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Inheritance of the number and thickness of cell layers in barley aleurone tissue (Hordeum vulgare L.): an approach using F2–F3 progeny

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Abstract

The aleurone tissue of cereal grains, nutritionally rich in minerals and vitamins, is an important target for the improvement of cereals. Inheritance of the thickness and the number of cell layers in barley aleurone was studied on the F2–F3 progeny of an Erhard Frederichen × Criolla Negra cross in which the parental lines have three or two aleurone layers, respectively. F3 grain was sampled from each F2 plant and 96.8% of the entire F3 grain population was classified as being either the 2- or 3-layer type. Using microsatellite, single nucleotide polymorphism (SNP) and morphological markers on 190 F2 plants, a linkage map was built. Three quantitative trait loci (QTLs) affecting aleurone traits were revealed on chromosome 5H (max. LOD = 5.83) and chromosome 7H (max. LOD = 4.45) by interval mapping, and on chromosome 2H by marker analysis with an unmapped marker. These QTLs were consistent with genetic sub-models involving either 2-cell type dominance for 7H and 2H, or putative partial dominance for 5H where 2-cell-layer dominance and additivity gave similar LODs. The number of aleurone cell layers and aleurone thickness were strongly correlated and QTL results for these traits were alike. An SNP marker of sal1, an orthologue of the maize multilayer aleurone gene was mapped to the 7HL chromosome arm. However, the 7H QTL did not co-locate with the barley sal1 SNP, suggesting that an additional gene is involved in determining aleurone traits. These new mapping data allow comparisons to be made with related studies.

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References

  • Antoine C, Lullien-Pellerin V, Abecassis J, Rouau X (2002) Nutritional interest of the wheat seed aleurone layer. Sci Aliments 22:545–556

    Article  CAS  Google Scholar 

  • Becraft PW, Stinard PS, McCarty D (1996) Crinkly4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409

    Article  PubMed  CAS  Google Scholar 

  • Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129:5217–5225

    PubMed  CAS  Google Scholar 

  • Bertoia LM, Magoja JL (1985) Perennial teosinte-Gaspe hybrids: preliminary results on inheritance of pericarp and aleurone layer thickness. Maize Genet Coop News Lett 59:68–69

    Google Scholar 

  • Bonnett OT (1961) Morphology and development. In: Coffman FA (ed) Oats and oat improvement. American Association of Agronomy, Madison, pp 41–74

    Google Scholar 

  • Bosnes M, Harris E, Aigeltinger L, Olsen OA (1987) Morphology and ultrastructure of 11 shrunken endosperm mutants. Theor Appl Genet 74:177–187

    Article  Google Scholar 

  • Bosnes M, Weideman F, Olsen OA (1992) Endosperm differentiation in barley wild-type and sex mutants. Plant J 2:661–674

    Google Scholar 

  • Brown RC, Lemmon BE, Olsen OA (1994) Endosperm development in barley: microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252

    Article  PubMed  Google Scholar 

  • Chanliaud E, Balfourier F, Oury FX, Charmet G, Beckert M, Duperrier B, Peyron S, Abecassis J, Leenhardt F, Remesy C, Messager A (2005) An integrated approach to improve bread nutritional quality. In: Cauvain SP, Salmon SS, Young LS (eds) Using cereal science and technology for the benefit of consumers. Proceedings of 12th International ICC Cereal and Bread Congress, Harrogate, pp 371–375

  • Cheung WY, Hubert N, Landry BS (1993) A simple and rapid DNA microextraction method for plant, animal, and insect suitable for RAPD and other PCR analyses. PCR Methods Appl 3:69–70

    PubMed  CAS  Google Scholar 

  • Chung MC, Wu HK (1983) The development of rice caryopsis. Natl Sci Counc Mon 11:959–976

    Google Scholar 

  • Consonni G, Gavazzi G, Dolfini S (2005) Genetic analysis as a tool to investigate molecular mechanisms underlying seed development in maize. Ann Bot 96:353–362

    Article  PubMed  CAS  Google Scholar 

  • de Miranda LT (1980) Inheritance and linkages of multiple aleurone layering. Maize Genet Coop News Lett 54:15–18

