Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution

Genome sequencing has demonstrated that besides frequent small-scale duplications, large-scale duplication events such as whole genome duplications (WGDs) are found on many branches of the evolutionary tree of life. Especially in the plant lineage, there is evidence for recurrent WGDs, and the ancestor of all angiosperms was in fact most likely a polyploid species. The number of WGDs found in sequenced plant genomes allows us to investigate questions about the roles of WGDs that were hitherto impossible to address. An intriguing observation is that many plant WGDs seem associated with periods of increased environmental stress and/or fluctuations, a trend that is evident for both present-day polyploids and palaeopolyploids formed around the Cretaceous–Palaeogene (K–Pg) extinction at 66 Ma. Here, we revisit the WGDs in plants that mark the K–Pg boundary, and discuss some specific examples of biological innovations and/or diversifications that may be linked to these WGDs. We review evidence for the processes that could have contributed to increased polyploid establishment at the K–Pg boundary, and discuss the implications on subsequent plant evolution in the Cenozoic.

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Inferring putative ancient whole-genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions

GigaScience ◽

10.1093/gigascience/giaa004 ◽

2020 ◽

Vol 9 (2) ◽

Cited By ~ 8

Author(s):

Zheng Li ◽

Michael S Barker

Keyword(s):

Gene Family ◽

False Positive Rate ◽

Nuclear Gene ◽

Plant Evolution ◽

Plant Genome ◽

Total Evidence ◽

Whole Genome ◽

Green Plants ◽

Whole Genome Duplications ◽

Genome Duplications

Abstract Background Polyploidy, or whole-genome duplications (WGDs), repeatedly occurred during green plant evolution. To examine the evolutionary history of green plants in a phylogenomic framework, the 1KP project sequenced >1,000 transcriptomes across the Viridiplantae. The 1KP project provided a unique opportunity to study the distribution and occurrence of WGDs across the green plants. As an accompaniment to the capstone publication, this article provides expanded methodological details, results validation, and descriptions of newly released datasets that will aid researchers who wish to use the extended data generated by the 1KP project. Results In the 1KP capstone analyses, we used a total evidence approach that combined inferences of WGDs from Ks and phylogenomic methods to infer and place 244 putative ancient WGDs across the Viridiplantae. Here, we provide an expanded explanation of our approach by describing our methodology and walk-through examples. We also evaluated the consistency of our WGD inferences by comparing them to evidence from published syntenic analyses of plant genome assemblies. We find that our inferences are consistent with whole-genome synteny analyses and our total evidence approach may minimize the false-positive rate throughout the dataset. Conclusions We release 383,679 nuclear gene family phylogenies and 2,306 gene age distributions with Ks plots from the 1KP capstone paper. These resources will be useful for many future analyses on gene and genome evolution in green plants.

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Whole-genome microsynteny-based phylogeny of angiosperms

10.21203/rs.3.rs-51378/v1 ◽

2020 ◽

Author(s):

Tao Zhao ◽

Jiayu Xue ◽

Arthur Zwaenepoel ◽

Shu-min Kao ◽

Zhen Li ◽

...

Keyword(s):

Phylogenetic Trees ◽

Sister Group ◽

Whole Genome ◽

Plant Genomes ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Group Relationships ◽

Plant Families ◽

Dynamic Structures ◽

Early Diverging Eudicots

Abstract Plant genomes are generally very complex and dynamic structures, and vary greatly in size, organization, and architecture. This is mainly due to the often-excessive numbers of transposable and repetitive elements, as well as to the fact that many plants are ancient or recent polyploids. Such (recurrent) whole-genome duplications are usually followed by genomic rearrangements, gene transpositions and gene loss, making local gene order-based phylogenetic inference particularly challenging. Nevertheless, microsynteny, i.e. the conservation of local gene content and order, has been recognized as a valuable and alternative phylogenetic character to sequence-based characters (nucleotides or amino acids) for the inference of phylogenetic trees, but to date its application for reconstructing larger phylogenies has been, for several reasons, limited. Here, by combining synteny network analysis, matrix representation, and maximum likelihood, we have reconstructed a microsynteny-based phylogenetic tree for more than 120 available high-quality plant genomes, representing more than 50 different plant families and 30 plant orders within the angiosperms. Comparisons with sequence alignment-based trees and current phylogenetic classifications show that we reconstruct very accurate and robust phylogenies, albeit with sometimes important alternative sister-group relationships. For instance, our synteny-based tree positioned Vitales as early-diverging eudicots, Saxifragales belongs to superasterids, and magnoliids as sister to monocots. We discuss how synteny-based phylogeny can be complementary to traditional methods and could provide additional insights into some long-standing controversial phylogenetic relationships.

