Intrinsic karyotype stability and gene copy number variations may have laid the foundation for tetraploid wheat formation

Zhang, Huakun; Bian, Yao; Gou, Xiaowan; Dong, Yuzhu; Rustgi, Sachin; Zhang, Bangjiao; Xu, Chunming; Li, Ning; Bao, Qiyu; Han, Fangpu; Wettstein, Diter von; B, Liu

doi:10.1073/pnas.1319598110

Cited by 83 publications

(108 citation statements)

References 35 publications

(55 reference statements)

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“…Rearrangements also largely followed a pattern where putatively homeologous segments were exchanged (only one out of the 53 translocations was an exception). These types of compensated changes were also found in synthetic neoallotetraploid B. napus (Xiong et al, 2011) and synthetic allotetraploid wheats (Zhang et al, 2013a). Thus, T. mirus provides another example in which alterations in parental gene balance appear to be tolerated more than alterations in total gene copy number, as expected based on the gene balance hypothesis (Birchler, 2012).…”

Section: Parental Divergencesupporting

confidence: 59%

“…The trend towards underrepresentation of (intergenomic) translocation heterozygotes in T. mirus suggests some segregating translocations may be disadvantageous (Supplementary Tables S3-S8). In resynthesized allotetraploid B. napus and several allotetraploid wheats, lineages displaying the highest fertility were those that had the lowest number of alterations (Xiong et al, 2011;Zhang et al, 2013a).…”

Section: Parental Divergencementioning

confidence: 99%

“…Future work could test whether a diploid-like meiotic regulation has already arisen by analyzing meiosis in these and other meiotically stable candidates from natural populations and synthetic allotetraploid lines. Interestingly, the establishment of some allotetraploid wheat species has been associated with certain diploid progenitor combinations generating chromosomally stable lineages from the first generation (Zhang et al, 2013a).…”

Section: Chromosomal Variation In Neoallotetraploid Populationsmentioning

confidence: 99%

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

et al. 2014

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Cytological studies have shown many newly formed allopolyploids (neoallopolyploids) exhibit chromosomal variation as a result of meiotic irregularities, but few naturally occurring neoallopolyploids have been examined. Little is known about how long chromosomal variation may persist and how it might influence the establishment and evolution of allopolyploids in nature. In this study we assess chromosomal composition in a natural neoallotetraploid, Tragopogon mirus, and compare it with T. miscellus, which is an allotetraploid of similar age (~40 generations old). We also assess whether parental gene losses in T. mirus correlate with entire or partial chromosome losses. Of 37 T. mirus individuals that were karyotyped, 23 (62%) were chromosomally additive of the parents, whereas the remaining 14 individuals (38%) had aneuploid compositions. The proportion of additive versus aneuploid individuals differed from that found previously in T. miscellus, in which aneuploidy was more common (69%; Fisher's exact test, P = 0.0033). Deviations from parental chromosome additivity within T. mirus individuals also did not reach the levels observed in T. miscellus, but similar compensated changes were observed. The loss of T. dubius-derived genes in two T. mirus individuals did not correlate with any chromosomal changes, indicating a role for smaller-scale genetic alterations. Overall, these data for T. mirus provide a second example of prolonged chromosomal instability in natural neoallopolyploid populations.

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Section: Parental Divergencesupporting

confidence: 59%

Section: Parental Divergencementioning

confidence: 99%

Section: Chromosomal Variation In Neoallotetraploid Populationsmentioning

confidence: 99%

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

et al. 2014

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“…Notably, aneuploidy is frequently associated with nascent polyploidization in plants (Xiong et al, 2011;Chester et al, 2012;Zhang et al, 2013b); however, whether these are ephemeral by-products of wholegenome duplication or represent an important contributing factor to polyploid genome evolution, especially at the onset stage of polyploid formation, remains uninvestigated. However, the latter possibility is likely, given that, in contrast to nucleotide mutation, many types of aneuploidy can be readily reverted back to euploidy following subsequent meiotic segregation yet might as well impart their impacts (heritable variation in gene expression) to the euploid progeny (Henry et al, 2010;Gao et al, 2016).…”

mentioning

confidence: 99%

Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat

Zhang

Gong

et al. 2017

Plant Physiol.

