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Functional & Integrative Genomics

, Volume 9, Issue 2, pp 219–229 | Cite as

Whole genome approaches to identify early meiotic gene candidates in cereals

  • William D. Bovill
  • Priyanka Deveshwar
  • Sanjay Kapoor
  • Jason A. Able
Original Paper

Abstract

Early events during meiotic prophase I underpin not only viability but the variation of a species from generation to generation. Understanding and manipulating processes such as chromosome pairing and recombination are integral for improving plant breeding. This study uses comparative genetics, quantitative trait locus (QTL) analysis and a transcriptomics-based approach to identify genes that might have a role in genome-wide recombination control. Comparative genetics and the analysis of the yeast and Arabidopsis sequenced genomes has allowed the identification of early meiotic candidates that are conserved in wheat, rice and barley. Secondly, scoring recombination frequency as a phenotype for QTL analysis across wheat, rice and barley mapping populations has enabled us to identify genomic regions and candidate genes that could be involved in genome-wide recombination. Transcriptome data for candidate genes indicate that they are expressed in meiotic tissues. Candidates identified included a non-annotated expressed protein, a DNA topoisomerase 2-like candidate, RecG, RuvB and RAD54 homologues.

Keywords

Genome-wide recombination QTL Comparative genetics Transcriptomics Meiosis 

Notes

Acknowledgements

The authors thank Dr Amanda Able (School of Agriculture, Food & Wine, The University of Adelaide) for reviewing this manuscript and Dr Junjian Ni for assistance in obtaining the raw rice mapping data used in this study. This research was supported by the Australian government under the Australia–India Strategic Research Fund (AISRF) and the Indian government through the Department of Science and Technology (DST).

Supplementary material

10142_2008_97_MOESM1_ESM.pdf (167 kb)
S1. Putative orthologues of meiotic genes previously identified in yeast and/or Arabidopsis that were identified in the wheat, rice and barley genomes. Genes listed have been grouped according to their meiotic functional class. Gene acronyms, their source species (Sc Saccharomyces cerevisiae, At Arabidopsis thaliana), gene name, transcript assembly (TA) number or EST accession (if no TA was identified), TBLASTX values and references are shown. Yeast and Arabidopsis genes in the same shade of grey that are directly above or below one another represent orthologues (DOC 166 KB).

