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Consensus species tree from concatenated and coalescence-based analysis of 234 single copy orthogroups with results from gene tree querying of putative paralogs. A) Mapping results of synteny-derived paralogs from the rice and sorghum genomes displayed as total number of unique least common ancestor (LCA) nodes with bootstrap values ≥ 80. Results show placement of rho, sigma, and tau WGD events. B) Mapping results of K s plot-derived paralogs with 22 (number for sigma event) or more total unique LCAs and boostrap values ≥ 80 for Poales species only. C) Mapping results of gene tree-derived paralogs with 235 (number for sigma event) or more total unique LCAs and boostrap values ≥ 80 for monocot species only. Previously published WGD events are identified and placed on the tree, including a shared Zingiberaceae event (gamma), a palm event, and an Agavoideae event, represented as gold diamonds. If previously named, the Greek character representing the event is also displayed. Higher support for rho, sigma, and tau is identified relative to the synteny-derived paralogs and other potential WGD events in Juncus, Cyperus, and Restionaceae are also identified.
Source publication
Comparisons of flowering plant genomes reveal multiple rounds of ancient polyploidy characterized by large intra-genomic syntenic blocks. Three such whole genome duplication (WGD) events, designated as rho (ρ), sigma (σ), and tau (τ), have been identified in the genomes of cereal grasses. Precise dating of these WGD events is necessary to investiga...
Citations
... First, clarifying where apparent reticulate relationships may actually stem from differential retention of homologs after whole-genome duplication. For example, the reticulations we inferred at the base of the BOP-PACMAD clade, the large crown radiation of grasses, could potentially be remnants from the rho whole-genome duplication event at the stem of Poaceae (McKain et al., 2016;Zhang et al., 2024). Second, correlating reticulation frequency with ecological and morphological predictors to identify the physical mechanisms of lateral transfers, which remain speculative . ...
Grasses (Poaceae) comprise around 11,800 species and are central for human livelihoods and terrestrial ecosystems. Knowing their relationships and evolutionary history is key to comparative research and crop breeding. Advances in genome-scale sequencing allow for increased breadth and depth of phylogenomic analyses, making it possible to infer a new reference species tree of the family.
We inferred a comprehensive species tree of grasses by combining new and published sequences for 331 nuclear genes from genome, transcriptome, target enrichment and shotgun data. Our 1,153-tip tree covers 79% of grass genera (including 21 genera sequenced for the first time) and all but two small tribes. We compared it to a 910-tip plastome tree.
The nuclear phylogeny matches that of the plastome at most deep branches, with only a few instances of incongruence. Gene tree–species tree reconciliation suggests that reticulation events occurred repeatedly in the history of grasses.
We provide a robust framework for the grass tree of life to support research on grass evolution, including modes of reticulation, and genetic diversity for sustainable agriculture.
... Interestingly, RA1 and RA1-like paralogs genes are exclusive of grasses and show different patterns of retentions and losses, as is usually observed after genome duplication events [48][49][50]. It is well documented that differential gene loss or subfunctionalization and neofunctionalization of retained copies, as the case presented here, may promote morphological, physiological, and ecological diversification, in particular, in grasses [51,52]. ...
RAMOSA1 (RA1) is a Cys2-His2-type (C2H2) zinc finger transcription factor that controls plant meristem fate and identity and has played an important role in maize domestication. Despite its importance, the origin of RA1 is unknown, and the evolution in plants is only partially understood. In this paper, we present a well-resolved phylogeny based on 73 amino acid sequences from 48 embryophyte species. The recovered tree topology indicates that, during grass evolution, RA1 arose from two consecutive SUPERMAN duplications, resulting in three distinct grass sequence lineages: RA1-like A, RA1-like B, and RA1; however, most of these copies have unknown functions. Our findings indicate that RA1 and RA1-like play roles in the nucleus despite lacking a traditional nuclear localization signal. Here, we report that copies diversified their coding region and, with it, their protein structure, suggesting different patterns of DNA binding and protein–protein interaction. In addition, each of the retained copies diversified regulatory elements along their promoter regions, indicating differences in their upstream regulation. Taken together, the evidence indicates that the RA1 and RA1-like gene families in grasses underwent subfunctionalization and neofunctionalization enabled by gene duplication.
