Abstract

BackgroundAllopolyploid speciation requires rapid evolutionary reconciliation of two diverged genomes and gene regulatory networks. Here we describe global patterns of gene expression accompanying genomic merger and doubling in inter-specific crosses in the cotton genus (Gossypium L.).ResultsEmploying a micro-array platform designed against 40,430 unigenes, we assayed gene expression in two sets of parental diploids and their colchicine-doubled allopolyploid derivatives. Up to half of all genes were differentially expressed among diploids, a striking level of expression evolution among congeners. In the allopolyploids, most genes were expressed at mid-parent levels, but this was achieved via a phenomenon of genome-wide expression dominance, whereby gene expression was either up- or down-regulated to the level of one of the two parents, independent of the magnitude of gene expression. This massive expression dominance was approximately equal with respect to direction (up- or down-regulation), and the same diploid parent could be either the dominant or the recessive genome depending on the specific genomic combination. Transgressive up- and down-regulation were also common in the allopolyploids, both for genes equivalently or differentially expressed between the parents.ConclusionOur data provide novel insights into the architecture of gene expression in the allopolyploid nucleus, raise questions regarding the responsible underlying mechanisms of genome dominance, and provide clues into the enigma of the evolutionary prevalence of allopolyploids.

Highlights

  • Allopolyploid speciation requires rapid evolutionary reconciliation of two diverged genomes and gene regulatory networks

  • We first evaluated differential expression between the two diploid parents involved in each cross (G. arboreum (A2) and G. bickii (G1); G. arboreum (A2) and G. thurberi (D1)), postulating that the degree of parental divergence would be correlated with the amount of non-additivity in their respective synthetic allopolyploid (2(A2D1) and 2(A2G1))

  • As all plants were grown under common controlled conditions, we expected only modest expression differentiation among diploids, but high levels of expression divergence were observed; 42.0% and 53.0% of the 40,300 unigenes were differentially expressed between G. arboreum (A-genome group) and G. bickii (G-genome group), and G. arboreum and G. thurberi (D-genome group), respectively (Figures 1 and 2, panels A)

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Summary

Introduction

Allopolyploid speciation requires rapid evolutionary reconciliation of two diverged genomes and gene regulatory networks. We describe global patterns of gene expression accompanying genomic merger and doubling in inter-specific crosses in the cotton genus (Gossypium L.). The reunion of two diverged genomes in a common nucleus during allopolyploid speciation entails a suite of genomic accommodations [1214], including non-additivity of gene expression [15,16], and expression partitioning among tissues and organs (page number not for citation purposes). We detected a diverse spectrum of transgressive gene expression types and levels. These results provide a novel perspective on allopolyploid gene regulation and hint at the underlying genetic basis of allopolyploid adaptation

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