References

  1. Appels R (2003) A consensus molecular genetic map for wheat—a cooperative international effort. In Proceedings of the 10th International Wheat Genetics Symposium(Ed, Progna, N. E.) Paestum, Italy, pp 211–214Google Scholar
  2. Barr AR, Jefferies SP, Broughton S, Chalmers KJ, Kretschmer JM, Boyd WJR, Collins HM, Roumeliotis S, Logue SJ, Coventry SJ, Moody DB, Read BJ, Poulsen D, Lance RCM, Platz GJ, Park RF, Panozzo JF, Karakousis A, Lim P, Verbyla AP, Eckermann PJ (2003) Mapping and QTL analysis of the barley population Alexis x Sloop. Aust J Agr Res 54:1117–1123CrossRefGoogle Scholar
  3. Boden SA, Shadiac N, Tucker EJ, Langridge P, Able JA (2007) Expression and functional analysis of TaASY1 during meiosis of bread wheat (Triticum aestivum). BMC Mol. Biol. 8:65PubMedCrossRefGoogle Scholar
  4. Bovill WD, Ma W, Ritter K, Collard BCY, Davis M, Wildermuth GB, Sutherland MW (2006) Identification of novel QTL for resistance to crown rot in the doubled haploid wheat population ‘W21MMT70’ x ‘Mendos’. Plant Breed 125:538–543CrossRefGoogle Scholar
  5. Brevis JC, Chicaiza O, Khan IA, Jackson L, Morris CF, Dubcovsky J (2008) Agronomic and quality evaluation of common wheat near-isogenic lines carrying the leaf rust resistance gene Lr47. Crop Sci 48:1441–1451CrossRefGoogle Scholar
  6. Childs KL, Hamilton JP, Zhu W, Ly E, Cheung F, Wu H, Rabinowicz PD, Town CD, Buell CR, Chan AP (2007) The TIGR plant transcript assemblies database. Nucleic Acids Res 35:D846–D851PubMedCrossRefGoogle Scholar
  7. Chu S, DeRisi J, Eisen M, Mulholland J, Botstein D, Brown PO, Herskowitz I (1998) The transcriptional program of sporulation in budding yeast. Science 282:699–705PubMedCrossRefGoogle Scholar
  8. Collard BCY, Grams RA, Bovill WD, Percy CD, Jolley R, Lehmensiek A, Wildermuth GB, Sutherland MW (2005) Development of molecular markers for crown rot resistance in wheat: mapping of QTLs for seedling resistance in a 2-49 × Janz population. Plant Breed 124:1–6CrossRefGoogle Scholar
  9. Cox BS, Parry JM (1968) The isolation, genetics and survival characteristics of ultraviolet-light sensitive mutants in yeast. Mutat Res 6:37–55PubMedGoogle Scholar
  10. Crismani W, Baumann U, Sutton T, Shirley N, Webster T, Spangenberg G, Langridge P, Able JA (2006) Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat. BMC Genomics 7:267PubMedCrossRefGoogle Scholar
  11. Esch E, Syzmaniak JM, Yates H, Pawlowski WP, Buckler ES (2007) Using crossover breakpoints in recombinant inbred lines to identify quantitative trait loci controlling the global recombination frequency. Genetics 177:1851–1858PubMedCrossRefGoogle Scholar
  12. Goff SA, Ricke D, Lan T-H, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D, Hutchison D, Martin C, Katagiri F, Lange BM, Moughamer T, Xia Y, Budworth P, Zhong J, Miguel T, Paszkowski U, Zhang S, Colbert M, Sun W-l, Chen L, Cooper B, Park S, Wood TC, Mao L, Quail P, Wing R, Dean R, Yu Y, Zharkikh A, Shen R, Sahasrabudhe S, Thomas A, Cannings R, Gutin A, Pruss D, Reid J, Tavtigian S, Mitchell J, Eldredge G, Scholl T, Miller RM, Bhatnagar S, Adey N, Rubano T, Tusneem N, Robinson R, Feldhaus J, Macalma T, Oliphant A, Briggs S (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  13. Hartung F, Puchta H (2000) Molecular characterisation of two paralogous SPO11 homologues in Arabidopsis thaliana. Nucleic Acids Res 28:1548–1554PubMedCrossRefGoogle Scholar
  14. Higgins J, Sanchez-Moran E, Armstrong SJ, Jones GH, Franklin FCH (2005) The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over. Gene Dev 19:2488–2500PubMedCrossRefGoogle Scholar
  15. Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384PubMedCrossRefGoogle Scholar
  16. Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38:233–271PubMedCrossRefGoogle Scholar
  17. Lehmensiek A, Eckermann PJ, Verbyla AP, Appels R, Sutherland MW, Daggard G (2005) Curation of wheat maps to improve map accuracy and QTL detection. Aust J Agr Res 56:1347–1354CrossRefGoogle Scholar
  18. Linde-Laursen I, Heslop-Harrison JS, Shepherd KW, Taketa S (1997) The barley genome and its relationship with the wheat genomes. A survey with an internationally agreed recommendation for barley chromosome nomenclature. Hereditas 126:1–16CrossRefGoogle Scholar
