Gene and Transposable Element Expression Evolution Following Recent and Past Polyploidy Events in Spartina (Poaceae) Delphine Giraud, Oscar Lima, Mathieu Rousseau-Gueutin, Armel Salmon, Malika Ainouche To cite this version: Delphine Giraud, Oscar Lima, Mathieu Rousseau-Gueutin, Armel Salmon, Malika Ainouche. Gene and Transposable Element Expression Evolution Following Recent and Past Polyploidy Events in Spartina (Poaceae). Frontiers in Genetics, 2021, 12, 10.3389/fgene.2021.589160. hal-03216905 HAL Id: hal-03216905 https://hal.archives-ouvertes.fr/hal-03216905 Submitted on 4 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. 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Distributed under a Creative Commons Attribution| 4.0 International License fgene-12-589160 March 19, 2021 Time: 12:36 # 1 ORIGINAL RESEARCH published: 25 March 2021 doi: 10.3389/fgene.2021.589160 Gene and Transposable Element Expression Evolution Following Recent and Past Polyploidy Events in Spartina (Poaceae) Delphine Giraud1, Oscar Lima1, Mathieu Rousseau-Gueutin2, Armel Salmon1 and Malika Aïnouche1* 1 UMR CNRS 6553 Ecosystèmes, Biodiversité, Evolution (ECOBIO), Université de Rennes 1, Rennes, France, 2 IGEPP, INRAE, Institut Agro, Univ Rennes, Le Rheu, France Gene expression dynamics is a key component of polyploid evolution, varying in nature, intensity, and temporal scales, most particularly in allopolyploids, where two or more sub-genomes from differentiated parental species and different repeat contents are merged. Here, we investigated transcriptome evolution at different evolutionary time scales among tetraploid, hexaploid, and neododecaploid Spartina species (Poaceae, Chloridoideae) that successively diverged in the last 6–10 my, Edited by: at the origin of differential phenotypic and ecological traits. Of particular interest Yves Van de Peer, are the recent (19th century) hybridizations between the two hexaploids Spartina Ghent University, Belgium alterniflora (2n = 6x = 62) and S. maritima (2n = 6x = 60) that resulted in Reviewed by: Pamela Soltis, two sterile F1 hybrids: Spartina × townsendii (2n = 6x = 62) in England and University of Florida, United States Spartina × neyrautii (2n = 6x = 62) in France. Whole genome duplication of Clayton J. Visger, S. × townsendii gave rise to the invasive neo-allododecaploid species Spartina anglica California State University, Sacramento, United States (2n = 12x = 124). New transcriptome assemblies and annotations for tetraploids and *Correspondence: the enrichment of previously published reference transcriptomes for hexaploids and Malika Aïnouche the allododecaploid allowed identifying 42,423 clusters of orthologs and distinguishing [email protected] 21 transcribed transposable element (TE) lineages across the seven investigated Specialty section: Spartina species. In 4x and 6x mesopolyploids, gene and TE expression changes were This article was submitted to consistent with phylogenetic relationships and divergence, revealing weak expression Plant Genomics, a section of the journal differences in the tetraploid sister species Spartina bakeri and Spartina versicolor Frontiers in Genetics (<2 my divergence time) compared to marked transcriptome divergence between the Received: 30 July 2020 hexaploids S. alterniflora and S. maritima that diverged 2–4 mya. Differentially expressed Accepted: 23 February 2021 genes were involved in glycolysis, post-transcriptional protein modifications, epidermis Published: 25 March 2021 development, biosynthesis of carotenoids. Most detected TE lineages (except SINE Citation: Giraud D, Lima O, elements) were found more expressed in hexaploids than in tetraploids, in line with Rousseau-Gueutin M, Salmon A and their abundance in the corresponding genomes. Comparatively, an astonishing (52%) Aïnouche M (2021) Gene and Transposable Element Expression expression repatterning and deviation from parental additivity were observed following Evolution Following Recent and Past recent reticulate evolution (involving the F1 hybrids and the neo-allododecaploid Polyploidy Events in Spartina S. anglica), with various patterns of biased homoeologous gene expression, including (Poaceae). Front. Genet. 