REVIEW published: 28 July 2020 doi: 10.3389/fgene.2020.00792 Genomics of Evolutionary Novelty in Hybrids and Polyploids Gonzalo Nieto Feliner 1* , Josep Casacuberta 2 and Jonathan F. Wendel 3 1 Department of Biodiversity and Conservation, Real Jardín Botánico, CSIC, Madrid, Spain, 2 Center for Research in Agricultural Genomics, CRAG (CSIC-IRTA-UAB-UB), Barcelona, Spain, 3 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, United States 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 Edited by: selection. We focus on these issues here, considering the types of molecular genetic Jianping Wang, University of Florida, United States and genomic processes that might be set in motion by the saltational event of Reviewed by: genome merger between two diverged species, either with or without genome Jeffrey Joseph Doyle, doubling, and how these various processes can contribute to novel phenotypes. Cornell University, United States Genetic mechanisms include the infusion of new alleles and the genesis of novel Douglas Soltis, University of Florida, United States structural variation including translocations and inversions, homoeologous exchanges, Jeremy Coate, transposable element mobilization and novel insertional effects, presence-absence Reed College, United States, in collaboration with reviewer JD variation and copy number variation. Polyploidy generates massive transcriptomic and *Correspondence: regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory Gonzalo Nieto Feliner factors, small RNAs and other genome interactions that cascade from single-gene nieto@rjb.csic.es expression change up through entire networks of transformed regulatory modules. We Specialty section: highlight both these novel combinatorial possibilities and the range of temporal scales This article was submitted to over which such complexity might be generated, and thus exposed to natural selection Plant Genomics, and drift. a section of the journal Frontiers in Genetics Keywords: adaptation, allopolyploidy, gene and genome duplication, transposable elements, hybridization, Received: 28 April 2020 phenotypic novelty, radiation lag-time model Accepted: 03 July 2020 Published: 28 July 2020 Citation: INTRODUCTION Nieto Feliner G, Casacuberta J and Wendel JF (2020) Genomics One of the remarkable realizations of the genomics era is that hybridization—crosses between of Evolutionary Novelty in Hybrids individuals from populations that are distinguishable on the basis of one or more heritable and Polyploids. Front. Genet. 11:792. characters (Harrison, 1990)—and interspecific gene flow—the successful movement of genes doi: 10.3389/fgene.2020.00792 among populations (Ellstrand, 2014)—are far more prevalent than previously recognized. Frontiers in Genetics | www.frontiersin.org 1 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty Genomic data from a wide range of model and non-model Abbott et al., 2016; Payseur and Rieseberg, 2016) have revealed organisms have both confirmed and greatly extended the numerous hybrid lineages across the living world. Ever since pre-existing notion that natural hybridization is a frequent hybridization and introgression started to be inferred from phenomenon in the living world, and not only in plants (Mallet, incongruence between gene-trees, it has been realized that an 2005; Soltis and Soltis, 2009; Green et al., 2010; Fontaine et al., alternative neutral process—incomplete lineage sorting (ILS) or 2015; Leducq et al., 2016; Elgvin et al., 2017; Meier et al., 2017; deep coalescence—could lead to similar phylogenetic patterns. Lamichhaney et al., 2018), and that it often leads to interspecific Favored by large populations sizes and short speciation times, the gene flow. The observation that hybridization is associated with occurrence of ILS is still often inferred whenever evidence for allopolyploid speciation has long been recognized, and in fact introgression is lacking. However, a number of methodological this became fundamental in plant evolutionary thinking, with the approaches, the most widely used of which is the ABBA-BABA original evidence primarily consisting of cytological observations test, are now available to tease apart the two phenomena (Joly that peaked in the 1970s (Stebbins, 1940, 1971; Grant, 1981). The et al., 2009; Green et al., 2010; Blanco-Pastor et al., 2012). What advent of molecular markers magnified this interest, stimulating remains a matter of some debate is how often hybridization plays research into polyploidy across the phylogenetic spectrum of a creative role in evolution, or phrased alternatively, whether the angiosperms and using both natural and synthetic allopolyploids advantages accrued from natural hybridization are responsible (reviewed in, e.g., Soltis and Soltis, 2012; Soltis et al., 2015, 2016; for the pervasiveness of this phenomenon. The influential ideas Van de Peer et al., 2017). This interest continues apace today, as of Mayr (1963) that hybridization was an evolutionary dead- evidenced by the present special issue of Frontiers. end began to be challenged after breakthrough discoveries in Among the more surprising insights to emerge from this birds and insects (Mavárez and Linares, 2008; Grant and Grant, research is that the genomes of all modern angiosperms contain 2009, 2017; Salazar et al., 2010), but the relative importance vestiges of multiple past rounds of polyploidy (Jiao et al., 2011; of hybridization in lineage diversification remains a subject of Soltis et al., 2016; Leebens-Mack et al., 2019; but see Ruprecht active debate. Some posit that hybridization, even if frequent, et al., 2017a), some ancient and in many cases some quite is likely transient in genomes and thus of little evolutionary recent, with each event superimposed on the genomic remnants relevance (Barton, 2013; Servedio et al., 2013); according to this of earlier rounds of doubling. A second realization is that view, merged genomes mostly evolve in the direction of purging each whole genome doubling (WGD) event has been followed incompatibilities (Schumer et al., 2016, 2018). The opposite by incompletely understood genome fractionation processes view, that natural hybridization may contribute positively to (Wendel, 2015; Soltis et al., 2016; Bird et al., 2018; Cheng et al., adaptation, differentiation and speciation, is embraced by many 2018; Wendel et al., 2018), as well as myriad immediate and empirically oriented evolutionary biologists (Rieseberg, 1991; longer-term responses to genome merger and doubling at the Arnold, 1993; Wang et al., 2001; Mallet, 2007; Abbott et al., genomic, expression, and cellular levels (Yoo et al., 2014; Wendel, 2010, 2013; Butlin and Ritchie, 2013; Sætre, 2013; Soltis, 2015; Soltis et al., 2016; Sharbrough et al., 2017; Doyle and Coate, 2013; Yakimowski and Rieseberg, 2014; Grant and Grant, 2019). Thus, the architecture of modern plant genomes reflects, 2017; Nieto Feliner et al., 2017; Ottenburghs, 2018; Wagner, in part, the residuals from the superimposed joint action of 2018), impressed as they are by the ever-increasing number WGD and fractionation, these twin processes encompassing the of discoveries of gene-tree conflict in datasets. In part, these “wondrous cycles of polyploidy” (Wendel, 2015). two views are fueled by the contrast between the burgeoning One consequence of the pervasiveness of polyploidy and its number of lineages that are unveiled by molecular phylogenetic dynamism over time is the widely held view that whole-genome studies to have a hybrid ancestry and the tiny fraction of doubling plays an important role in generating phenotypic cases in which we understand how hybridization may have novelty. This topic has been the subject of speculation for led to adaptation (and/or phenotypically relevant drift) and decades (Levin, 1983; Soltis, 2013; Soltis P. S. et al., 2014; diversification (Schumer et al., 2014). We suspect that this Vanneste et al., 2014; Edger et al., 2015; Tank et al., 2015; Van scarcity of well-understood examples reflects both insufficiency de Peer et al., 2017), but to date the number of cases where in our understanding of the genetic bases of adaptive traits and polyploidy itself has been convincingly connected to specific their inherent diversity and context dependency, as well as the phenotypic innovations remains relatively small. Part of the temporal disconnect between hybridization events (ancient and challenge in demonstrating this connection is that adaptation recent) and adaptation to ecological conditions that may no and diversification take place over a diverse spectrum of time- longer be present. scales, as do the various genomic diversification and fractionation Allopolyploidization and homoploid hybrid speciation, of processes set in motion by polyploidy. course, comprise just two of the many possible evolutionary In addition to hybridization with WGD (allopolyploidy), outcomes of interspecific genetic exchange (Runemark et al., evidence abounds for the occurrence of homoploid hybridization, 2019). Others include reinforcement (Hopkins, 2013), genetic that is, hybridization and gene flow without WGD (Mallet, assimilation (Levin et al., 1996; Ehrenreich and Pfennig, 2016), 2007; Pennisi, 2016; Runemark et al., 2019). Three decades of formation of various kinds of hybrid zones (Barton and Hewitt, molecular phylogenetic studies (e.g., Sang et al., 1995; Barrier 1985; Harrison, 1993; Abbott, 2017), and adaptive or neutral et al., 1999; Blanco-Pastor et al., 2012; García et al., 2017; introgression (Rieseberg and Wendel, 1993; Heliconius Genome Marques et al., 2017; Folk et al., 2018) and more recent genomic Consortium, 2012; Schmickl et al., 2017; Suarez-Gonzalez et al., scrutiny (Baack and Rieseberg, 2007; Twyford and Ennos, 2012; 2018b; Edelman et al., 2019). These many possibilities serve to Frontiers in Genetics | www.frontiersin.org 2 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty illustrate both the prevalence and complexity of the outcomes adaptation, phenotypic novelty, and diversification, as opposed of secondary contact among divergent lineages, and additional, to simply transient effects. Using examples mostly from plants seemingly unlikely possibilities continue to emerge. For instance, we highlight genetic and genomic consequences of genome inter-ploidy gene flow between lineages that “should be” merger that create potentially adaptive phenotypes. Our intention reproductively isolated turns out to characterize the evolution of is not to be comprehensive nor encyclopedic, but instead to many allopolyploid lineages or diploid-allopolyploid complexes present an overview of the possible mechanisms by which new (Grant, 1981; Zohren et al., 2016; Hohmann and Koch, 2017; phenotypes may arise as a result of interspecific gene flow. As Marburger et al., 2019; Monnahan et al., 2019). an organizational framework, we arrange these effects into three There are also connections between hybrid zones and categories, noting that these are not