scholarly journals Analysis of fungal genomes reveals commonalities of intron gain or loss and functions in intron-poor species

Author(s):  
Chun Shen Lim ◽  
Brooke N Weinstein ◽  
Scott W Roy ◽  
Chris M Brown

Abstract Previous evolutionary reconstructions have concluded that early eukaryotic ancestors including both the last common ancestor of eukaryotes and of all fungi had intron-rich genomes. By contrast, some extant eukaryotes have few introns, underscoring the complex histories of intron-exon structures, and raising the question as to why these few introns are retained. Here we have used recently available fungal genomes to address a variety of questions related to intron evolution. Evolutionary reconstruction of intron presence and absence using 263 diverse fungal species supports the idea that massive intron reduction through intron loss has occurred in multiple clades. The intron densities estimated in various fungal ancestors differ from zero to 7.6 introns per one kbp of protein-coding sequence. Massive intron loss has occurred not only in microsporidian parasites and saccharomycetous yeasts, but also in diverse smuts and allies. To investigate the roles of the remaining introns in highly-reduced species, we have searched for their special characteristics in eight intron-poor fungi. Notably, the introns of ribosome associated genes RPL7 and NOG2 have conserved positions; both intron-containing genes encoding snoRNAs. Furthermore, both the proteins and snoRNAs are involved in ribosome biogenesis, suggesting that the expression of the protein-coding genes and non-coding snoRNAs may be functionally coordinated. Indeed, these introns are also conserved in three-quarters of fungi species. Our study shows that fungal introns have a complex evolutionary history and underappreciated roles in gene expression.

2020 ◽  
Author(s):  
Chun Shen Lim ◽  
Brooke N. Weinstein ◽  
Scott W. Roy ◽  
Chris M. Brown

ABSTRACTCurrent evolutionary reconstructions predict that early eukaryotic ancestors including both the last common ancestor of eukaryotes and of all fungi had intron-rich genomes. However, some extant eukaryotes have few introns, raising the question as to why these few introns are retained. Here we have used recently available fungal genomes to address this question. Evolutionary reconstruction of intron presence and absence using 263 diverse fungal species support the idea that massive intron loss has occurred in multiple clades. The intron densities estimated in the fungal ancestral states differ from zero to 8.28 introns per one kbp of protein-coding gene. Massive intron loss has occurred not only in microsporidian parasites and saccharomycetous yeasts (0.01 and 0.05 introns/kbp on average, respectively), but also in diverse smuts and allies (e.g. Ustilago maydis, Meira miltonrushii and Malassezia globosa have 0.06, 0.10 and 0.20 introns/kbp, respectively). To investigate the roles of introns, we searched for their special characteristics using 1302 orthologous genes from eight intron-poor fungi. Notably, most of these introns are found close to the translation initiation codons. Our transcriptome and translatome data analyses showed that these introns are from genes with both higher mRNA expression and translation efficiency. Furthermore, these introns are common in specific classes of genes (e.g. genes involved in translation and Golgi vesicle transport), and rare in others (e.g. base-excision repair genes). Our study shows that fungal introns have a complex evolutionary history and underappreciated roles in gene expression.


2020 ◽  
Vol 117 (49) ◽  
pp. 31267-31277
Author(s):  
Huei-Mien Ke ◽  
Hsin-Han Lee ◽  
Chan-Yi Ivy Lin ◽  
Yu-Ching Liu ◽  
Min R. Lu ◽  
...  