12:589160. doi: 10.3389/fgene.2021.589160 genes involved in epigenetic regulation. Downregulation of TEs was observed in both Frontiers in Genetics| www.frontiersin.org 1 March 2021| Volume 12| Article 589160 fgene-12-589160 March 19, 2021 Time: 12:36 # 2 Giraud et al. Transcriptome Evolution in Spartina Polyploids hybrids and accentuated in the neo-allopolyploid. Our results reinforce the view that allopolyploidy represents springboards to new regulatory patterns, offering to worldwide invasive species, such as S. anglica, the opportunity to colonize stressful and fluctuating environments on saltmarshes. Keywords: allopolyploidy, hybridization, transcriptome evolution, transposable elements (TE), Spartina INTRODUCTION emergence of novel variation, traits and phenotypes (Finigan et al., 2012), thus contributing to species adaptation and long- Gene expression dynamics is a key component of polyploid term diversification (Comai, 2005; Conant and Wolfe, 2008; evolution, and has received considerable interest in the last Jackson and Chen, 2010; Madlung, 2013; Tank et al., 2015; decades, where studies on various polyploid systems revealed Van de Peer et al., 2017). an important role of whole genome duplication (WGD) in Expression evolution in polyploids has been extensively modulating diverse and novel gene expression patterns (Chen, explored by testing their deviation from an expected 2007; Flagel et al., 2008; Yoo et al., 2014). Comparative transcriptomic “parental additivity.” This non-additive parental analyses indicate that the evolution of duplicated gene expression expression may be perceived by considering either the overall has a temporal dimension, and that immediate responses gene expression level (usually measured by comparisons with to polyploidy may not only last over long periods, but the average expression of both parental species, i.e., Mid-Parent also contribute to the long-term processes of diploidization Value; MPV) or by considering the relative contribution of and fractionation (Wendel et al., 2018). One of the key each homoeologous copy to the total expression level (Grover parameters of this dynamics is the divergence level between et al., 2012). The high frequency of biases in the respective the genomes being merged and duplicated during the polyploid contributions of homeologs reported in various allopolyploids speciation process (Buggs et al., 2012; Tayalé and Parisod, 2013). lead to the “genomic dominance” concept whereby one parental Neopolyploids are usually classified as autopolyploids, where (homoeologous) subgenome expression state is exhibited in homologous genomes (i.e., within species) are duplicated, or as strong preference over the other parental expression state allopolyploids involving duplication of more or less divergent (Flagel and Wendel, 2009). (homoelogous) genomes reunited in the same nucleus following Recent studies provide accumulating evidence that interspecific hybridization (Stebbins, 1971; reviewed in Doyle the “dominant” subgenome is early established following et al., 2008). Most autopolyploids so far explored exhibit hybridization and may be maintained over generations (Edger moderate transcriptome or proteome alteration compared to et al., 2017; Bird et al., 2018). This, very interestingly, permits their diploid progenitors (Albertin et al., 2005; Parisod et al., to connect the short-term genome dominance phenomenon 2010b; del Pozo and Ramirez-Parra, 2014; Visger et al., 2019; to the long-term fractionation process affecting polyploid Song et al., 2020). In contrast, allopolyploidy seems to be genomes (Wendel et al., 2018), where biases in gene loss accompanied by profound parental expression repatterning in between duplicated homoeologous genomes result from the naturally formed neopolyploids (Hegarty et al., 2006; Chelaifa selection against loss of the most expressed copy (Schnable et al., 2010b; Buggs et al., 2011), experimentally resynthesized et al., 2011). The corollary is that following allopolyploidy, allopolyploids and/or their naturally established counterparts the “dominant” subgenome (the highest expressed) is more (Wendel, 2000; Chen and Ni, 2006; Ha et al., 2009; Soltis et al., likely to be retained than the “recessive” subgenome (the lowest 2015), such as in oilseed rape, wheat, cotton, or coffea (Akhunova expressed) that becomes the most fractionated (Cheng et al., et al., 2010; Higgins et al., 2012; Combes et al., 2013; Yoo 2018). As expected, subgenome dominance is not observed in et al., 2013; Wu et al., 2018). These dynamics reflect both the neo-autopolyploids (Garsmeur et al., 2014) suggesting a major effects of the reunion of divergent regulatory networks (resulting role of the composition of the two subgenomes being merged from hybridization) and the effects of genetic redundancy in this process, notably in their content of transposable or (resulting from WGD), all