mutually exclusive and homoploid hybrid speciation (Hodges et al., 1996), and often occur in concert: (1) responses at the genetic and genomic between adaptive introgression and homoploid hybrid speciation level, such as structural diversity or copy number variation; (Brower, 2013). In fact, some authors propose that these (2) responses at the gene expression and regulatory level, such outcomes of hybridization represent different stages of a as neo- and subfunctionalization of duplicated loci; and (3) continuum of speciation (Seehausen et al., 2014; Lowry and responses at combinatorial genomic and expression-levels, such Gould, 2016; Roux C. et al., 2016). This notion illustrates as cytonuclear interactions or transposable element activity. how hybridization usually occurs in a complex spatial and temporal context (Abbott et al., 2013; Sætre, 2013). Multiple different factors, such as levels of divergence and ecological RESPONSES TO GENOME MERGER AT opportunity, may determine whether raw genetic variance THE GENETIC AND GENOMIC LEVEL introduced by hybridization—two to three orders of magnitude greater than that introduced by mutation, according to Genic Introgression Grant and Grant (1994)—facilitates adaptive divergence or Plant genomes vary enormously in virtually every feature contributes to evolutionary novelty. That the ultimate outcomes used to describe their composition or “suite of residents,” of natural hybridization and allopolyploidy depend on numerous including, from the smallest scale to the largest, nucleotide interacting factors sieved by selection over various timescales composition, gene and regulatory sequences, genic content and and ecological contexts makes predictions extremely difficult copy numbers, repetitive sequences and transposable element (Butlin and Ritchie, 2013), and favors expectations that somehow content, chromosome numbers, genome size (Wendel et al., incorporate stochasticity, e.g., an evolutionary novelty hybrid 2016) and a spectrum of epigenetic features. As populations zone model (Arnold, 1997). Examples of this stochasticity in and species diverge, so will their genomes, though not the short term includes hybrid unviability of some genotypes necessarily monotonically across categories of genomic change even in F1 hybrids between conspecific genotypes of an nor homogeneously among lineages. Nonetheless, the divergence inbreeding species (Bomblies and Weigel, 2007) and post-F1 of lineages is inevitably associated with the accumulation of hybrids between species due to Bateson-Dobzhansky-Muller multiple forms of mutational differences, again, small to large. (BDM) incompatibilities and/or breakdown of coadaptive gene At the simplest level, divergence is associated with changes in complexes following recombination (Christe et al., 2016). gene sequence, either in coding or regulatory sequences, and thus Given the numerous avenues by which genetic exchanges genomic reunions associated with hybridization and/or WGD may occur between differentiated genomes, we thought it timely may lead to new genic contexts with possible effects on selectively to consider the question of how this merger might ultimately relevant phenotypes (Figure 1). lead to novel phenotypes and adaptation. We leave aside the In principle, hybridization-induced infusion of diverged or classic but still debated topic of heterosis, which refers to novel genes might be considered the most straightforward the process by which hybrids, including allopolyploids, may form of evolutionarily relevant introgression to detect following exhibit greater biomass, speed of development, and fertility hybridization, as it is a straightforward matter now to assay than both parents (Birchler et al., 2010; Hochholdinger and gene sequences. Accordingly, it is not surprising to find recent Baldauf, 2018). At the outset, hybridization leads to infusion examples of adaptation or at least phenotypic novelty caused of new genetic material, which is either rapidly removed by by genic introgression. An elegant early example was from selection and/or drift, or partially removed, leaving behind Senecio (Kim et al., 2008), who showed that introgression of a transformed genome. But in most cases, even involving the RAY locus from the diploid hybrid species S. squalidus iconic examples such as Iris (Martin et al., 2006), Helianthus into the tetraploid S. vulgaris causes the formation of bilaterally (Rieseberg et al., 2003), and Populus (Suarez-Gonzalez et al., symmetrical flowers (ray florets) on the periphery of the 2016, 2018b) the specific identity and connections between heads that otherwise are discoid. The introgressed RAY locus introgressed material and adaptive phenotypes remains elusive comprises a cluster of cycloidea-like genes, which encode DNA- or at least incompletely defined. In this light, and perhaps as binding proteins known to cause asymmetry in Antirrhinum a form of foreshadowing, we therefore consider the spectrum (Luo et al., 1996). One of the more remarkable features of the of novel molecular genetic and genomic processes that may introgressed RAY locus story is that the gene flow surmounted be set in motion by the saltational genomic shock of merger, a seemingly improbable reproductive barrier, from diploid to both with and without genome doubling. Our focus is on the tetraploid. How this occurs is unclear, but interploidal gene possible selective advantages of hybridized genomes that lead to flow is a recurring theme (see below). An added notable Frontiers in Genetics | www.frontiersin.org 3 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty Coding or regulatory sequences Introgression of new alleles Homoeolog exchanges Ortholog divergence Gene and genome duplication Genic gain and loss Interaction of subfunctionalized TE content Gene expression homoeologs changes due to whole genome effects Neo- and subfunctionalization of duplicated TFs F1 WGD TFTF tarjet target changes for miRNA in allopolyploids Demethylation (overexpression) Genome size of a homoeolog Promoter DNA methylation Chromosomal divergence TE-promoted Adaptation to cold, photoperiods... LD blocks Cytonuclear divergence TE-induced changes of gene New stress responses CN variation of genes and repeats expression Homoeologous Increased seed oil content network rewiring Divergence of Genome merger Potential causes of diploid lineages and doubling phenotypic novelty Evolutionary time FIGURE 1 | Schematic evolutionary diagram depicting changes accompanying divergence of two diploid lineages, followed by phenomena enabled by or set in motion by hybridization and genome doubling, either separately or together. Shown is a sampling of genetic and genomic mechanisms subsequent to hybridization and an allopolyploid event that could, over time (arrow at bottom), lead to novel adaptation and phenotypes. Many of these phenomena and consequences may be latent for hundreds to millions of years. Box colors indicate categories of change in the order discussed in the text: responses at the genomic and genetic level (green); responses at the gene expression and regulatory level (cyan); responses at the combinatorial genomic and expression levels (mauve). See text for elaboration of these and many other examples. CN, copy number; HE, homoeologous exchange; LD, linkage disequilibrium; miRNA, microRNA; TE, transposable element; TF, transcription factor; WGD, whole genome duplication. At present the relative importance and prevalence of these phenomena following hybridization vs. polyploidy is unknown, but in many cases the two organismal-level processes independently set in motion at least some of the illustrated genomic responses. dimension to this example is that the gene flow apparently naïve and native A. lyrata genes, and so selection has favored is adaptive, as ray florets promote outcrossing and thereby their replacement. infuse genetic variation into the otherwise selfing S. vulgaris The preceding examples of adaptive genic introgression (Kim et al., 2008). represent the unusual cases where adaptation has been at least A second beautiful example of inter-ploidal gene flow and arguably causally connected to specific genes. Far more numerous adaptation to the polyploid condition is the paper (Marburger are examples where genomic evidence for adaptive introgression et al., 2019) on diploid and autopolyploid Arabidopsis arenosa is convincing, but either the responsible genes have not been and A. lyrata in Europe. Both species have diploid and identified or they have not been directly linked to phenotypes autopolyploid populations and experience at least occasional that are unequivocally connected to adaptation (Suarez-Gonzalez diploid-tetraploid gene flow. By resequencing 92 individuals et al., 2016, 2018a; Hübner et al., 2019; Janzen et al., 2019; from 30 populations collected from a broad range of both Mitchell et al., 2019). A recent case in point is for cultivated species, Marburger et al. (2019) demonstrate that interspecific sunflowers (Hübner et al., 2019), where genomic resequencing of introgression has occurred bidirectionally, and that some about 400 cultivated lines, Native American landraces and wild A. arenosa introgression peaks into A. lyrata are both narrow accessions from 11 wild species demonstrated that 1.5% of the and associated with strong signatures of selection. Remarkably, genes in cultivated sunflower arose via interspecific introgression these small regions of interspecific introgression include key from wild species. Many of these genes are connected to genes known to be important in stabilizing meiosis following biotic resistance such as downy mildew resistance, implicating WGD, suggesting that adaptation to polyploidy was mediated by selection for disease resistance as being responsible for adaptive interspecific gene flow. A fascinating twist on this story is that interspecific gene flow. Similar examples of either intentional or the A. arenosa alleles introgressed into A. lyrata are posited to unintentional adaptive introgression are common in our major have been favored because WGD in the former species is older cultivated crops (Janzen et al., 2019). than in the latter. Thus, its alleles at meiosis-stabilizing genes The preceding examples all involve either introgression are better adapted to the tetraploid condition than the more between closely related congeners or wild-domesticated Frontiers in Genetics | www.frontiersin.org 4 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty comparisons. In these instances the temporal window for evidence which implicate, but do not prove, that WGD was detecting adaptive introgression may be maximized relative to responsible for evolutionary specializations or adaptations. other scales of divergence, in that as the latter increases, along with time since divergence, there is less certainty with respect to Structural Diversity the relevant ecology (and hence insight into selective pressure). Merger of differentiated genomes leads not