Skip to main content
SpringerLink
Log in

Physical analysis of the complex rye (Secale cereale L.) Alt4 aluminium (aluminum) tolerance locus using a whole-genome BAC library of rye cv. Blanco

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Rye is a diploid crop species with many outstanding qualities, and is important as a source of new traits for wheat and triticale improvement. Rye is highly tolerant of aluminum (Al) toxicity, and possesses a complex structure at the Alt4 Al tolerance locus not found at the corresponding locus in wheat. Here we describe a BAC library of rye cv. Blanco, representing a valuable resource for rye molecular genetic studies, and assess the library’s suitability for investigating Al tolerance genes. The library provides 6 × genome coverage of the 8.1 Gb rye genome, has an average insert size of 131 kb, and contains only ~2% of empty or organelle-derived clones. Genetic analysis attributed the Al tolerance of Blanco to the Alt4 locus on the short arm of chromosome 7R, and revealed the presence of multiple allelic variants (haplotypes) of the Alt4 locus in the BAC library. BAC clones containing ALMT1 gene clusters from several Alt4 haplotypes were identified, and will provide useful starting points for exploring the basis for the structural variability and functional specialization of ALMT1 genes at this locus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akhunov ED, Akhunova AR, Dvořák J (2005) BAC libraries of Triticum urartu, Aegilops speltoides and Ae. tauschii, the diploid ancestors of polyploid wheat. Theor Appl Genet 111:1617–1622

    Article  PubMed  CAS  Google Scholar 

  • Aniol A (1983) Aluminium uptake by roots of two winter wheat varieties of different tolerance to aluminium. Biochem Physiol Pflanzen 178:11–20

    CAS  Google Scholar 

  • Aniol A (2004) Chromosomal location of aluminium tolerance genes in rye. Plant Breed 123:132–136

    Article  CAS  Google Scholar 

  • Aniol A, Gustafson JP (1984) Chromosome location of genes controlling aluminum tolerance in wheat, rye, and triticale. Can J Genet Cytol 26:701–705

    Google Scholar 

  • Ayliffe MA, Lawrence GJ, Ellis JG, Pryor AJ (1994) Heteroduplex molecules formed between allelic sequences cause nonparental RAPD bands. Nucleic Acids Res 22:1632–1636

    Article  PubMed  CAS  Google Scholar 

  • Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 274:227–274

    Article  PubMed  CAS  Google Scholar 

  • Cenci A, Chantret N, Kong X, Gu Y, Anderson OD, Fahima T, Distelfeld A, Dubcovsky J (2003) Construction and characterization of a half million clone BAC library of durum wheat (Triticum turgidium ssp. durum). Theor Appl Genet 107:931–939

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Shirley NJ, Saeed M, Pallotta M, Gustafson JP (2008) An ALMT1 gene cluster controlling aluminum tolerance at the Alt4 locus of rye (Secale cereale L.). Genetics 179:669–682

    Article  PubMed  CAS  Google Scholar 

  • Ehdaie B, Whitkus RW, Waines JG (2003) Root biomass, water-use efficiency, and performance of wheat-rye translocations of chromosomes 1 and 2 in spring bread wheat ‘Pavon’. Crop Sci 43:710–717

    Google Scholar 

  • Fontecha G, Silva-Navas J, Benito C, Mestres MA, Espino FJ, Hernández-Riquer MV, Gallego FJ (2007) Candidate gene identification of an aluminum-activated organic acid transporter gene at the Alt4 locus for aluminum tolerance in rye (Secale cereale L.). Theor Appl Genet 114:249–260

    Article  PubMed  CAS  Google Scholar 

  • Furukawa J, Yamaji N, Wang H, Mitani N, Murata Y, Sato K, Katsuhara M, Takeda K, Ma JF (2007) An aluminum-activated citrate transporter in barley. Plant Cell Physiol 48:1081–1091

    Article  PubMed  CAS  Google Scholar 

  • Gallego FJ, Calles B, Benito C (1998) Molecular markers linked to the aluminum tolerance gene Alt1 in rye (Secale cereale L.). Theor Appl Genet 97:1104–1109

    Article  CAS  Google Scholar 

  • Graybosch RA (2001) Uneasy unions: quality effects of rye chromatin transfers to wheat. J Cereal Sci 33:3–16

    Article  CAS  Google Scholar 

  • Gustafson JP, Ross K (1990) Control of alien gene expression for aluminum tolerance in wheat. Genome 33:9–12

    CAS  Google Scholar 

  • Hackauf B, Wehling P (2005) Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics. Theor Appl Genet 110:832–845