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Selective Gene Loss of Visual and Olfactory Guanylyl Cyclase Genes Following the Two Rounds of Vertebrate-Specific Whole-Genome Duplications

Genome Biology and Evolution ◽

10.1093/gbe/evaa192 ◽

2020 ◽

Vol 12 (11) ◽

pp. 2153-2167

Author(s):

Matthias Gesemann ◽

Stephan C F Neuhauss

Keyword(s):

Visual Information ◽

Bright Light ◽

Feedback Regulation ◽

Cell Types ◽

Whole Genome ◽

Whole Genome Duplications ◽

Intracellular Signals ◽

Genome Duplications ◽

Duplication Events ◽

Specific Species

Abstract Photoreceptors convey visual information and come in two flavors; dim-light and bright-light dedicated rod and cones. Both cell types feature highly specialized phototransduction cascades that convert photonic energy into intracellular signals. Although a substantial amount of phototransduction gene ohnologs are expressed either in rods or cones, visual guanylyl cyclases (GCs) involved in the calcium (Ca2+) dependent feedback regulation of phototransduction are neither rod nor cone specific. The co-existence of visual GCs in both photoreceptor types suggests that specialization of these ohnologs occurred despite their overlapping expression. Here, we analyze gene retention and inactivation patterns of vertebrate visual and closely related olfactory GCs following two rounds (2R) of vertebrate-specific whole-genome duplication events (2R WGD). Although eutherians generally use two visual and one olfactory GC, independent inactivation occurred in some lineages. Sauropsids (birds, lizards, snakes, turtles, and crocodiles) generally have only one visual GC (GC-E). Additionally, turtles (testodes) also lost the olfactory GC (GC-D). Pseudogenization in mammals occurred in specific species/families likely according to functional needs (i.e., many species with reduced vision only have GC-E). Likewise, some species not relying on scent marks lack GC-D, the olfactory GC enzyme. Interestingly, in the case of fish, no species can be found with fewer than three (two visual and one olfactory) genes and the teleost-specific 3R WGD can increase this number to up to five. This suggests that vision in fish now requires at least two visual GCs.

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microRNAs as Indicators into the Causes and Consequences of Whole Genome Duplication Events

10.1101/2021.09.01.458616 ◽

2021 ◽

Author(s):

Kevin J Peterson ◽

Alan Beavan ◽

Peter Chabot ◽

Mark L McPeek ◽

Davide Pisani ◽

...

Keyword(s):

Molecular Evolution ◽

Alternative Hypothesis ◽

Causal Mechanism ◽

Whole Genome ◽

Mrna Targets ◽

Whole Genome Duplications ◽

Regulatory Circuits ◽

Genome Duplications ◽

Duplication Events ◽

Mirna Seed

Whole genome duplications (WGDs) have long been considered the causal mechanism underlying the dramatic increase in vertebrate morphological complexity relative to invertebrates. This is due to the retention and neo-functionalization of paralogues generated during these events, evolving new regulatory circuits, and ultimately morphological novelty. Nonetheless, an alternative hypothesis suggests that behind the retention of most paralogues is not neo-functionalization, but instead the degree of the inter-connectivity of the intended gene product, as well as the mode of the WGD itself. Here, we explore both the causes and consequences of WGD by examining the distribution, expression, and molecular evolution of microRNAs (miRNAs) in both gnathostome vertebrates as well as chelicerate arthropods. We find that although the number of miRNA paralogues tracks the number of WGDs experienced within the lineage, few of these paralogues experienced changes to the seed sequence, and thus are functionally equivalent relative to their mRNA targets. Nonetheless, the paralogues generated by the gnathostome 2R allotetraploidization event are retained in higher numbers on one sub-genome relative the second, with the miRNAs found on the preferred set of paralogons showing both higher expression of mature miRNA transcripts and slower molecular evolution of the precursor miRNA sequences. Importantly, WGDs do not result in the creation of miRNA novelty, nor do WGDs correlate to increases in complexity. Instead, it is the number of miRNA seed sequences in the genome itself that not only better correlate to instances in complexification, but also mechanistically explain why complexity increases when new miRNA families are established.

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Inferring putative ancient whole genome duplications in the 1000 Plants (1KP) initiative: access to gene family phylogenies and age distributions

10.1101/735076 ◽

2019 ◽

Cited By ~ 2

Author(s):

Zheng Li ◽

Michael S Barker

Keyword(s):