only to transfer An interesting recent example in this respect is from Tibetan of genes but also to the incorporation of structural variants Cupressus (Ma et al., 2019), where a variety of transcriptomic in a novel genomic context. Structural variants (SVs) include and population genetic tools were used to demonstrate that differences in copy number (copy number variation; CNV) of adaptation to colder and drier environments in one species genes and repeats, presence-absence variation (PAV), various was enabled via introgression from a second species, perhaps forms of chromosomal change such as inversions (Huang 200,000 years ago. Detecting the footprints of selection will be and Rieseberg, 2020) and translocations, and homoeologous more difficult, however, as equilibrium is restored following exchanges (HEs; see Mason and Wendel, this issue). In fact, selective sweeps. the two or more co-resident genomes of allopolyploids almost Challenges in detecting adaptive introgression are not certainly contain structural variations, which have been shown just restricted to older events, because even recent adaptive to accumulate in all plant genomes studied (Saxena et al., 2014; introgression may be difficult to distinguish from other causes Fuentes et al., 2019; Gabur et al., 2019; Schiessl et al., 2019). of patterns of variation. Clinal variation across environmental Thus, divergence of two diploids is accompanied by the natural gradients, for example, may arise from local differentiation, or, accumulation of structural differences, which then become as in the case of Cupressus cited above (Ma et al., 2019), from combined in a common nucleus during allopolyploidization. asymmetric interspecific introgression (see also, e.g., Welch and The scale of structural variation within and among plant Rieseberg, 2002; Rieseberg et al., 2003; Arnold et al., 2010; species represents an extraordinary discovery of the genomics Scascitelli et al., 2010; Whitney et al., 2010; Leroy et al., 2020). era; that is, rather than SVs being rare, one-off mutants, plant A powerful approach for distinguishing adaptive introgression genomes appear to be rife with this form of diversity, so much from other sources of variation entails the combined use so that “reference genomes” are now widely thought of as of genome-wide tools, now accessible for most non-model providing only a snapshot of the “pangenome” that actually organisms, with demographic and population genetic modeling characterizes a species (or group of species) (Golicz et al., (Pease et al., 2016; Aeschbacher et al., 2017; Martin and Jiggins, 2016; Danilevicz et al., 2020). Different rice lines, for example, 2017; Ma et al., 2019). Genome-wide approaches also provide collectively contain at least 1.5 million SVs (Fuentes et al., 2019), insight into key questions such as whether introgression is and even in a relatively limited sampling of 19 maize inbreds and scattered or localized across the genome, how it has been 14 teosintes, approximately 4000 genes experience either CNV or shaped by selection (Suarez-Gonzalez et al., 2016), and whether PAV (Swanson-Wagner et al., 2010). Similarly, about 9% of the adaptively introgressed alleles had diverged in the donor species 26,000 genes in a sampling of 80 Arabidopsis lines are missing (Parchman et al., 2013; Bay and Ruegg, 2017; Leroy et al., in at least one line (Tan et al., 2012), and in a sampling of 2020). These considerations are finding increasing utility in 115 cucumber lines, variation caused by SVs affects 1676 genes the rescue of genetically impoverished or threatened species (Zhang et al., 2015). Accordingly, there is every reason to suspect (Hamilton and Miller, 2016). that CNVs and PAVs can affect phenotypes and be relevant to These many challenges associated with the passage of time, natural selection and adaptation. historical ecological inference, and interpretation of patterns of Evidence in support of this assertion now abounds, some genetic diversity also apply to our understanding of adaptation from natural systems (Winzer et al., 2012; Flagel et al., 2014), following ancient episodes of polyploidy. In most cases, it is but mostly from the crop literature (e.g., Wang et al., 2015; unknown whether older WGD events involved autopolyploidy Zhang et al., 2015; Gabur et al., 2019; Schiessl et al., 2019). or allopolyploidy, and thus even though it might be clear Importantly, from the standpoint of the present article, examples that there are functionally divergent homoeologs (including from polyploid crops are accumulating (Gaeta et al., 2007; subfunctionalized and neofunctionalized), it is not at all evident Gabur et al., 2019; Schiessl et al., 2019), including oilseed rape whether this divergence represents evolution at the polyploid (Brassica napus), potatoes (Solanum tuberosum), and bread wheat level or whether this reflects merger of pre-existing differences. (Triticum aestivum). Traits for which SVs have been implicated Comparative genomics often, however, yields important clues, as causative include some that are readily envisioned to be as in the example of the butterfly (Pieridae)-glucosinolate “arms responsive to natural selection, such as flowering time and frost race” in the Brassicales (Edger et al., 2015), where gene and tolerance (Gabur et al., 2019; Schiessl et al., 2019). Given the scale genome duplication is implicated in novel chemical defenses in and scope of SVs in all plants studied to date, it seems likely that the plants as well as countermeasures in the butterflies. Similarly their role in adaptive processes will increasingly be recognized as suggestive evidence is common in other plant groups (Sato et al., important, and especially in the adaptation and diversification of 2012; Vanneste et al., 2014; Lohaus and Van de Peer, 2016), nascent allopolyploids, which are forged from the merger of two and certain classes of genes and transcription factors involved in genomes that bring to the union differing suites of SVs. stress responses have been found to be repeatedly preferentially In addition to small scale SVs affecting copy number or retained following WGDs in 25 different angiosperm lineages presence/absence of genes, exons, small repeats and the like, (Wu et al., 2019). These examples collectively provide tantalizing larger structural mutations abound in polyploids, resulting from Frontiers in Genetics | www.frontiersin.org 5 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty processes such as reciprocal and non-reciprocal homoeologous point is the remarkable study by Wang et al. (2018), who exchanges (HEs) (Mason and Wendel, this issue). These showed that in allopolyploid cotton, the suites of Topologically mutations, which affect genomic regions ranging from smaller Associated Domains (TADs) within and between chromosomes telomeric regions to interstitial segments to entire chromosome are significantly altered by allopolyploidy relative to the diploid arms, have the capacity to simultaneously alter genic and progenitors, and that some homoeologous chromosomal regions non-genic PAVs and copy number dosages on a massive become spatially associated whereas others do not. Similarly, scale. Classically recognized as homoeologous translocations or Zhang et al. (2019) recently showed that in autopolyploid transpositions, the genomics era and the successful sequencing Arabidopsis thaliana, chromosome doubling led to an increase of polyploid plants ushered in an increasing realization that in interchromosomal interactions and decreased association of HEs represent a fundamental mechanism of allopolyploid more closely adjacent intrachromosomal sites. The effects of these genome evolution and for generating diversity. Recent illustrative types of spatial and organizational alterations on gene expression examples include peanuts (Arachis hypogaea; Bertioli et al., 2019; dynamics and all of the downstream reverberations that lead to Zhuang et al., 2019), Tragopogon (Chester et al., 2012), quinoa phenotypes are largely unknown. Yet some data are beginning (Chenopodium quinoa; Jarvis et al., 2017), Brassica (Hurgobin to close this circle; Zhang et al. (2019), for example, also showed et al., 2018; Samans et al., 2018), tobacco (Nicotiana tabacum; that the altered chromatin interactions were associated with Chen et al., 2018) and allopolyploid rice (constructed from Oryza specific changes in gene expression and histone modifications sativa subsp. indica × subsp. japonica; Sun et al., 2017; Li C. that might affect phenotypes, including for the key flowering et al., 2019). Increasing evidence suggests that in many systems regulator Flowering Locus C. HEs may occur genome-wide and be sequential, ongoing, and Above the level of the genome, a burgeoning but highly variable in size. In principle, this process can generate a limitless fragmented literature exists bearing on one or more aspects of pool of genetically variable progeny over time, with each genomic the suite of scaling and stoichiometric changes set in motion by combination carrying its own particular suite of chromosome polyploidy, as elegantly and comprehensively reviewed recently segment copy numbers. One might imagine that the immense by Doyle and Coate (2019). Notwithstanding the examples cited range of genomic diversity generated by an ongoing process of in their review and in other parts of the present perspective piece, HE would be paralleled by phenotypic diversity, and thus it the fact remains that nearly all polyploidy-induced phenotypes, might represent a potent force for adaptation and evolutionary structural, metabolic, or physiological, that one might consider change in polyploids. phenotypically relevant to adaptation, in either natural settings Hints that HEs might generate selectively relevant phenotypic or in domesticated plants, represent emergent, downstream diversity during allopolyploid evolution extend back at least to features of complex cascading networks of genic, regulatory and 2007 (Gaeta et al., 2007), and their association with PAVs has biosynthetic programs. As such, it is perhaps unsurprising that now been clearly established (Sun et al., 2017; Hurgobin et al., understanding the “genotype to phenotype” (G-to-P) mapping 2018; Li C. et al., 2019). In Brassica, HEs affect flowering time, equation remains elusive for nearly all traits distinguishing disease resistance, and glucosinolate metabolism (Hurgobin et al., diploid from allopolyploid congeners. Partial solutions to the 2018). In rice allopolyploids, genome-wide gene expression and G-to-P equation are provided for some complex traits using tools methylation states are massively altered by HEs, which also are from multiple “omics” and scales. Examples including ploidy- associated with diverse phenotypes (Sun et al., 2017; Li C. et al., related invasiveness potential in goldenrods (Wuet al., 2020), 2019; and unpubl.); most impressively, these outcomes arise in growth rate and phenotypic traits such as cell size and