    Google Scholar 

  • Del Rosario AR, Briones VP, Vidal AJ, Juliano BO (1968) Composition and endosperm structure of developing and mature rice kernel. Cereal Chem 45:225–235

    Google Scholar 

  • Duangploy S, Zuber MS, Cumbie BG (1976) Inheritance of multiple aleurone layering. Maize Genet Coop News Letter 50:90–91

    Google Scholar 

  • Felker FC, Peterson DM, Nelson OE (1985) Anatomy of immature grains of eight maternal effect shrunken endosperm barley mutants. Am J Bot 72:248–256

    Article  Google Scholar 

  • Franckowiak JD (1997) Revised linkage maps for morphological markers in barley, Hordeum vulgare. Barley Genet Newsl 26:9–21

    Google Scholar 

  • Geisler-Lee J, Gallie DR (2005) Aleurone cell identity is suppressed following connation in maize kernels. Plant Physiol 139:204–212

    Article  PubMed  CAS  Google Scholar 

  • Gruis DF, Guo H, Selinger D, Tian Q, Olsen OA (2006) Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize. Plant Physiol 141:898–909

    Article  PubMed  CAS  Google Scholar 

  • Harz CO (1885)-Landwirtschaftliche Samenkunde. P. Parey, Berlin 1362 p

  • Karakousis A, Gustafson JP, Chalmers KJ, Barr AR, Landgridge P (2003) A consensus map of barley integrating SSR, RFLP and AFLP markers. Aust J Agric Res 54:1173–1185

    Article  CAS  Google Scholar 

  • Kessler S, Seiki S, Sinha N (2002) Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position. Development 129:1859–1869

    PubMed  CAS  Google Scholar 

  • Korol A, Ronin Y, Kirzhner V (1996) Linkage between loci of quantitative traits and marker loci. Resolution power of three statistical approaches in single marker analysis. Biometrics 52:426–441

    Article  PubMed  CAS  Google Scholar 

  • Lander E, Green P (1987) Construction of multilocus genetic maps in humans. Proc Nat Acad Sci USA 84:2363–2367

    Article  PubMed  CAS  Google Scholar 

  • Li JZ, Sjakste TG, Röder MS, Ganal MW (2003) Development and genetic mapping of 127 new microsatellite markers in barley. Theor.Appl.Genet 107:1021–1027

    Article  PubMed  CAS  Google Scholar 

  • Lid SE, Krekling RH, Meeley RB, Ranch J, Opsahl-Ferstad HG, Olsen OA (2004) The maize disorganized aleurone layer1 and 2 (dil1, dil2) mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378

    Article  PubMed  CAS  Google Scholar 

  • Michalek W, Weschke W, Pleisner KP, Graner A (2002) EST analysis in barley defines a unigene set comprising 4000 genes. Theor Appl Genet 104:97–103

    Article  PubMed  Google Scholar 

  • Nelson OE, Chang MT (1974) Effect of multiple aleurone layers on the protein and aminoacid content of maize endosperm. Crop Sci 14:374–380

    Article  CAS  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:214–227

    Article  Google Scholar 

  • Pillen K, Binder A, Kreuzkam B, Ramsay L, Vaugh R, Förster J, Léon J (2000) Mapping new EMBL-derived barley microsatellites and their use in differentiating German barley cultivars. Theor Appl Genet 101:652–660

    Article  CAS  Google Scholar 

  • Ramsay L, Macaulay M, degli Ivanissevich S, MacLean K, Cardle L, Fuller J, Edwards KJ, Tuvesson S, Morgante M, Massari A, Maestri E, Marmiroli M, Sjakste T, Ganal M, Powell W, Waugh R (2000) A simple sequence repeat-based linkage map of barley. Genetics 156:1997–2005

    PubMed  CAS  Google Scholar 

  • Ravel C, Praud S, Murigneux A, Canaguier A, Sapet F, Samson D, Balfourier F, Dufour F, Chalhoub B, Brunel D, Beckert M, Charmet G (2006) Single-Nucleotide Polymorphisms (SNPs) frequency in a set of selected lines of bread wheat (Triticum aestivum L.). Genome 49:1131–1139

