malitsky S, Almekias-Siegl E, Levy M, Vautrin S, Berges H, Friedlander G, Kartvelishvily E, Ben-Zvi G, Alkan N, Uauy C, Kanyuka K, Jetter R, Distelfeld A, Aharoni A (2016) A metabolic gene cluster in the wheat W1 and the barley Cer-cqu loci determines beta-diketone biosynthesis and glaucousness. Plant Cell 28:1440–1460. https://doi.org/10.1105/tpc.16.00197
Huang D, Feurtado JA, Smith MA, Flatman LK, Koh C, Cutler AJ (2017) Long noncoding miRNA gene represses wheat β-diketone waxes. Proc Natl Acad Sci USA 114:E3149–E3158. https://doi.org/10.1073/pnas.1617483114
International Wheat Genome Sequencing C, investigators IRp, Appels R, Eversole K, Feuillet C (2018) Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science 361:eaar7191. https://doi.org/10.1126/science.aar7191
Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129:440–450. https://doi.org/10.1104/pp.003533
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39. https://doi.org/10.1111/j.1469-8137.2010.03514.x
Jetter R, Riederer M (2016) Localization of the transpiration barrier in the epi- and intracuticular waxes of eight plant species: water transport resistances are associated with fatty acyl rather than alicyclic components. Plant Physiol 170:921–934. https://doi.org/10.1104/pp.15.01699
Kerstiens G (1996) Cuticular water permeability and its physiological significance. J Exp Bot 47:1813–1832. https://doi.org/10.1093/jxb/47.12.1813
Koch K, Barthlott W, Koch S, Hommes A, Wandelt K, Mamdouh W, De-Feyter S, Broekmann P (2006) Structural analysis of wheat wax (Triticum aestivum, c.v. ‘Naturastar’ L.): from the molecular level to three dimensional crystals. Planta 223:258–270. https://doi.org/10.1007/s00425-005-0081-3
Kosambi DD (1944) The geometric method in mathematical statistics. Am Math Mon. https://doi.org/10.1007/978-81-322-3676-4_17
Kurdyukov S, Faust A, Nawrath C, Bar S, Voisin D, Efremova N, Franke R, Schreiber L, Saedler H, Metraux JP, Yephremov A (2006) The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 18:321–339. https://doi.org/10.1105/tpc.105.036079
Lettice LA, Heaney SJH, Purdie LA, Li L, de Beer P, Oostra BA, Goode D, Elgar G, Hill RE, de Graaff E (2003) A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12:1725–1735. https://doi.org/10.1093/hmg/ddg180
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li C-l, Li T-t, Liu T-x, Sun Z-p, Bai G-h, Jin F, Wang Y, Wang Z-h (2017) Identification of a major QTL for flag leaf glaucousness using a high-density SNP marker genetic map in hexaploid wheat. J Integr Agric 16:445–453. https://doi.org/10.1016/s2095-3119(16)61339-4
Li T, Sun Y, Liu T, Wu H, An P, Shui Z, Wang J, Zhu Y, Li C, Wang Y, Jetter R, Wang Z (2019) TaCER1-1A is involved in cuticular wax alkane biosynthesis in hexaploid wheat and responds to plant abiotic stresses. Plant, Cell Environ 42:3077–3091. https://doi.org/10.1111/pce.13614
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. https://doi.org/10.1006/meth.2001
Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter W-D, Pruitt RE (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. https://doi.org/10.1006/dbio.1997.8671
Long YM, Chao WS, Ma GJ, Xu SS, Qi LL (2017) An innovative SNP genotyping method adapting to multiple platforms and throughputs. Theor Appl Genet 130:597–607. https://doi.org/10.1007/s00122-016-2838-4
Marklund SCR, Marklund L, Sandberg K, Andersson L (1995) Extensive mtDNA diversity in horses revealed by PCR-SSCP analysis. Anim Genet 26:193–196. https://doi.org/10.1111/j.1365-2052.1995.tb03162.x
Mason RE, Mondal S, Beecher FW, Pacheco A, Jampala B, Ibrahim AMH, Hays DB (2010) QTL associated with heat susceptibility index in wheat (Triticum aestivum L.) under short-term reproductive stage heat stress. Euphytica 174:423–436. https://doi.org/10.1007/s10681-010-0151-x
Mikkelsen JD (1978) The effects of inhibitors on the biosynthesis of the long chain lipids with even carbon numbers in barley spike epicuticular wax. Carlsberg Res Commun 43:15–35. https://doi.org/10.1007/BF02906546
Mishra A, Singh A, Sharma M, Kumar P, Roy J (2016) Development of EMS-induced mutation population for amylose and resistant starch variation in bread wheat (Triticum aestivum) and identification of candidate genes responsible for amylose variation. BMC Plant Biol 16:217. https://doi.org/10.1186/s12870-016-0896-z
