Mechanistic insights into the evolution of DUF26-containing proteins in land plants

AbstractLarge protein families are a prominent feature of plant genomes and their size variation is a key element for adaptation in plants. Here we infer the evolutionary history of a representative protein family, the DOMAIN OF UNKNOWN FUNCTION (DUF) 26-containing proteins. The DUF26 first appeared in secreted proteins. Domain duplications and rearrangements led to the emergence of CYSTEINE-RICH RECEPTOR-LIKE PROTEIN KINASES (CRKs) and PLASMODESMATA-LOCALIZED PROTEINS (PDLPs). While the DUF26 itself is specific to land plants, structural analyses of Arabidopsis PDLP5 and PDLP8 ectodomains revealed strong similarity to fungal lectins. Therefore, we propose that DUF26-containing proteins constitute a novel group of plant carbohydrate-binding proteins. Following their appearance, CRKs expanded both through tandem duplications and preferential retention of duplicates in whole genome duplication events, whereas PDLPs evolved according to the dosage balance hypothesis. Based on our findings, we suggest that the main mechanism of expansion in new gene families is small-scale duplication, whereas genome fractionation and genetic drift after whole genome multiplications drive families towards dosage balance.

Download Full-text

Synteny-Guided Resolution of Gene Trees Clarifies the Functional Impact of Whole-Genome Duplications

Molecular Biology and Evolution ◽

10.1093/molbev/msaa149 ◽

2020 ◽

Vol 37 (11) ◽

pp. 3324-3337

Author(s):

Elise Parey ◽

Alexandra Louis ◽

Cédric Cabau ◽

Yann Guiguen ◽

Hugues Roest Crollius ◽

...

Keyword(s):

Gene Families ◽

Sequence Evolution ◽

Whole Genome ◽

Gene Trees ◽

Ensembl Database ◽

Whole Genome Duplications ◽

Gene Copies ◽

Genome Duplications ◽

Phenotypic Robustness ◽

New Gene

Abstract Whole-genome duplications (WGDs) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here, we present Synteny-guided CORrection of Paralogies and Orthologies (SCORPiOs), a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-My-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,394) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

Download Full-text

Synteny-guided resolution of gene trees clarifies the functional impact of whole genome duplications

10.1101/2020.01.30.926915 ◽

2020 ◽

Author(s):

Elise Parey ◽

Alexandra Louis ◽

Cédric Cabau ◽

Yann Guiguen ◽

Hugues Roest Crollius ◽

...

Keyword(s):

Gene Families ◽

Sequence Evolution ◽

Whole Genome ◽

Gene Trees ◽

Ensembl Database ◽

Whole Genome Duplications ◽

Gene Copies ◽

Genome Duplications ◽

Phenotypic Robustness ◽

New Gene

AbstractWhole genome duplications (WGD) have major impacts on the evolution of species, as they produce new gene copies contributing substantially to adaptation, isolation, phenotypic robustness, and evolvability. They result in large, complex gene families with recurrent gene losses in descendant species that sequence-based phylogenetic methods fail to reconstruct accurately. As a result, orthologs and paralogs are difficult to identify reliably in WGD-descended species, which hinders the exploration of functional consequences of WGDs. Here we present SCORPiOs, a novel method to reconstruct gene phylogenies in the context of a known WGD event. WGDs generate large duplicated syntenic regions, which SCORPiOs systematically leverages as a complement to sequence evolution to infer the evolutionary history of genes. We applied SCORPiOs to the 320-million-year-old WGD at the origin of teleost fish. We find that almost one in four teleost gene phylogenies in the Ensembl database (3,391) are inconsistent with their syntenic contexts. For 70% of these gene families (2,387), we were able to propose an improved phylogenetic tree consistent with both the molecular substitution distances and the local syntenic information. We show that these synteny-guided phylogenies are more congruent with the species tree, with sequence evolution and with expected expression conservation patterns than those produced by state-of-the-art methods. Finally, we show that synteny-guided gene trees emphasize contributions of WGD paralogs to evolutionary innovations in the teleost clade.

Download Full-text

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.

Download Full-text

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

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2013.0353 ◽

2014 ◽

Vol 369 (1648) ◽

pp. 20130353 ◽

Cited By ~ 90

Author(s):

Kevin Vanneste ◽

Steven Maere ◽

Yves Van de Peer

Keyword(s):

Large Scale ◽

Plant Evolution ◽

Small Scale ◽

Whole Genome ◽

Polyploid Species ◽

Plant Genomes ◽

Whole Genome Duplications ◽

Genome Duplications ◽

Duplication Events ◽

Biological Innovations

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.

Download Full-text

Whole genome duplication and transposable element proliferation drive genome expansion in Corydoradinae catfishes

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.2732 ◽

2018 ◽

Vol 285 (1872) ◽

pp. 20172732 ◽

Cited By ~ 10

Author(s):

Sarah Marburger ◽

Markos A. Alexandrou ◽

John B. Taggart ◽

Simon Creer ◽

Gary Carvalho ◽

...