Mushroom-forming fungi in the order Agaricales represent an independent origin of bioluminescence in the tree of life; yet the diversity, evolutionary history, and timing of the origin of fungal luciferases remain elusive. We sequenced the genomes and transcriptomes of five bonnet mushroom species (Mycenaspp.), a diverse lineage comprising the majority of bioluminescent fungi. Two species with haploid genome assemblies ∼150 Mb are among the largest in Agaricales, and we found that a variety of repeats betweenMycenaspecies were differentially mediated by DNA methylation. We show that bioluminescence evolved in the last common ancestor of mycenoid and the marasmioid clade of Agaricales and was maintained through at least 160 million years of evolution. Analyses of synteny across genomes of bioluminescent species resolved how the luciferase cluster was derived by duplication and translocation, frequently rearranged and lost in mostMycenaspecies, but conserved in theArmillarialineage. Luciferase cluster members were coexpressed across developmental stages, with the highest expression in fruiting body caps and stipes, suggesting fruiting-related adaptive functions. Our results contribute to understanding a de novo origin of bioluminescence and the corresponding gene cluster in a diverse group of enigmatic fungal species.


GigaScience ◽  
2019 ◽  
Vol 8 (7) ◽  
Author(s):  
Aki Ohdera ◽  
Cheryl L Ames ◽  
Rebecca B Dikow ◽  
Ehsan Kayal ◽  
Marta Chiodin ◽  
...  

Abstract Background Anthozoa, Endocnidozoa, and Medusozoa are the 3 major clades of Cnidaria. Medusozoa is further divided into 4 clades, Hydrozoa, Staurozoa, Cubozoa, and Scyphozoa—the latter 3 lineages make up the clade Acraspeda. Acraspeda encompasses extraordinary diversity in terms of life history, numerous nuisance species, taxa with complex eyes rivaling other animals, and some of the most venomous organisms on the planet. Genomes have recently become available within Scyphozoa and Cubozoa, but there are currently no published genomes within Staurozoa and Cubozoa. Findings Here we present 3 new draft genomes of Calvadosia cruxmelitensis (Staurozoa), Alatina alata (Cubozoa), and Cassiopea xamachana (Scyphozoa) for which we provide a preliminary orthology analysis that includes an inventory of their respective venom-related genes. Additionally, we identify synteny between POU and Hox genes that had previously been reported in a hydrozoan, suggesting this linkage is highly conserved, possibly dating back to at least the last common ancestor of Medusozoa, yet likely independent of vertebrate POU-Hox linkages. Conclusions These draft genomes provide a valuable resource for studying the evolutionary history and biology of these extraordinary animals, and for identifying genomic features underlying venom, vision, and life history traits in Acraspeda.


2017 ◽  
Vol 474 (14) ◽  
pp. 2277-2299 ◽  
Author(s):  
Anthony J. Michael

Since the emergence of the last common ancestor from which all extant life evolved, the metabolite repertoire of cells has increased and diversified. Not only has the metabolite cosmos expanded, but the ways in which the same metabolites are made have diversified. Enzymes catalyzing the same reaction have evolved independently from different protein folds; the same protein fold can produce enzymes recognizing different substrates, and enzymes performing different chemistries. Genes encoding useful enzymes can be transferred between organisms and even between the major domains of life. Organisms that live in metabolite-rich environments sometimes lose the pathways that produce those same metabolites. Fusion of different protein domains results in enzymes with novel properties. This review will consider the major evolutionary mechanisms that generate biosynthetic diversity: gene duplication (and gene loss), horizontal and endosymbiotic gene transfer, and gene fusion. It will also discuss mechanisms that lead to convergence as well as divergence. To illustrate these mechanisms, one of the original metabolisms present in the last universal common ancestor will be employed: polyamine metabolism, which is essential for the growth and cell proliferation of archaea and eukaryotes, and many bacteria.


2021 ◽  
Author(s):  
Julian Vosseberg ◽  
Michelle Schinkel ◽  
Sjoerd Gremmen ◽  
Berend Snel

Spliceosomal introns are a unique feature of eukaryotic genes. Previous studies have established that many introns were present in the protein-coding genes of the last eukaryotic common ancestor (LECA). Intron positions shared between genes that duplicated before LECA could in principle provide insight into the emergence of the first introns. In this study we use ancestral intron position reconstructions in two large sets of duplicated families to systematically identify these ancient paralogous intron positions. We found that 20-35% of introns inferred to have been present in LECA were shared between paralogs. These shared introns, which likely preceded ancient duplications, were widespread across different functions, with the notable exception of nuclear transport. Since we observed a clear signal of pervasive intron loss prior to LECA, it is likely that substantially more introns were shared at the time of duplication than we can detect in LECA. The large extent of shared introns indicates an early origin of introns during eukaryogenesis and suggests an early origin of a nuclear structure, before most of the other complex eukaryotic features were established.


