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1.  Analysis of EST data of the marine protist Oxyrrhis marina, an emerging model for alveolate biology and evolution 
BMC Genomics  2014;15:122.
Background
The alveolates include a large number of important lineages of protists and algae, among which are three major eukaryotic groups: ciliates, apicomplexans and dinoflagellates. Collectively alveolates are present in virtually every environment and include a vast diversity of cell shapes, molecular and cellular features and feeding modes including lifestyles such as phototrophy, phagotrophy/predation and intracellular parasitism, in addition to a variety of symbiotic associations. Oxyrrhis marina is a well-known model for heterotrophic protist biology, and is now emerging as a useful organism to explore the many changes that occurred during the origin and diversification of dinoflagellates by virtue of its phylogenetic position at the base of the dinoflagellate tree.
Results
We have generated and analysed expressed sequence tag (EST) sequences from the alveolate Oxyrrhis marina in order to shed light on the evolution of a number of dinoflagellate characteristics, especially regarding the emergence of highly unusual genomic features. We found that O. marina harbours extensive gene redundancy, indicating high rates of gene duplication and transcription from multiple genomic loci. In addition, we observed a correlation between expression level and copy number in several genes, suggesting that copy number may contribute to determining transcript levels for some genes. Finally, we analyze the genes and predicted products of the recently discovered Dinoflagellate Viral Nuclear Protein, and several cases of horizontally acquired genes.
Conclusion
The dataset presented here has proven very valuable for studying this important group of protists. Our analysis indicates that gene redundancy is a pervasive feature of dinoflagellate genomes, thus the mechanisms involved in its generation must have arisen early in the evolution of the group.
doi:10.1186/1471-2164-15-122
PMCID: PMC3942190  PMID: 24512041
Dinoflagellates; Alveolates; Chromatin; Genome; Oxyrrhis
2.  A Mutation in the FHA Domain of Coprinus cinereus Nbs1 Leads to Spo11-Independent Meiotic Recombination and Chromosome Segregation 
G3: Genes|Genomes|Genetics  2013;3(11):1927-1943.
Nbs1, a core component of the Mre11-Rad50-Nbs1 complex, plays an essential role in the cellular response to DNA double-strand breaks (DSBs) and poorly understood roles in meiosis. We used the basidiomycete Coprinus cinereus to examine the meiotic roles of Nbs1. We identified the C. cinereus nbs1 gene and demonstrated that it corresponds to a complementation group previously known as rad3. One allele, nbs1-2, harbors a point mutation in the Nbs1 FHA domain and has a mild spore viability defect, increased frequency of meiosis I nondisjunction, and an altered crossover distribution. The nbs1-2 strain enters meiosis with increased levels of phosphorylated H2AX, which we hypothesize represent unrepaired DSBs formed during premeiotic replication. In nbs1-2, there is no apparent induction of Spo11-dependent DSBs during prophase. We propose that replication-dependent DSBs, resulting from defective replication fork protection and processing by the Mre11-Rad50-Nbs1 complex, are competent to form meiotic crossovers in C. cinereus, and that these crossovers lead to high levels of faithful chromosome segregation. In addition, although crossover distribution is altered in nbs1-2, the majority of crossovers were found in subtelomeric regions, as in wild-type. Therefore, the location of crossovers in C. cinereus is maintained when DSBs are induced via a Spo11-independent mechanism.