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Aneuploidy, a condition of unbalanced chromosome content, represents a large-effect mutation that bears significant relevance to human health and microbe adaptation. As such, extensive studies of aneuploidy have been conducted in unicellular model organisms and cancer cells. Aneuploidy also frequently is associated with plant polyploidization, but its impact on gene expression and its relevance to polyploid genome evolution/functional innovation remain largely unknown. Here, we used a panel of diverse types of whole-chromosome aneuploidy of hexaploid wheat (Triticum aestivum), all under the common genetic background of cv Chinese Spring, to systemically investigate the impact of aneuploidy on genome-, subgenome-, and chromosome-wide gene expression. Compared with prior findings in haploid or diploid aneuploid systems, we unravel additional and novel features of alteration in global gene expression resulting from the two major impacts of aneuploidy, cisand trans-regulation, as well as dosage compensation. We show that the expression-altered genes map evenly along each chromosome, with no evidence for coregulating aggregated expression domains. However, chromosomes and subgenomes in hexaploid wheat are unequal in their responses to aneuploidy with respect to the number of genes being dysregulated. Strikingly, homeologous chromosomes do not differ from nonhomologous chromosomes in terms of aneuploidy-induced trans-acting effects, suggesting that the three constituent subgenomes of hexaploid wheat are largely uncoupled at the transcriptional level of gene regulation. Together, our findings shed new insights into the functional interplay between homeologous chromosomes and interactions between subgenomes in hexaploid wheat, which bear implications to further our understanding of allopolyploid genome evolution and efforts in breeding new allopolyploid crops.

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“…Genomic asymmetry for agronomically important traits has been reported among the three genomes (A, B and D) of common wheat (Feldman et al, 2012). Although Chinese Spring wheat (a natural hexaploid wheat) is estimated to have lost 10,000 to 16,000 genes after allohexaploidization (Brenchley et al, 2012), the structural changes found in the hexaploid genomes had mainly occurred at the tetraploid stage (Zhang et al, 2013). Furthermore, based on the wheat syntenome, Pont et al (2013) reported overdominance of the D genome against the tetraploid genome (AABB) after the second allohexaploidization.…”

Section: Introductionmentioning

confidence: 99%

Comparison of genome-wide gene expression patterns in the seedlings of nascent allohexaploid wheats produced by two combinations of hybrids

et al. 2015

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Allopolyploidization in plants is an important event that enhances heterosis and environmental adaptation. Common wheat, Triticum aestivum (AABBDD), which is an allohexaploid that evolved from an allopolyploidization event between T. turgidum (AABB) and Aegilops tauschii (DD), shows more growth vigor and wider adaptation than tetraploid wheats. To better understand the molecular basis for the heterosis of hexaploid wheat, we systematically analyzed the genomewide gene expression patterns of two combinations of newly hybridized triploids (ABD), their chromosome-doubled hexaploids (AABBDD), stable synthetic hexaploids (AABBDD) and natural hexaploids, in addition to their parents, T. turgidum (AABB) and Ae. tauschii (DD), using a microarray to reconstruct the events of allopolyploidization and genome stabilization. Overall comparisons of gene expression profiles showed that the newly generated hexaploids exhibited gene expression patterns similar to those of their maternal tetraploids, irrespective of hybrid combination. With successive generations, the gene expression profiles of nascent hexaploids became less similar to the maternal profiles, and belonged to a separate cluster from the natural hexaploids. Triploids revealed characteristic expression patterns, suggesting endosperm effects. In the newly hybridized triploids (ABD) of two independent synthetic lines, approximately onefifth of expressed genes displayed non-additive expression; the number of these genes decreased with polyploidization and genome stabilization. Approximately 20% of the non-additively expressed genes were transmitted across generations throughout allopolyploidization and successive self-pollinations, and 43 genes overlapped between the two combinations, indicating that shared gene expression patterns can be seen during allohexaploidization. Furthermore, four of these 43 genes were involved in starch and sucrose metabolism, suggesting that these metabolic events play key roles in the hybrid vigor of hexaploid wheat.

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Intrinsic karyotype stability and gene copy number variations may have laid the foundation for tetraploid wheat formation

Cited by 83 publications

References 35 publications

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

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

Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat

Comparison of genome-wide gene expression patterns in the seedlings of nascent allohexaploid wheats produced by two combinations of hybrids

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