Extensive homoeologous genome exchanges in allopolyploid crops revealed by mRNAseq‐based visualization

Abstract

SummaryPolyploidy, the possession of multiple sets of chromosomes, has been a predominant factor in the evolution and success of the angiosperms. Although artificially formed allopolyploids show a high rate of genome rearrangement, the genomes of cultivars and germplasm used for crop breeding were assumed stable and genome structural variation under the artificial selection process of commercial breeding has remained little studied. Here, we show, using a repurposed visualization method based on transcriptome sequence data, that genome structural rearrangement occurs frequently in varieties of three polyploid crops (oilseed rape, mustard rape and bread wheat), meaning that the extent of genome structural variation present in commercial crops is much higher than expected. Exchanges were found to occur most frequently where homoeologous chromosome segments are collinear to telomeres and in material produced as doubled haploids. The new insights into genome structural evolution enable us to reinterpret the results of recent studies and implicate homoeologous exchanges, not deletions, as being responsible for variation controlling important seed quality traits in rapeseed. Having begun to identify the extent of genome structural variation in polyploid crops, we can envisage new strategies for the global challenge of broadening crop genetic diversity and accelerating adaptation, such as the molecular identification and selection of genome deletions or duplications encompassing genes with trait‐controlling dosage effects.

Validation of an updated Associative Transcriptomics platform for the polyploid crop species Brassica napus by dissection of the genetic architecture of erucic acid and tocopherol isoform variation in seeds

“…The clear signals in the transcript abundance‐based association analysis confirms the stability of differential gene expression across the panel, and its utility for the identification of association signals. Regions of the genome previously associated with seed glucosinolate content (selected alongside erucic content in Canola quality rapeseed) show particularly strong transcript abundance associations, which we interpret as consequences of the extensive structural variation in these regions of the genome (He et al ., ). The new AT platform generates strong signals because of the large, diverse panel and superior number of markers assigned to homoeologues, properties lacking in the platform reported previously (Harper et al ., ).…”

“…() and He et al . (). Association studies have to meet many demands to maximize the probability of identifying marker–trait associations.…”

“…The growth conditions, sampling of plant material, RNA extraction and transcriptome sequencing was carried out as described by He et al . (). The RNA‐seq data from each accession line were mapped onto recently developed ordered Brassica A and C pan‐transcriptomes (He et al ., ) as reference sequences ( maq 0.7.1; Li et al ., ).…”

The causes and consequences of subgenome dominance in hybrids and recent polyploids

“…Not only were numerous HEs identified between individuals, but HEs showed a significant subgenome bias, resulting in more C subgenome regions replaced with A subgenome regions than A subgenome regions being replaced with C subgenome regions (Chalhoub et al ., ). These findings were supported by subsequent studies in B. napus and other allopolyploid crops (He et al ., ; Samans et al ., ), including similar subgenome biased patterns in natural cotton allopolyploids (Guo et al ., ), octoploid strawberry (Tennessen et al ., ), and synthetic AADD wheat tetraploids (Gou et al ., ).…”

Homoeologous exchanges cause extensive dosage‐dependent gene expression changes in an allopolyploid crop

“…Because of this apparent asymmetry, these events have been referred to using a wide range of terms (Butruille et al ., ; Osborn et al ., ; Doyle et al ., ; Chalhoub et al ., ) which have obscured both their single causative mode of formation and their ubiquitous occurrence. Homoeologous exchanges are indeed evident in all allopolyploid genomes, including crops ( Coffea arabica , Lashermes et al ., ; Brassica napus , Chalhoub et al ., ; Gossypium hirsutum , Li et al ., ; Brassica juncea and Triticum aestivum , He et al ., ; Arachis hypogaeae , Bertioli et al ., ), wild plant species ( Tragopogon miscellus , Chester et al ., ; Arabidopsis suecica , Henry et al ., ) and some nonplant organisms (e.g. Saccharomyces pastorianus , Usher & Bond, ).…”