Abstract
Although allopolyploids are common in nature and in agriculture, knowledge of their origin, evolution and genomic regulation is limited. We study synthetic allotetraploids of Arabidopsis thaliana and Arabidopsis arenosa as well as the natural allotetraploid Arabidopsis suecica. To elucidate the composition and behavior of the allotetraploid genome, we used chromosome painting with probes from contiguous regionsof chromosome 4 of A. thaliana and fluorescent in-situ hybridization with centromeric (CEN) probes specific for each parental genome. We documented the presence of 16 A. arenosa and 10 A. thaliana chromosomes and demonstrate that two different A. arenosa chromosomes are homeologous to chromosome 4 of A. thaliana. Although chromosome pairing in pollen mother cells was predominantly homologous, CENs of different parental origin coalesced at early prophase I, but resolved into proper pairs by metaphase. In addition, CENs of homologous chromosomes were not paired in tapetum cells and endopolyploidy without strict polyteny was evident by the large number of independent CENs. Thus, the Arabidopsis synthetic allopolyploids were capable of homologous pairing as early as three generations after their formation. This indicates that diploid-like pairing is not the result of adaptive mutations in genes that regulate pairing nor the result of structural remodeling of the genomes: rather, it is likely that either the parents provided genes controlling pairing behavior or that features of the parental chromosomes hinder homeologous pairing.
Similar content being viewed by others
References
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.
Bernard P, Allshire R (2002) Centromeres become unstuck without heterochromatin. Trends Cell Biol 12: 419.
Comai L (2000) Genetic and epigenetic interactions in allopolyploid plants. Plant Mol Biol 43: 387‐399.
Comai L, Tyagi AP, Winter K et al. (2000) Phenotypic instability and rapid gene silencing in newly formed arabidopsis allotetraploids. Plant Cell 12: 1551‐1568.
Dej KJ, Orr‐Weaver TL (2000). Separation anxiety at the centromere. Trends Cell Biol 10: 392‐399.
de Jong JH, Stam P (1985) The association ofcen tromeres of nonhomologous chromosomes at meiotic prophase in Beta vulgaris L. Can J Genet Cytol 27: 165‐171.
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.
Henikoff S, Comai L (1998) A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307‐318.
Hylander N (1957) Cardaminopsis suecica (Fr.) Hiit., a northern amphidiploid species. Bull Jard Bot Bruxelles 27: 591‐604.
Kamm A, Galasso I, Schmidt T, Heslop‐Harrison JS (1995) Analysis of a repetitive DNA family from Arabidopsis arenosa and relationships between Arabidopsis species. Plant Mol Biol 27: 853‐862.
Kashkush K, Feldman M, Levy AA (2002) Gene loss, silencing and activation in a newly synthesized wheat allotetraploid. Genetics 160: 1651‐1659.
Kim NS, Armstrong KC, Fedak G, Ho K, Park NI (2002) A microsatellite sequence from the rice blast fungus (Magnaporthe grisea) distinguishes between the centromeres of Hordeum vulgare and H. bulbosum in hybrid plants. Genome 45: 165‐174.
Lee HS, Chen ZJ (2001) Protein‐coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 98: 6753‐6758.
Liu B, Brubaker CL, Mergeai G, Cronn RC, Wendel JF (2001) Polyploid formation in cotton is not accompanied by rapid genomic changes. Genome 44: 321‐330.
Loeve A (1961) Hylandra–a new genus of Cruciferae. Svensk Botanisk Tidskrift 55: 211‐217.
Luo MC, Dubcovsky J, Dvorak J (1996) Recognition ofho meology by the wheat Ph1 locus. Genetics 144: 1195‐1203.
Lysak MA, Fransz PF, Ali HB, Schubert I (2001) Chromosome painting in Arabidopsis thaliana. Plant J 28: 689‐697.
Madlung A, Masuelli RW, Watson B, Reynolds SH, Davison J, Comai L (2002) Remodeling of DNA methylation and phenotypic and transcriptional changes in synthetic Arabidopsis allotetraploids. Plant Physiol 129: 733‐746.
Maluszynska J, Heslop‐Harrison JS (1991) Localization of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1: 159‐166.
Martinez‐Perez E, Shaw P, Moore G (2001) The Ph1 locus is needed to ensure specific somatic and meiotic centromere association. Nature 411: 204‐207.
Martinez‐Perez E, Shaw PJ, Moore G (2000) Polyploidy induces centromere association. J Cell Biol 148: 233‐238.
Moore G (2002) Meiosis in allopolyploids–the importance of 'Teflon' chromosomes. Trends Genet 18: 456‐463.
Mummenhoff K, Hurka H (1995) Allopolyploid origin of Arabidopsis suecica (Fries) Norrlin: evidence from chloroplast and nuclear genome markers. Bot Acta 108: 449‐456.
Myung K, Datta A, Chen C, Kolodner RD (2001) SGS1, the Saccharomyces cerevisiae homologue ofB LM and WRN, suppresses genome instability and homeologous recombination. Nat Genet 27: 113‐116.
O'Kane SRJ, Schaal BA, Al‐Shehbaz IA (1996) The origins of Arabidopsis suecica (Brassicaceae) as indicated by nuclear rDNA sequences. Systematic Botany 21: 559‐566.
Ozkan H, Feldman M (2001) Genotypic variation in tetraploid wheat affecting homoeologous pairing in hybrids with Aegilops peregrina. Genome 44: 1000‐1006.
Pikaard CS (1999) Nucleolar dominance and silencing of transcription. Trends Plant Sci 4: 478‐483.
Ross KJ, Fransz P, Jones GH (1996) A light microscopic atlas of meiosis in Arabidopsis thaliana. Chromosome Res 4: 507‐516.
Round EK, Flowers SK, Richards EJ (1997) Arabidopsis thaliana centromere regions: genetic map positions and repetitive DNA structure. Genome Res 7: 1045‐1053.
Schmidt M, Acarkan A, Boivin K (2001) Comparative structural genomics in the Brassicaceae family. Plant Physiol Biochem 39: 253‐262.
Schranz ME, Osborn TC (2000) Novel flowering time variation in the resynthesized polyploid Brassica napus. J Hered 91: 242‐246.
Sears ER (1976) Genetic control ofch romosome pairing in wheat. Annu Rev Genet 10: 31‐51.
Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA (2001) Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. Plant Cell 13: 1749‐1759.
Soltis DE, Soltis PS (1995) The dynamic nature of polyploid genomes. Proc Natl Acad Sci USA 92: 8089‐8091.
Weiss H, Maluszynska J (2001) Molecular cytogenetics analysis of polyploidization in the anther tapetum of diploid and autotetraploid Arabidopsis thaliana plant. Ann Bot (Lond) 87: 729‐735.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Comai, L., Tyagi, A.P. & Lysak, M.A. FISH analysis of meiosis in Arabidopsis allopolyploids. Chromosome Res 11, 217–226 (2003). https://doi.org/10.1023/A:1022883709060
Issue Date:
DOI: https://doi.org/10.1023/A:1022883709060