Abstract
Polyploidization can have a significant ecological and evolutionary impact by providing substantially more genetic material that may result in novel phenotypes upon which selection may act. While the effects of polyploidization are broadly reviewed across the plant tree of life, the reproducibility of these effects within naturally occurring, independently formed polyploids is poorly characterized. The flowering plant genus Tragopogon (Asteraceae) offers a rare glimpse into the intricacies of repeated allopolyploid formation with both nascent (< 90 years old) and more ancient (mesopolyploids) formations. Neo- and mesopolyploids in Tragopogon have formed repeatedly and have extant diploid progenitors that facilitate the comparison of genome evolution after polyploidization across a broad span of evolutionary time. Here, we examine four independently formed lineages of the mesopolyploid Tragopogon castellanus for homoeolog expression changes and fractionation after polyploidization. We show that expression changes are remarkably similar among these independently formed polyploid populations with large convergence among expressed loci, moderate convergence among loci lost, and stochastic silencing. We further compare and contrast these results for T. castellanus with two nascent Tragopogon allopolyploids. While homoeolog expression bias was balanced in both nascent polyploids and T. castellanus, the degree of additive expression was significantly different, with the mesopolyploid populations demonstrating more non-additive expression. We suggest that gene dosage and expression noise minimization may play a prominent role in regulating gene expression patterns immediately after allopolyploidization as well as deeper into time, and these patterns are conserved across independent polyploid lineages.
Highlights
The consequences of plant polyploidization have been a subject of intense interest for several decades
Polyploids are categorized as either autopolyploids, which are formed from a whole-genome duplication within a single species, or allopolyploids, which are generated by the combination of entire genomes from two different species (Kihara and Ono, 1926)
Both parental species are phylogenetically distinct and appeared as members of two distinct clades based on ITS phylogeny as estimated in Mavrodiev et al (2005); namely, clade Majores s. l. [incl. clade Hebecarpus] (T. crocifolius) and clade Tragopogon (T. lamottei) (Mavrodiev et al, 2008)
Summary
The consequences of plant polyploidization have been a subject of intense interest for several decades (reviewed in Wendel, 2000, 2015; Doyle et al, 2008; Leitch and Leitch, 2008; Van de Peer et al, 2009; Barker et al, 2012; Soltis et al, 2016). Many changes occur in the generations immediately after polyploidization including changes in genome size (reviewed in Soltis et al, 2003; Leitch et al, 2008; Leitch and Leitch, 2013) spanning the extremes in both gain (e.g., Paris japonica Pellicer et al, 2010) and loss (e.g., Utricularia gibba Ibarra-Laclette et al, 2013), expression (Chen and Pikaard, 1997; reviewed in Adams and Wendel, 2005b; Chaudhary et al, 2009; Hu et al, 2015), epigenetic modifications (Shaked et al, 2001; Salmon et al, 2005; reviewed in Chen, 2007; Madlung and Wendel, 2013; Cheng et al, 2016), transposon activity (reviewed in Woodhouse et al, 2014; Vicient and Casacuberta, 2017; Wendel et al, 2018) as well as changes in protein folding and dosage (reviewed in Birchler and Veitia, 2010, 2012; Pires and Conant, 2016) These changes are variable across lineages (Anssour and Baldwin, 2010; reviewed in Soltis et al, 2016) and may occur in repeated cycles (Soltis and Soltis, 1999; Buggs et al, 2012; reviewed in Wendel, 2015; Soltis et al, 2016). Homoeolog functions may diverge from the parentally inherited state such that functions are partitioned between homoeologs (subfunctionalization), or copies may develop novel functionality (neofunctionalization)
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