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Fine mapping and metabolic and physiological characterization of the glume glaucousness inhibitor locus Iw3 derived from wild wheat

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This research provided the first view of metabolic and physiological effect of a tissue-specific glaucousness inhibitor in wheat and laid foundation for map-based cloning of the Iw3 locus.

Abstract

Cuticular wax constitutes the outermost layer of plant skin, and its composition greatly impacts plant appearance and plant–environment interaction. Epicuticular wax in the upper part of adult wheat plants can form the glaucousness, which is associated with drought tolerance. In this research, we characterized a glume-specific glaucousness inhibitor, Iw3, by fine mapping, physiological, and molecular approaches. Iw3 inhibits glaucousness formation by altering wax composition. Compared to the wild type, Iw3 eliminated β-diketone, reduced 47 % primary alcohols, but increased aldehyde 400-fold and alkanes fivefold, which led to 30 % reduction of total glume wax load. Loss of the glaucousness increased cuticle permeability, suggesting an important role in drought sensitivity. Genetically, the glaucousness-inhibiting effect by Iw3 is partially dominant in a dosage-dependent manner. We localized the Iw3 locus within a 0.13-cM interval delimited by marker loci Xpsp3000 and XWL3096. Of the 53 wax genes assayed, we detected transcription changes in nine genes by Iw3, downregulation of Cer4-1 and upregulation of other five Cer4 and three KCS homologs. All these results provided initial insights into Iw3-mediated regulation of wax metabolism and paved way for in-depth characterization of the Iw3 locus and the glaucousness-related β-diketone pathway.

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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 74:989–1002

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bernard A, Joubès J (2013) Arabidopsis cuticular waxes: advances in synthesis, export and regulation. Prog Lipid Res 52:110–129

    Article  PubMed  CAS  Google Scholar 

  • Bianchi G (1995) Plant waxes. In: Hamilton RJ (ed) Waxes: chemistry, molecular biology and functions. The Oily Press, Dundee, pp 175–222

    Google Scholar 

  • Bianchi G, Figini ML (1986) Epicuticular waxes of glaucous and nonglaucous durum wheat lines. J Agric Food Chem 34:429–433

    Article  CAS  Google Scholar 

  • Cheesbrough TM, Kolattukudy PE (1984) Alkane biosynthesis by decarbonylation of aldehydes catalyzed by a particulate preparation from Pisum sativum. Proc Natl Acad Sci USA 81:6613–6617

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Devos KM, Bryan GJ, Collins AJ, Stephenson P, Gale MD (1995) Application of two microsatellite sequences in wheat storage proteins as molecular markers. Theor Appl Genet 90:247–252

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Greer S, Wen M, Bird D, Wu X, Samuels L, Kunst L, Jetter R (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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Huang L, Brooks SA, Li W, Fellers JP, Trick HN, Gill BS (2003) Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics 164:655–664

    PubMed Central  PubMed  CAS  Google Scholar 

  • Janda J, Safár J, Kubaláková M, Bartos J, Kovárová P, Suchánková P, Pateyron S, Cíhalíková J, Sourdille P, Simková H, Faivre-Rampant P, Hribová E, Bernard M, Lukaszewski A, Dolezel J, Chalhoub B (2006) Advanced resources for plant genomics: a BAC library specific for the short arm of wheat chromosome 1B. Plant J 47:977–986

    Article  PubMed  CAS  Google Scholar 

  • Jefferson PG, Johnson DA, Asay KH (1989) Epicuticular wax production, water status and leaf temperature in Triticeae range grasses of contrasting visible glaucousness. Can J Plant Sci 69:513–519

    Article  Google Scholar 

  • Johnson DA, Richards RA, Turner NC (1983) Yield, water relations, gas exchange, and surface reflectances of near-isogenic wheat lines differing in glaucousness. Crop Sci 23:318–325

    Article  Google Scholar 

  • Joppa LR, Cantrell RG (1990) Chromosomal location of genes for grain protein content of wild tetraploid wheat. Crop Sci 30:1059–1064