cell wall even the first few generations of selfing from a single founder composition among A. thaliana plants having different levels following artificial allopolyploid synthesis (e.g., Chester et al., of autopolyploidy (Corneillie et al., 2019), and even the rapid 2012; Sun et al., 2017; Hurgobin et al., 2018), demonstrating that rise to global prominence of angiosperms following ancient HEs likely are a potent force for evolutionary novelty following WGD events (Simonin and Roddy, 2018). As noted by Doyle allopolyploid speciation, at least in some groups. and Coate in citing Don Levin nearly 40 years ago (1983), “the role of polyploidy per se in the development of evolutionary Whole-Genome Effects novelty remains one of the outstanding questions in flowering plant A poorly understood but undoubtedly significant dimension of evolution”. At the same time, Doyle and Coate offer promising polyploidy concerns the evolutionary relevance of the myriad ideas for a research agenda directed at this question, and as cascading effects set in motion by the doubling (in the pointed out elsewhere in the present review, the tools and case of autopolyploidy) or summing of genome sizes into a technologies available today are getting us closer to this holy grail. common nucleus. This additivity, by itself, is known to trigger Some of these are alluded to in the following section. diverse regulatory alterations in gene expression, translation, biosynthesis of metabolites and structures, cells sizes and shapes, organ size, physiology, and almost any aspect of plant RESPONSES AT THE GENE development that one studies. Even at the level of the genome, EXPRESSION AND REGULATORY LEVEL recent studies using chromosome conformation capture, or Hi- C (Grob, 2020), have demonstrated that genome merger and Duplicate Gene Expression Evolution WGD also dramatically alter the positional relationships and One of the revelations of the genomics era, unsurprising in associations among chromosomes in the nucleus. A case in hindsight, is that the merger of two or more differentiated Frontiers in Genetics | www.frontiersin.org 6 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty genomes, in the case of allopolyploidy, or the doubling of a single in terms of protein function if the genes encoded by the two genome, in the case of autopolyploidy, causes massive, genome- homoeologs are functionally equivalent and do not differ in wide alteration in gene expression patterns. These alterations expression domains. Accordingly, evolutionary relevance is more accompany both hybridization and polyploidy separately, likely in situations where different “function” has been inferred encompassing both immediate or short-term consequences of for two homoeologs, either prior to hybridization and WGD genome merger as well as evolved responses that arise over or as an evolved feature subsequent to polyploidization. These thousands to millions of years subsequent to WGD (Flagel two cases are quite different in terms of our understanding et al., 2008). This temporal partitioning is useful when thinking of the timing of evolutionary divergence, that is, whether about the evolutionary relevance of gene expression evolution, homoeolog functional differences arose at the diploid or the as it seems likely that many or perhaps most evolved responses polyploid level. Distinguishing between these two cases often were in fact enabled by relatively ancient polyploidy events, is not possible because the progenitor diploids are unknown but that the adaptive signatures of such evolutionary change or extinct, and in this respect a number of plant genera have remain either obscure or are no longer evident. One example become particularly useful models (Soltis et al., 2016), including of this might be the well-known “radiation lag-time” hypothesis Gossypium, Nicotiana, Arabidopsis, Tragopogon, Senecio, Glycine, (Schranz et al., 2012; but see Tank et al., 2015; Landis et al., Brassica, Spartina, Aegilops-Triticum. 2018), which was proposed to explain an observation of a Functional divergence and other forms of delay, or lag phase, between inferred ancient polyploidy events neofunctionalization of homoeologs involves the acquisition and diversification. Irrespective of the effects of polyploidy of novel expression domains, interactions, or protein function on net diversification rates, the notion that doubled genomes following their merger in a common polyploid nucleus, and it may “have time” to generate adaptive phenotypes represents an is the duplicate gene outcome of most interest to adaptation. important idea for understanding the evolutionary potential of Other possible fates of duplicated genes, not wholly separable polyploidy. Phrased alternatively, unlike the case in conventional from neofunctionalization, include subfunctionalization, where diploids, the additive complement of genes, regulatory elements, ancestral aggregate expression space or function is partitioned and other genomic components that comprise a nascent developmentally or in a tissue-specific fashion following polyploid (auto- or allo-) represent a vast storehouse of raw polyploidy, non-functionalization (mutational loss of one or material for later, and perhaps much later adaptive responses to the other homoeolog), dosage subfunctionalization (Gout environmental change, niche expansion, or any other biotic or and Lynch, 2015), and several other related outcomes. These abiotic evolutionary opportunity. and other possibilities regarding the evolutionary fates of Numerous phenomena and analytical frameworks are gene duplication have been extensively reviewed (e.g., Conant encompassed by the terms “expression evolution” or “regulatory and Wolfe, 2008; Flagel and Wendel, 2009; Panchy et al., evolution,” ranging from those focused on single pairs of 2016; Cheng et al., 2018). While these categorizations are duplicated genes (homoeologs) to others involving entire conceptually useful, most empirical examples defy a simple networks of coexpression for hundreds to thousands of characterization, as divergence often involves multiple steps and duplicated genes. Many of these topics have been amply reviewed various combinations of duplication, loss, subfunctionalization (Yoo et al., 2014; Soltis et al., 2015, 2016; Wendel, 2015; Panchy and neofunctionalization. et al., 2016; Van de Peer et al., 2017; Bird et al., 2018; Cheng An excellent example of neo- and subfunctionalization et al., 2018; Wendel et al., 2018). Here our attention is directed concerns a pair of genes in the Brassicaceae duplicated by a at the connections, known or suspected, between expression or polyploidy event about 23 MYA (Liu and Adams, 2010). The regulatory evolution and plant phenotypes. two paralogs SHORT SUSPENSOR (SSP), involved in paternal An early and illustrative example of differential homoeolog control of zygote elongation in A. thaliana, and Brassinosteroid expression (“homoeolog bias”; Grover et al., 2012), is from Kinase 1 (BSK1), involved in brassinosteroid signal transduction, allopolyploid (AD genome) cotton (Gossypium), where it was have diverged in function, with BSK1 retaining its ancestral shown that the two co-resident, alternative homoeologs (A, D) role in hormone signaling. SSP, however, diverged following had differential contributions to the total transcript pool, and duplication to acquire a role in zygote elongation, while losing that this homoeolog ratio varied widely among genes (Adams its plesiomorphic role in signal transduction through loss of et al., 2003). In the most extreme cases, reciprocal silencing its kinase domain. A second illustrative example concerns the of alternative homoeologs was observed for different tissues; fate of duplicated MADS-box transcription factors in columbine for example, in petals and stamens, only the D homoeolog (Aquilegia) flowers (Sharma and Kramer, 2013). Duplication of was expressed, whereas in ovary walls of the same flower, ancestral APETALA3 genes in the Ranunculaceae appears to have only the A homoeolog was expressed. Whereas not all genes been followed by a combination of neo- and subfunctionalization in every allopolyploid exhibits this degree of homoeolog bias, of different paralogs, while contributing to the evolution of the phenomenon itself is an ubiquitous feature of polyploids a novel floral whorl where the innermost stamens have been (Grover et al., 2012; Yoo et al., 2014), and it may be that there converted to sterile staminodes. A third example concerns are few if any homoeologous gene pairs in any species that the free-threshing Q locus in hexaploid wheat (Zhang et al., contribute equally to the transcript pool in all tissues. Thus, 2011), which encodes an AP2-type transcription factor. This homoeolog bias appears to be a rule rather than an exception. Yet locus has a complex history of duplication and differential differing transcript ratios may not be evolutionarily meaningful paralog loss among diploid wheat lineages during the evolution Frontiers in Genetics | www.frontiersin.org 7 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty of Triticum/Aegilops. Diverged paralogs were reunited in a (Adams et al., 2003, 2004; Flagel et al., 2008; Yoo et al., 2014; common nucleus with polyploid wheat formation, and this Song and Chen, 2015; Ding and Chen, 2018). This regulatory was followed both by protein evolution in one homoeolog and rewiring of the transcriptome likely has numerous combinatorial pseudogenization/subfunctionalization of other homoeologs. causes stemming from altered cell and nuclear volumes (Doyle This example entails a complex combination of ancient and Coate, 2019), biochemical and biophysical stoichiometric paralogy, non-functionalization, reunion of divergent paralogs, disruptions (Bottani et al., 2018; Hu and Wendel, 2019), and and interaction of subfunctionalized homoeologs. These specific changed cis and trans controls on gene expression (Bao et al., examples of post-duplication evolutionary divergence differ 2019). All of these phenomena are related to various forms of greatly in their timing, underlying molecular bases, and epigenetic modification and chromatin remodeling, including ecological settings. It remains to be seen whether commonalities changes in DNA methylation and various histone modifications, in any of these attributes will emerge in the future as additional for both autopolyploids and allopolyploids (Song and Chen, examples are revealed. 