    Article  PubMed  CAS  Google Scholar 

  • Hoffmann B (2008) Alteration of drought tolerance of winter wheat caused by translocation of rye chromosome segment 1RS. Cereal Res Commun 36:269–278

    Article  Google Scholar 

  • Isidore E, Scherrer B, Bellec A, Budin K, Faivre-Rampant P, Waugh R, Keller B, Caboche M, Feuillet C, Chalhoub B (2005) Direct targeting and rapid isolation of BAC clones spanning a defined chromosome region. Funct Integr Genomics 5:97–103

    Article  PubMed  CAS  Google Scholar 

  • Keller B, Feuillet C (2000) Colinearity and gene density in grass genomes. Trends Plant Sci 5:246–251

    Article  PubMed  CAS  Google Scholar 

  • Kim BY, Baier AC, Somers DJ, Gustafson JP (2001) Aluminum tolerance in triticale, wheat, and rye. Euphytica 120:329–337

    Article  CAS  Google Scholar 

  • Kim W, Johnson JW, Baenziger PS, Lukaszewski AJ, Gaines CS (2004) Agronomic effect of wheat-rye translocation carrying rye chromatin (1R) from different sources. Crop Sci 44:1254–1258

    Google Scholar 

  • Lijavetzky D, Muzzi G, Wicker T, Keller B, Wing R, Dubcovsky J (1999) Construction and characterization of a bacterial artificial chromosome (BAC) library for the A genome of wheat. Genome 42:1176–1182

    Article  PubMed  CAS  Google Scholar 

  • Ling P, Chen XM (2005) Construction of a hexaploid wheat (Triticum aestivum L.) bacterial artificial chromosome library for cloning genes for stripe rust resistance. Genome 48:1028–1036

    Article  PubMed  CAS  Google Scholar 

  • Luo M-C, Thomas C, You FM, Hsiao J, Ouyang S, Buell CR, Malandro M, McGuire PE, Anderson OD, Dvorak J (2003) High-throughput fingerprinting of bacterial artificial chromosomes using the SNaPshot labeling kit and sizing of restriction fragments by capillary electrophoresis. Genomics 82:378–389

    Article  PubMed  CAS  Google Scholar 

  • Madej LJ (1996) Worldwide trends in rye growing and breeding. Vortr Pflanzenzücht 35:1–6

    Google Scholar 

  • Matos M, Camacho MV, Pérez-Flores V, Pernaute B, Pinto-Carnide O, Benito C (2005) A new aluminum tolerance gene located on rye chromosome arm 7RS. Theor Appl Genet 111:360–369

    Article  PubMed  CAS  Google Scholar 

  • Miftahudin, Chikmawati T, Ross K, Scoles GJ, Gustafson JP (2005) Targeting the aluminum tolerance gene Alt3 region in rye, using rice/rye micro-colinearity. Theor Appl Genet 110:906–913

    Article  PubMed  CAS  Google Scholar 

  • Moreno-Sevilla B, Baenziger PS, Peterson CJ, Graybosch RA, McVey DV (1995) The 1BL/1RS translocation: agronomic performance of F3-derived lines from a winter wheat cross. Crop Sci 35:1051–1055

    Google Scholar 

  • Moullet O, Zhang H-B, Lagudah ES (1999) Construction and characterisation of a large DNA insert library from the D genome of wheat. Theor Appl Genet 99:305–313

    Article  Google Scholar 

  • Mugwira LM, Elgawhary SM, Patel KI (1976) Differential tolerances of triticale, wheat, rye, and barley to aluminum in nutrient solution. Agron J 68:782–787

    Article  CAS  Google Scholar 

  • Oettler G (2005) The fortune of a botanical curiosity—Triticale: past, present and future. J Agric Sci 143:329–346

    Article  Google Scholar 

  • Rabinovich SV (1998) Importance of wheat-rye translocations for breeding modern cultivars of Triticum aestivum L. Euphytica 100:323–340

    Article  Google Scholar 

  • Saisho D, Myoraku E, Kawasaki S, Sato K, Takeda K (2007) Construction and characterization of a bacterial artificial chromosome (BAC) library from the Japanese malting barley variety ‘Haruna Nijo’. Breed Sci 57:29–38

    Article  Google Scholar 

  • Sasaki T, Yamamoto Y, Ezaki B, Katsuhara M, Ahn SJ, Ryan PR, Delhaize E, Matsumoto H (2004) A wheat gene encoding an aluminum-activated malate transporter. Plant J 37:645–653

