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

Abstract

SummaryStructural variation is a major source of genetic diversity and an important substrate for selection. In allopolyploids, homoeologous exchanges (i.e. between the constituent subgenomes) are a very frequent type of structural variant. However, their direct impact on gene content and gene expression had not been determined.Here, we used a tissue-specific mRNA-Seq dataset to measure the consequences of homoeologous exchanges (HE) on gene expression in Brassica napus, a representative allotetraploid crop.We demonstrate that expression changes are proportional to the change in gene copy number triggered by the HEs. Thus, when homoeologous gene pairs have unbalanced transcriptional contributions before the HE, duplication of one copy does not accurately compensate for loss of the other and combined homoeologue expression also changes. These effects are, however, mitigated over time.This study sheds light on the origins, timing and functional consequences of homeologous exchanges in allopolyploids. It demonstrates that the interplay between new structural variation and the resulting impacts on gene expression, influences allopolyploid genome evolution.

Inherited allelic variants and novel karyotype changes influence fertility and genome stability in Brassica allohexaploids

“…In Population III the fixed translocation of a fragment from chromosome A07 to chromosome C6 had no significant influence on fertility. The presence of this translocation in one of two parents of a B. napus mapping population has previously been shown to reduce fertility (Lloyd et al ., ). In synthetic B. napus hybrids translocations between the A and C subgenomes were reported to be biased towards accumulation of translocations in which A‐genome fragments replace large fragments of the C subgenome (Samans et al ., ), which also may indicate selection against translocations in the other direction due to negative effects on fertility.…”

“…In Population I the complete loss of univalent chromosomes B3 and B7 did have a negative impact on plant fertility, possibly related to one or more genes present on these particular chromosomes. Many complex cellular mechanisms that determine plant fertility are governed by genes requiring specific dosage balance and simultaneous expression (Lloyd et al ., ), and whose loss is therefore expected to reduce fertility. A multitude of gene dosage/copy number‐dependent traits have been identified in B. napus , some influencing plant reproductive systems such as flowering time (Schiessl et al ., ).…”

DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids

“…The most pervasive and immediate genetic consequence of nascent polyploidy is disruption of normal meiosis due to mismatches between the meiotic machinery of diploids that now must adapt to handle the abruptly doubled chromosome set (Hollister, ; Mercier et al ., ; Bomblies et al ., ). Consequently, multivalents and univalents occur due to compromised pairing fidelity, resulting in homoeologous exchanges (HEs) and aneuploidy (Pecinka et al ., ; Higgins et al ., ; Lloyd et al ., ). Conceivably, while most aneuploidies that cause deficiency and/or chromosome‐wide dosage imbalance will be rapidly purged due to lethality or lack of fitness, many progenies with HEs may remain and be transgenerationally persistent due to the frequent (Gou et al ., ), but not ever‐present (Zhang et al ., ; Gong et al ., ; Lloyd et al ., ), mutual functional compensation of homoeologs (Xiong et al ., ; Chester et al ., ).…”

“…Consequently, multivalents and univalents occur due to compromised pairing fidelity, resulting in homoeologous exchanges (HEs) and aneuploidy (Pecinka et al ., ; Higgins et al ., ; Lloyd et al ., ). Conceivably, while most aneuploidies that cause deficiency and/or chromosome‐wide dosage imbalance will be rapidly purged due to lethality or lack of fitness, many progenies with HEs may remain and be transgenerationally persistent due to the frequent (Gou et al ., ), but not ever‐present (Zhang et al ., ; Gong et al ., ; Lloyd et al ., ), mutual functional compensation of homoeologs (Xiong et al ., ; Chester et al ., ). HEs generate alterations of the otherwise 2 : 2 homoeolog ratio, and hence may impact epigenetic stabilities (e.g.…”

“…It was recently shown in allotetraploid rapeseed ( Brassica napus ) that significant and nonadditive gene expression alterations can be traced to HEs (Lloyd et al ., ). However, it remains unclear if and to what extent changes in DNA methylation are correlated with HEs and gene expression.…”