Keyword(s):

Transposable Element ◽

Genome Size ◽

Size Variation ◽

Whole Genome ◽

Evolutionary Potential ◽

Posterior Density ◽

Genome Size Variation ◽

Genome Duplications ◽

Duplication Events ◽

Highest Posterior Density

Genome size varies significantly across eukaryotic taxa and the largest changes are typically driven by macro-mutations such as whole genome duplications (WGDs) and proliferation of repetitive elements. These two processes may affect the evolutionary potential of lineages by increasing genetic variation and changing gene expression. Here, we elucidate the evolutionary history and mechanisms underpinning genome size variation in a species-rich group of Neotropical catfishes (Corydoradinae) with extreme variation in genome size—0.6 to 4.4 pg per haploid cell. First, genome size was quantified in 65 species and mapped onto a novel fossil-calibrated phylogeny. Two evolutionary shifts in genome size were identified across the tree—the first between 43 and 49 Ma (95% highest posterior density (HPD) 36.2–68.1 Ma) and the second at approximately 19 Ma (95% HPD 15.3–30.14 Ma). Second, restriction-site-associated DNA (RAD) sequencing was used to identify potential WGD events and quantify transposable element (TE) abundance in different lineages. Evidence of two lineage-scale WGDs was identified across the phylogeny, the first event occurring between 54 and 66 Ma (95% HPD 42.56–99.5 Ma) and the second at 20–30 Ma (95% HPD 15.3–45 Ma) based on haplotype numbers per contig and between 35 and 44 Ma (95% HPD 30.29–64.51 Ma) and 20–30 Ma (95% HPD 15.3–45 Ma) based on SNP read ratios. TE abundance increased considerably in parallel with genome size, with a single TE-family (TC1-IS630-Pogo) showing several increases across the Corydoradinae, with the most recent at 20–30 Ma (95% HPD 15.3–45 Ma) and an older event at 35–44 Ma (95% HPD 30.29–64.51 Ma). We identified signals congruent with two WGD duplication events, as well as an increase in TE abundance across different lineages, making the Corydoradinae an excellent model system to study the effects of WGD and TEs on genome and organismal evolution.

Download Full-text

Early stages of functional diversification in the Rab GTPase gene family revealed by genomic and localization studies in Paramecium species

Molecular Biology of the Cell ◽

10.1091/mbc.e16-06-0361 ◽

2017 ◽

Vol 28 (8) ◽

pp. 1101-1110 ◽

Cited By ~ 4

Author(s):

Lydia J. Bright ◽

Jean-Francois Gout ◽

Michael Lynch

Keyword(s):

Gene Family ◽

Gene Families ◽

Rab Gtpase ◽

Rab Proteins ◽

Whole Genome ◽

Amino Acid Residues ◽

Functional Diversification ◽

Whole Genome Duplications ◽

Genome Duplications ◽

New Gene

New gene functions arise within existing gene families as a result of gene duplication and subsequent diversification. To gain insight into the steps that led to the functional diversification of paralogues, we tracked duplicate retention patterns, expression-level divergence, and subcellular markers of functional diversification in the Rab GTPase gene family in three Paramecium aurelia species. After whole-genome duplication, Rab GTPase duplicates are more highly retained than other genes in the genome but appear to be diverging more rapidly in expression levels, consistent with early steps in functional diversification. However, by localizing specific Rab proteins in Paramecium cells, we found that paralogues from the two most recent whole-genome duplications had virtually identical localization patterns, and that less closely related paralogues showed evidence of both conservation and diversification. The functionally conserved paralogues appear to target to compartments associated with both endocytic and phagocytic recycling functions, confirming evolutionary and functional links between the two pathways in a divergent eukaryotic lineage. Because the functionally diversifying paralogues are still closely related to and derived from a clade of functionally conserved Rab11 genes, we were able to pinpoint three specific amino acid residues that may be driving the change in the localization and thus the function in these proteins.

Download Full-text

Constraining the timing of whole genome duplication in plant evolutionary history

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.0912 ◽

2017 ◽

Vol 284 (1858) ◽

pp. 20170912 ◽

Cited By ~ 18

Author(s):

James W. Clark ◽

Philip C. J. Donoghue

Keyword(s):

Whole Genome Duplication ◽

Genome Duplication ◽

Gene Families ◽

Plant Evolution ◽

Resistance Testing ◽

Whole Genome ◽

Evolutionary Innovation ◽

Major Genome ◽

Duplication Events ◽

Clock Analysis

Whole genome duplication (WGD) has occurred in many lineages within the tree of life and is invariably invoked as causal to evolutionary innovation, increased diversity, and extinction resistance. Testing such hypotheses is problematic, not least since the timing of WGD events has proven hard to constrain. Here we show that WGD events can be dated through molecular clock analysis of concatenated gene families, calibrated using fossil evidence for the ages of species divergences that bracket WGD events. We apply this approach to dating the two major genome duplication events shared by all seed plants ( ζ ) and flowering plants ( ɛ ), estimating the seed plant WGD event at 399–381 Ma, and the angiosperm WGD event at 319–297 Ma. These events thus took place early in the stem of both lineages, precluding hypotheses of WGD conferring extinction resistance, driving dramatic increases in innovation and diversity, but corroborating and qualifying the more permissive hypothesis of a ‘lag-time’ in realizing the effects of WGD in plant evolution.

