Creating new interspecific hybrid and polyploid crops

Mason, Annaliese S.; Batley, Jacqueline

doi:10.1016/j.tibtech.2015.06.004

Cited by 71 publications

(44 citation statements)

References 56 publications

(87 reference statements)

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“…Our findings have added new insights toward deeper understanding of an allopolyploid genome with respect to its gene regulatory and functional interplay and its phenotypic manifestation, which bears significance in the context of polyploidy, a ubiquitous and cyclic event associated with the evolutionary history of all higher plants (Doyle et al, 2008;Van de Peer et al, 2009;Jiao et al, 2011). Our results also may have implications in the translational aspect of functional genomics studies with respect to creating novel crops via hybridization and polyploidization (Mason and Batley, 2015).…”

Section: Discussionmentioning

confidence: 67%

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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Section: Discussionmentioning

confidence: 67%

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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“…For example, plant breeders have crossed domesticated species to wild species to introduce resistance to a variety of pathogens in wheat, potato, and canola (Mason and Batley 2015), and almost all maize grown in the United States is grown from intraspecific hybrid seeds, which has increased yield and provided improved resistance to biotic and abiotic factors (Crow 1998). Vintners and brewers have created interspecific hybrids to select for traits such as lower acetic acid concentration (Bellon et al 2015), and many incidental fungal hybrids have been discovered in brewing and industry, including Pichia sorbitophila (Louis et al 2012), and various hybrids across the Saccharomyces clade (Gonzalez et al 2006, 2008; Muller and McCusker 2009; Hittinger 2013; Bellon et al 2015), most notably the lager-brewing yeast, Saccharomyces pastorianus (Tamai et al 1998; Dunn and Sherlock 2008; Walther et al 2014; Baker et al 2015; Gibson and Liti 2015; Peris et al 2016).…”

Section: Introductionmentioning

confidence: 99%

Loss of Heterozygosity Drives Adaptation in Hybrid Yeast

Heil

DeSevo

Pai

et al. 2017

Molecular Biology and Evolution

116

109

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Hybridization is often considered maladaptive, but sometimes hybrids can invade new ecological niches and adapt to novel or stressful environments better than their parents. The genomic changes that occur following hybridization that facilitate genome resolution and/or adaptation are not well understood. Here, we examine hybrid genome evolution using experimental evolution of de novo interspecific hybrid yeast Saccharomyces cerevisiae × Saccharomyces uvarum and their parentals. We evolved these strains in nutrient-limited conditions for hundreds of generations and sequenced the resulting cultures identifying numerous point mutations, copy number changes, and loss of heterozygosity (LOH) events, including species-biased amplification of nutrient transporters. We focused on a particularly interesting example, in which we saw repeated LOH at the high-affinity phosphate transporter gene PHO84 in both intra- and interspecific hybrids. Using allele replacement methods, we tested the fitness of different alleles in hybrid and S. cerevisiae strain backgrounds and found that the LOH is indeed the result of selection on one allele over the other in both S. cerevisiae and the hybrids. This is an example where hybrid genome resolution is driven by positive selection on existing heterozygosity and demonstrates that even infrequent outcrossing may have lasting impacts on adaptation.

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“…An added significance to explore the transgenerational dynamics of karyotypic alteration (i.e., the evolutionary trajectories of karyotypic evolution) lies in the fact that evolved karyotypic stabilization is an essential property for nascent polyploidy to be persistent over evolutionary timescales and contribute to species diversification. Furthermore, knowledge gained regarding the extent and trend of karyotypic evolution, its transgenerational heritability and phenotypic consequences, as well as the mechanisms whereby karyotype stabilization can be achieved in newly formed polyploids may provide useful clues to more judicious utilization of the synthetic hybridization/allopolyploidization strategy for crop improvement (Mason and Batley 2015). …”

Section: Introductionmentioning

confidence: 99%

Transgenerationally Precipitated Meiotic Chromosome Instability Fuels Rapid Karyotypic Evolution and Phenotypic Diversity in an Artificially Constructed Allotetraploid Wheat (AADD)

Gou

Bian

et al. 2018

Molecular Biology and Evolution

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Although a distinct karyotype with defined chromosome number and structure characterizes each biological species, it is intrinsically labile. Polyploidy or whole-genome duplication has played a pervasive and ongoing role in the evolution of all eukaryotes, and is the most dramatic force known to cause rapid karyotypic reconfiguration, especially at the initial stage. However, issues concerning transgenerational propagation of karyotypic heterogeneity and its translation to phenotypic diversity in nascent allopolyploidy, at the population level, have yet to be studied in detail. Here, we report a large-scale examination of transgenerationally propagated karyotypic heterogeneity and its phenotypic manifestation in an artificially constructed allotetraploid with a genome composition of AADD, that is, involving two of the three progenitor genomes of polyploid wheat. Specifically, we show that 1) massive organismal karyotypic heterogeneity is precipitated after 12 consecutive generations of selfing from a single euploid founder individual, 2) there exist dramatic differences in aptitudes between subgenomes and among chromosomes for whole-chromosome gain and/or loss and structural variations, 3) majority of the numerical and structural chromosomal variations are concurrent due to mutual contingency and possible functional constraint, 4) purposed and continuous selection and propagation for euploidy over generations did not result in enhanced karyotype stabilization, and 5) extent of karyotypic variation correlates with variability of phenotypic manifestation. Together, our results document that allopolyploidization catalyzes rampant and transgenerationally heritable organismal karyotypic heterogeneity that drives population-level phenotypic diversification, which lends fresh empirical support to the still contentious notion that whole-genome duplication enhances organismal evolvability.

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Creating new interspecific hybrid and polyploid crops

Cited by 71 publications

References 56 publications

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

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

Loss of Heterozygosity Drives Adaptation in Hybrid Yeast

Transgenerationally Precipitated Meiotic Chromosome Instability Fuels Rapid Karyotypic Evolution and Phenotypic Diversity in an Artificially Constructed Allotetraploid Wheat (AADD)

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