Müller C (2006) Plant-insect interactions on cuticular surfaces. In: Riederer M, Müller C (eds) Annual plant reviews, Volume 23: Biology of the plant cuticle. https://doi.org/10.1002/9780470988718.ch13
Mondal S, Mason RE, Huggins T, Hays DB (2015) QTL on wheat (Triticum aestivum L.) chromosomes 1B, 3D and 5A are associated with constitutive production of leaf cuticular wax and may contribute to lower leaf temperatures under heat stress. Euphytica 201:123–130. https://doi.org/10.1007/s10681-014-1193-2
Moore G, Devos KM, Wang Z, Gale MD (1995) Cereal genome evolution: grasses, line up and form a circle. Curr Biol 5:737–739. https://doi.org/10.1016/S0960-9822(95)00148-5
Neinhuis C, Koch K, Barthlott W (2001) Movement and regeneration of epicuticular waxes through plant cuticles. Planta 213:427–434. https://doi.org/10.1007/s004250100530
Nishijima R, Tanaka C, Yoshida K, Takumi S (2018) Genetic mapping of a novel recessive allele for non-glaucousness in wild diploid wheat Aegilops tauschii: implications for the evolution of common wheat. Genetica 146:249–254. https://doi.org/10.1007/s10709-018-0012-4
Owen R, Huanquan Z, Hepworth SR, Patricia L, Reinhard J, Ljerka K (2006) CER4 encodes an alcohol-forming fatty acyl-coenzyme A reductase involved in cuticular wax production in Arabidopsis. Plant Physiol 142:866–877. https://doi.org/10.2307/20205980
Peters JL, Cnudde F, Gerats T (2003) Forward genetics and map-based cloning approaches. Trends Plant Sci 8:484–491. https://doi.org/10.1016/j.tplants.2003.09.002
Reina-Pinto JJ, Yephremov A (2009) Surface lipids and plant defenses. Plant Physiol Biochem 47:540–549. https://doi.org/10.1016/j.plaphy.2009.01.004
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707. https://doi.org/10.1146/annurev.arplant.59.103006.093219
Shepherd T, Wynne Griffiths D (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499. https://doi.org/10.1111/j.1469-8137.2006.01826.x
Steinmuller D, Tevini M (1985) Action of ultraviolet radiation (UV-B) upon cuticular waxes in some crop plants. Planta 164:557–564. https://doi.org/10.1007/BF00395975
Tsunewaki K (1966) Comparative gene analysis of common wheat and its ancestral species. II. Waxiness, growth habit and awnedness. J Genet Mol Biol 19:175–229. https://doi.org/10.30047/JGMB.200912.0003
Tsunewaki K, Ebana K (1999) Production of near-isogenic lines of common wheat for glaucousness and genetic basis of this trait clarified by their use. Genes Genet Syst 74:33–41. https://doi.org/10.1266/ggs.74.33
Tulloch AP (1973) Composition of leaf surface waxes of Triticum species: variation with age and tissue. Phytochemistry 12:2225–2232. https://doi.org/10.1016/0031-9422(73)85124-6
Van Oojien JW et al (2006) JoinMap 4, software for the calculation of genetic linkage maps in experimental populations. Kyazma B.V, Wageningen
von Wettstein-Knowles P (1979) Genetics and biosynthesis of plant epicuticular waxes. In: Appelqvist LÅ, Liljenberg C (eds) Advances in the biochemistry and physiology of plant lipids. Elsevier/North Holland Biomedical Press. https://doi.org/10.1042/bst0080236
von Wettstein-Knowles P, Søgaard B (1980) The cer-cqu region in barley: gene cluster or multifunctional gene. Carlsberg Res Commun 45:125–141. https://doi.org/10.1007/bf02906514
Wang A, Xia Q, Xie W, Dumonceaux T, Zou J, Datla R, Selvaraj G (2002) Male gametophyte development in bread wheat (Triticum aestivum L.): molecular, cellular, and biochemical analyses of a sporophytic contribution to pollen wall ontogeny. Plant J Cell Mol Biol 30:613–623. https://doi.org/10.1046/j.1365-313x.2002.01313.x
Wang J, Li W, Wang W (2014) Fine mapping and metabolic and physiological characterization of the glume glaucousness inhibitor locus Iw3 derived from wild wheat. Theor Appl Genet 127:831–841. https://doi.org/10.1007/s00122-014-2260-8
Wang Y, Wang J, Chai G, Li C, Hu Y, Chen X, Wang Z (2015a) Developmental changes in composition and morphology of cuticular waxes on leaves and spikes of glossy and glaucous wheat (Triticum aestivum L.). PLoS ONE 10:e0141239. https://doi.org/10.1371/journal.pone.0141239
Wang Y, Wang M, Sun Y, Hegebarth D, Li T, Jetter R, Wang Z (2015b) Molecular characterization of TaFAR1 involved in primary alcohol biosynthesis of cuticular wax in hexaploid wheat. Plant Cell Physiol 56:1944–1961. https://doi.org/10.1093/pcp/pcv112
Wang Y, Wang M, Sun Y, Wang Y, Li T, Chai G, Jiang W, Shan L, Li C, Xiao E, Wang Z (2015c) FAR5, a fatty acyl-coenzyme A reductase, is involved in primary alcohol biosynthesis of the leaf blade cuticular wax in wheat (Triticum aestivum L.). J Exp Bot 66:1165–1178. https://doi.org/10.1093/jxb/eru457
