The legacy of diploid progenitors in allopolyploid gene expression patterns

Allopolyploidization (hybridization and whole-genome duplication) is a common phenomenon in plant evolution with immediate saltational effects on genome structure and gene expression. New technologies have allowed rapid progress over the past decade in our understanding of the consequences of allopolyploidy. A major question, raised by early pioneer of this field Leslie Gottlieb, concerned the extent to which gene expression differences among duplicate genes present in an allopolyploid are a legacy of expression differences that were already present in the progenitor diploid species. Addressing this question necessitates phylogenetically well-understood natural study systems, appropriate technology, availability of genomic resources and a suitable analytical framework, including a sufficiently detailed and generally accepted terminology. Here, we review these requirements and illustrate their application to a natural study system that Gottlieb worked on and recommended for this purpose: recent allopolyploids of Tragopogon (Asteraceae). We reanalyse recent data from this system within the conceptual framework of parental legacies on duplicate gene expression in allopolyploids. On a broader level, we highlight the intellectual connection between Gottlieb's phrasing of this issue and the more contemporary framework of cis- versus trans- regulation of duplicate gene expression in allopolyploid plants.

Insights into the evolution of duplicate gene expression in polyploids from GossypiumThis paper is one of a selection of papers published in the Special Issue on Systematics Research.

Polyploidy is a prominent mechanism of speciation in plants that can lead to novel phenotypes. Polyploidy is characterized by novel genetic and genomic consequences that provide raw material for morphological evolution. Polyploids often exhibit changes in genome organization and gene expression compared with their diploid progenitors. The five allopolyploid cotton (Gossypium) species and newly created cotton neopolyploids have been developed as a useful group for studies of duplicated gene expression in polyploids. Here I review recent studies on the evolution of duplicate gene expression in polyploid cotton. In addition I present new expression data from cotton neopolyploids that address the effects on expression of adding a third genome in an allohexaploid, and that provide insights into fine scale organ-specific silencing. Substantial changes in gene expression have occurred in homoeologous genes (gene pairs duplicated by polyploidy), including organ-specific gene silencing and subfunctionalization. Many of the changes in gene expression have occurred on an evolutionary timescale, whereas others occur immediately after genome merger and within a few generations. Abiotic stress can affect the expression of homoeologous gene expression, causing expression partitioning between homoeologs. To examine the effects of interspecific hybridization, without chromosome doubling, on gene expression, interspecific hybrids have been studied. Extensive variation in allelic expression was observed upon hybridization that varied by gene, organ, and genotype. Several hypotheses have been proposed for why gene expression is altered in allopolyploids and interspecific hybrids.