    Article  CAS  Google Scholar 

  • King RW, Pv Wettstein-Knowles (2000) Epicuticular waxes and regulation of ear wetting and pre-harvest sprouting in barley and wheat. Euphytica 112:157–166

    Article  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Kosma DK, Bourdenx B, Bernard A, Parsons EP, Lu S, Joubes J, Jenks MA (2009) The impact of water deficiency on leaf cuticle lipids of Arabidopsis. Plant Physiol 151:1918–1929

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Large EC (1954) Growth stages in cereals illustration of the feekes scale. Plant Pathol 3:128–129

    Article  Google Scholar 

  • Lee SB, Suh MC (2013) Recent advances in cuticular wax biosynthesis and its regulation in Arabidopsis. Mol Plant 6:246–249

    Article  PubMed  CAS  Google Scholar 

  • Li W, Huang L, Gill BS (2008) Recurrent deletions of puroindoline genes at the grain hardness locus in four independent lineages of polyploid wheat. Plant Physiol 146:200–212

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu XM, Fritz AK, Reese JC, Wilde GE, Gill BS, Chen MS (2005) H9, H10, and H11 compose a cluster of Hessian fly-resistance genes in the distal gene-rich region of wheat chromosome 1AS. Theor Appl Genet 110:1473–1480

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Ni Z, Peng H, Song W, Liu Z, Sun Q (2006) Molecular mapping of a dominant non-glaucousness gene from synthetic hexaploid wheat (Triticum aestivum L.). Euphytica 155:71–78

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lolle SJ, Berlyn GP, Engstrom EM, Krolikowski KA, Reiter WD, 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

    Article  PubMed  CAS  Google Scholar 

  • Monneveux P, Reynolds MP, González-Santoyo H, Peña RJ, Mayr L, Zapata F (2004) Relationships between grain yield, flag leaf morphology, carbon isotope discrimination and ash content in irrigated wheat. J Agron Crop Sci 190:395–401

    Article  Google Scholar 

  • Nelson JC, Deynze AE, Sorrells ME, Autrique E, Lu YH, Merlino M, Atkinson M, Leroy P (1995) Molecular mapping of wheat. Homoeologous group 2. Genome 38:516–524

    Article  PubMed  CAS  Google Scholar 

  • Peng J, Korol AB, Fahima T, Röder MS, Ronin YI, Li YC, Nevo E (2000) Molecular genetic maps in wild emmer wheat, Triticum dicoccoides: genome-wide coverage, massive negative interference, and putative quasi-linkage. Genome Res 10:1509–1531

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pennisi E (2008) Plant genetics. The blue revolution, drop by drop, gene by gene. Science 320:171–173

    Article  PubMed  CAS  Google Scholar 

  • Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704

    Article  PubMed  CAS  Google Scholar 

  • Reddy L, Friesen TL, Meinhardt SW, Chao S, Faris JD (2008) Genomic analysis of the Snn1 locus on wheat chromosome arm 1BS and the identification of candidate genes. Plant Genome J 1:55

    Article  CAS  Google Scholar 

  • Richards RA, Rawson HM, Johnson DA (1986) Glaucousness in wheat: its development and effect on water-use efficiency, gas exchange and photosynthetic tissue temperature. Aust J Plant Physiol 13:465–473

    Google Scholar 

  • Röder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023

    PubMed Central  PubMed  Google Scholar 

  • Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Ann Rev Plant Biol 59:683–707

    Article  CAS  Google Scholar 

  • Seo PJ, Park CM (2011) Cuticular wax biosynthesis as a way of inducing drought resistance. Plant Signal Behav 6:1043–1045

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Seo PJ, Lee SB, Suh MC, Park MJ, Go YS, Park CM (2011) The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. Plant cell 23:1138–1152

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shepherd T, Wynne Griffiths D (2006) The effects of stress on plant cuticular waxes. New Phytol 171:469–499