  19. Meddows TR, Savory AP, Lloyd RG (2004) RecG helicase promotes DNA double-strand break repair. Mol Microbiol 52:119–132PubMedCrossRefGoogle Scholar
  20. Mezard C (2006) Meiotic recombination hotspots in plants. Biochem Soc T 34:531–534CrossRefGoogle Scholar
  21. Mezard C, Vignard J, Drouaud J, Mercier R (2007) The road to crossovers: plants have their say. Trends Genet 23(2):91–99PubMedCrossRefGoogle Scholar
  22. Osakabe K, Abe K, Yoshioka T, Osakabe Y, Todoriki S, Ichikawa H, Hohn B, Toki S (2006) Isolation and characterization of the RAD54 gene from Arabidopsis thaliana. Plant J 48:827–842PubMedCrossRefGoogle Scholar
  23. Paques F, Haber JE (1999) Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol R 63:349–404Google Scholar
  24. Price AH, Tomos AD (1997) Genetic dissection of root growth in rice (Oryza sativa L.). II: mapping quantitative trait loci using molecular markers. Theor Appl Genet 95:143–152CrossRefGoogle Scholar
  25. Primig M, Williams RM, Winzler EA, Tevzadze GC, Conway AR, Hwang SY, Davis RW, Esposito RE (2002) The core meiotic transcriptome in budding yeasts. Nat Genet 26:415–423Google Scholar
  26. Riley R, Chapman V (1958) Genetic control of the cytologically diploid behaviour of hexaploid wheat. Nature 182:713–715CrossRefGoogle Scholar
  27. Roeder GS (1997) Meiotic chromosomes: it takes two to tango. Gene Dev 11:2600–2621PubMedCrossRefGoogle Scholar
  28. Sanchez-Moran E, Santos J-L, Jones GH, Franklin FCH (2007) ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis. Gene Dev 21:2220–2233PubMedCrossRefGoogle Scholar
  29. Sears ER (1976) Genetic control of chromosome pairing in wheat. Annu Rev Genet 10:31–51PubMedCrossRefGoogle Scholar
  30. Shaked H, Melamed-Bessudo C, Levy AA (2005) High-frequency gene targeting in Arabidopsis plants expressing the yeast RAD54 gene. P Natl Acad Sci U S A 102:12265–12269CrossRefGoogle Scholar
  31. Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kanteny R, Munkvold JD, Miftahudin, Mahmoud A, Ma X, Gustafson PJ, Qi LL, Echalier B, Gill BS, Mathews DE, Lazo GR, Chao S, Anderson OD, Edwards H, Linkiewicz AM, Dubcovsky J, Akhunov ED, Dvorak J, Zhang D, Nguyen HT, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Hossain K, Kalavacharla V, Kianian SF, Choi D-W, Close TJ, Dilbirligi M, Gill KS, Steber C, Walker-Simmons MK, McGuire PE, Qualset CO (2003) Comparative DNA sequence analysis of wheat and rice genomes. Genome Res 13:1818–1827PubMedGoogle Scholar
  32. Van Os H, Stam P, Visser RGF, Van Eck HJ (2005) RECORD: a novel method for ordering loci on a genetic linkage map. Theor Appl Genet 112:30–40PubMedCrossRefGoogle Scholar
  33. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTL. Heredity 93:77–78CrossRefGoogle Scholar
  34. Wang S, Basten CJ, Zeng Z-B (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. (http://statgen.ncsu.edu/qtlcart/WQTLCart.htm)
  35. Wenzl P, Li H, Carling J, Zhou M, Raman H, Paul E, Hearnden P, Maier C, Xia L, Caig V, Ovesna J, Cakir M, Poulsen D, Wang J, Raman R, Smith K, Muehlbauer G, Chalmers K, Kleinhofs A, Huttner E, Kilian A (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206PubMedCrossRefGoogle Scholar
  36. West SC (1997) Processing of recombination intermediates by the RuvABC proteins. Annu Rev Genet 31:213–244PubMedCrossRefGoogle Scholar
  37. Whitby MC, Lloyd RG (1995) Branch migration of three-strand recombination intermediates by RecG, a possible pathway for securing exchanges initiated by 3′-tailed duplex DNA. EMBO J 14:3302–3310PubMedGoogle Scholar
  38. Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • William D. Bovill
    • 1
  • Priyanka Deveshwar
    • 2
  • Sanjay Kapoor
    • 2
  • Jason A. Able
    • 1
    • 3
  1. 1.School of Agriculture, Food & WineThe University of AdelaideGlen OsmondAustralia
  2. 2.Interdisciplinary Center for Plant Genomics and Department of Plant Molecular BiologyUniversity of Delhi South CampusNew DelhiIndia
  3. 3.Molecular Plant Breeding Cooperative Research CentreGlen OsmondAustralia

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