Conserved Molecular Function and Regulatory Subfunctionalization of the LORELEI Gene Family in Brassicaceae

AbstractA signaling complex comprising members of the LORELEI (LRE)-LIKE GPI-anchored protein (LLG) and Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) families perceive RAPID ALKALINIZATION FACTOR (RALF) peptides and regulate growth, development, reproduction, and immunity in Arabidopsis thaliana. Duplications in each component, which potentially could generate thousands of combinations of this signaling complex, are also evident in other angiosperms. Widespread duplication in angiosperms raises the question what evolutionary mechanisms underlie the expansion and retention of these gene families, as duplicated genes are typically rendered non-functional. As genetic and genomic resources make it a tractable model system, here we investigated this question using LLG gene family evolution and function in Brassicaceae. We first established that the LLG homologs in the Brassicaceae resulted from duplication events that pre-date the divergence of species in this family. Complementation of vegetative phenotypes in llg1 by LRE, LLG2, and LLG3 showed that the molecular functions of LLG homologs in A. thaliana are conserved. We next tested the possibility that differences in gene expression (regulatory subfunctionalization), rather than functional divergence, played a role in retention of these duplicated genes. For this, we examined the function and expression of LRE and LLG1 in A. thaliana and their single copy ortholog in Cleome violacea (Clevi LRE/LLG1), a representative species outside the Brassicaceae, but from the same order (Brassicales). We showed that expression of LLG1 and LRE did not overlap in A. thaliana and that Clevi-LRE/LLG1 expression in C. violacea encompassed all the expression domains of A. thaliana LRE + LLG1. Still, complementation experiments showed that LLG1 rescued reproductive phenotypes in lre and that Clevi LRE/LLG1 rescued both vegetative and reproductive phenotypes in llg1 and lre. Additionally, we found that expression of LLG2 and LLG3 in A. thaliana have also diverged from the expression of their corresponding single copy ortholog (Clevi LLG2/LLG3) in C. violacea. Our findings demonstrated how regulatory subfunctionalization, rather than functional divergence, underlies the retention of the LLG gene family in Brassicaceae. Our findings on the regulatory divergence and functional conservation provide an experimental framework to characterize the combinatorial assembly and function of this critical plant cell signaling complex.

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Integrating phylogenetic and network approaches to study gene family evolution: the case of the AGAMOUS family of floral genes

10.1101/195669 ◽

2017 ◽

Author(s):

Daniel S. Carvalho ◽

James C. Schnable ◽

Ana Maria R. Almeida

Keyword(s):

Gene Family ◽

Functional Divergence ◽

Gene Tree ◽

Gene Families ◽

Gene Family Evolution ◽

Phylogenetic Methods ◽

Combined Use ◽

Approaches To Study ◽

Additional Support ◽

Network Approaches

AbstractThe study of gene family evolution has benefited from the use of phylogenetic tools, which can greatly inform studies of both relationships within gene families and functional divergence. Here, we propose the use of a network-based approach that in combination with phylogenetic methods can provide additional support for models of gene family evolution. We dissect the contributions of each method to the improved understanding of relationships and functions within the well-characterized family of AGAMOUS floral development genes. The results obtained with the two methods largely agreed with one another. In particular, we show how network approaches can provide improved interpretations of branches with low support in a conventional gene tree. The network approach used here may also better reflect known and suspected patterns of functional divergence relative to phylogenetic methods. Overall, we believe that the combined use of phylogenetic and network tools provide more robust assessments of gene family evolution.

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Comparable Rates of Gene Loss and Functional Divergence After Genome Duplications Early in Vertebrate Evolution

Genetics ◽

10.1093/genetics/147.3.1259 ◽

1997 ◽

Vol 147 (3) ◽

pp. 1259-1266 ◽

Cited By ~ 5

Author(s):

Joseph H Nadeau ◽

David Sankoff

Keyword(s):