    Article  PubMed  CAS  Google Scholar 

  • Shimazaki K, Doi M, Assmann SM, Kinoshita T (2007) Light regulation of stomatal movement. Ann Rev Plant Biol 58:219–247

    Article  CAS  Google Scholar 

  • Simmonds JR, Fish LJ, Leverington-Waite MA, Wang Y, Howell P, Snape JW (2007) Mapping of a gene (Vir) for a non-glaucous, viridescent phenotype in bread wheat derived from Triticum dicoccoides, and its association with yield variation. Euphytica 159:333–341

    Article  CAS  Google Scholar 

  • Somers DJ, Isaac P, Edwards K (2004) A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor Appl Genet 109:1105–1114

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Tulloch AP (1973) Composition of leaf surface waxes of Triticum species: variation with age and tissue. Phytochem 12:2225–2232

    Article  CAS  Google Scholar 

  • Vioque J, Kolattukudy PE (1997) Resolution and purification of an aldehyde-generating and an alcohol-generating fatty acyl-coa reductase from pea leaves (Pisum sativum L.). Arch Biochem Biophys 340:64–72

    Article  PubMed  CAS  Google Scholar 

  • von Wettstein-Knowles P (1995) Biosynthesis and genetics of waxes. In: Hamilton RJ (ed) Waxes: chemistry, molecular biology and functions. The Oily Press Dundee, UK, pp 91–129

    Google Scholar 

  • von Wettstein-Knowles P (2012) Plant Waxes eLS. Wiley, New York, pp 1–11

    Google Scholar 

  • Qi LL, Echalier B, Chao S, Lazo GR, Butler GE, Anderson OD, Akhunov ED, Dvorak J, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Bermudez-Kandianis CE, Greene RA, Kantety R, LaR CM, Munkvold JD, Sorrells SF, Sorrells ME, Dilbirligi M, Sidhu D, Erayman M, Randhawa HS, Sandhu D, Bondareva SN, Gill KS, Mahmoud AA, Ma X-F, Miftahudin, Gustafson JP, Wennerlind EJ, Nduati V, Gonzalez-Hernandez JL, Anderson JA, Peng JH, Lapitan NLV, Hossain KG, Kalavacharla V, Kianian SF, Pathan MS, Zhang DS, Nguyen HT, Choi D-W, Close TJ, McGuire PE, Qualset CO, Gill BS (2004) A chromosome bin map of 10,000 expressed sequence tag loci and distribution of genes among the three genomes of polyploid wheat. Genetics 168:701–712

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yahiaoui N, Srichumpa P, Dudler R, Keller B (2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J 37:528–538

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Wang W, Li W (2013) Genetic interactions underlying the biosynthesis and inhibition of b-diketones in wheat and their impact on glaucousness and cuticle permeability. PLoS One 8:e54129

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Justin Faris for providing seeds of LDN, LDN-TDIC 1B, and the RSL population. This research is supported by South Dakota Agricultural Experiment Station (Brookings, SD) and South Dakota Wheat Commission (Pierre, SD). JW’s stay in US is supported by a fellowship from the Ministry of Education of the People’s Republic of China.

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The authors declare that they have no conflict of interest.

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Correspondence to Wanlong Li.

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Communicated by I. D. Godwin.

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Supplementary Table 1s PCR primers used for marker genotyping (DOCX 13 kb)

122_2014_2260_MOESM2_ESM.docx

Supplementary Table 2s Transcription fold changes of cuticular wax-related genes in Iw3-NIL in comparison to iw3-NIL (DOCX 14 kb)

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Wang, J., Li, W. & Wang, W. Fine mapping and metabolic and physiological characterization of the glume glaucousness inhibitor locus Iw3 derived from wild wheat. Theor Appl Genet 127, 831–841 (2014). https://doi.org/10.1007/s00122-014-2260-8

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  • DOI: https://doi.org/10.1007/s00122-014-2260-8

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