    Article  PubMed  CAS  Google Scholar 

  • Rychlik W, Rhoads RE (1989) A computer program for choosing optimal oligonucleotides for filter hybridization, sequencing and in vitro amplification of DNA. Nucleic Acids Res 17:8543–8551

    Article  PubMed  CAS  Google Scholar 

  • Sawicki J (1950) Studies on the structure of the aleurone layer in varieties of the cultivated barley Hordeum sativum Jess. Bull Int Acad Pol Sc et Let Cracovie Sér B 10:101–148

    Google Scholar 

  • Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen OA (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Nat Acad Sci USA 10:6552–6557

    Article  CAS  Google Scholar 

  • Stein N, Prasad M, Scholz U, Thiel T, Zhang H, Wolf M, Kota R, Varshney RK, 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

    Article  PubMed  CAS  Google Scholar 

  • Suzuki M, Latshaw S, Settles M, Koch K, Curtis HL, McCarty D (2006) The Wpk1/Vp8 gen regulates aleurone differentiation in a region-specific pattern. In: Proceedings of 48th annual genetics conference, Asilomar, CA Poster 115, p 93

  • Tian Q, Olsen L, Sun B, Lid SE, Brown RC, Lemmon BE, Fosnes K, Gruis DF, Opsahl-Sorteberg HG, Otegui MS, Olsen OA (2007) Subcellular localization and functional domain studies of DEFECTIVE KERNEL1 in maize and arabidopsis suggest a model for aleurone cell fate specification involving CRINKLY4 and SUPERNUMERARY ALEURONE LAYER1. Plant Cell 19:3127–3145

    Article  PubMed  CAS  Google Scholar 

  • Thiel T, Michalek W, Varshney RK, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genet 106:411–422

    PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins G (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Wisniewski JP, Rogowsky PM (2004) Vacuole H+-translocating inorganic pyrophosphatase (Vpp1) marks partial aleurone cell fate in cereal endosperm development. Plant Mol Biol 56:325–337

    Article  PubMed  CAS  Google Scholar 

  • Wolf MJ, Cutler HC, Zuber MS, Khoo U (1972) Maize with multilayer aleurone of high protein content. Crop Sci 12:440–442

    Article  Google Scholar 

  • Zhang LY, Bernard M, Leroy P, Feuillet C, Sourdille P (2005) High transferability of bread wheat EST-derived SSRs to other cereals. Theor Appl Genet 111:677–687

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We are grateful to W. Podyma and I. Loskutov for providing seeds of barley germplasm, A. Graner and M. Röder for SSR primers from IPK, L. Zhang and P. Sourdille for CFE markers, C. Dupré (†) and P. A. Meunier for cryogenic microtome sectioning and microscopy, G. Gay and N. Guilhot for microscopy and QTL pictures, and FX. Oury and F. Vear for critical reading of the manuscript.

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Authors and Affiliations

  1. INRA, UMR1095, Amélioration et Santé des Plantes, 234 avenue du Brézet, 63100, Clermont-Ferrand, France

    Louis Jestin, Catherine Ravel, Sylvie Auroy, Bastien Laubin, Marie-Reine Perretant, Caroline Pont & Gilles Charmet

  2. Université Blaise-Pascal, UMR1095, Campus des Cézeaux, 63170, Aubière, France

    Louis Jestin, Catherine Ravel, Sylvie Auroy, Bastien Laubin, Marie-Reine Perretant, Caroline Pont & Gilles Charmet

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  1. Louis Jestin
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  2. Catherine Ravel
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  3. Sylvie Auroy
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  4. Bastien Laubin
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  5. Marie-Reine Perretant
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  6. Caroline Pont
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  7. Gilles Charmet
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Correspondence to Louis Jestin.

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Communicated by A. Graner.

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Jestin, L., Ravel, C., Auroy, S. et al. Inheritance of the number and thickness of cell layers in barley aleurone tissue (Hordeum vulgare L.): an approach using F2–F3 progeny. Theor Appl Genet 116, 991–1002 (2008). https://doi.org/10.1007/s00122-008-0730-6

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  • DOI: https://doi.org/10.1007/s00122-008-0730-6

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