Gene Family ◽

Protein Function ◽

Gene Loss ◽

Functional Divergence ◽

Gene Families ◽

High Rate ◽

Vertebrate Evolution ◽

Duplicated Genes ◽

Apparent Contradiction ◽

Genome Duplications

Duplicated genes are an important source of new protein functions and novel developmental and physiological pathways. Whereas most models for fate of duplicated genes show that they tend to be rapidly lost, models for pathway evolution suggest that many duplicated genes rapidly acquire novel functions. Little empirical evidence is available, however, for the relative rates of gene loss vs. divergence to help resolve these contradictory expectations. Gene families resulting from genome duplications provide an opportunity to address this apparent contradiction. With genome duplication, the number of duplicated genes in a gene family is at most 2n, where n is the number of duplications. The size of each gene family, e.g., 1, 2, 3,..., 2n, reflects the patterns of gene loss vs. functional divergence after duplication. We focused on gene families in humans and mice that arose from genome duplications in early vertebrate evolution and we analyzed the frequency distribution of gene family size, i.e., the number of families with two, three or four members. All the models that we evaluated showed that duplicated genes are almost as likely to acquire a new and essential function as to be lost through acquisition of mutations that compromise protein function. An explanation for the unexpectedly high rate of functional divergence is that duplication allows genes to accumulate more neutral than disadvantageous mutations, thereby providing more opportunities to acquire diversified functions and pathways.

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Ecological correlates of gene family size: the draft genome of the redheaded pine sawfly Neodiprion lecontei

10.1101/2021.03.14.435331 ◽

2021 ◽

Author(s):

Kim Vertacnik ◽

Danielle Herrig ◽

R Keating Godfrey ◽

Tom Hill ◽

Scott Geib ◽

...

Keyword(s):

Gene Family ◽

Family Size ◽

Draft Genome ◽

Gene Families ◽

Gene Family Evolution ◽

Gene Gain ◽

Ecological Specialization ◽

Dietary Specialization ◽

Pine Sawfly ◽

Neodiprion Lecontei

A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a non-eusocial hymenopteran and exemplar of a pine-specialized lineage evolved from angiosperm-feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions and characterized their genomic distributions and evolutionary history. Our results suggest that expansions of bitter gustatory receptor (GR), clan 3 cytochrome P450 (CYP3), and antimicrobial peptide (AMP) subfamilies may have contributed to pine adaptation. By contrast, there was no evidence of recent gene family contraction via pseudogenization. Next, we compared the number of genes in these same families across insect taxa that vary in diet, dietary specialization, and social behavior. In Hymenoptera, herbivory was associated with large GR and small olfactory receptor (OR) families, eusociality was associated with large OR and small AMP families, and--unlike investigations among more closely related taxa--ecological specialization was not related to gene family size. Overall, our results suggest that gene families that mediate ecological interactions may expand and contract predictably in response to particular selection pressures, however, the ecological drivers and temporal pace of gene gain and loss likely varies considerably across gene families.

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Evolutionary history of dimethylsulfoniopropionate (DMSP) demethylation enzyme DmdA in marine bacteria

10.1101/766360 ◽

2019 ◽

Author(s):

Laura Hernández ◽

Alberto Vicens ◽

Luis Enrique Eguiarte ◽

Valeria Souza ◽

Valerie De Anda ◽

...

Keyword(s):

Gene Family ◽

Evolutionary History ◽

Common Ancestor ◽

Functional Divergence ◽

Gene Families ◽

Recent Common Ancestor ◽

Common Ancestry ◽

Demethylation Pathway ◽

History Of ◽

New Gene

ABSTRACTDimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton, is predominantly degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: 1) a recent common ancestor of DmdA and GcvT, 2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and 3) pre-adapted enzymes to DMSP prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to exposition to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur rich atmosphere and anoxic ocean, compared to recent Roseobacter ecoparalogs (copies performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.

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Birth-and-death evolution of the fatty acyl-CoA reductase (FAR) gene family and diversification of cuticular hydrocarbon synthesis in Drosophila

10.1101/509588 ◽

2019 ◽

Cited By ~ 1

Author(s):

Cédric Finet ◽

Kailey Slavik ◽

Jian Pu ◽

Sean B. Carroll ◽

Henry Chung

Keyword(s):

