Genetics. 2005 July; 170(3): 1239–1245.
Rapid and Repeatable Elimination of a Parental Genome-Specific DNA Repeat (pGc1R-1a) in Newly Synthesized Wheat Allopolyploids
Fangpu Han, George Fedak, Wanli Guo, and Bao Liu

Abstract

Recent work in the Triticum-Aegilops complex demonstrates that allopolyploidization is associated with an array of changes in low-copy coding and noncoding sequences. Nevertheless, the behavior and fate of repetitive DNA elements that constitute the bulk of nuclear DNA of these plant species is less clear following allopolyploidy. To gain further insight into the genomic events that accompany allopolyploid formation, we investigated fluorescence in situ hybridization (FISH) patterns of a parental-specific, tandem DNA repeat (pGc1R-1) on three sets of newly synthesized amphiploids with different parental species. It was found that drastic physical elimination of pGc1R-1 copies occurred in all three amphiploids in early generations. DNA gel-blot analysis confirmed the FISH data and estimates indicated that ~70–90% of the copies of the pGc1R-1 repeat family were eliminated from the amphiploids by the second to third selfed generations. Thus, allopolyploidy in Triticum-Aegilops can be accompanied by rapid and extensive elimination of parental-specific repetitive DNA sequences, which presumably play a role in the initial stabilization of the nascent amphiploid plants.

ALLOPOLYPLOIDS, derived from interspecific or intergeneric hybridizations, contain two or more divergent homeologous genomes. Following initial hybridization and genome doubling, the newly formed amphiploid may undergo a one-step speciation process that can be a traumatic experience to the combined allopolyploid genomes (reviewed in Leitch and Bennett 1997; Matzke et al. 1999; Comai 2000; Wendel 2000; Rieseberg 2001; Adams and Wendel 2004; Feldman and Levy 2005). Indeed, a number of recent reports have documented rapid genetic and epigenetic instability that often accompany nascent allopolyploidy (reviewed in Pikaard 2001; Levy and Feldman 2002, 2004; Liu and Wendel 2002; Comai et al. 2003; Lawton-Rauh 2003; Osborn et al. 2003b; Chen et al. 2004; Madlung and Comai 2004; Soltis et al. 2004; Ma and Gustafson 2005).

A series of studies on newly synthesized allopolyploids of Triticeae, and particularly of the Triticum-Aegilops complex, has been particularly revealing in detecting rapid genomic and epigenomic changes (Ozkan et al. 2001; Shaked et al. 2001; Han et al. 2003, 2004; Ma et al. 2004). Among the changes it was found that the most tantalizing but still mysterious phenomenon was rapid, reproducible, and often nonrandom elimination of low-copy, coding and noncoding DNA sequences (Feldman et al. 1997; Liu et al. 1998; Ozkan et al. 2001; Shaked et al. 2001; Kashkush et al. 2002; Ma et al. 2004). Surprisingly, probably due to intrinsic difficulties in monitoring changes in only some members of a given repetitive DNA family, little attention has been paid to the behavior and fate of this type of sequence, which constitutes the bulk of these plant genomes. Nonetheless, for the few relevant studies available, a generic finding is that reduction in copy number of some DNA repeats appeared to be associated with interspecific hybridization and allopolyploidy in Triticeae. For example, it was found that, on the basis of DNA gel-blot analysis, although the DNA repeat pAesKB52 hybridized to Aegilops speltoides, Ae. sharonensis, and Ae. longissima—three probable diploid progenitors to the B genome of various polyploid wheats—it did not hybridize to any of the polyploid wheat species tested, thus suggesting elimination and/or extensive sequence divergence of the DNA repeat since allopolyploid formation (Anamthawat-Jonsson and Heslop-Harrison 1993).

Moreover, significant reduction in copy numbers of Spelt1, a repetitive subtelomeric DNA family that represents 2% of the Ae. speltoides genome, was found in natural tetra- and hexaploid wheat, Triticum tugidum and T. aestivum, as well as in the first generations of amphiploids that have Ae. speltoides as a parent (Pestsova et al. 1998; Salina et al. 2004). Similarly, a dispersed repetitive DNA family (pSp89.XI) that is Ae. Speltoides specific was also found to have a much reduced abundance in tetra- and hexaploid wheat (Daud and Gustafson 1996). Finally, a global comparison of the C-values (genome sizes) of newly synthesized wheat amphiploids and their parents indicates nonadditivity and significant downsizing of the amphiploid genomes, although specific sequences underlying the reduction were not identified (Ozkan et al. 2003). More significantly, this less-than-proportional increase in genome size in a polyploid species expected from the addition of its diploid progenitors appeared to be a widespread phenomenon in flowering plants (Leitch and Bennett 2004). Thus, it is clear that, similar to the situation for some of the unstable low-copy sequences that have been extensively studied (reviewed in Feldman and Levy 2005), some repetitive DNA families may be extremely labile following allopolyploidization in plants and may undergo gradual or drastic elimination. Nonetheless, because none of the above studies has used independently synthesized multiple sets of new amphiploids with known exact parental plants, it remains inconclusive with regard to elimination or divergence as a cause for the observed phenomenon or the timing and repeatability of its occurrence.

Chromosome Changes in Evolution