Genomics of Evolutionary Novelty in Hybrids and Polyploids.

Gonzalo Nieto Feliner,Josep Casacuberta,Jonathan F Wendel

doi:10.3389/fgene.2020.00792

Gonzalo Nieto Feliner, Josep Casacuberta + Show 1 more

Open Access

https://doi.org/10.3389/fgene.2020.00792

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Abstract

It has long been recognized that hybridization and polyploidy are prominent processes in plant evolution. Although classically recognized as significant in speciation and adaptation, recognition of the importance of interspecific gene flow has dramatically increased during the genomics era, concomitant with an unending flood of empirical examples, with or without genome doubling. Interspecific gene flow is thus increasingly thought to lead to evolutionary innovation and diversification, via adaptive introgression, homoploid hybrid speciation and allopolyploid speciation. Less well understood, however, are the suite of genetic and genomic mechanisms set in motion by the merger of differentiated genomes, and the temporal scale over which recombinational complexity mediated by gene flow might be expressed and exposed to natural selection. We focus on these issues here, considering the types of molecular genetic and genomic processes that might be set in motion by the saltational event of genome merger between two diverged species, either with or without genome doubling, and how these various processes can contribute to novel phenotypes. Genetic mechanisms include the infusion of new alleles and the genesis of novel structural variation including translocations and inversions, homoeologous exchanges, transposable element mobilization and novel insertional effects, presence-absence variation and copy number variation. Polyploidy generates massive transcriptomic and regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory factors, small RNAs and other genome interactions that cascade from single-gene expression change up through entire networks of transformed regulatory modules. We highlight both these novel combinatorial possibilities and the range of temporal scales over which such complexity might be generated, and thus exposed to natural selection and drift.

Highlights

The observation that hybridization is associated with allopolyploid speciation has long been recognized, and this became fundamental in plant evolutionary thinking, with the original evidence primarily consisting of cytological observations that peaked in the 1970s (Stebbins, 1940, 1971; Grant, 1981)
Given the scale and scope of Structural variants (SVs) in all plants studied to date, it seems likely that their role in adaptive processes will increasingly be recognized as important, and especially in the adaptation and diversification of nascent allopolyploids, which are forged from the merger of two genomes that bring to the union differing suites of SVs
We know that duplicated genes experience a diversity of evolutionary trajectories, being either lost, epigenetically silenced, or retained but with altered expression regulation and possible neofunctionalization or subfunctionalization, and that some of these outcomes may be tissue or organ-specific

Summary

Introduction

One of the remarkable realizations of the genomics era is that hybridization—crosses between individuals from populations that are distinguishable on the basis of one or more heritable characters (Harrison, 1990)—and interspecific gene flow—the successful movement of genes among populations (Ellstrand, 2014)—are far more prevalent than previously recognized.Genomics of Evolutionary NoveltyGenomic data from a wide range of model and non-model organisms have both confirmed and greatly extended the pre-existing notion that natural hybridization is a frequent phenomenon in the living world, and in plants (Mallet, 2005; Soltis and Soltis, 2009; Green et al, 2010; Fontaine et al, 2015; Leducq et al, 2016; Elgvin et al, 2017; Meier et al, 2017; Lamichhaney et al, 2018), and that it often leads to interspecific gene flow. Divergence is associated with changes in gene sequence, either in coding or regulatory sequences, and genomic reunions associated with hybridization and/or WGD may lead to new genic contexts with possible effects on selectively relevant phenotypes (Figure 1).

Results

Conclusion