... The WGT groups (WGT and WGT+SSD) were subjected to additional filtering based on the distribution of the synonymous divergence (Ks) between paralogs in Cakile. The FASTKs pipeline (McKain et al., 2016) was used to obtain the Ks distribution for Cakile and assess pairwise ortholog divergence between Cakile and Brassica to Arabidopsis, and Cakile to Brassica. In this pipeline, CDS sequences for each sample were aligned against themselves with an e-value cutoff of 1e-40 using BLAST (Altschul et al., 1990). ...
Premise
The origin of diversity is a fundamental biological question. Gene duplications are one mechanism that provides raw material for the emergence of novel traits, but evolutionary outcomes depend on which genes are retained and how they become functionalized. Yet, following different duplication types (polyploidy and tandem duplication), the events driving gene retention and functionalization remain poorly understood. Here we used Cakile maritima , a species that is tolerant to salt and heavy metals and shares an ancient whole‐genome triplication with closely related salt‐sensitive mustard crops ( Brassica ), as a model to explore the evolution of abiotic stress tolerance following polyploidy.
Methods
Using a combination of ionomics, free amino acid profiling, and comparative genomics, we characterize aspects of salt stress response in C. maritima and identify retained duplicate genes that have likely enabled adaptation to salt and mild levels of cadmium.
Results
Cakile maritima is tolerant to both cadmium and salt treatments through uptake of cadmium in the roots. Proline constitutes greater than 30% of the free amino acid pool in C. maritima and likely contributes to abiotic stress tolerance. We find duplicated gene families are enriched in metabolic and transport processes and identify key transport genes that may be involved in C. maritima abiotic stress tolerance.
Conclusions
These findings identify pathways and genes that could be used to enhance plant resilience and provide a putative understanding of the roles of duplication types and retention on the evolution of abiotic stress response.
... Interestingly, RA1 and RA1-like paralogs genes are exclusive of grasses and show different patterns of retentions and losses as is usually observed after genome duplication events [48][49][50]. It is well documented that differential gene loss or subfunctionalization and neofunctionalization of retained copies, as the case presented here, may promote morphological, physiological, and ecological diversification, in particular, in grasses [51,52]. ...
RAMOSA1 (RA1) is a Cys2-His2-type (C2H2) zinc finger transcription factor that controls plant meristem fate and identity and has played an important role in maize domestication. Despite its importance, the origin of RA1 is unknown and the evolution in plants is partially understood. In this paper, we present a well resolved phylogeny based on 73 amino acid sequences from 48 embryophyte species. The recovered tree topology indicates that, during grass evolution, RA1 arose from two consecutive SUPERMAN duplications resulting in three distinct grass sequence lineages: RA1-like A, RA1-like B, and RA1; however, most of these copies have unknown functions. Our findings indicate that RA1 and RA1-like play roles in the nucleus despite lacking a traditional nuclear localization signal. Here we report that copies diversified their coding region and, with it, their protein structure, suggesting different patterns of DNA binding and protein-protein interaction. In addition, each of the retained copies diversified regulatory elements along their promoter regions, indicating differences in their upstream regulation. Taken together, we propose that the RA1 and RA1-like gene families in grasses may have undergone subfunctionalization and neofunctionalization enabled by gene duplication.
... Allopolyploidy (i.e., resulting from hybridization and genome doubling) has long been recognized as an important mode of plant speciation (Soltis & Soltis, 2009) and causing complex genomic interactions linked to the fate of new hybrid individuals (Qiu et al., 2020). The Chloridoideae lineages went through multiple chromosome rearrangements to varying degrees after the qWGD event, which has long been suggested to predate the origin of grasses (Mckain et al., 2016;Paterson et al., 2004). The genomic analysis revealed that bermudagrass experienced an additional WGD event after its divergence from other grasses. ...
