Advertisement

Plant Cell Reports

, Volume 36, Issue 8, pp 1277–1285 | Cite as

Dynamic nucleolar activity in wheat × Aegilops hybrids: evidence of C-genome dominance

  • Ghader MirzaghaderiEmail author
  • Zinat Abdolmalaki
  • Mohsen Zohouri
  • Zeinab Moradi
  • Annaliese S. Mason
Original Article

Abstract

Key message

NOR loci of C-subgenome are dominant in wheat × Aegilops interspecific hybrids, which may have evolutionary implications for wheat group genome dynamics and evolution.

Abstract

After interspecific hybridisation, some genes are often expressed from only one of the progenitor species, shaping subsequent allopolyploid genome evolution processes. A well-known example is nucleolar dominance, i.e. the formation of cell nucleoli from chromosomes of only one parental species. We studied nucleolar organizing regions (NORs) in diploid Aegilops markgrafii (syn: Ae. caudata; CC), Ae. umbellulata (UU), allotetraploids Aegilops cylindrica (CcCcDcDc) and Ae. triuncialis (CtCtUtUt), synthetic interspecific F1 hybrids between these two allotetraploids and bread wheat (Triticum aestivum, AABBDD) and in F3 generation hybrids with genome composition AABBDDCtCtUtUt using silver staining and fluorescence in situ hybridization (FISH). In Ae. markgrafii (CC), NORs of both 1C and 5C or only 5C chromosome pairs were active in different individual cells, while only NORs on 1U chromosomes were active in Ae. umbellulata (UU). Although all 35S rDNA loci of the Ct subgenome (located on 1Ct and 5Ct) were active in Ae. triuncialis, only one pair (occupying either 1Cc or 5Cc) was active in Ae. cylindrica, depending on the genotype studied. These C-genome expression patterns were transmitted to the F1 and F3 generations. Wheat chromosome NOR activity was variable in Ae. triuncialis × T. aestivum F1 seeds, but silenced by the F3 generation. No effect of maternal or paternal cross direction was observed. These results indicate that C-subgenome NOR loci are dominant in wheat × Aegilops interspecific hybrids, which may have evolutionary implications for wheat group genome dynamics and allopolyploid evolution.

Keywords

Nucleolar dominance 35S rRNA gene Polyploidization Interspecific hybridization 

Notes

Acknowledgements

This research was financially supported by the University of Kurdistan, Sanandaj. The authors declare that they have no competing interests. The first author acquired some data (FISH of Ae. triuncialis and its subgenomes) at Andreas Houben’s lab at IPK, Germany. ASM is supported by DFG Emmy Noether award MA6473/1-1.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical standards

The manuscript has not been submitted to more than one journal for simultaneous consideration. No data have been fabricated or manipulated to support our conclusions. We have acknowledged and cited the work of others to the best of our knowledge. All authors read and approved the final manuscript.

Supplementary material

299_2017_2152_MOESM1_ESM.pptx (11.9 mb)
Supplementary material 1 (PPTX 12148 kb)

