Rapid and Repeatable Elimination of a Parental Genome-Specific DNA Repeat (pGc1R-1a) in Newly Synthesized Wheat Allopolyploids

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 ‫%09-07ف‬ 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.A LLOPOLYPLOIDS, derived from interspecific or copy, coding and noncoding DNA sequences (Feldman et al. 1997;Liu et al. 1998;Ozkan et al. 2001; Shaked intergeneric hybridizations, contain two or more divergent homeologous genomes. Following initial hyet al. 2001; Kashkush et al. 2002;Ma et al. 2004). Surprisingly, probably due to intrinsic difficulties in monitoring bridization and genome doubling, the newly formed amphiploid may undergo a one-step speciation process changes in only some members of a given repetitive DNA family, little attention has been paid to the behavthat can be a traumatic experience to the combined allopolyploid genomes (reviewed in Leitch and Benior and fate of this type of sequence, which constitutes the bulk of these plant genomes. polyploid wheats-it did not hybridize to any of the polyploid wheat species tested, thus suggesting elimina-A series of studies on newly synthesized allopolyploids of Triticeae, and particularly of the Triticum-Aegilops tion and/or extensive sequence divergence of the DNA repeat since allopolyploid formation (Anamthawatcomplex, has been particularly revealing in detecting rapid genomic and epigenomic changes (Ozkan et al. Jonsson and Heslop-Harrison 1993). 2001; Shaked et al. 2001;Han et al. 2003Han et al. , 2004Ma et Moreover, significant reduction in copy numbers of al. 2004). Among the changes it was found that the most Spelt1, a repetitive subtelomeric DNA family that repretantalizing but still mysterious phenomenon was rapid, sents 2% of the Ae. speltoides genome, was found in reproducible, and often nonrandom elimination of lownatural tetra-and hexaploid wheat,

Extensive and Heritable Epigenetic Remodeling and Genetic Stability Accompany Allohexaploidization of Wheat

“…It should be pointed out that some of the previously uncovered rapid genomic changes associated with wheat allopolyploidization such as elimination of coding and noncoding sequences have been documented as highly reproducible in randomly chosen individuals from multiple independently formed lines (Feldman et al 1997;Liu et al 1998a,b;Ozkan et al 2001;Han et al 2005). Therefore, this type of rapid genetic instability likely has played some roles in the initial establishment and eventual speciation of T. aestivum (Levy and Feldman 2004;Feldman and Levy 2005;Feldman and Levy 2009).…”

“…Previous studies employing newly synthesized allopolyploid wheat lines have documented that the onset of both the tetra-and hexapolyploidization events is associated with rapid and extensive structural genomic instabilities including elimination of coding and noncoding sequences (Feldman et al 1997;Liu et al 1998b;Ozkan et al 2001;Han et al 2005) and changes in DNA methylation (Liu et al 1998a;Shaked et al 2001). Nonetheless, analysis at many unbiased loci from a genome-wide perspective was conducted thus far only at the tetraploid level (Shaked et al 2001;Qi et al 2010), while either only a few preselected loci known to be labile (chromosome-and genome-specific sequences) or a set of selected microsatellite loci have been investigated at the hexaploid level to detect allohexaploidy-associated rapid genomic changes (Feldman et al 1997;Liu et al 1998a,b;Ozkan et al 2001;Mestiri et al 2010).…”

Numerous and Rapid Nonstochastic Modifications of Gene Products in Newly SynthesizedBrassica napusAllotetraploids

“…Similarly, He et al (2003) underlined the nonrandom feature of gene expression alterations in synthetic and natural hexaploid wheat. Recently, Han et al (2005) demonstrated that a tandem DNA repeat was reproducibly lost in three sets of newly synthesized TriticumAegilops allopolyploids. On the other hand, Wang et al (2004Wang et al ( , 2006 inferred stochastic changes of gene expression in A. suecica allotetraploids.…”

The BOY NAMED SUE Quantitative Trait Locus Confers Increased Meiotic Stability to an Adapted Natural Allopolyploid of Arabidopsis

“…Many of the genomic changes observed in recent allopolyploids, such as in Tragopogon miscellus (Chester et al, 2012), Brassica napus (Gaeta et al, 2007;Szadkowski et al, 2010;Xiong et al, 2011), or cotton (Gossypium hirsutum; Flagel et al, 2012), are consistent with homoeologous exchanges. In other cases, the observed genomic changes may have a different origin, such as some of the changes reported in wheat (Triticum aestivum; Feldman et al, 1997;Han et al, 2005;Zhang et al, 2013). Furthermore, rapid changes did not ensue in newly synthesized allotetraploid cotton (Liu et al, 2001;Xiong et al, 2011), suggesting that different allopolyploids might respond differently to the challenge.…”