Bermudagrass ( Cynodon dactylon ) is a globally distributed, extensively used warm‐season turf and forage grass with high tolerance to salinity and drought stress in alkaline environments. However, the origin of the species and genetic mechanisms for salinity tolerance in the species are basically unknown. Accordingly, we set out to study evolution divergence events in the Cynodon genome and to identify genes for salinity tolerance. We developed a 604.0 Mb chromosome‐level polyploid genome sequence for bermudagrass ‘A12359’ ( n = 18). The C. dactylon genome comprises 2 complete sets of homoeologous chromosomes, each with approximately 30 000 genes, and most genes are conserved as syntenic pairs. Phylogenetic study showed that the initial Cynodon species diverged from Oropetium thomaeum approximately 19.7–25.4 million years ago (Mya), the A and B subgenomes of C. dactylon diverged approximately 6.3–9.1 Mya, and the bermudagrass polyploidization event occurred 1.5 Mya on the African continent. Moreover, we identified 82 candidate genes associated with seven agronomic traits using a genome‐wide association study, and three single‐nucleotide polymorphisms were strongly associated with three salt resistance genes: RAP2‐2 , CNG channels, and F14D7.1 . These genes may be associated with enhanced bermudagrass salt tolerance. These bermudagrass genomic resources, when integrated, may provide fundamental insights into evolution of diploid and tetraploid genomes and enhance the efficacy of comparative genomics in studying salt tolerance in Cynodon .
... The copyright holder for this preprint this version posted January 4, 2024. ; https://doi.org/10.1101/2024.01.04.574202 doi: bioRxiv preprint reconciliations (Chen et al., 2000;Pfeil et al., 2005;McKain et al., 2016;Thomas et al., 2017;Zwaenepoel and Van de Peer, 2019a). The most recent iterations of these methods account for variation in the background rate of small scale duplications (SSD) across a phylogeny when testing for the presence of WGD Van de Peer, 2019a, 2020). ...
Premise
The history of angiosperms is marked by repeated rounds of ancient whole-genome duplications (WGDs). Here we use state of the art methods to provide an up-to-date view of the distribution of WGDs in the history of angiosperms that considers both the uncertainty introduced by inference methods and alternative phylogenetic hypotheses.
Methods
Transcriptomic and genomic data were used to infer and place WGDs across two hypothesized angiosperm phylogenies. Initial WGD hypotheses were made using rate corrections to the distribution of synonymous divergences (K s ) of paralogs and orthologs. WGD hypotheses were tested using syntenic inferences and Bayesian models of duplicate gene gain and loss across the phylogeny.
Key results
The number of ancient WGDs in the history of angiosperms (∼170) is largely similar across different inference methods, but there is often variation in the precise placement of WGDs on the phylogeny. K s based methods often yield alternative hypothesized WGD placements largely due to variation in substitution rates among lineages. Phylogenetic models of duplicate gene gain and loss are more robust to topological variation, allowing for post hoc testing of WGD hypotheses. However, errors in species tree inference can still produce spurious WGD hypotheses regardless of method used.
Conclusions
Here we show that different WGD inference methods largely agree on an average of 3.5 WGD in the history of angiosperm species. However, the precise placement of WGDs on the phylogeny is subject to the inference method and tree topology. As researchers continue to test hypotheses regarding the impacts ancient WGDs have on angiosperm evolution, it is important to consider the uncertainty of the phylogeny as well as WGD inference methods.
... Gene duplications are prevalent in these gene lineages. An ancient duplication in the lineage leading to the grass family likely generated the two main VRS1-and GT1-like lineages (35,39). Wheat and barley share a second duplication that excludes brachypodium. ...