2014 ◽  
Vol 111 (10) ◽  
pp. 3763-3768 ◽  
Author(s):  
James T. Kratzer ◽  
Miguel A. Lanaspa ◽  
Michael N. Murphy ◽  
Christina Cicerchi ◽  
Christina L. Graves ◽  
...  

Uricase is an enzyme involved in purine catabolism and is found in all three domains of life. Curiously, uricase is not functional in some organisms despite its role in converting highly insoluble uric acid into 5-hydroxyisourate. Of particular interest is the observation that apes, including humans, cannot oxidize uric acid, and it appears that multiple, independent evolutionary events led to the silencing or pseudogenization of the uricase gene in ancestral apes. Various arguments have been made to suggest why natural selection would allow the accumulation of uric acid despite the physiological consequences of crystallized monosodium urate acutely causing liver/kidney damage or chronically causing gout. We have applied evolutionary models to understand the history of primate uricases by resurrecting ancestral mammalian intermediates before the pseudogenization events of this gene family. Resurrected proteins reveal that ancestral uricases have steadily decreased in activity since the last common ancestor of mammals gave rise to descendent primate lineages. We were also able to determine the 3D distribution of amino acid replacements as they accumulated during evolutionary history by crystallizing a mammalian uricase protein. Further, ancient and modern uricases were stably transfected into HepG2 liver cells to test one hypothesis that uricase pseudogenization allowed ancient frugivorous apes to rapidly convert fructose into fat. Finally, pharmacokinetics of an ancient uricase injected in rodents suggest that our integrated approach provides the foundation for an evolutionarily-engineered enzyme capable of treating gout and preventing tumor lysis syndrome in human patients.


PeerJ ◽  
2021 ◽  
Vol 9 ◽  
pp. e11799
Author(s):  
Jan A. Veenstra

Background Some insulin/IGF-related peptides (irps) stimulate a receptor tyrosine kinase (RTK) that transfers the extracellular hormonal signal into an intracellular response. Other irps, such as relaxin, do not use an RTK, but a G-protein coupled receptor (GPCR). This is unusual since evolutionarily related hormones typically either use the same or paralogous receptors. In arthropods three different irps, i.e. arthropod IGF, gonadulin and Drosophila insulin-like peptide 7 (dilp7), likely evolved from a gene triplication, as in several species genes encoding these three peptides are located next to one another on the same chromosomal fragment. These arthropod irps have homologs in vertebrates, suggesting that the initial gene triplication was perhaps already present in the last common ancestor of deuterostomes and protostomes. It would be interesting to know whether this is indeed so and how insulin might be related to this trio of irps. Methodology Genes encoding irps as well as their putative receptors were identified in genomes and transcriptomes from echinoderms and hemichordates. Results A similar triplet of genes coding for irps also occurs in some ambulacrarians. Two of these are orthologs of arthropod IGF and dilp7 and the third is likely a gonadulin ortholog. In echinoderms, two novel irps emerged, gonad stimulating substance (GSS) and multinsulin, likely from gene duplications of the IGF and dilp7-like genes respectively. The structures of GSS diverged considerably from IGF, which would suggest they use different receptors from IGF, but no novel irp receptors evolved. If IGF and GSS use different receptors, and the evolution of GSS from a gene duplication of IGF is not associated with the appearance of a novel receptor, while irps are known to use two different types of receptors, the ancestor of GSS and IGF might have acted on both types of receptors while one or both of its descendants act on only one. There are three ambulacrarian GPCRs that have amino acid sequences suggestive of being irp GPCRs, two of these are orthologs of the gonadulin and dilp7 receptors. This suggests that the third might be an IGF receptor, and that by deduction, GSS only acts on the RTK. The evolution of GSS from IGF may represent a pattern, where IGF gene duplications lead to novel genes coding for shorter peptides that activate an RTK. It is likely this is how insulin and the insect neuroendocrine irps evolved independently from IGF. Conclusion The local gene triplication described from arthropods that yielded three genes encoding irps was already present in the last common ancestor of protostomes and deuterostomes. It seems plausible that irps, such as those produced by neuroendocrine cells in the brain of insects and echinoderm GSS evolved independently from IGF and, thus, are not true orthologs, but the result of convergent evolution.


