Abstract
Variation in chromosome number due to polyploidy can seriously compromise meiotic stability. In autopolyploids, the presence of more than two homologous chromosomes may result in complex pairing patterns and subsequent anomalous chromosome segregation. In this context, chromocenter, centromeric, telomeric and ribosomal DNA locus topology and DNA methylation patterns were investigated in the natural autotetraploid, Arabidopsis arenosa. The data show that homologous chromosome recognition and association initiates at telomeric domains in premeiotic interphase, followed by quadrivalent pairing of ribosomal 45S RNA gene loci (known as NORs) at leptotene. On the other hand, centromeric regions at early leptotene show pairwise associations rather than associations in fours. These pairwise associations are maintained throughout prophase I, and therefore likely to be related to the diploid-like behavior of A. arenosa chromosomes at metaphase I, where only bivalents are observed. In anthers, both cells at somatic interphase as well as at premeiotic interphase show 5-methylcytosine (5-mC) dispersed throughout the nucleus, contrasting with a preferential co-localization with chromocenters observed in vegetative nuclei. These results show for the first time that nuclear distribution patterns of 5-mC are simultaneously reshuffled in meiocytes and anther somatic cells. During prophase I, 5-mC is detected in extended chromatin fibers and chromocenters but interestingly is excluded from the NORs what correlates with the pairing pattern.
Similar content being viewed by others
References
Armstrong SJ, Jones GH (2003) Meiotic cytology and chromosome behaviour in wild-type Arabidopsis thaliana. J Exp Bot 54:1–10
Armstrong SJ, Franklin FC, Jones GH (2001) Nucleolus-associated telomere clustering and pairing precede meiotic chromosome synapsis in Arabidopsis thaliana. J Cell Sci 114:4207–4217
Bomblies K, Weigel D (2007) Arabidopsis: a model genus for speciation. Curr Opin Genet Dev 17:500–504
Bozza CG, Pawlowski WP (2008) The cytogenetics of homologous chromosome pairing in meiosis in plants. Cytogenet Genome Res 120:313–319
Chen ZJ, Pikaard CS (1997) Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. Proc Natl Acad Sci USA 94:3442–3447
Clauss MJ, Koch MA (2006) Poorly known relatives of Arabidopsis thaliana. Trends Plant Sci 11:449–459
Comai L, Tyagi AP, Lysak MA (2003) FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res 11:217–226
Corredor E, Lukaszewski AJ, Pachón P, Allen DC, Naranjo T (2007) Terminal regions of wheat chromosomes select their pairing partners in meiosis. Genetics 177:699–706
Fransz P, De Jong JH, Lysak M, Castiglione MR, Schubert I (2002) Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate. Proc Natl Acad Sci USA 99:14584–14589
Fransz P, ten Hoopen R, Tessadori F (2006) Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res 14:71–78
Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435–R444
Ijdo JW, Wells RA, Baldini A, Reeders ST (1991) Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780
Mathieu O, Jasencakova Z, Vaillant I, Gendrel AV, Colot V, Schubert I, Tourmente S (2003) Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Arabidopsis. Plant Cell 15:2929–2939
Mitchell-Olds T, Clauss MJ (2002) Plant evolutionary genomics. Curr Opin Plant Biol 5:74–79
Naranjo T, Corredor E (2008) Nuclear architecture and chromosome dynamics in the search of the pairing partner in meiosis in plants. Cytogenet Genome Res 120:320–330
Pontes O, Neves N, Silva M, Lewis MS, Madlung A, Comai L, Viegas W, Pikaard CS (2004) Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome. Proc Natl Acad Sci USA 101:18240–18245
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:e1157
Preuss SB, Costa-Nunes P, Tucker S, Pontes O, Lawrence RJ, Mosher R, Kasschau KD, Carrington JC, Baulcombe DC, Viegas W, Pikaard CS (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684
Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4:507–516
Sanchez-Moran E, Armstrong SJ, Santos JL, Franklin FC, Jones GH (2002) Variation in chiasma frequency among eight accessions of Arabidopsis thaliana. Genetics 162:1415–1422
Santos JL, Alfaro D, Sanchez-Moran E, Armstrong SJ, Franklin FC, Jones GH (2003) Partial diploidization of meiosis in autotetraploid Arabidopsis thaliana. Genetics 165:1533–1540
Scott RJ, Spielman M (2006) Genomic imprinting in plants and mammals: how life history constrains convergence. Cytogenet Genome Res 113:53–67
Storchová Z, Breneman A, Cande J, Dunn J, Burbank K, O’Toole E, Pellman D (2006) Genome-wide genetic analysis of polyploidy in yeast. Nature 443:541–547
Sybenga J (1996) Chromosome pairing affinity and quadrivalent formation in polyploids: do segmental allopolyploids exist? Genome 39:1176–1184
Tessadori F, Schulkes RK, van Driel R, Fransz P (2007) Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis. Plant J 50:848–857
Weiss H, Maluszynska J (2000) Chromosomal rearrangement in autotetraploid plants of Arabidopsis thaliana. Hereditas 133:255–261
Yang X, Timofejeva L, Ma H, Makaroff CA (2006) The Arabidopsis SKP1 homolog ASK1 controls meiotic chromosome remodeling and release of chromatin from the nuclear membrane and nucleolus. J Cell Sci 119:3754–3763
Zhang W, Lee HR, Koo DH, Jiang J (2008) Epigenetic modification of centromeric chromatin: hypomethylation of DNA sequences in the CENH3-associated chromatin in Arabidopsis thaliana and maize. Plant Cell 20:25–34
Acknowledgments
We are grateful to H. Sofia Pereira for the critical review. A.L. Carvalho and M. Delgado are funded by Fellowships (grants SRRH/BD/13830/03 and SFRH/BPD/27219/2006, respectively), and the work was financed by FCT/POCTI/59389/04 (P·I. N.Neves) from the Fundação para a Ciência e a Tecnologia.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Scott Russell.
A. Carvalho and M. Delgado contributed equally to this work.
Rights and permissions
About this article
Cite this article
Carvalho, A., Delgado, M., Barão, A. et al. Chromosome and DNA methylation dynamics during meiosis in the autotetraploid Arabidopsis arenosa . Sex Plant Reprod 23, 29–37 (2010). https://doi.org/10.1007/s00497-009-0115-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-009-0115-2