Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing

Abstract

Most eukaryotes have genomes that exhibit high levels of gene redundancy, much of which seems to have arisen from one or more cycles of genome doubling. Polyploidy has been particularly prominent during flowering plant evolution, yielding duplicated genes (homoeologs) whose expression may be retained or lost either as an immediate consequence of polyploidization or on an evolutionary timescale. Expression of 40 homoeologous gene pairs was assayed by cDNA-single-stranded conformation polymorphism in natural (1-to 2-million-yr-old) and synthetic tetraploid cotton (Gossypium) to determine whether homoeologous gene pairs are expressed at equal levels after polyploid formation. Silencing or unequal expression of one homoeolog was documented for 10 of 40 genes examined in ovules of Gossypium hirsutum. Assays of homoeolog expression in 10 organs revealed variable expression levels and silencing, depending on the gene and organ examined. Remarkably, silencing and biased expression of some gene pairs are reciprocal and developmentally regulated, with one homoeolog showing silencing in some organs and the other being silenced in other organs, suggesting rapid subfunctionalization. Duplicate gene expression was examined in additional natural polyploids to characterize the pace at which expression alteration evolves. Analysis of a synthetic tetraploid revealed homoeolog expression and silencing patterns that sometimes mirrored those of the natural tetraploid. Both long-term and immediate responses to polyploidization were implicated. Data suggest that some silencing events are epigenetically induced during the allopolyploidization process.

Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement

“…13). However, in a specific tissue or developmental stage, 20-40% of homoeologous gene pairs showed biased A-or D-homoeolog expression (Supplementary Table 17), which is consistent with the published data 4,34 and may lead to subfunctionalization because of expression divergence 35 . There were slightly more genes with expression bias toward the D homoeologs than toward the A homoeologs (Supplementary Fig.…”

The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection

“…The short read lengths of next-generation sequencing hinder assembly through complex regions, and fragmented draft and reference genomes usually lack skewed (G+C)-content sequences and repetitive intergenic sequences. Furthermore, in allopolyploid species, homoeolog expression dominance or bias, and specifically differential homoelog gene expression, has often been detected, for instance in Gossypium [15][16][17] Triticum 18,19 and Arabidopsis 20,21 , but the role of this phenomenon in selection for phenotypic traits remains mechanistically mysterious 22 .…”

Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

“…Doubling a single 'diploid' genome results in an autotetraploid, while doubling chromosomes in interspecific hybrids leads to the production of allotetraploids. Using this method, many synthetic (newly created or human-made) allopolyploids, including Brassica (combination of any two genomes among Brassica oleracea, B. rapa and B. nigra), (28,29) cotton (Gossypium aboreum x G. thurberi or G. bickii), (30,31) wheat (T. monococcum x Aegilops sharonensis), (32,33) and Triticale (Triticum x Secale), (34) have been generated de novo in the laboratory. Synthetic polyploids are excellent genetic materials for comparative analysis of gene expression and genomic changes in the early stages of polyploid formation because the exact progenitors are known, whereas the progenitors of many natural allopolyploids, except such recent polyploids as Spartina, (35) Tragopogon (36) and Senecio, (37) are unknown or unavailable.…”

“…Silenced rRNA genes are reactivated in floral organs, which suggests a developmental role of activated or silenced homoeologous genes in allopolyploids, (84) which argues against the notion that reactivation of silenced RNA genes in microspores (pollen) is due to separation of repressors during meiosis. (75) In cotton many if not most homoeologous genes that display unequal expression in allotetraploids exhibit organ-specific expression patterns (30) (Fig. 2B, A3).…”