Gene Family ◽

Nuclear Gene ◽

Plant Evolution ◽

Plant Genome ◽

Total Evidence ◽

Whole Genome ◽

Data Set ◽

Green Plants ◽

Whole Genome Duplications ◽

Genome Duplications

AbstractPolyploidy or whole genome duplications (WGDs) repeatedly occurred during green plant evolution. To examine the evolutionary history of green plants in a phylogenomic framework, the 1KP project sequenced over 1000 transcriptomes across the Viridiplantae. The 1KP project provided a unique opportunity to study the distribution and occurrence of WGDs across the green plants. In the 1KP capstone analyses, we used a total evidence approach that combined inferences of WGDs from Ks and phylogenomic methods to infer and place ancient WGDs. Overall, 244 putative ancient WGDs were inferred across the Viridiplantae. Here, we describe these analyses and evaluate the consistency of the WGD inferences by comparing them to evidence from published syntenic analyses of plant genome assemblies. We find that our inferences are consistent with whole genome synteny analyses and our total evidence approach may minimize the false positive rate throughout the data set. Given these resources will be useful for many future analyses on gene and genome evolution in green plants, we release 383,679 nuclear gene family phylogenies and 2,306 gene age distribution (Ks) plots from the 1KP capstone paper.

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Degree of Functional Divergence in Duplicates Is Associated with Distinct Roles in Plant Evolution

Molecular Biology and Evolution ◽

10.1093/molbev/msaa302 ◽

2020 ◽

Author(s):

Akihiro Ezoe ◽

Kazumasa Shirai ◽

Kousuke Hanada

Keyword(s):

Gene Duplication ◽

Related Species ◽

Plant Evolution ◽

Whole Genome ◽

Duplicated Genes ◽

Closely Related Species ◽

Whole Genome Duplications ◽

New Genes ◽

Genome Duplications ◽

Tandem Duplications

Abstract Gene duplication is a major mechanism to create new genes. After gene duplication, some duplicated genes undergo functionalization, whereas others largely maintain redundant functions. Duplicated genes comprise various degrees of functional diversification in plants. However, the evolutionary fate of high and low diversified duplicates is unclear at genomic scale. To infer high and low diversified duplicates in Arabidopsis thaliana genome, we generated a prediction method for predicting whether a pair of duplicate genes was subjected to high or low diversification based on the phenotypes of knock-out mutants. Among 4,017 pairs of recently duplicated A. thaliana genes, 1,052 and 600 are high and low diversified duplicate pairs, respectively. The predictions were validated based on the phenotypes of generated knock-down transgenic plants. We determined that the high diversified duplicates resulting from tandem duplications tend to have lineage-specific functions, whereas the low diversified duplicates produced by whole-genome duplications are related to essential signaling pathways. To assess the evolutionary impact of high and low diversified duplicates in closely related species, we compared the retention rates and selection pressures on the orthologs of A. thaliana duplicates in two closely related species. Interestingly, high diversified duplicates resulting from tandem duplications tend to be retained in multiple lineages under positive selection. Low diversified duplicates by whole-genome duplications tend to be retained in multiple lineages under purifying selection. Taken together, the functional diversities determined by different duplication mechanisms had distinct effects on plant evolution.

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No evidence for the radiation time lag model after whole genome duplications in Teleostei

10.1101/099663 ◽

2017 ◽

Author(s):

Sacha Laurent ◽

Nicolas Salamin ◽

Marc Robinson-Rechavi

Keyword(s):

Time Lag ◽

Land Plant ◽

Plant Evolution ◽

Whole Genome ◽

Long Term Effects ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Lag Model ◽

Evolutionary Success ◽

Radiation Time

AbstractThe short and long term effects of polyploidization on the evolutionary fate of lineages is still unclear despite much interest. First recognized in land plants, it has become clear that polyploidization is widespread in eukaryotes, notably at the origin of vertebrates and teleost fishes. Many hypotheses have been proposed to link the evolutionary success of lineages and whole genome duplications. For instance, the radiation time lag model suggests that paleopolyploidy would favour the apparition of key innovations, although the evolutionary success would not become apparent until a later dispersion event. Some results indicate that this model may be observed during land plant evolution. In this work, we test predictions of the radiation time lag model using both fossil data and molecular phylogenies in ancient and more recent teleost whole genome duplications. We fail to find any evidence of delayed evolutionary success after any of these events and conclude that paleopolyploidization still remains to be unambiguously linked to evolutionary success in fishes.

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Phylogeny and Multiple Independent Whole-Genome Duplication Events in the Brassicales

10.1101/789040 ◽

2019 ◽

Cited By ~ 4

Author(s):

Makenzie E. Mabry ◽

Julia M. Brose ◽

Paul D. Blischak ◽

Brittany Sutherland ◽

Wade T. Dismukes ◽

...