2015; Ding and Chen, 2018). In addition to examples involving duplicated genes connected A beautiful example of the relevance of these epigenetic to specific phenotypes, broader surveys of patterns of gene phenomena to novel plant phenotypes associated with retention following polyploidy have implicated certain classes of allopolyploidy concerns flowering time in domesticated genes in morphological innovation or in adaptation to various forms of allotetraploid (AD genome) cotton (Song et al., 2017). environmental conditions. Transcription factors, for example, Wild forms of both Gossypium barbadense and G. hirsutum have been shown to be preferentially retained following ancient contain hypermethylated forms of both homoeologs (A, D) of polyploidy events (De Smet et al., 2013; Li et al., 2016), and CONSTANS-LIKE 2 (COL2) and are photoperiod sensitive. As many of these retained ancient homoeologs later become modern a consequence of domestication, however, DNA methylation paralogs with differing roles in regulatory development and was lost for the D homoeolog, leading to higher expression of plant morphology (reviewed in Rensing, 2014). Schilling et al. COL2D and the all-important photoperiod insensitivity that (2020) studied 201 wheat MIKC-type MADS-box genes, showing allowed cotton production to thrive outside of the subtropics. both preferential retention and even gene family expansion A second example concerns circadian clock genes in Arabidopsis for genes involved in adaptation to different environmental hybrids and allotetraploids (Ni et al., 2009), where histone conditions, abiotic and biotic stresses, and flowering time. These modifications were linked to increased biomass, vigor, and and other studies indicate that transcription factor retention starch accumulation. A third example of an epigenetically and divergence appears to be an important aspect of polyploid mediated plant trait accompanying polyploidy, recent or ancient, diversification. Insight into the nature of this preferential is the possible epigenetic neofunctionalization of a parentally retention was recently provided by Panchy et al. (2019), who imprinted polycomb group protein in grasses (Dickinson et al., showed that rapid evolution of cis binding sites generates novel 2012), which may have contributed to the evolution of the TF expression patterns that lead to subfunctionalization and globally important large endosperm found in cereals. Finally, Lu neofunctionalization as well as complex combinations of new and et al. (2020) recently observed that the polyploid populations of ancestral expression states. Solidago canadensis, which have a more southerly distribution Additional insights into the evolution of duplicated genes has than their diploid counterparts, and which have a lower freezing emerged from studies of suites of genes tracing to a common tolerance, had lower expression levels but more copies of a key progenitor genome, rather than a common class or category gene (ScICE1) involved in freezing tolerance. In this case the of gene. An exemplar study in this respect is that of De Smet authors suggested that promoter DNA methylation has repressed et al. (2017) who demonstrated a pattern of coordinated gene expression, leading to polyploid adaptation accompanying expression following ancient polyploidy in A. thaliana. In this range expansion. case a suite of 92 homoeologous gene pairs were identified which It seems likely that we have only just begun to understand the shared a common pattern of tissue-specific gene expression, relationships among epigenetic responses to polyploidy and novel but with the two homoeologous suites being partitioned such phenotypes or adaptation, but given the scale and the scope of that one was expressed mostly in aerial tissues while the other both polyploidy and its unavoidable epigenetic consequences, it was expressed predominantly in roots. This remarkable example seems probable that many new examples will soon emerge. of coordinated homoeolog evolution among diverse sets of Finally, we note the potentially important observation that genes has parallels to recent discoveries from using coexpression reciprocal homoeolog silencing, as described for different organs network approaches, discussed below. of the same plant in Gossypium (Adams et al., 2003, 2004), can arise immediately upon polyploid formation. Moreover, Altered Epigenetic Landscapes the same tissue-specific expression pattern has been observed The observation that global patterns of gene expression are in natural allopolyploids 1–2 million years following initial dramatically altered by a change in ploidy (above) led to the polyploid formation. This suggests the tantalizing possibility that supposition that at least part of this response must have an there has been stable maintenance of an epigenetic mutation since epigenetic basis. This supposition was confirmed by studies the initial formation of allopolyploid Gossypium. Adams et al. of synthetic polyploids and interspecific F1 hybrids, plants (2004) noted the important temporal dimension of this epigenetic in which there has been virtually no chance for mutational suppression of gene expression, suggesting that epigenetic effects yet which exhibit massive gene expression modification subfunctionalization may provide a selective constraint favoring Frontiers in Genetics | www.frontiersin.org 8 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty duplicate gene retention, in that both homoeologs would be Altered Cis and Trans Relationships necessary to enable expression in alternative tissues. To the Allopolyploidy entails the merger of two suites of partially extent that this is true, epigenetic subfunctionalization might diverged cis- and trans-regulatory elements, and as such gene provide a latent reservoir of hundreds to thousands of genes, expression is expected to be altered due to the several new which “become exposed to an evolutionary filter only after forms of regulatory interactions in the polyploid nucleus additional epigenetic and genetic evolution” (Adams et al., 2004, (Bottani et al., 2018; Hu and Wendel, 2019). These expectations p. 2225) perhaps thousands to millions of years later. The recently were illuminated in an experiment where reciprocal F1 scale of the phenomenon of homoeolog bias and reciprocal hybrids were constructed between cultivated and wild accessions silencing, as noted above, suggests that epigenetic maintenance of the allotetraploid cotton species G. hirsutum (Bao et al., via subfunctionalization may prove to be a significant facet of 2019). Although the goal was to understand the nature of polyploid evolution. the domestication process, the study revealed a surprisingly high level of trans-regulatory control of gene expression (54– Small RNA Duplication and Divergence 64%), higher than observed in comparable studies in diploids. Another genomic facet of hybridization and polyploidy is the Bao et al. (2019) proposed the explanation that with the attendant combining of diverged populations of small RNAs onset of allopolyploidy, trans factors throughout the genome (sRNAs), including microRNAs (miRNAs) and several classes instantaneously acquire duplicated homoeologous suites of cis of small interfering RNAs (siRNAs) (Ng et al., 2012; Wendel elements with which to interact. This aspect of allopolyploidy et al., 2016; D’Ario et al., 2017). Each of these classes of generates extensive and novel cis-trans interactions, especially for 21 to 24 nucleotide RNAs has a suppressive effect on either trans variants. As noted by Bao et al. (2019), “This phenomenon gene or transposable element (TE) expression, and all are of enhanced trans regulatory evolution may be a general and subject to the novel trans-regulatory controls established by previously unrecognized feature of polyploidy, perhaps helping genome merger. As such, the combination of two populations to explain evolutionary novelty in recently formed allopolyploid of diverged sRNAs has the potential to change patterns of plants.” It seems probable that in the next few years specific gene expression, TE activity, and all of the developmental examples will emerge where novel phenotypes are causally programs and phenotypes that might result from this altered connected to these new regulatory interactions. regulatory environment. Micro RNAs, for example, are known to be important players in stress responses and other forms of ecological adaptation (Song et al., 2019; Yu et al., 2019), which raises the possibility that these small regulatory molecules might COMBINATORIAL GENOMIC AND facilitate neofunctionalization of duplicated stress-related and EXPRESSION-LEVEL RESPONSES other signaling genes (Palacios et al., 2019). A growing literature attests to the effects of polyploidy Novel Cytonuclear Combinations on expression of small RNAs (reviewed in Ng et al., 2012; Allopolyploid formation not only results in the merger of two Wendel et al., 2016). As with protein-coding genes, in most nuclear genomes, but because it is directional there is a pollen studies at least some sRNAs are non-additively expressed (e.g., donor and an ovule donor. The latter is the source of the Li et al., 2014; Xie and Zhang, 2015; Cavé-Radet et al., 2019; cytoplasm with its mitochondria and plastids in perhaps 80% of Palacios et al., 2019; Wei et al., 2019), being subject to novel angiosperms (Corriveau and Coleman, 1988), and accordingly trans regulation. sRNA non-additivity in polyploids may be the nascent allopolyploid and all descendant lineages have unsurprising in that this also has been observed within species organellar genomes tracing to the maternal diploid parent. This as well, as in maize hybrids (Crisp et al., 2020). For miRNAs, directional asymmetry also is accompanied by a genic imbalance, this non-additivity will affect downstream gene regulation, so as polyploidization results in a doubling of nuclear gene content in principle non-additivity should have consequences for plant (for a tetraploid) with a more uncertain quantitative effect on phenotypes; for siRNAs, non-additive siRNA expression could, in cytoplasmic genome number (Sharbrough et al., 2017; Doyle trans, affect epigenetic silencing or activation of TEs (transposon and Coate, 2019). Because organellar genomes diverge during elements), which could also exert effects on neighboring protein- diploid divergence, in many of the same ways as those discussed coding genes and eventually cause phenotypic alterations (see above for nuclear genomes, and because many aspects of plant below). There are, however, surprisingly few examples of where physiology and development involve finely tuned integration sRNA divergence has been causally connected to novel traits in of plastidial and mitochondrial processes with anterograde polyploids. In cotton allopolyploids, for example, homoeologous and retrograde nuclear-organellar signaling, there has been a MYB2 transcription factors, regulated by miR828 and miR858, long interest in the evolutionary dimension of this cytonuclear are important regulators of cotton fiber development (Guan relationship (reviewed in, e.g., Bock et al., 2014; Sharbrough et al., 2014). These miRNAs have functionally diverged with et al., 2017; Fishman and Sweigart, 2018). This work includes respect to their targeting preferences, and are inferred to observational, experimental, and statistical evidence bearing on contribute in a novel manner to polyploid cotton fiber growth. the fitness of different cytonuclear combinations