doi:10.1534/g3.113.007906
PMCID: PMC3815056  PMID: 24062528
MRN complex; Coprinus cinereus; recombination; DNA replication; meiosis
3.  Conserved Meiotic Machinery in Glomus spp., a Putatively Ancient Asexual Fungal Lineage 
Arbuscular mycorrhizal fungi (AMF) represent an ecologically important and evolutionarily intriguing group of symbionts of land plants, currently thought to have propagated clonally for over 500 Myr. AMF produce multinucleate spores and may exchange nuclei through anastomosis, but meiosis has never been observed in this group. A provocative alternative for their successful and long asexual evolutionary history is that these organisms may have cryptic sex, allowing them to recombine alleles and compensate for deleterious mutations. This is partly supported by reports of recombination among some of their natural populations. We explored this hypothesis by searching for some of the primary tools for a sustainable sexual cycle—the genes whose products are required for proper completion of meiotic recombination in yeast—in the genomes of four AMF and compared them with homologs of representative ascomycete, basidiomycete, chytridiomycete, and zygomycete fungi. Our investigation used molecular and bioinformatic tools to identify homologs of 51 meiotic genes, including seven meiosis-specific genes and other “core meiotic genes” conserved in the genomes of the AMF Glomus diaphanum (MUCL 43196), Glomus irregulare (DAOM-197198), Glomus clarum (DAOM 234281), and Glomus cerebriforme (DAOM 227022). Homology of AMF meiosis-specific genes was verified by phylogenetic analyses with representative fungi, animals (Mus, Hydra), and a choanoflagellate (Monosiga). Together, these results indicate that these supposedly ancient asexual fungi may be capable of undergoing a conventional meiosis; a hypothesis that is consistent with previous reports of recombination within and across some of their populations.
doi:10.1093/gbe/evr089
PMCID: PMC3184777  PMID: 21876220
comparative genomics; meiosis; fungi; arbuscular mycorrhizal fungi; genome evolution; ancient asexuals
4.  Phylogeny of Parasitic Parabasalia and Free-Living Relatives Inferred from Conventional Markers vs. Rpb1, a Single-Copy Gene 
PLoS ONE  2011;6(6):e20774.
Background
Parabasalia are single-celled eukaryotes (protists) that are mainly comprised of endosymbionts of termites and wood roaches, intestinal commensals, human or veterinary parasites, and free-living species. Phylogenetic comparisons of parabasalids are typically based upon morphological characters and 18S ribosomal RNA gene sequence data (rDNA), while biochemical or molecular studies of parabasalids are limited to a few axenically cultivable parasites. These previous analyses and other studies based on PCR amplification of duplicated protein-coding genes are unable to fully resolve the evolutionary relationships of parabasalids. As a result, genetic studies of Parabasalia lag behind other organisms.
Principal Findings
Comparing parabasalid EF1α, α-tubulin, enolase and MDH protein-coding genes with information from the Trichomonas vaginalis genome reveals difficulty in resolving the history of species or isolates apart from duplicated genes. A conserved single-copy gene encodes the largest subunit of RNA polymerase II (Rpb1) in T. vaginalis and other eukaryotes. Here we directly sequenced Rpb1 degenerate PCR products from 10 parabasalid genera, including several T. vaginalis isolates and avian isolates, and compared these data by phylogenetic analyses. Rpb1 genes from parabasalids, diplomonads, Parabodo, Diplonema and Percolomonas were all intronless, unlike intron-rich homologs in Naegleria, Jakoba and Malawimonas.
Conclusions/Significance
The phylogeny of Rpb1 from parasitic and free-living parabasalids, and conserved Rpb1 insertions, support Trichomonadea, Tritrichomonadea, and Hypotrichomonadea as monophyletic groups. These results are consistent with prior analyses of rDNA and GAPDH sequences and ultrastructural data. The Rpb1 phylogenetic tree also resolves species- and isolate-level relationships. These findings, together with the relative ease of Rpb1 isolation, make it an attractive tool for evaluating more extensive relationships within Parabasalia.
doi:10.1371/journal.pone.0020774
PMCID: PMC3111441  PMID: 21695260
5.  Correction: An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis 
PLoS ONE  2008;3(9):10.1371/annotation/029c403b-10aa-47af-9e99-11451de76b85.
doi:10.1371/annotation/029c403b-10aa-47af-9e99-11451de76b85
PMCID: PMC3935636
6.  An Expanded Inventory of Conserved Meiotic Genes Provides Evidence for Sex in Trichomonas vaginalis 
PLoS ONE  2008;3(8):e2879.