Crop engineering and de novo domestication using gene editing are new frontiers in agriculture. However, outside of well-studied crops and model systems, prioritizing engineering targets remains challenging. Evolution can guide us, revealing genes with deeply conserved roles that have repeatedly been selected in the evolution of plant form. Homologs of the transcription factor genes GRASSY TILLERS1 ( GT1 ) and SIX-ROWED SPIKE1 ( VRS1 ) have repeatedly been targets of selection in domestication and evolution, where they repress growth in many developmental contexts. This suggests a conserved role for these genes in regulating growth repression. To test this, we determined the roles of GT1 and VRS1 homologs in maize ( Zea mays ) and the distantly related grass brachypodium ( Brachypodium distachyon ) using gene editing and mutant analysis. In maize, gt1; vrs1-like1 ( vrl1 ) mutants have derepressed growth of floral organs. In addition, gt1; vrl1 mutants bore more ears and more branches, indicating broad roles in growth repression. In brachypodium, Bdgt1; B dvrl1 mutants have more branches, spikelets, and flowers than wild-type plants, indicating conserved roles for GT1 and VRS1 homologs in growth suppression over ca. 59 My of grass evolution. Importantly, many of these traits influence crop productivity. Notably, maize GT1 can suppress growth in arabidopsis ( Arabidopsis thaliana ) floral organs, despite ca . 160 My of evolution separating the grasses and arabidopsis. Thus, GT1 and VRS1 maintain their potency as growth regulators across vast timescales and in distinct developmental contexts. This work highlights the power of evolution to inform gene editing in crop improvement.
... Genomic studies have shed light on the nature and processes of gene evolution, with variation in DNA and RNA sequence data enabling development of robust phylogenies [1]. Multiple polyploidy or whole-genome duplication (WGD) events have played a major part in plant speciation and genome evolution [2,3] with the separation of Poales from other monocotyledonous orders around 60-110 million years ago (Mya) [4]. The ρ WGD event occurred Mya, at the end of the Cretaceous period [5][6][7] and marked separation of the BOP (Bambusoideae, Oryzoideae, and Pooideae) clade, which includes rice, oats, and wheat, from other grass lineages [8][9][10][11]. ...
... Genome size shows very substantial variation in the BOP clade, from 271 Mb in Brachypodium and 389 Mb in rice [17,18], to more than 4,000 Mb in many diploid Triticeae and a similar size in Aveneae (both x = 7) [19,20]. Genome variation and chromosome reorganization have been shown to be important in plant breeding [2][3][4]. Further work is needed to understand the interplay between repetitive DNA proliferation, insertion/ retention bias in the BOP clade, and how to harness this biology to enhance traits of agronomic importance. ...
... Among grasses, polyploidy has played a major part in the earliest (c. 110 Mya, with the ρ event) [4] and most recent (< 1 Mya, for example with tetraploid and hexaploid oat and wheat) events in Oryzoideae and Pooideae [11]. In the BOP clade, genomic expansion (Fig. 1) and chromosome reorganization with a number of welldefined events (Fig. 2) complementing wheat [19], indicate that gene duplication, gain, and loss have played a relatively small role. ...
Background
The BOP (Bambusoideae, Oryzoideae, and Pooideae) clade of the Poaceae has a common ancestor, with similarities to the genomes of rice, Oryza sativa (2n = 24; genome size 389 Mb) and Brachypodium, Brachypodium distachyon (2n = 10; 271 Mb). We exploit chromosome-scale genome assemblies to show the nature of genomic expansion, structural variation, and chromosomal rearrangements from rice and Brachypodium, to diploids in the tribe Aveneae (e.g., Avena longiglumis, 2n = 2x = 14; 3,961 Mb assembled to 3,850 Mb in chromosomes).
Results
Most of the Avena chromosome arms show relatively uniform expansion over the 10-fold to 15-fold genome-size increase. Apart from non-coding sequence diversification and accumulation around the centromeres, blocks of genes are not interspersed with blocks of repeats, even in subterminal regions. As in the tribe Triticeae, blocks of conserved synteny are seen between the analyzed species with chromosome fusion, fission, and nesting (insertion) events showing deep evolutionary conservation of chromosome structure during genomic expansion. Unexpectedly, the terminal gene-rich chromosomal segments (representing about 50 Mb) show translocations between chromosomes during speciation, with homogenization of genome-specific repetitive elements within the tribe Aveneae. Newly-formed intergenomic translocations of similar extent are found in the hexaploid A. sativa.
Conclusions
The study provides insight into evolutionary mechanisms and speciation in the BOP clade, which is valuable for measurement of biodiversity, development of a clade-wide pangenome, and exploitation of genomic diversity through breeding programs in Poaceae.
