A hallmark of angiosperm genome organization is gene redundancy. Redundant genome segments have been identified in the composition and architecture of modern-day angiosperm genomes suggesting one or more ancient genome duplication events [1
]. This has led to considerable interest in the evolution of the resulting duplicated genes. A key issue has been the identification of factors that enhance the retention of duplicate gene pairs and their potential for adaptive diversification or subfunctionalization (the partitioning of ancestral function). Mechanisms such as the maintenance of gene dosage and epistatic interactions [4
] and epigenetically regulated expression subfunctionalization [6
] have been implicated in aiding duplicate gene retention. These processes describe mechanisms of retention for ancient
duplicate genes and naturally lead to questions about the evolutionary behavior of duplicate gene pairs in more recently formed polyploid species.
Members of the cotton genus provide a phylogenetic framework to study the evolution of duplicate gene expression in recent polyploids because five diverse allopolyploid species are thought to have diverged from a single allopolyploidization event [8
], and models of the ancestral diploid progenitor species (denoted by A2
) have been identified (Figure ). In addition, extensive genomic resources, such as comprehensive expressed sequence tag (EST) libraries [9
], microarray platforms [10
], and BAC libraries [12
] have greatly extended research capabilities. Synthesis of an F1
hybrid, combining the A- and D-genome diploid model species, offers the opportunity to untangle the effects of genomic merger from those arising from genome doubling and subsequent evolutionary change. This phylogenetic framework facilitates the study of gene expression from co-resident genomes on two temporal scales, from the onset of hybridization to a longer-term evolutionary timeframe encompassed by the natural allotetraploid species.
Figure 1 Phylogenetic context and inference of homoeologous expression evolution in Gossypium. (A) Phylogentic relationships among the cotton accessions used in this study. An allopolyploidy event between A- and D-genome diploid species (red star) created modern (more ...)
Adams et al [6
] demonstrated that homoeolog expression in allotetraploid cotton has been strongly influenced by developmentally regulated, organ-specific silencing, resulting in subfunctionalization of the aggregate ancestral expression profile. This subfunctionalization may occur immediately after polyploidization or may arise over a longer period of evolutionary resolution [13
]. The net effect is a process that appears to impose a form of selective retention on both homoeologs. Thus, expression subfunctionalization leads to prolonged duplicate gene retention, which may in turn enhance the potential for spatial, temporal, or functional divergence of duplicated genes.
Here we employ a novel microarray technology, which uses homoeolog specific probe sets, to assess the relative contribution of 1,383 homoeologous gene pairs to the transcriptome of natural allopolyploid Gossypium hirsutum and a synthetic, diploid F1 hybrid (denoted as AD1 and F1, respectively). We show that the two genomes contribute unequally to the total transcriptome of the allopolyploid. By comparing these entities we demonstrate that, for a substantial fraction of the genome, homoeolog expression biases occur immediately with the onset of genomic merger. In addition, a greater number of homoeolog expression biases appear in allopolyploid cotton that likely were not instigated by genomic merger. These findings indicate that upon allopolyploid formation, homoeolog expression biases happen in two, distinct temporal phases.