Download Full-text

Phylogenetic Analysis of T-Box Genes Demonstrates the Importance of Amphioxus for Understanding Evolution of the Vertebrate Genome

Genetics ◽

10.1093/genetics/156.3.1249 ◽

2000 ◽

Vol 156 (3) ◽

pp. 1249-1257

Author(s):

Ilya Ruvinsky ◽

Lee M Silver ◽

Jeremy J Gibson-Brown

Keyword(s):

Phylogenetic Analysis ◽

Whole Genome Duplication ◽

Genome Duplication ◽

Gene Families ◽

Vertebrate Evolution ◽

Whole Genome ◽

Vertebrate Genome ◽

T Box ◽

Genetic Complexity ◽

History Of

Abstract The duplication of preexisting genes has played a major role in evolution. To understand the evolution of genetic complexity it is important to reconstruct the phylogenetic history of the genome. A widely held view suggests that the vertebrate genome evolved via two successive rounds of whole-genome duplication. To test this model we have isolated seven new T-box genes from the primitive chordate amphioxus. We find that each amphioxus gene generally corresponds to two or three vertebrate counterparts. A phylogenetic analysis of these genes supports the idea that a single whole-genome duplication took place early in vertebrate evolution, but cannot exclude the possibility that a second duplication later took place. The origin of additional paralogs evident in this and other gene families could be the result of subsequent, smaller-scale chromosomal duplications. Our findings highlight the importance of amphioxus as a key organism for understanding evolution of the vertebrate genome.

Download Full-text

A Comprehensive Phylogenetic and Bioinformatics Survey of Lectins in the Fungal Kingdom

Journal of Fungi ◽

10.3390/jof7060453 ◽

2021 ◽

Vol 7 (6) ◽

pp. 453

Author(s):

Annie Lebreton ◽

François Bonnardel ◽

Yu-Cheng Dai ◽

Anne Imberty ◽

Francis M. Martin ◽

...

Keyword(s):

Evolutionary Relationship ◽

Large Family ◽

Gene Families ◽

Carbohydrate Binding ◽

Sequence Motifs ◽

Fungal Lectin ◽

Quaternary Structures ◽

High Degree ◽

Carbohydrate Ligand ◽

Fungal Kingdom

Fungal lectins are a large family of carbohydrate-binding proteins with no enzymatic activity. They play fundamental biological roles in the interactions of fungi with their environment and are found in many different species across the fungal kingdom. In particular, their contribution to defense against feeders has been emphasized, and when secreted, lectins may be involved in the recognition of bacteria, fungal competitors and specific host plants. Carbohydrate specificities and quaternary structures vary widely, but evidence for an evolutionary relationship within the different classes of fungal lectins is supported by a high degree of amino acid sequence identity. The UniLectin3D database contains 194 fungal lectin 3D structures, of which 129 are characterized with a carbohydrate ligand. Using the UniLectin3D lectin classification system, 109 lectin sequence motifs were defined to screen 1223 species deposited in the genomic portal MycoCosm of the Joint Genome Institute. The resulting 33,485 putative lectin sequences are organized in MycoLec, a publicly available and searchable database. These results shed light on the evolution of the lectin gene families in fungi.

Download Full-text

Whole-genome sequencing from the New Zealand Saccharomyces cerevisiae population reveals the genomic impacts of novel microbial range expansion

G3 Genes|Genome|Genetics ◽

10.1093/g3journal/jkaa027 ◽

2020 ◽

Vol 11 (1) ◽

Author(s):

Peter Higgins ◽

Cooper A Grace ◽

Soon A Lee ◽

Matthew R Goddard

Keyword(s):

Saccharomyces Cerevisiae ◽

New Zealand ◽

Whole Genome Sequencing ◽

Genome Sequencing ◽

Range Expansion ◽

Copy Number ◽

Small Scale ◽

Whole Genome ◽

Copy Number Changes ◽

The Impact

Abstract Saccharomyces cerevisiae is extensively utilized for commercial fermentation, and is also an important biological model; however, its ecology has only recently begun to be understood. Through the use of whole-genome sequencing, the species has been characterized into a number of distinct subpopulations, defined by geographical ranges and industrial uses. Here, the whole-genome sequences of 104 New Zealand (NZ) S. cerevisiae strains, including 52 novel genomes, are analyzed alongside 450 published sequences derived from various global locations. The impact of S. cerevisiae novel range expansion into NZ was investigated and these analyses reveal the positioning of NZ strains as a subgroup to the predominantly European/wine clade. A number of genomic differences with the European group correlate with range expansion into NZ, including 18 highly enriched single-nucleotide polymorphism (SNPs) and novel Ty1/2 insertions. While it is not possible to categorically determine if any genetic differences are due to stochastic process or the operations of natural selection, we suggest that the observation of NZ-specific copy number increases of four sugar transporter genes in the HXT family may reasonably represent an adaptation in the NZ S. cerevisiae subpopulation, and this correlates with the observations of copy number changes during adaptation in small-scale experimental evolution studies.

Download Full-text