within and It seems probable that additional examples will soon emerge between species (Bock et al., 2014; Case et al., 2016; Roux F. et al., from functional analysis of the omnipresent alterations in sRNA 2016) as well as a vast literature on cytonuclear incompatibility expression in polyploids. (Fishman and Sweigart, 2018) and the important topic of Frontiers in Genetics | www.frontiersin.org 9 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty cytoplasmic male sterility in crop plants (Chen et al., 2017). That In fact, TE proliferation and TE elimination by transposon- specific cytonuclear combinations can affect plant phenotype mediated recombination and deletion-biased double strand has now been firmly established. This was recently convincingly break (DSB) repair are two of the primary drivers of genome demonstrated by Flood et al. (2020) for 1,859 phenotypes in all expansion and shrinkage during land plant evolution (Pellicer possible cybrid combinations among seven A. thaliana lines. et al., 2018). These processes can play out saltationally to generate With respect to hybridization and polyploidy, mounting large changes in genome size even over short evolutionary time evidence suggests that cytonuclear molecular coevolutionary scales. As an example, the proliferation of a few retrotransposon responses will be common. One source of evidence is “global”; families explains the doubling of the genome size of Oryza for example, nuclear genes encoding organellar processes australiensis relative to rice (Piegu et al., 2006). Similarly, the are preferentially restored to single-copy status following 3-fold difference in genome sizes among different diploid cotton polyploidy events (De Smet et al., 2013), presumably to (Gossypium) species reflects the differential dynamics of TE restore “normal” stoichiometric relationships with organellar- proliferation and clearance since these species shared a common encoded proteins. Another example is that of the D-genome ancestor (Hawkins et al., 2009). Even within species there can wheat species Aegilops tauschii, which has a homoploid be extensive TE polymorphism (Carpentier et al., 2019; Noshay hybrid origin and which has preferentially retained genes et al., 2019). Thus, the TE component of plant genomes is from its maternal A-genome ancestry for nuclear genes highly variable in plants, even among closely related species and that encode cytonuclear enzyme complexes (Li N. et al., often within species. 2019). At a more granular level, Gong et al. (2012, 2014) In the context of the present review, the merger of two studied RuBisCO in allopolyploids of five different model different genomes will inevitably combine two different TE genera, Arabidopsis, Arachis, Brassica, Gossypium, and Nicotiana, populations, which is of particular relevance because the presence demonstrating that paternal copies of the nuclear-encoded and mobility of TEs impact genomes in many ways. First, their small subunit (rbcS) experience gene conversion such that transposition induces new insertions, which in most cases will their sequences became maternal-like, and also that there was be selectively neutral or slightly deleterious, but in other cases preferential expression of the maternal rbcS copies. These could provide a selective advantage (Arkhipova, 2018). Second, putative coevolutionary responses were not found, however, in their repetitive nature offers numerous pairs of sequences that some other genera, e.g., Tragopogon (Sehrish et al., 2015) and can recombine, and accordingly, TEs are a major source of Cucumis (Zhai et al., 2019). structural variants, including genic CNV and PAV, as discussed A potential connection to phenotype, and an example that earlier (see Structural diversity, above, see also Fuentes et al., integrates several of the mechanisms discussed in the present 2019). And third, TEs are a rich source of new genes and gene review, is from Wu et al. (unpublished), who studied synthetic functions and can directly or indirectly regulate gene expression allopolyploids synthesized from reciprocal crosses between rice (Lisch, 2013). Indeed, TEs are an important source of promoters O. sativa subsp. sativa and subsp. japonica. Each generation of and transcriptional regulatory elements. Transcription is the first selfing was accompanied by multiple homoeologous exchanges step of transposition, and TEs contain internal promoters to (see earlier discussion), collectively affecting all members of facilitate their own expression. The insertion of TEs within or the chromosome complement, such that after four generations close to genes can therefore alter the expression of neighboring of selfing the resulting individuals were genomic mosaics of genes by providing additional transcription factor binding sites the two founding parents. Importantly, some genomic regions or alternative promoters and splicing signals, a phenomenon were preferentially and reciprocally biased with respect to frequently found in both animal (Chuong et al., 2017) and plant maternal vs. paternal progenitor in that they were repeatedly genomes (Lisch, 2013). associated with only one of the two parental cytoplasms, whereas Transposon elements accumulate in certain regions of the other chromosomal regions were exclusively maintained as genome (e.g., centromeres and pericentromeric regions) where heterozygotes, suggesting hetero-cytonuclear interactions. they can fulfill important structural functions, as for example As with many of the other phenomena discussed here, the supporting the specification and function of centromeres foregoing synopsis suggests an adaptive dimension to cytonuclear (Lermontova et al., 2015). But this non-homogeneous interactions that may be set in motion through hybridization and accumulation in chromosomes also impacts genic evolution. genome doubling. In filamentous fungi, the “two-speed genomes” concept has been developed to describe the concentration of the fast- Effects on Transposable Element Activity evolving virulence effectors in TE-rich compartments of the Transposon elements are mobile genetic elements that genome (Dong et al., 2015). The formation of TE islands and account for a large but variable fraction of virtually all differentiated genomic regions showing distinct evolutionary eukaryotic genomes, including plants. As an example, LTR- rates could allow for the rapid evolution required for adaptation retrotransposons, which together with miniature inverted-repeat to new environments while preserving the basic genic machinery transposable elements (MITEs) constitute the most prevalent (Schrader and Schmitz, 2019), as has been shown for the invasive and active class of TEs in plants (Casacuberta and Santiago, ant Cardiocondyla obscurior (Schrader et al., 2014). Although 2003), account for only 2.5% of the small and compact genome this phenomenon has not been described as such in plants of Utricularia gibba (Ibarra-Laclette et al., 2013) but 90% of the (Lanciano and Mirouze, 2018), there are accumulating examples gigantic genome of Fritillaria spp. (Ambrožová et al., 2011). of TE impact on the evolution of different plant resistances to Frontiers in Genetics | www.frontiersin.org 10 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty biotic and abiotic stress, such as disease resistance in pepper splicing upon insertion. As an example, an Helitron insertion (Kim et al., 2017) and aluminum resistance in a wide range into a host susceptibility factor gene causes its alternative splicing of land plants (Pereira and Ryan, 2019), and it has long been leading to resistance to maize rough dwarf disease (Liu et al., known that plant disease resistant genes frequently concentrate 2020). Moreover, as noted above, TEs are the main target of in resistance gene clusters which are also rich in TEs (Richter and epigenetic silencing, and therefore, the insertion of a TE within Ronald, 2000). Moreover, the differential distribution of genes or close to a gene may bring the silencing machinery to this gene with respect to their age or function in genomic compartments altering its expression (Zhang H. et al., 2018). In addition to defined by a different TE content has recently been shown bringing new promoters and promoter elements, TEs can also be in plants, including tomato (Jouffroy et al., 2016) and melon the source of small RNAs that regulate gene expression (McCue (Morata et al., 2018b), suggesting that TE-rich compartments and Slotkin, 2012), and in particular that of defense-related genes may facilitate rapid adaptation in plants. In addition, TEs can (Poretti et al., 2020), and it has been recently shown that they also modify the local recombination rate along chromosomes. can also contribute long non-coding RNAs that regulate plant Indeed, a recent study in natural populations of Arabis alpina has stress responses (Lv et al., 2019). TEs are therefore an important shown that TEs can create linkage disequilibrium blocks defining force that facilitates plant, and also animal (Rech et al., 2019) and adaptive loci that concentrate environment-responsive genes yeast (Esnault et al., 2019), adaptation to stress. This confirms (Choudhury et al., 2019). McClintock’s revolutionary hypothesis on the role of mobile Given their ubiquity, extraordinary variability even within genetic elements in overcoming the threat of environmental species, and propensity to function as genomic architects, it is shock by reorganizing the genome (McClintock, 1984). likely that TEs are important internal drivers of plant evolution McClintock’s proposal regarding the “shock” that follows and adaptation. However, TEs also pose a hazard for genome genome merger has been amply evidenced by data showing integrity, as they are a cause of potentially deleterious mutations that plant hybridization and polyploidization frequently trigger and chromosome instability. For this reason, TE activity is TE activation (Vicient and Casacuberta, 2017). Transcriptional highly repressed by different mechanisms, the most important activation of TEs has been reported in synthetic Arabidopsis being epigenetic silencing driven by DNA methylation (Kim polyploids (Madlung et al., 2005), wheat amphiploids (Kashkush and Zilberman, 2014; Zhang H. et al., 2018). TEs are the et al., 2003), allopolyploid coffee (Lopes et al., 2013), and in main target of epigenetic silencing marks in the genome, and rice lines derived from introgressive hybridization with Zizania TE distribution closely matches that of DNA methylation (El latifolia (Wang et al., 2010), among others. This activation of TEs Baidouri et al., 2015). The equilibrium between efficient silencing in hybrids and polyploids has been shown to be accompanied mechanisms to control TEs, and the escape of some TEs in many cases by a modification of the siRNAs that target TEs from this control under particular circumstances, allows for TE (Springer et al., 2016). Moreover, TE mobilization and increase maintenance and genome plasticity