Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat

Abstract

Allopolyploidization has been a driving force in plant evolution. Formation of common wheat (Triticum aestivum L.) represents a classic example of successful speciation via allopolyploidy. Nevertheless, the immediate chromosomal consequences of allopolyploidization in wheat remain largely unexplored. We report here an in-depth investigation on transgenerational chromosomal variation in resynthesized allohexaploid wheats that are identical in genome constitution to common wheat. We deployed sequential FISH, genomic in situ hybridization (GISH), and homeolog-specific pyrosequencing, which enabled unequivocal identification of each of the 21 homologous chromosome pairs in each of >1,000 individual plants from 16 independent lines. We report that wholechromosome aneuploidy occurred ubiquitously in early generations (from selfed generation S 1 to >S 20 ) of wheat allohexaploidy although at highly variable frequencies (20-100%). In contrast, other types of gross structural variations were scant. Aneuploidy included an unexpected hidden type, which had a euploid chromosome number of 2n = 42 but with simultaneous loss and gain of nonhomeologous chromosomes. Of the three constituent subgenomes, B showed the most lability for aneuploidy, followed by A, but the recently added D subgenome was largely stable in most of the studied lines. Chromosome loss and gain were also unequal across the 21 homologous chromosome pairs. Pedigree analysis showed no evidence for progressive karyotype stabilization even with multigenerational selection for euploidy. Profiling of two traits directly related to reproductive fitness showed that although pollen viability was generally reduced by aneuploidy, the adverse effect of aneuploidy on seed-set is dependent on both aneuploidy type and synthetic line.chromosome dynamics | hidden aneuploidy | synthetic wheat | wheat evolution H exaploid common wheat (Triticum aestivum L.) is a major food crop with international significance, the evolution of which is characterized by two sequential allopolyploidization events: one leading to formation of allotetraploid wheat (T. turgidum L.) and the other to allohexaploid wheat (T. aestivum) (1, 2). Despite decades of research, the mechanisms by which the initial allopolyploid individuals became stabilized, established, and accumulate to successful speciation remains largely unknown in this important crop. In theory, chromosome-level perturbation should be among the first manifestations of nascent allopolyploidization. Indeed, two recent molecular cytogenetic studies, in resynthesized allotetraploid Brassica napus lines (3) and young natural allotetraploid Tragopogon miscellus populations (4), respectively, have provided unique insights into the chromosomal dynamics associated with nascent allotetraploidy. Being at the resolution of individual chromosomes, these studies have documented a surprisingly high incidence of both structural and numerical changes in nascent allotetraploid plants (3, 4). It was found that early generations of resynthesized allotetrap...

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“…More importantly, we could not detect any signs of homoeologous recombination in the progeny of A. suecica, while the dosage irregularities observed in several of the synthetic progeny were consistent with homoeologous pairing and recombination (Figures 2 and 3). These results support the idea that A. suecica has evolved mechanisms for avoiding homoeologous pairing and are consistent with a recent study in wheat, documenting widespread aneuploidy in synthetic allohexaploids of wheat but no evidence for homoeologous exchanges (Zhang et al, 2013). The authors hypothesized that the presence of the functional allele of Ph1 in the tetraploid wheat parent used to produce the synthetic allohexaploid suppressed homoeologous pairing (Zhang et al, 2013).…”

“…In our populations of F1 and F2 allopolyploids, we observed widespread aneuploidy and dosage imbalances, similar to those observed in newly synthesized allopolyploids of others species (Xiong et al, 2011;Chester et al, 2012;Zhang et al, 2013). Dosage imbalance was also present in the progeny of the natural A. suecica, indicating that, while it is clearly more fit than the synthetic allopolyploid, its meioses are often irregular.…”

“…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.…”

Patterns of chromosomal variation in natural populations of the neoallotetraploid Tragopogon mirus (Asteraceae)

“…More natural and synthetic polyploid systems need to be studied to determine how widely these putative 'rules' apply. For example, in contrast to B. napus and T. miscellus, chromosomal variation in synthetic lines of allohexaploid wheat did not adhere to a compensated pattern, and no chromosomal rearrangements were detected (Zhang et al, 2013b).…”

Polyploidy and genome evolution in plants

“…Although great strides have been made in determining the processes by which DNA content is reduced following polyploidy, few studies have addressed the second aspect of diploidization: the mechanisms by which entire chromosomes are lost. Only recently have synthetic polyploid studies demonstrated the high prevalence of chromosomal instability immediately after genome duplication (Mestiri et al 2010;Xiong et al 2011;Chester et al 2012;Zhang et al 2013). While aneuploidy has been found to negatively correlate with fertility in synthetic Brassica napus polyploids ) and pollen viability in synthetic wheat polyploids (Zhang et al 2013), the fact that chromosome number is no longer a suitable corollary for polyploidy history (e.g.…”