    Article  PubMed  CAS  Google Scholar 

  • Scherrer B, Isidore E, Klein P, Kim J, Bellec A, Chalhoub B, Keller B, Feuillet C (2005) Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17:361–374

    Article  PubMed  CAS  Google Scholar 

  • Shen B, Wang DM, McIntyre CL, Liu CJ (2005) A ‘Chinese Spring’ wheat (Triticum aestivum L.) bacterial artificial chromosome library and its use in the isolation of SSR markers for targeted genome regions. Theor Appl Genet 111:1489–1494

    Article  PubMed  CAS  Google Scholar 

  • Shi B-J, Collins NC, Miftahudin, Schnurbusch T, Langridge P, Gustafson JP (2007) Construction of a rye cv. Blanco BAC library, and progress towards cloning the rye Alt3 aluminium (aluminum) tolerance gene. Vortr Pflanzenzücht 71:205–209

    Google Scholar 

  • Šimková H, Šafář J, Suchánková P, Kovářová P, Bartoš J, Kubaláková M, Janda J, Číhalíková J, Mago R, Lelley T, Doležel J (2008) A novel resource for genomics of Triticeae: BAC library specific for the short arm of rye (Secale cereale L.) chromosome 1R (1RS). BMC Genomics 9:237

    Article  PubMed  CAS  Google Scholar 

  • Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060

    Article  PubMed  CAS  Google Scholar 

  • Tenhola-Roininen T, Immonen S, Tanhuanpää P (2006) Rye doubled haploids as a research and breeding tool—a practical point of view. Plant Breed 125:584–590

    Article  Google Scholar 

  • Tomerius A-M, Miedaner T, Geiger HH (2008) A model calculation approach towards the optimization of a standard scheme of seed-parent line development in hybrid rye breeding. Plant Breed 127:433–440

    Article  Google Scholar 

  • Varshney RK, Beier U, Khlestkina EK, Kota R, Korzun V, Graner A, Börner A (2007) Single nucleotide polymorphisms in rye (Secale cereale L.): discovery, frequency, and applications for genome mapping and diversity studies. Theor Appl Genet 114:1105–1116

    Article  PubMed  CAS  Google Scholar 

  • Villareal RL, Bañuelos O, Mujeeb-Kazi A, Rajaram S (1998) Agronomic performance of chromosomes 1B and T1BL.1RS near-isolines in the spring bread wheat Seri M82. Euphytica 103:195–202

    Article  Google Scholar 

  • Wang Q, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103:17644–17649

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Raman H, Zhou M, Ryan PR, Delhaize E, Hebb DM, Coombes N, Mendham N (2007) High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 115:265–276

    Article  PubMed  CAS  Google Scholar 

  • Yu Y, Tomkins JP, Waugh R, Frisch DA, Kudrna D, Kleinhofs A, Brueggeman RS, Muehlbauer GJ, Wise RP, Wing RA (2000) A bacterial artificial chromosome library for barley (Hordeum vulgare L.) and the identification of clones containing putative resistance genes. Theor Appl Genet 101:1093–1099

    Article  CAS  Google Scholar 

  • Zhang H-B, Zhao X, Ding X, Paterson AH, Wing RA (1995) Preparation of megabase-size DNA from plant nuclei. Plant J 7:175–184

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Construction of the BAC library was commissioned by the USDA-Agriculture Research Service. This work was also funded by the Australian Research Council, the Grains Research and Development Corporation and the South Australian Government. We gratefully acknowledge James Chand for technical assistance.

Author information

Authors and Affiliations

  1. Australian Centre for Plant Functional Genomics (ACPFG), School of Agriculture, Food and Wine, University of Adelaide, PMB1, Glen Osmond, SA, 5064, Australia

    B.-J. Shi, J. Button, J. Miyazaki, M. Pallotta, N. Gustafson, H. Zhou, P. Langridge & N. C. Collins

  2. USDA-ARS, 206 Curtis Hall, University of Missouri, Columbia, MO, 65211-7020, USA

    J. P. Gustafson

Authors
  1. B.-J. Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. P. Gustafson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Button
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Miyazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Pallotta
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. Gustafson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. P. Langridge
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. N. C. Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. P. Gustafson.

Additional information

Communicated by M. Xu.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 897 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shi, BJ., Gustafson, J.P., Button, J. et al. Physical analysis of the complex rye (Secale cereale L.) Alt4 aluminium (aluminum) tolerance locus using a whole-genome BAC library of rye cv. Blanco. Theor Appl Genet 119, 695–704 (2009). https://doi.org/10.1007/s00122-009-1080-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-009-1080-8

Keywords

Search

Navigation