... The evolutionary complexity and diverse habitats of the QTP and MP provided multiple ecological niches for the survival and proliferation of Stipa plants (Guo et al., 1983;Liu et al., 2014;Qiao, 2019). Many researchers believe that cooling during the Pliocene significantly promoted the origin and expansion of temperate biotic communities (particularly for the subfamily Pooideae), which benefitted from key morphological innovations and genome duplication events in a spikelet (Sandve et al., 2011;Vigeland et al., 2013;McKain et al., 2016;Linder et al., 2018). Whole-genome duplication events have been observed exclusively in the New World clade of Stipeae, specifically in genera such as Austrostipa (Tkach et al., 2021), while no such events have been detected in Old World Stipa genera (Zhang et al., 2022). ...
Phylogenetic analysis provides crucial insights into the evolutionary relationships and diversification patterns within specific taxonomic groups. In this study, we aimed to identify the phylogenetic relationships and explore the evolutionary history of Stipa using transcriptomic data. Samples of 12 Stipa species were collected from the Qinghai-Tibet Plateau and Mongolian Plateau, where they are widely distributed, and transcriptome sequencing was performed using their fresh spikelet tissues. Using bidirectional best BLAST analysis, we identified two sets of one-to-one orthologous genes shared between Brachypodium distachyon and the 12 Stipa species (9397 and 2300 sequences, respectively), as well as 62 single-copy orthologous genes. Concatenation methods were used to construct a robust phylogenetic tree for Stipa, and molecular dating was used to estimate divergence times. Our results indicated that Stipa originated during the Pliocene. In approximately 0.8 million years, it diverged into two major clades each consisting of native species from the Mongolian Plateau and the Qinghai-Tibet Plateau, respectively. The evolution of Stipa was closely associated with the development of northern grassland landscapes. Important external factors such as global cooling during the Pleistocene, changes in monsoonal circulation, and tectonic movements contributed to the diversification of Stipa. This study provided a highly supported phylogenetic framework for understanding the evolution of the Stipa genus in China and insights into its diversification patterns.
... This may be attributable to the size of the wheat genome, which is 40 and 5 times larger than the rice and maize genomes, respectively, suggesting a positive correlation between genome size and the number of encoded WRKY family TFs. Over the course of its evolution, maize has undergone a minimum of three whole-genome duplication events, contributing to the presence of multiple copies of genes [35,36]. Together, these results suggest that members of the WRKY family have undergone substantial evolutionary expansion in plant species. ...
Members of the WRKY transcription factor (TF) family are unique to plants and serve as important regulators of diverse physiological processes, including the ability of plants to manage biotic and abiotic stressors. However, the functions of specific WRKY family members in the context of maize responses to fungal pathogens remain poorly understood, particularly in response to Ustilago maydis (DC.) Corda (U. maydis), which is responsible for the devastating disease known as corn smut. A systematic bioinformatic approach was herein employed for the characterization of the maize WRKY TF family, leading to the identification of 120 ZmWRKY genes encoded on 10 chromosomes. Further structural and phylogenetic analyses of these TFs enabled their classification into seven different subgroups. Segmental duplication was established as a major driver of ZmWRKY family expansion in gene duplication analyses, while the Ka/Ks ratio suggested that these ZmWRKY genes had experienced strong purifying selection. When the transcriptional responses of these genes to pathogen inoculation were evaluated, seven U. maydis-inducible ZmWRKY genes were identified, as validated using a quantitative real-time PCR approach. All seven of these WKRY proteins were subsequently tested using a yeast one-hybrid assay approach, which revealed their ability to directly bind the ZmSWEET4b W-box element, thereby controlling the U. maydis-inducible upregulation of ZmSWEET4b. These results suggest that these WRKY TFs can control sugar transport in the context of fungal infection. Overall, these data offer novel insight into the evolution, transcriptional regulation, and functional characteristics of the maize WRKY family, providing a basis for future research aimed at exploring the mechanisms through which these TFs control host plant responses to common smut and other fungal pathogens.