Fatty Acid ◽

Gene Family ◽

Cuticular Hydrocarbon ◽

Evolutionary Model ◽

Gene Families ◽

Single Copy ◽

Fatty Acyl ◽

Comparative Approach ◽

Hydrocarbon Synthesis ◽

Functional Studies

AbstractThe birth-and-death evolutionary model proposes that some members of a multigene family are phylogenetically stable and persist as a single copy over time whereas other members are phylogenetically unstable and undergo frequent duplication and loss. Functional studies suggest that stable genes are likely to encode essential functions, while rapidly evolving genes reflect phenotypic differences in traits that diverge rapidly among species. One such class of rapidly diverging traits are insect cuticular hydrocarbons (CHCs), which play dual roles in chemical communications as short-range recognition pheromones as well as protecting the insect from desiccation. Insect CHCs diverge rapidly between related species leading to ecological adaptation and/or reproductive isolation. Because the CHC and essential fatty acid biosynthetic pathways share common genes, we hypothesized that genes involved in the synthesis of CHCs would be evolutionary unstable, while those involved in fatty acid-associated essential functions would be evolutionary stable. To test this hypothesis, we investigated the evolutionary history of the fatty acyl-CoA reductases (FARs) gene family that encodes enzymes in CHC synthesis. We compiled a unique dataset of 200 FAR proteins across 12 Drosophila species. We uncovered a broad diversity in FAR content which is generated by gene duplications, subsequent gene losses, and alternative splicing. We also show that FARs expressed in oenocytes and presumably involved in CHC synthesis are more unstable than FARs from other tissues. We suggest that a comparative approach investigating the birth-and-death evolution of gene families can identify candidate genes involved in rapidly diverging traits between species.

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The whale shark genome reveals patterns of vertebrate gene family evolution

eLife ◽

10.7554/elife.65394 ◽

2021 ◽

Vol 10 ◽

Author(s):

Milton Tan ◽

Anthony K Redmond ◽

Helen Dooley ◽

Ryo Nozu ◽

Keiichi Sato ◽

...

Keyword(s):

Gene Family ◽

Human Cancer ◽

Gene Families ◽

Immune Defense ◽

Gene Family Evolution ◽

Whale Shark ◽

Ancestral Gene ◽

Long Read ◽

Pathogen Recognition Receptors ◽

Major Increase

Chondrichthyes (cartilaginous fishes) are fundamental for understanding vertebrate evolution, yet their genomes are understudied. We report long-read sequencing of the whale shark genome to generate the best gapless chondrichthyan genome assembly yet with higher contig contiguity than all other cartilaginous fish genomes, and studied vertebrate genomic evolution of ancestral gene families, immunity, and gigantism. We found a major increase in gene families at the origin of gnathostomes (jawed vertebrates) independent of their genome duplication. We studied vertebrate pathogen recognition receptors (PRRs), which are key in initiating innate immune defense, and found diverse patterns of gene family evolution, demonstrating that adaptive immunity in gnathostomes did not fully displace germline-encoded PRR innovation. We also discovered a new Toll-like receptor (TLR29) and three NOD1 copies in the whale shark. We found chondrichthyan and giant vertebrate genomes had decreased substitution rates compared to other vertebrates, but gene family expansion rates varied among vertebrate giants, suggesting substitution and expansion rates of gene families are decoupled in vertebrate genomes. Finally, we found gene families that shifted in expansion rate in vertebrate giants were enriched for human cancer-related genes, consistent with gigantism requiring adaptations to suppress cancer.

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Evolutionary history of dimethylsulfoniopropionate (DMSP) demethylation enzyme DmdA in marine bacteria

PeerJ ◽

10.7717/peerj.9861 ◽

2020 ◽

Vol 8 ◽

pp. e9861

Author(s):

Laura Hernández ◽

Alberto Vicens ◽

Luis E. Eguiarte ◽

Valeria Souza ◽

Valerie De Anda ◽

...

Keyword(s):

Gene Family ◽

Marine Bacteria ◽

Evolutionary History ◽

Functional Divergence ◽

Gene Families ◽

Recent Common Ancestor ◽

Demethylation Pathway ◽

History Of ◽

New Gene ◽

Enzymatic Adaptation

Dimethylsulfoniopropionate (DMSP), an osmolyte produced by oceanic phytoplankton and bacteria, is primarily degraded by bacteria belonging to the Roseobacter lineage and other marine Alphaproteobacteria via DMSP-dependent demethylase A protein (DmdA). To date, the evolutionary history of DmdA gene family is unclear. Some studies indicate a common ancestry between DmdA and GcvT gene families and a co-evolution between Roseobacter and the DMSP-producing-phytoplankton around 250 million years ago (Mya). In this work, we analyzed the evolution of DmdA under three possible evolutionary scenarios: (1) a recent common ancestor of DmdA and GcvT, (2) a coevolution between Roseobacter and the DMSP-producing-phytoplankton, and (3) an enzymatic adaptation for utilizing DMSP in marine bacteria prior to Roseobacter origin. Our analyses indicate that DmdA is a new gene family originated from GcvT genes by duplication and functional divergence driven by positive selection before a coevolution between Roseobacter and phytoplankton. Our data suggest that Roseobacter acquired dmdA by horizontal gene transfer prior to an environment with higher DMSP. Here, we propose that the ancestor that carried the DMSP demethylation pathway genes evolved in the Archean, and was exposed to a higher concentration of DMSP in a sulfur-rich atmosphere and anoxic ocean, compared to recent Roseobacter eco-orthologs (orthologs performing the same function under different conditions), which should be adapted to lower concentrations of DMSP.