References

  1. Appels R, Gerlach W, Dennis E, Swift H, Peacock W (1980) Molecular and chromosomal organization of DNA sequences coding for the ribosomal RNAs in cereals. Chromosoma 78:293–311CrossRefGoogle Scholar
  2. Brasileiro-Vidal AC, Cuadrado A, Brammer SP, Zanatta ACA, Prestes AM, Moraes-Fernandes MIB, Guerra M (2003) Chromosome characterization in Thinopyrum ponticum (Triticeae, Poaceae) using in situ hybridization with different DNA sequences. Genet Mol Biol 26:505–510CrossRefGoogle Scholar
  3. Cermeno M, Orellana J, Santos J, Lacadena J (1984) Nucleolar activity and competition (amphiplasty) in the genus Aegilops. Heredity 53:603–611CrossRefGoogle Scholar
  4. Chandrasekhara C, Mohannath G, Blevins T, Pontvianne F, Pikaard CS (2016) Chromosome-specific NOR inactivation explains selective rRNA gene silencing and dosage control in Arabidopsis. Genes Dev 30:177–190PubMedPubMedCentralGoogle Scholar
  5. Chen ZJ, Comai L, Pikaard CS (1998) Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. Proc Natl Acad Sci USA 95:14891–14896CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cuadrado A, Cardoso M, Jouve N (2008) Increasing the physical markers of wheat chromosomes using SSRs as FISH probes. Genome 51:809–815CrossRefPubMedGoogle Scholar
  7. Fakhri Z, Mirzaghaderi G, Ahmadian S, Mason AS (2016) Unreduced gamete formation in wheat × Aegilops spp. hybrids is genotype specific and prevented by shared homologous subgenomes. Plant Cell Rep 35:1143–1154CrossRefPubMedGoogle Scholar
  8. Fradkin M, Greizerstein E, Ferrari M, Poggio L (2016) Nucleolar activity in Triticum × Thinopyrum hybrids with different ploidy level. Plant Biosyst:doi. doi: 10.1080/11263504.11262016.11218973 Google Scholar
  9. Frankel O, Gerlach W, Peacock W (1987) The ribosomal RNA genes in synthetic tetraploids of wheat. Theor Appl Genet 75:138–143CrossRefGoogle Scholar
  10. Friebe B, Schubert V, Blüthner W, Hammer K (1992) C-banding pattern and polymorphism of Aegilops caudata and chromosomal constitutions of the amphiploid T. aestivumAe. caudata and six derived chromosome addition lines. Theor Appl Genet 83:589–596CrossRefPubMedGoogle Scholar
  11. Friebe B, Jiang J, Tuleen N, Gill BS (1995) Standard karyotype of Triticum umbellulatum and the characterization of derived chromosome addition and translocation lines in common wheat. Theor Appl Genet 90:150–156CrossRefPubMedGoogle Scholar
  12. Gerlach W, Bedbrook J (1979) Cloning and characterization of ribosomal RNA genes from wheat and barley. Nucleic Acids Res 7:1869–1885CrossRefPubMedPubMedCentralGoogle Scholar
  13. Grummt I, Längst G (2013) Epigenetic control of RNA polymerase I transcription in mammalian cells. BBA-Gene Regul Mech 1829:393–404Google Scholar
  14. Guo X, Han F (2014) Asymmetric epigenetic modification and elimination of rDNA sequences by polyploidization in wheat. Plant Cell 26:4311–4327CrossRefPubMedPubMedCentralGoogle Scholar
  15. Idziak D, Hasterok R (2008) Cytogenetic evidence of nucleolar dominance in allotetraploid species of Brachypodium. Genome 51:387–391CrossRefPubMedGoogle Scholar
  16. Jiang J, Gill B (1994) New 18S·26S ribosomal RNA gene loci: chromosomal landmarks for the evolution of polyploid wheats. Chromosoma 103:179–185CrossRefPubMedGoogle Scholar
  17. Książczyk T, Kovarik A, Eber F, Huteau V, Khaitova L, Tesarikova Z, Coriton O, Chèvre A-M (2011) Immediate unidirectional epigenetic reprogramming of NORs occurs independently of rDNA rearrangements in synthetic and natural forms of a polyploid species Brassica napus. Chromosoma 120:557–571CrossRefPubMedGoogle Scholar
  18. Lacadena J, Cermeno M, Orellana J, Santos J (1984) Evidence for wheat-rye nucleolar competition (amphiplasty) in triticale by silver-staining procedure. Theor Appl Genet 67:207–213CrossRefPubMedGoogle Scholar
  19. Lawrence RJ, Earley K, Pontes O, Silva M, Chen ZJ, Neves N, Viegas W, Pikaard CS (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609CrossRefPubMedGoogle Scholar
  20. Martini G, O’dell M, Flavell R (1982) Partial inactivation of wheat nucleolus organisers by the nucleolus organiser chromosomes from Aegilops umbellulata. Chromosoma 84:687–700CrossRefGoogle Scholar