while maintaining genome in copy number has also been reported for different hybrids integrity. TEs are mostly quiescent and are only activated in and polyploids, including tobacco (Petit et al., 2010), wheat particular developmental stages (Martínez and Slotkin, 2012) (Yaakov and Kashkush, 2012) and Brassica (Sarilar et al., 2013) or under stress (Galindo-González et al., 2017). This activation allopolyploids, in Biscutella laevigata autopolyploids (Bardil of TEs by stress, and probably also during development, likely et al., 2015), and in sunflower hybrids (Kawakami et al., 2010). is the result of the combination of the presence of specific However, in other allopolyploids or interspecific crosses no activator sequences in TE promoters (Galindo-González et al., evidence of an increase of TE content was shown. For example, 2017), and the alleviation of epigenetic silencing in these no changes were observed in TE regulation after an interspecific situations (Gutzat and Mittelsten Scheid, 2012). The activation cross between A. thaliana and A. lyrata (Göbel et al., 2018), and of TEs under stress allows for the generation of new variability no TE burst was detected after polyploidization of A. arenosa in situations to which the genome is not necessarily well- (Baduel et al., 2019). Moreover, an increase of TE-related siRNAs adapted. In addition, the insertion of TEs with stress-related was recently reported in Spartina allopolyploids, suggesting a promoters close to genes could result in the stress-related strengthening of TE repression accompanying polyploidization expression of a new set of genes offering new possibilities (Cavé-Radet et al., 2019). for adaptation to new environmental conditions. Interestingly, An important dimension of TE mobilization following TE integrations are frequently not random, and it recently genome merger is that this varies among TE families, and has been shown that some LTR-retrotransposons preferentially the same TE may proliferate in some polyploids while being target environmentally responsive genes (Quadrana et al., 2019), eliminated in others. As an example, Sabine retrotransposons generating new genetic or epigenetic variability that could proliferated following polyploidy in some Aegilops (wheat) facilitate rapid adaptation to new environments. polyploids while being eliminated in others (Senerchia et al., Although LTR-retrotransposons are the most obvious 2014), even while other retrotransposon families (BARE1, candidates for altering adjacent gene expression, other TEs Romani) experienced a more uniform proliferation. Different also have this potential. In particular, MITEs, which are TE families are regulated dissimilarly and their responses to the present in high copy number and are enriched in genic methylation and siRNA changes that accompany genome merger regions (Casacuberta and Santiago, 2003), frequently contain may vary accordingly. At present there is little understanding of transcription factor binding sites (Morata et al., 2018a). In this extraordinary variation in TE responses to polyploidy, but addition, TEs of different types have been shown to alter gene we can imagine that this reflects an equivalent level of diversity Frontiers in Genetics | www.frontiersin.org 11 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty with respect to divergence in progenitor TE populations and interconnected meshworks of lower level “omic” processes. We their repression and activation dynamics among parental diploids expect that we are entering a period during which this omics- in each genus. In this respect, it has recently been shown that enabled view of adaptation and evolutionary change will rapidly there is a correlation between TE mobilization in Nicotiana expand, concomitant with the application of a suite of enabling allopolyploids and the quantitative imbalance in parental TE technologies to model experimental and natural systems. loads (Mhiri et al., 2019). But even in the absence of TE activation, A foreshadowing of this form of evolutionary exploration is polyploidy may result in an increase in TE content due to offered by the development of coexpression network analysis, relaxed purifying selection at duplicated loci (Ågren et al., 2016; in which entire transcriptomes are interrogated for patterns of Baduel et al., 2019). genic and “modular” coexpression, or lack thereof. The logic In summary, merging two different genomes, with or without for this rests on the assumption stated above, i.e., that genes polyploidization, will combine in a single genome two different work in concert rather than in isolation to generate phenotypes. TE populations, together with the siRNAs that target them, and Many aspects of genic coexpression network analysis have been this may result in changes in the epigenetic modifications at TEs amply reviewed (e.g., Serin et al., 2016; Emamjomeh et al., and neighboring genes and in the regulation of genes and TEs. 2017; Ruprecht et al., 2017b; Contreras-Lopez et al., 2018; Given the prevalence of TEs, their frequent association with Joehanes, 2018; Rao and Dixon, 2019); here our attention is genes, and their potential for insertional mutagenesis following focused on applications involving adaptation following genome genome merger, it seems probable that they are important players duplication and/or merger. in the creation of novel traits and adaptation in polyploids. As Recent studies have demonstrated that gene regulatory explained above, the importance of TEs in creating phenotypic rewiring often follows duplication (Gupta and Tsiantis, 2018), variability in plants is well established (Lisch, 2013), and examples and that entire modules of genic coexpression may be duplicated of the role of TEs in creating new adaptive alleles are slowly and retained in plants. Ruprecht et al. (2016), for example, accumulating. For example, TEs have been recently shown showed that in Arabidopsis a module for cell wall biosynthesis to create adaptive alleles that modify flowering time (Huang has become replicated and deployed differentially for different et al., 2017; Liang et al., 2019; Niu et al., 2019), facilitate local types of cell walls. Pfeifer et al. (2014) showed that genic climate adaptation (He et al., 2018), and trigger new responses coexpression in bread wheat grains was partitioned into 25 to biotic (Poretti et al., 2020) and abiotic (Lv et al., 2019) “modules”, 23 of which contained biased suites of homoeologs stresses, sometimes by facilitating the formation of complex from each of the hexaploid’s three co-resident (A, B, D) biosynthetic pathways (Xu et al., 2017). However, direct evidence genomes. More recently, Takahagi et al. (2018) conducted of TEs generating new adaptive phenotypes as a consequence coexpression analysis of 727 RNAseq data sets from bread of the merging of two genomes remains scarce. As one wheat, reiterating and extending these findings of differential example, for TE families targeting environmentally responsive homoeolog composition of key modules (here meaning suites genes, activation may introduce target variability at these loci, of coexpressed genes) involved in many biological processes, potentially facilitating rapid adaptation (Quadrana et al., 2019). including chloroplast biogenesis, RNA metabolism, putative An added dimension to this scenario is that relaxed purifying defense response, putative posttranscriptional modification, and selection in polyploids (due to duplication) can also result in lipid metabolism. In contrast, Alabdullah et al. (2019) examined accumulation of TEs close to environmentally responsive genes how polyploidization in wheat affected meiotic genes, using 130 (Baduel et al., 2019). The combination of TE activation and the RNA-seq samples to define co-expressed gene modules. Among relaxed purifying selection that frequently accompanies genome the three modules significantly correlated with meiosis, most merger provides a powerful mechanism for the generation of genes retained all three homoeologous copies, and genes within novel allelic combinations for stress-related or other adaptive these modules also exhibited balanced homoeologous expression. responses. We note that in principle adaptation may be facilitated Though the foregoing studies were not designed to evaluate by selection on even a single TE insertion affecting a single gene, whether homoeologous-genome modular portioning of genic as illustrated by the beautiful example of the peppered moth coxpression arose prior to or subsequent to polyploidization, it industrial melanism mutation (Hof et al., 2016), or it might is likely that these modular structures represent network level involve the evolution of complex pathways, as has been shown transcriptomic adjustment to the polyploid condition. for the nicotine synthesis in Nicotiana (Xu et al., 2017). Explicit tests of this diploid-polyploid temporal partitioning have recently been performed using allopolyploid (AD-genome) Disrupted/Altered Regulatory Networks cotton (Gossypium), which contains two genomes (A, D) which It may be useful to consider that each of the many mechanisms diverged 5–10 million years ago (mya) in diploid lineages that introduced in the foregoing sections, from simple genic or became reunited during polyploid formation 1–2 mya. Hu et al. regulatory SNPs through novel transposable element activity, (2016) studied gene coexpression networks in developing seeds ultimately shape phenotypes via their propagation through of diploid as well as allopolyploid species, Network comparisons complex networks of gene regulation, transcription and among species indicated that the global network topology of translation, and higher order biochemical, physiological allopolyploid cotton was asymmetric, resembling one of its and biosynthetic processes (Gottlieb, 1984). To this extent, two diploid progenitors (the A-genome diploid) more than nearly all selectively relevant phenotypes likely represent that of the other (D-genome parent). A novel feature of this emergent properties resulting from high-level multidimensional, study was that it extended, by example, concepts of homoeolog Frontiers in Genetics | www.frontiersin.org 12 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty bias, dominance, and transgressive expression to the network tissue or organ-specific. For these and other consequences of modular level. They further showed that the transcriptomic genome merger discussed here, some have considered whether architecture in developing polyploid cotton seeds is a partial there might be evolutionary “rules” or mechanisms that are combination of the modules observed in the two diploid predictive of specific outcomes (Adams and Wendel, 2005; progenitors, and that domestication of wild allopolyploid cotton Doyle et al., 2008; Soltis et al., 2016; Wendel et al., 2018). One led to a more tightly integrated (more highly coexpressed) generality is that the early stages of genome merger and doubling modular