2008 ◽  
Vol 212 (4) ◽  
pp. 544-562 ◽  
Author(s):  
Matthew W. Tocheri ◽  
Caley M. Orr ◽  
Marc C. Jacofsky ◽  
Mary W. Marzke

Open Biology ◽  
2015 ◽  
Vol 5 (4) ◽  
pp. 150030 ◽  
Author(s):  
Dean C. Semmens ◽  
Isabel Beets ◽  
Matthew L. Rowe ◽  
Liisa M. Blowes ◽  
Paola Oliveri ◽  
...  

Neuropeptides are ancient regulators of physiology and behaviour, but reconstruction of neuropeptide evolution is often difficult owing to lack of sequence conservation. Here, we report that the receptor for the neuropeptide NGFFFamide in the sea urchin Strongylocentrotus purpuratus (phylum Echinodermata) is an orthologue of vertebrate neuropeptide-S (NPS) receptors and crustacean cardioactive peptide (CCAP) receptors. Importantly, this has facilitated reconstruction of the evolution of two bilaterian neuropeptide signalling systems. Genes encoding the precursor of a vasopressin/oxytocin-type neuropeptide and its receptor duplicated in a common ancestor of the Bilateria. One copy of the precursor retained ancestral features, as seen in highly conserved vasopressin/oxytocin–neurophysin-type precursors. The other copy diverged, but this took different courses in protostomes and deuterostomes. In protostomes, the occurrence of a disulfide bridge in neuropeptide product(s) of the precursor was retained, as in CCAP, but with loss of the neurophysin domain. In deuterostomes, we see the opposite scenario—the neuropeptides lost the disulfide bridge, and neurophysin was retained (as in the NGFFFamide precursor) but was subsequently lost in vertebrate NPS precursors. Thus, the sea urchin NGFFFamide precursor and receptor are ‘missing links’ in the evolutionary history of neuropeptides that control ecdysis in arthropods (CCAP) and regulate anxiety in humans (NPS).


Biology ◽  
2021 ◽  
Vol 10 (10) ◽  
pp. 1001
Author(s):  
Zhiqing Xue ◽  
Josef Greimler ◽  
Ovidiu Paun ◽  
Kerry Ford ◽  
Michael H. J. Barfuss ◽  
...  

The contrasting evolutionary histories of endemic versus related cosmopolitan species provide avenues to understand the spatial drivers and limitations of biodiversity. Here, we investigated the evolutionary history of three New Zealand endemic Deschampsia species, and how they are related to cosmopolitan D. cespitosa. We used RADseq to test species delimitations, infer a dated species tree, and investigate gene flow patterns between the New Zealand endemics and the D. cespitosa populations of New Zealand, Australia and Korea. Whole plastid DNA analysis was performed on a larger worldwide sampling. Morphometrics of selected characters were applied to New Zealand sampling. Our RADseq review of over 55 Mbp showed the endemics as genetically well-defined from each other. Their last common ancestor with D. cespitosa lived during the last ten MY. The New Zealand D. cespitosa appears in a clade with Australian and Korean samples. Whole plastid DNA analysis revealed the endemics as members of a southern hemisphere clade, excluding the extant D. cespitosa of New Zealand. Both data provided strong evidence for hybridization between D. cespitosa and D. chapmanii. Our findings provide evidence for at least two migration events of the genus Deschampsia to New Zealand and hybridization between D. cespitosa and endemic taxa.


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