  21. McClintock B (1934) The relationship of a particular chromosomal element to the development of the nucleoli in Zea mays. Zeit Zellforsch Mik Anat 21:294–328CrossRefGoogle Scholar
  22. McStay B (2006) Nucleolar dominance: a model for rRNA gene silencing. Genes Dev 20:1207–1214CrossRefPubMedGoogle Scholar
  23. Michalak P (2014) Evidence for maternal imprinting of 45S ribosomal RNA genes in Xenopus hybrids. Dev Genes Evol 224:125–128CrossRefPubMedGoogle Scholar
  24. Michalak K, Maciak S, Kim YB, Santopietro G, Oh JH, Kang L, Garner HR, Michalak P (2015) Nucleolar dominance and maternal control of 45S rDNA expression. Proc R Soc B 282:20152201CrossRefPubMedPubMedCentralGoogle Scholar
  25. Miller T, Hutchinson J, Reader S (1983) The identification of the nucleolus organiser chromosomes of diploid wheat. Theor Appl Genet 65:145–147CrossRefPubMedGoogle Scholar
  26. Mirzaghaderi G, Fathi N (2015) Unreduced gamete formation in wheat: Aegilops triuncialis interspecific hybrids leads to spontaneous complete and partial amphiploids. Euphytica 206:67–75CrossRefGoogle Scholar
  27. Mirzaghaderi G, Houben A, Badaeva ED (2014) Molecular-cytogenetic analysis of Aegilops triuncialis and identification of its chromosomes in the background of wheat. Mol cytogenet 7:91CrossRefPubMedPubMedCentralGoogle Scholar
  28. Navashin M (1934) Chromosome alterations caused by hybridization and their bearing upon certain general genetic problems. Cytologia 5:169–203CrossRefGoogle Scholar
  29. Neves N, Silva M, Heslop-Harrison J, Viegas W (1997) Nucleolar dominance in triticales: control by unlinked genes. Chromosome Res 5:125–131CrossRefPubMedGoogle Scholar
  30. Orellana J, Santos J, Lacadena J, Cermeno M (1984) Nucleolar competition analysis in Aegilops ventricosa and its amphiploids with tetraploid wheats and diploid rye by the silver-staining procedure. Can J Genet Cytol 26:34–39CrossRefGoogle Scholar
  31. Pikaard CS (2000a) The epigenetics of nucleolar dominance. Trends Genet 16:495–500CrossRefPubMedGoogle Scholar
  32. Pikaard CS (2000b) Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. Plant Mol Biol 43:163–177CrossRefPubMedGoogle Scholar
  33. Pikaard CS (2001) Nucleolar dominance. Wiley, Encyclopedia of Life SciencesGoogle Scholar
  34. Pontes O, Lawrence RJ, Silva M, Preuss S, Costa-Nunes P, Earley K, Neves N, Viegas W, Pikaard CS (2007) Postembryonic establishment of megabase-scale gene silencing in nucleolar dominance. PLoS One 2:e1157CrossRefPubMedPubMedCentralGoogle Scholar
  35. Pontvianne F, Blevins T, Chandrasekhara C, Feng W, Stroud H, Jacobsen SE, Michaels SD, Pikaard CS (2012) Histone methyltransferases regulating rRNA gene dose and dosage control in Arabidopsis. Genes Dev 26:945–957CrossRefPubMedPubMedCentralGoogle Scholar
  36. Reeder RH (1974) Ribosomes from eukaryotes: genetics. In: Nomura M (ed) Ribosomes. Cold Spring Harbor Laboratory Press, New York, pp 489–519Google Scholar
  37. Sochorová J, Coriton O, Kuderová A, Lunerová J, Chèvre A-M, Kovařík A (2016) Gene conversion events and variable degree of homogenization of rDNA loci in cultivars of Brassica napus. Ann Bot 119:13–26CrossRefPubMedPubMedCentralGoogle Scholar
  38. Soltis DE, Buggs RJ, Doyle JJ, Soltis PS (2010) What we still don’t know about polyploidy. Taxon 59:1387–1403Google Scholar
  39. Thomas JB, Kaltsikes PJ (1983) Effect of chromosomes 1B and 6B on nucleolus formation in hexaploid triticale. Can J Genet Cytol 25:292–297CrossRefGoogle Scholar
  40. Tucker S, Vitins A, Pikaard CS (2010) Nucleolar dominance and ribosomal RNA gene silencing. Curr Opin Cell Biol 22:351–356CrossRefPubMedPubMedCentralGoogle Scholar
  41. Turowski TW, Tollervey D (2015) Cotranscriptional events in eukaryotic ribosome synthesis. Wiley Interdiscip Rev RNA 6:129–139CrossRefPubMedGoogle Scholar
  42. Vanichanon A, Blake N, Sherman J, Talbert L (2003) Multiple origins of allopolyploid Aegilops triuncialis. Theor Appl Genet 106:804–810CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Agronomy and Plant Breeding, Faculty of AgricultureUniversity of KurdistanSanandajIran
  2. 2.Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and NutritionJustus Liebig UniversityGiessenGermany

Personalised recommendations