Homoeolog expression bias and expression level dominance in allopolyploids.

Polyploidy is now recognized as a characteristic feature of all angiosperm genomes (Jiao et al., 2011), and remains an important speciation process today (Wendel, 2000; Comai, 2005; Doyle et al., 2008; Leitch & Leitch, 2008; Soltis & Soltis, 2009; Soltis et al., 2010). In allopolyploids, genomic merger and doubling are associated with myriad non-Mendelian interactions and processes, including sequence elimination (Shaked et al., 2001; Ozkan et al., 2003; Han et al., 2005; Skalicka et al., 2005; Anssour et al., 2009; Tate et al., 2009; Jackson & Chen, 2010), alterations of epigenetic marks (Shaked et al., 2001;Madlung et al., 2002; Rapp&Wendel, 2005; Chen, 2007; Doyle et al., 2008; Kovarik et al., 2008b; Soltis & Soltis, 2009; Soltis et al., 2010), activation of genes and retroelements (O’Neill et al., 1998; Kashkush et al., 2003; Kraitshtein et al., 2010) and several kinds of homoeologous interactions and exchanges (Gaeta et al., 2007; Kovarik et al., 2008a; Salmon et al., 2010; Szadkowski et al., 2010). Changes in duplicate gene expression are no less diverse, spanning the spectrum from expression conservation, relative to that of the diploid progenitors, to silencing of one homoeolog, to novel patterns of upand down-regulation (transgressive expression). Each of these transcriptomic responses varies in magnitude among allopolyploid species and individuals, among tissues and organ types within any one system, and with respect to the time since polyploid formation (Flagel et al., 2008; Flagel & Wendel, 2010). The phenotypic consequences of alterations in gene expression associated with hybridization and polyploidy are many and varied (Ni et al., 2009; Swanson-Wagner et al., 2009), underscoring the importance of understanding the expression level consequences of genomemerger and doubling. The advent and subsequent widespread utilization ofmicroarray and next-generation sequencing technologies has led to a rapid increase in explorations of gene expression in a variety of polyploid plants. These many efforts have generated a sufficient body of empirical data that generalizations are beginning to emerge concerning transcriptome changes in allopolyploids. For example, in every allopolyploid examined to date, some fraction of the duplicate gene pairs will be expressed unequally, and this suite of unequally expressed genes may itself favor one of the co-resident genomes, leading to a transcriptome that is unequally expressed with respect to the component genomes. While these generalizations are broadly applicable, much remains to be learned regarding the mechanistic underpinnings of duplicate gene expression change, the proximate and ultimate causes of inter-taxon and inter-organ variation in the response dynamics to polyploidy, and the functional, ecological, and evolutionary significance of duplicate gene expression modification. In addition to unequal expression of two homoeologs, other phenomena have been described which are even more poorly understood and for which fewer examples have yet been published. One of these is the concept of genome dominance (or genome expression dominance), which describes the expression condition in an allopolyploid where, for a given gene, the total expression of homoeologs is statistically the same as only one of the polyploid parents. This phenomenon was originally described for cotton allopolyploids by Rapp et al. (2009), confirmed and extended by Flagel & Wendel (2010), and subsequently described for both Spartina (Chelaifa et al., 2010) and Coffea (Bardil et al., 2011). This phenomenon is distinct from homoeolog expression bias (sometimes referred to as transcriptome dominance on a genome-wide basis), which describes the relative expression of homoeologs. Moreover, similar words are being used for rather different phenomena. Schnable et al. (2011), for example, invoked the term genomic dominance in maize, in a paper in which they demonstrated that the two subgenomes derived from the most recent polyploidy event in maize have experienced differential gene loss, with an accompanying gene expression bias favoring the more conserved subgenome (Schnable et al., 2011). By other accounts (Chen, 2007; Flagel & Wendel, 2010), this would be considered homoeolog expression bias (or transcriptome dominance) of ancient homoeologs. This inconsistency of conceptual application of the term genomic dominance also applies to the preferential expression of one subgenome of wheat (Akhunova et al., 2010), and to the patterns of biased expression in the fractionated subgenomes of paleohexaploid Brassica rapa (Cheng et al., 2012; Tang et al., 2012). This semantic and conceptual confusion appears to be gaining foothold in the literature; the phenomenon of preferential expression of one parental genome relative to the other in a polyploid species is termed genomic dominance in two recent reviews (Freeling et al., 2012; Schnable et al., 2012), citing both Schnable et al. (2011) and Flagel & Wendel (2010), and the term has also been applied to genomic modifications (Nicolas et al., 2012). Further complicating matters is the classical genetic concept associated with the term ‘dominance’, which conveys the relative expression hierarchy among a set of alleles. Against this backdrop of terminological and conceptual inconsistency, we thought it might be useful to briefly review the primary phenotypes of gene expression modification associated with allopolyploidy. Toward that end we describe and distinguish expression pattern changes observed in hybrid and polyploid species, and suggest a terminology (homoeolog expression bias and expression level dominance; Table 1; Fig. 1) that we hope will increase clarity of communication.