Newly synthesized wheat allohexaploids display progenitor‐dependent meiotic stability and aneuploidy but structural genomic additivity

Abstract

Summary• To understand key mechanisms leading to stabilized allopolyploid species, we characterized the meiotic behaviour of wheat allohexaploids in relation to structural and genetic changes.• For that purpose, we analysed first generations of synthetic allohexaploids obtained through interspecific hybridization, followed by spontaneous chromosome doubling, between several genotypes of Triticum turgidum and Aegilops tauschii wheat species, donors of AB and D genomes, respectively.• As expected for these Ph1 (Pairing homoeologous 1) gene-carrying allopolyploids, chromosome pairing at metaphase I of meiosis essentially occurs between homologous chromosomes. However, the different synthetic allohexaploids exhibited progenitor-dependent meiotic irregularities, such as incomplete homologous pairing, resulting in univalent formation and leading to aneuploidy in the subsequent generation.• Stability of the synthetic allohexaploids was shown to depend on the considered genotypes of both AB and D genome progenitors, where few combinations compare to the natural wheat allohexaploid in terms of regularity of meiosis and euploidy. Aneuploidy represents the only structural change observed in these synthetic allohexaploids, as no apparent DNA sequence elimination or rearrangement was observed when analysing euploid plants with molecular markers, developed from expressed sequence tags (ESTs) as well as simple sequence repeat (SSR) and transposable element sequences.

Extensive chromosomal variation in a recently formed natural allopolyploid species,Tragopogon miscellus(Asteraceae)

“…Even allohexaploid wheat (T. aestivum), which is ca. 10,000 y old (63), still exhibits some chromosomal instability; aneuploids compose ∼1% of intervarietal populations (64) and ∼2-3% of cultivated lines (29).…”

“…Only a few chromosomal substitutions in Crepis and Cyrtanthus neoallopolyploids were detectable, because not all parental chromosomes were morphologically distinct; thus, these values are likely underestimates (18). Synthetic S 2 bread wheat (Triticum aestivum) lines exhibited 0-50% aneuploidy, with variation attributable to progenitor background (29). Instability in wheat neoallopolyploids probably could be increased further in the absence of Ph1, which prevents homeologous pairing (29,(53)(54)(55).…”

“…Synthetic S 2 bread wheat (Triticum aestivum) lines exhibited 0-50% aneuploidy, with variation attributable to progenitor background (29). Instability in wheat neoallopolyploids probably could be increased further in the absence of Ph1, which prevents homeologous pairing (29,(53)(54)(55).…”

“…S6 and Table S1) and showed a similar frequency of euploids (n = 2) and aneuploids that were either 2n = 25 (n = 1) or 2n = 24 (n = 7) ( Table 1). Such extensive variation in chromosomal copy number is unprecedented within natural populations, but has been reported for synthetic allotetraploid B. napus (25) and, to a lesser extent, for synthetic allohexaploid wheat (29).…”

“…In these plants, the numbers of chromosomes deviating above and below two copies are equal, giving 24 chromosomes. This is the first report of such extensive compensated aneuploidy in nature, although it has been found in experimental neoallopolyploids (23,29), and such chromosome substitutions have been used extensively in cereal breeding (30)(31)(32). Compensated aneuploidy in natural populations of T. miscellus provides a powerful mechanism influencing the inheritance and fixation of alleles in early allopolyploid evolution.…”