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Comprehensive genomic analysis of the DUF4228 gene family in land plants and expression profiling of ATDUF4228 under abiotic stresses

BMC Genomics ◽

10.1186/s12864-019-6389-3 ◽

2020 ◽

Vol 21 (1) ◽

Cited By ~ 2

Author(s):

Qi Yang ◽

Xiaocui Niu ◽

Xiaona Tian ◽

Xiujuan Zhang ◽

Jingyu Cong ◽

...

Keyword(s):

Gene Family ◽

Expression Profiling ◽

Abiotic Stresses ◽

Genomic Analysis ◽

Gene Families ◽

Land Plant ◽

Biological Functions ◽

Phylogenetic Groups ◽

Functional Conservation ◽

Group I

Abstract Background Domain of unknown function (DUF) proteins represent a number of gene families that encode functionally uncharacterized proteins in eukaryotes. The DUF4228 gene family is one of these families in plants that has not been described previously. Results In this study, we performed an extensive comparative analysis of DUF4228 proteins and determined their phylogeny in the plant lineage. A total of 489 high-confidence DUF4228 family members were identified from 14 land plant species, which sub-divided into three distinct phylogenetic groups: group I, group II and group III. A highly conserved DUF4228 domain and motif distribution existed in each group, implying their functional conservation. To reveal the possible biological functions of these DUF4228 genes, 25 ATDUF4228 sequences from Arabidopsis thaliana were selected for further analysis of characteristics such as their chromosomal position, gene duplications and gene structures. Ka/Ks analysis identified seven segmental duplication events, while no tandemly duplication gene pairs were found in A. thaliana. Some cis-elements responding to abiotic stress and phytohormones were identified in the upstream sequences of the ATDUF4228 genes. Expression profiling of the ATDUF4228 genes under abiotic stresses (mainly osmotic, salt and cold) and protein-protein interaction prediction suggested that some ATDUF4228 genes are may be involved in the pathways of plant resistance to abiotic stresses. Conclusion These results expand our knowledge of the evolution of the DUF4228 gene family in plants and will contribute to the elucidation of the biological functions of DUF4228 genes in the future.

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Ab Initio Construction and Evolutionary Analysis of Protein-Coding Gene Families with Partially Homologous Relationships: Closely Related Drosophila Genomes as a Case Study

Genome Biology and Evolution ◽

10.1093/gbe/evaa041 ◽

2020 ◽

Vol 12 (3) ◽

pp. 185-202

Author(s):

Xia Han ◽

Jindan Guo ◽

Erli Pang ◽

Hongtao Song ◽

Kui Lin

Keyword(s):

Gene Family ◽

De Novo ◽

Gene Families ◽

Gene Family Evolution ◽

Evolutionary Analysis ◽

Protein Coding ◽

Protein Coding Genes ◽

Genome Phylogeny ◽

Partial Homology

Abstract How have genes evolved within a well-known genome phylogeny? Many protein-coding genes should have evolved as a whole at the gene level, and some should have evolved partly through fragments at the subgene level. To comprehensively explore such complex homologous relationships and better understand gene family evolution, here, with de novo-identified modules, the subgene units which could consecutively cover proteins within a set of closely related species, we applied a new phylogeny-based approach that considers evolutionary models with partial homology to classify all protein-coding genes in nine Drosophila genomes. Compared with two other popular methods for gene family construction, our approach improved practical gene family classifications with a more reasonable view of homology and provided a much more complete landscape of gene family evolution at the gene and subgene levels. In the case study, we found that most expanded gene families might have evolved mainly through module rearrangements rather than gene duplications and mainly generated single-module genes through partial gene duplication, suggesting that there might be pervasive subgene rearrangement in the evolution of protein-coding gene families. The use of a phylogeny-based approach with partial homology to classify and analyze protein-coding gene families may provide us with a more comprehensive landscape depicting how genes evolve within a well-known genome phylogeny.

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The WTX/AMER1 gene family: evolution, signature and function

BMC Evolutionary Biology ◽

10.1186/1471-2148-10-280 ◽

2010 ◽

Vol 10 (1) ◽

pp. 280 ◽

Cited By ~ 12

Author(s):

Agnès Boutet ◽

Glenda Comai ◽

Andreas Schedl

Keyword(s):

Gene Family ◽

Gene Family Evolution ◽

And Function

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