Wang M, Wang Y, Wu H, Xu J, Li T, Hegebarth D, Jetter R, Chen L, Wang Z (2016) Three TaFAR genes function in the biosynthesis of primary alcohols and the response to abiotic stresses in Triticum aestivum. Sci Rep 6:25008. https://doi.org/10.1038/srep25008
Wang T, Xing J, Liu X, Yao Y, Hu Z, Peng H, Xin M, Zhou DX, Zhang Y, Ni Z (2018) GCN5 contributes to stem cuticular wax biosynthesis by histone acetylation of CER3 in Arabidopsis. J Exp Bot 69:2911–2922. https://doi.org/10.1093/jxb/ery077
Wettstein-Knowles PV (2016) Plant waxes. Wiley, Hoboken
Wu H, Qin J, Han J, Zhao X, Ouyang S, Liang Y, Zhang D, Wang Z, Wu Q, Xie J, Cui Y, Peng H, Sun Q, Liu Z (2013) Comparative high-resolution mapping of the wax inhibitors Iw1 and Iw2 in hexaploid wheat. PLoS ONE 8:e84691. https://doi.org/10.1371/journal.pone.0084691
Zhang Z, Wang W, Li W (2013) Genetic interactions underlying the biosynthesis and inhibition of beta-diketones in wheat and their impact on glaucousness and cuticle permeability. PLoS ONE 8:e54129. https://doi.org/10.1371/journal.pone.0054129
Zhang Z, Wei W, Zhu H, Challa GS, Bi C, Trick HN, Li W (2015) W3 is a new wax locus that is essential for biosynthesis of beta-diketone, development of glaucousness, and reduction of cuticle permeability in common wheat. PLoS ONE 10:e0140524. https://doi.org/10.1371/journal.pone.0140524
Zhou Q, Li C, Mishina K, Zhao J, Zhang J, Duan R, Ma X, Wang A, Meng Q, Komatsuda T, Chen G (2017) Characterization and genetic mapping of the β-diketone deficient eceriferum-b barley mutant. Theor Appl Genet 130:1169–1178. https://doi.org/10.1007/s00122-017-2877-5
Acknowledgements
The authors would like to thank Prof. Jianxin Shi (Shanghai Jiao Tong University) for the GC-FID and GC-MS analyses in his laboratory. This work was financially supported by the National Natural Science Foundation of China (31991214 and 91935304) and the National Key Research and Development Program of China (Grant No. 2017YFD0101004).
Author information
Authors and Affiliations
Contributions
ZN conceived the project. The w5 mutant was provided by MZ; LL and ZQ carried out experiments; LC and ZC participated in field trials; QS, HP, YY, ZH, MX, MY, WG, and TW assisted in revising the manuscript; LL analyzed the experimental results; and LL and ZN wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Albrecht E. Melchinger.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
122_2020_3543_MOESM1_ESM.tif
Fig. S1. Phenotypic comparison of Jing411, an F1 plant, and the w5 mutant. a The whole plant appearance of Jing411 (left), an F1 plant (middle), and the w5 mutant (right) at the heading period. Scale bar 10 cm; b Enlarged view of flag leaves, leaf sheaths and spikes of Jing411 (left), an F1 plant (middle), and the w5 mutant (right). Scale bar 5 cm. (TIFF 1410 kb)
122_2020_3543_MOESM2_ESM.tif
Fig. S2. Number of SNP markers with different polymorphisms between the glaucous pools and non-glaucous pools of the F2 population derived from the cross between the w5 and Jing411. a Distribution of the candidate SNPs per chromosome; b The physical positions of the SNPs on chromosome 7D according to the IWGSC RefSeq v1.0. (TIFF 66 kb)
122_2020_3543_MOESM3_ESM.tif
Fig. S3. Relative expression levels of the three high-confidence genes in the 194.4-kb region in the flag leaf sheath of Jimai22 and the w5 mutant, with TaActin used as the endogenous control. The bars represent standard deviations of the mean levels calculated from three biological replicates. Asterisks indicate that the difference is significant at *P < 0.05. (TIFF 57 kb)
122_2020_3543_MOESM4_ESM.tif
Fig. S4. Chromosome distribution of wax-related genes in wheat. The red font represents the gene located in this study. (TIFF 403 kb)
122_2020_3543_MOESM5_ESM.tif
Fig. S5. Sequence comparison of different IWGSC RefSeq versions. a IWGSC RefSeq v.1.0; b IWGSC RefSeq v.2.0. Scale bar 10 kb. Black triangles represent sequences gaps. (TIFF 72 kb)
Rights and permissions
About this article
Cite this article
Li, L., Qi, Z., Chai, L. et al. The semidominant mutation w5 impairs epicuticular wax deposition in common wheat (Triticum aestivum L.). Theor Appl Genet 133, 1213–1225 (2020). https://doi.org/10.1007/s00122-020-03543-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-020-03543-x