Polyploidy: Pitfalls and paths to a paradigm

Abstract

Investigators have long searched for a polyploidy paradigm-rules or principles that might be common following polyploidization (whole-genome duplication, WGD). Here we attempt to integrate what is known across the more thoroughly investigated polyploid systems on topics ranging from genetics to ecology. We found that while certain rules may govern gene retention and loss, systems vary in the prevalence of gene silencing vs. homeolog loss, chromosomal change, the presence of a dominant genome (in allopolyploids), and the relative importance of hybridization vs. genome doubling per se. In some lineages, aspects of polyploidization are repeated across multiple origins, but in other species multiple origins behave more stochastically in terms of genetic and phenotypic change. Our investigation also reveals that the path to synthesis is hindered by numerous gaps in our knowledge of even the best-known systems. Particularly concerning is the absence of linkage between genotype and phenotype. Moreover, most recent studies have focused on the genetic and genomic attributes of polyploidy, but rarely is there an ecological or physiological context. To promote a path to a polyploidy paradigm (or paradigms), we propose a major community goal over the next 10-20 yr to fill the gaps in our knowledge of well-studied polyploids. Before a meaningful synthesis is possible, more complete data sets are needed for comparison-systems that include comparable genetic, genomic, chromosomal, proteomic, as well as morphological, physiological, and ecological data. Also needed are more natural evolutionary model systems, as most of what we know about polyploidy continues to come from a few crop and genetic models, systems that often lack the ecological context inherent in natural systems and necessary for understanding the drivers of biodiversity.

Genetic mapping in polyploids

“…In these cases it is not always clear whether we are dealing with an autopolyploid that is gradually becoming rediploidised, or an allopolyploid from two very closely-related species (Soltis et al, 2016).…”

“…As alluded to already, intermediate modes of inheritance are theoretically possible if partially-preferential pairing occurs between homologues, resulting in on average more recombinations between certain homologues, and less between others (putative homoeologues). This intermediate inheritance pattern, originally termed segmental allopolyploidy (Stebbins, 1947) and more recently termed mixosomy (Soltis et al, 2016), poses additional challenges over those of purely polysomic or disomic behaviour. One of the main complications is the lack of fixed segregation ratios to test markers against (Allendorf and Danzmann, 1997), which is often used as a measure of marker quality (Stringham and Boehnke, 1996;Pompanon et al, 2005).…”

“…Again this category can be defined from a taxonomic perspective or a genetic perspective -as a hybridisation between two very closely-related species or subspecies, or as a polyploid which demonstrates a meiotic ___________________________________________________________________________________ Chapter 1 pairing behaviour that cannot be classified as fully disomic or fully polysomic (recently termed "mixosomic" (Soltis et al, 2016)). Throughout this thesis we rely on the genetic definition, as it is the pairing behaviour that influences how homologues recombine, upon which our methods to study inheritance are ultimately based.…”

“…Among allopolyploids, allohexaploid wheat (Triticum aestivum L.) is probably the most well-studied. If pairing and recombination between homoeologues occurs to a limited extent, the species may be referred to as "segmental allopolyploid" (Stebbins, 1947), traditionally deemed to have arisen from hybridisation between very closely-related species (Stebbins, 1947;Chester et al, 2012) but which may also be the result of partiallydiploidised autopolyploidy (Soltis et al, 2016). In many cases, a species cannot be clearly designated as one type or another, leading to uncertainty or debate on the subject Doyle and Sherman-Broyles, 2016).…”

“…Autopolyploids (and segmental allopolyploids) do not behave like diploids, and are therefore in most need of specialised methods and tools for subsequent genetic studies. In this review we focus primarily on the availability of tools and resources amenable to polysomic (and "mixosomic" (Soltis et al, 2016)) species, with less emphasis on allopolyploid-specific solutions. Although the development of novel methodologies for the genetic analysis of polyploids are interesting, without translation into a software tool for use by the research community they remain purely conceptual and with limited impact.…”