Keyword(s):

Evolutionary History ◽

Whole Genome ◽

Genome Survey ◽

Whole Genome Duplications ◽

The Family ◽

Genome Duplications ◽

Duplication Events ◽

History Of ◽

Inference Methods ◽

Ideal Group

ABSTRACTWhole-genome duplications (WGDs) are prevalent throughout the evolutionary history of plants. For example, dozens of WGDs have been phylogenetically localized across the order Brassicales, specifically, within the family Brassicaceae. However, while its sister family, Cleomaceae, has also been characterized by a WGD, its placement, as well as that of other WGD events in other families in the order, remains unclear. Using phylo-transcriptomics from 74 taxa and genome survey sequencing for 66 of those taxa, we infer nuclear and chloroplast phylogenies to assess relationships among the major families of the Brassicales and within the Brassicaceae. We then use multiple methods of WGD inference to assess placement of WGD events. We not only present well-supported chloroplast and nuclear phylogenies for the Brassicales, but we also putatively place Th-α and provide evidence for previously unknown events, including one shared by at least two members of the Resedaceae, which we name Rs-α. Given its economic importance and many genomic resources, the Brassicales are an ideal group to continue assessing WGD inference methods. We add to the current conversation on WGD inference difficulties, by demonstrating that sampling is especially important for WGD identification.

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Molecular evolution of GDP-L-galactose phosphorylase, a key regulatory gene in plant ascorbate biosynthesis

AoB Plants ◽

10.1093/aobpla/plaa055 ◽

2020 ◽

Vol 12 (6) ◽

Author(s):

Junjie Tao ◽

Zhuan Hao ◽

Chunhui Huang

Keyword(s):

Molecular Evolution ◽

Abiotic Stress Tolerance ◽

Regulatory Gene ◽

Purifying Selection ◽

Plant Evolution ◽

Rapid Expansion ◽

Whole Genome ◽

Evolutionary Patterns ◽

Whole Genome Duplications ◽

Genome Duplications

Abstract Ascorbic acid (AsA) is a widespread antioxidant in living organisms, and plays essential roles in the growth and development of animals and plants as well as in the response to abiotic stress tolerance. The GDP-L-galactose phosphorylase (GGP) is a key regulatory gene in plant AsA biosynthesis that can regulate the concentration of AsA at the transcriptional and translational levels. The function and regulation mechanisms of GGP have been well understood; however, the molecular evolutionary patterns of the gene remain unclear. In this study, a total of 149 homologous sequences of GGP were sampled from 71 plant species covering the major groups of Viridiplantae, and the phylogenetic relationships, gene duplication and molecular evolution analyses of the genes were systematically investigated. Results showed that GGP genes are present throughout the plant kingdom and five shared whole-genome duplications and several lineage-specific whole-genome duplications were found, which led to the rapid expansion of GGPs in seed plants, especially in angiosperms. The structure of GGP genes was more conserved in land plants, but varied greatly in green algae, indicating that GGP may have undergone great differentiation in the early stages of plant evolution. Most GGP proteins had a conserved motif arrangement and composition, suggesting that plant GGPs have similar catalytic functions. Molecular evolutionary analyses showed that GGP genes were predominated by purifying selection, indicating that the gene is functionally conserved due to its vital importance in AsA biosynthesis. Most of the branches under positive selection identified by the branch-site model were mainly in the chlorophytes lineage, indicating episodic diversifying selection may contribute to the evolution of GGPs, especially in the chlorophyte lineage. The conserved function of GGP and its rapid expansion in angiosperms maybe one of the reasons for the increase of AsA content in angiosperms, enabling angiosperms to adapt to changing environments.

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Size is not everything: rates of genome size evolution, not C -value, correlate with speciation in angiosperms

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.2289 ◽

2015 ◽

Vol 282 (1820) ◽

pp. 20152289 ◽

Cited By ~ 37

Author(s):

Mark N. Puttick ◽

James Clark ◽

Philip C. J. Donoghue

Keyword(s):

Genome Size ◽

Sister Group ◽

Land Plants ◽

Whole Genome ◽

Whole Genome Duplications ◽

Rates Of Evolution ◽

Genome Size Evolution ◽

Size Evolution ◽

Genome Duplications ◽

Duplication Events

Angiosperms represent one of the key examples of evolutionary success, and their diversity dwarfs other land plants; this success has been linked, in part, to genome size and phenomena such as whole genome duplication events. However, while angiosperms exhibit a remarkable breadth of genome size, evidence linking overall genome size to diversity is equivocal, at best. Here, we show that the rates of speciation and genome size evolution are tightly correlated across land plants, and angiosperms show the highest rates for both, whereas very slow rates are seen in their comparatively species-poor sister group, the gymnosperms. No evidence is found linking overall genome size and rates of speciation. Within angiosperms, both the monocots and eudicots show the highest rates of speciation and genome size evolution, and these data suggest a potential explanation for the megadiversity of angiosperms. It is difficult to associate high rates of diversification with different types of polyploidy, but it is likely that high rates of evolution correlate with a smaller genome size after genome duplications. The diversity of angiosperms may, in part, be due to an ability to increase evolvability by benefiting from whole genome duplications, transposable elements and general genome plasticity.

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