structure. These results for cotton seed development profoundly impact the molecular, genomic and physiological were recently extended to fiber development (Gallagher et al., machinery, as Barbara McClintock famously anticipated in 2020). Key results include the fact that notwithstanding a general her 1983 Nobel lecture, and as Feldman et al. (2012) captured preservation of network modular structure among the A- and in partitioning evolutionary change into “revolutionary,” that D-genome diploids and the allopolyploid, fewer than a quarter is, arising shortly after genome merger, versus “evolutionary,” of all homoeologs co-occured in the same module, showing namely change that accrues more gradually over time. Many substantial homoeologous expression rewiring (alteration of empirical examples of phenotypic and genomic innovation coexpression relationships) at the intramodular level. In addition, have been discussed here, reflecting a broad spectrum of most modules exhibit D-homoeolog expression bias, with few underlying mechanisms and phenotypes. Yet, notwithstanding showing A-homoeolog bias. the extraordinary advances of the last several decades and The preceding examples are illustrative of the various types the increasing use of breathtaking technologies for probing of expression change that accompany polyploid formation, genomes and transcriptomes, we still have only a rudimentary showing that not only is gene expression itself massively understanding of how genome merger generates phenotypic altered, but that this gene-level view has multiple parallels diversity and thereby contributes to evolutionary diversification. at the modular level of gene coexpression relationships. Yet, Also poorly understood is the relative importance of the many connections between these phenomena and demonstrations of genomic responses discussed here to adaptive evolution or adaptation or diversification remain mostly obscure, however, phenotypic innovation at the diploid vs. polyploid level. Both notwithstanding our growing understanding the relationships organismal processes entail genetic merger, which variously between modular genic content and biological processes. In this sets in motion a plethora of “omics” changes, as illustrated in respect one promising approach is to combine coexpression Figure 1, but it is unknown which if any of these responses are network analysis with standard tools from population genetics, more characteristic of diploid vs. polyploid evolution. Some as exemplified in a marvelous recent study on Theobroma cacao progress in this direction has emerged from studies designed from Brazil (Hämälä et al., 2020). Starting with the initial to assess this temporally partitioning, across multiple genera suggestion that evolutionary change often arises from allele (e.g., Flagel et al., 2008; Xu et al., 2014; Edger et al., 2017; frequency shifts simultaneously at multiple genes, Hämälä et al. Zhang D. et al., 2018), but this clearly is an area that warrants (2020) studied genic coexpression relationships for 31 individuals further investigation. from four geographically allopatric populations. Genes from It is of interest to consider the constraints that hinder our modules enriched for specific biological processes were combined understanding of the genetic basis of phenotypic innovation to explore whether they exhibited possible differential selection that follows polyploidy. To be sure, we do not yet understand between populations, using a coexpression-module-based form the full dimensionality of the genotype-to-phenotype equation, of the widely used FST and dXY. They showed that modules and thus our insight into phenotypes is limited by our present associated with biological processes such as protein modification, understanding of the propagation of information from the flowering, and water transport were implicated in polygenic genome through all of the “omics” into something emergent that adaptation, “even though individual genes that are members we call the phenotype (Casacuberta et al., 2016). In addition, of those groups do not bear strong signatures of selection.” though, we suggest that the early responses to genome merger Noting that this example is for possible differential adaptation of and/or doubling represent only the tip of the iceberg compared populations of a single diploid species rather than for the effects to later evolutionary innovation, which ultimately was enabled of introgression or polyploidization, it conceptually helps point or set in motion by genome merger but which remains latent, the way to identifying cases of adaptation stemming from the perhaps for millions of years, until ecological opportunity latter speciation and diversification processes. dovetails with novel genomic/omic recombinants. This temporal dimension is key to our perspective; genome merger sets the stage for both immediate and long-term evolutionary innovation. CONCLUDING REMARKS The retention of many to most duplicated genes and other genomic components in a polyploid serves as a massive reservoir Decades of inquiry have generated much insight into the of variation that may remain evolutionarily latent, perhaps evolution of merged genomes following polyploidy and for hundreds to thousands to millions of years. Only later, hybridization. For instance, we know that duplicated genes perhaps when exposed to altered selection pressures in novel experience a diversity of evolutionary trajectories, being either environment, will this variation lead to phenotypic innovation, lost, epigenetically silenced, or retained but with altered adaptation, and speciation. Yet this novel diversity may not expression regulation and possible neofunctionalization or have been possible without the ancient genomic infusion (or subfunctionalization, and that some of these outcomes may be infusions) from interspecific gene flow. That is, long-term Frontiers in Genetics | www.frontiersin.org 13 July 2020 | Volume 11 | Article 792 Nieto Feliner et al. Genomics of Evolutionary Novelty retention of duplicated genes, regulatory elements, and other phenomena in current lineages is complicated and this has fueled genomic components, may be responsible for evolutionary conflicting views (Mayrose et al., 2011; Abbott et al., 2013; Butlin diversification, even after extinction of the parental lineages and and Ritchie, 2013; Soltis P. S. et al., 2014). The evolutionary in novel environments relative to the progenitors. consequences of allopolyploidy and hybridization—particularly This possibility is consistent with the so-called radiation over the longer term—have been and will remain a matter of lag-time model following WGD, formulated on the basis interest into the future. Yet we see promise in our growing of phylogenetic and divergence-time data (Schranz et al., understanding of biological processes ranging in scale from 2012). According to this hypothesis, successful diversifications the molecular to the ecological. This enhanced understanding in groups that experience ancient polyploidy do not arise of the genotype-to-phenotype equation should increasingly due to the sudden genesis of novel key traits, but instead inform comparative and ecological analyses of adaptation, thus reflects subsequent phenomena over evolutionary time, including permitting an improved appreciation of the temporal dynamics changing environmental conditions. This perspective is also in and genomic underpinnings of polyploidy-fueled diversification. line with classical views that genome doubling provides a massive reservoir of duplicated genes for longer-term evolution of new functions (Stebbins, 1950; Ohno, 1970). Finally, as we note AUTHOR CONTRIBUTIONS above, the possibility of epigenetic “subfunctionalization” offers a mechanism for selective retention of duplicate genes for later All authors listed have made a substantial, direct and intellectual release from suppression and evaluation by natural selection contribution to the work, and approved it for publication. (Adams et al., 2003, 2004). Thus, there is now a confluence among classical notions and modern genomic perspectives regarding the importance FUNDING of long-term persistence of latent variation generated by hybridization and polyploidy on adaptation and diversification. This study was supported by the grants CGL2017-88500-P Additionally, population genetic considerations are relevant, (AEI/FEDER, EU) to GN and AGL2016-78992-R to JC from especially the extremely reduced effective population sizes that the Spanish Ministry of Economy and Competitivity, as well as are involved in the early stages of polyploid formation and Severo Ochoa Program for Centers of Excellence in R&D 2016– stabilization in many groups. These conditions minimize the 2020 (SEV-2015-0533) to JC, and by grants from the National importance of selection relative to drift, thus further facilitating Science Foundation to JW. the survival of less than perfectly adapted genomes and genotypes while highlighting the role of “chance” or stochasticity (Lynch, 2007) in generating genome complexity as well as ACKNOWLEDGMENTS biological diversity. Predicting long-term effects of phenomena that have profound We thank the United States and Spanish Fulbright Commissions impact on organisms, and whose evolutionary fate is heavily as well as the Real Jardín Botánico and Center for Research dependent on spatio-temporal contexts, is not yet possible. in Agricultural Genomics, which supported JW during a Even retrospectively constructing the detailed history of these sabbatical stay in Spain. REFERENCES Aeschbacher, S., Selby, J. P., Willis, J. H., and Coop, G. (2017). Population-genomic inference of the strength and timing of selection against gene flow. Proc. Natl. Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J., Bierne, N., et al. Acad. Sci. U.S.A. 114, 7061–7066. doi: 10.1073/pnas.1616755114 (2013). Hybridization and speciation. J. Evolution. Biol. 26, 229–246. doi: 10. Ågren, J. A., Huang, H. R., and Wright, S. I. (2016). 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(2015). Genome-wide Copyright © 2020 Nieto Feliner, Casacuberta and Wendel. This is an open-access mapping of structural variations reveals a copy number variant that determines article distributed under the terms of the Creative Commons Attribution License reproductive morphology in cucumber. Plant Cell 27, 1595–1604. doi: 10.1105/ (CC BY). The use, distribution or reproduction in other forums is permitted, provided tpc.114.135848 the original author(s) and the copyright owner(s) are credited and that the original Zhuang, W., Chen, H., Yang, M., Wang, J., Pandey, M. K., Zhang, C., et al. (2019). publication in this journal is cited, in accordance with accepted academic practice. No The genome of cultivated peanut provides insight into legume karyotypes, use, distribution or reproduction is permitted which does not comply with these terms. Frontiers in Genetics | www.frontiersin.org 21 July 2020 | Volume 11 | Article 792