Meiosis is a defining feature of eukaryotes but its phylogenetic distribution has not been broadly determined, especially among eukaryotic microorganisms (i.e. protists)—which represent the majority of eukaryotic ‘supergroups’. We surveyed genomes of animals, fungi, plants and protists for meiotic genes, focusing on the evolutionarily divergent parasitic protist Trichomonas vaginalis. We identified homologs of 29 components of the meiotic recombination machinery, as well as the synaptonemal and meiotic sister chromatid cohesion complexes. T. vaginalis has orthologs of 27 of 29 meiotic genes, including eight of nine genes that encode meiosis-specific proteins in model organisms. Although meiosis has not been observed in T. vaginalis, our findings suggest it is either currently sexual or a recent asexual, consistent with observed, albeit unusual, sexual cycles in their distant parabasalid relatives, the hypermastigotes. T. vaginalis may use meiotic gene homologs to mediate homologous recombination and genetic exchange. Overall, this expanded inventory of meiotic genes forms a useful “meiosis detection toolkit”. Our analyses indicate that these meiotic genes arose, or were already present, early in eukaryotic evolution; thus, the eukaryotic cenancestor contained most or all components of this set and was likely capable of performing meiotic recombination using near-universal meiotic machinery.
doi:10.1371/journal.pone.0002879
PMCID: PMC2488364  PMID: 18663385
7.  Draft Genome Sequence of the Sexually Transmitted Pathogen Trichomonas vaginalis 
Science (New York, N.Y.)  2007;315(5809):207-212.
We describe the genome sequence of the protist Trichomonas vaginalis, a sexually transmitted human pathogen. Repeats and transposable elements comprise about two-thirds of the ~160-megabase genome, reflecting a recent massive expansion of genetic material. This expansion, in conjunction with the shaping of metabolic pathways that likely transpired through lateral gene transfer from bacteria, and amplification of specific gene families implicated in pathogenesis and phagocytosis of host proteins may exemplify adaptations of the parasite during its transition to a urogenital environment. The genome sequence predicts previously unknown functions for the hydrogenosome, which support a common evolutionary origin of this unusual organelle with mitochondria.
doi:10.1126/science.1132894
PMCID: PMC2080659  PMID: 17218520
8.  Functional evolution of ADAMTS genes: Evidence from analyses of phylogeny and gene organization 
Background
The ADAMTS (A Disintegrin-like and Metalloprotease with Thrombospondin motifs) proteins are a family of metalloproteases with sequence similarity to the ADAM proteases, that contain the thrombospondin type 1 sequence repeat motifs (TSRs) common to extracellular matrix proteins. ADAMTS proteins have recently gained attention with the discovery of their role in a variety of diseases, including tissue and blood disorders, cancer, osteoarthritis, Alzheimer's and the genetic syndromes Weill-Marchesani syndrome (ADAMTS10), thrombotic thrombocytopenic purpura (ADAMTS13), and Ehlers-Danlos syndrome type VIIC (ADAMTS2) in humans and belted white-spotting mutation in mice (ADAMTS20).
Results
Phylogenetic analysis and comparison of the exon/intron organization of vertebrate (Homo, Mus, Fugu), chordate (Ciona) and invertebrate (Drosophila and Caenorhabditis) ADAMTS homologs has elucidated the evolutionary relationships of this important gene family, which comprises 19 members in humans.
Conclusions
The evolutionary history of ADAMTS genes in vertebrate genomes has been marked by rampant gene duplication, including a retrotransposition that gave rise to a distinct ADAMTS subfamily (ADAMTS1, -4, -5, -8, -15) that may have distinct aggrecanase and angiogenesis functions.
doi:10.1186/1471-2148-5-11
PMCID: PMC549037  PMID: 15693998

Results 1-8 (8)