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ELife Jan 2021Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205...
Laboratory experimental evolution provides a window into the details of the evolutionary process. To investigate the consequences of long-term adaptation, we evolved 205 populations (124 haploid and 81 diploid) for ~10,000,000 generations in three environments. We measured the dynamics of fitness changes over time, finding repeatable patterns of declining adaptability. Sequencing revealed that this phenotypic adaptation is coupled with a steady accumulation of mutations, widespread genetic parallelism, and historical contingency. In contrast to long-term evolution in , we do not observe long-term coexistence or populations with highly elevated mutation rates. We find that evolution in diploid populations involves both fixation of heterozygous mutations and frequent loss-of-heterozygosity events. Together, these results help distinguish aspects of evolutionary dynamics that are likely to be general features of adaptation across many systems from those that are specific to individual organisms and environmental conditions.
Topics: Adaptation, Biological; Diploidy; Evolution, Molecular; Mutation; Mutation Rate; Phenotype; Saccharomyces cerevisiae
PubMed: 33464204
DOI: 10.7554/eLife.63910 -
MBio Mar 2024In contrast to the canonical view that genomes cycle only between haploid and diploid states, many eukaryotes have dynamic genomes that change content throughout an...
In contrast to the canonical view that genomes cycle only between haploid and diploid states, many eukaryotes have dynamic genomes that change content throughout an individual's life cycle. However, the few detailed studies of microeukaryotic life cycles render our understanding of eukaryotic genome dynamism incomplete. Foraminifera (Rhizaria) are an ecologically important, yet understudied, clade of microbial eukaryotes with complex life cycles that include changes in ploidy and genome organization. Here, we apply fluorescence microscopy and image analysis techniques to over 2,800 nuclei in 110 cells to characterize the life cycle of strain Cold Spring Harbor (CSH), one of few cultivable foraminifera species. We show that haploidy and diploidy are brief moments in the life cycle and that nuclei endoreplicate up to 12,000 times the haploid genome size. We find that reorganizes a highly endoreplicated nucleus into thousands of haploid genomes through a non-canonical mechanism called , in which the nuclear envelope degrades and extrudes chromatin into the cytoplasm. Based on these findings, along with changes in nuclear architecture across the life cycle, we believe that uses spatio-temporal mechanisms to delineate germline and somatic DNA within a single nucleus. The analyses here extend our understanding of the genome dynamics across the eukaryotic tree of life.IMPORTANCEIn traditional depictions of eukaryotes (i.e., cells with nuclei), life cycles alternate only between haploid and diploid phases, overlooking studies of diverse microeukaryotic lineages (e.g., amoebae, ciliates, and flagellates) that show dramatic variation in DNA content throughout their life cycles. Endoreplication of genomes enables cells to grow to large sizes and perhaps to also respond to changes in their environments. Few microeukaryotic life cycles have been studied in detail, which limits our understanding of how eukaryotes regulate and transmit their DNA across generations. Here, we use microscopy to study the life cycle of strain CSH, an early-diverging lineage within the Foraminifera (an ancient clade of predominantly marine amoebae). We show that DNA content changes significantly throughout their life cycle and further describe an unusual process called , by which this species reorganizes a large nucleus with up to 12,000 genome copies into hundreds of small gametic nuclei, each with a single haploid genome. Our results are consistent with the idea that all eukaryotes demarcate germline DNA to pass on to offspring amidst more flexible somatic DNA and extend the known diversity of eukaryotic life cycles.
Topics: Foraminifera; Genome; Diploidy; Haploidy; DNA
PubMed: 38329358
DOI: 10.1128/mbio.03379-23 -
American Journal of Botany Oct 2022Parthenogenesis is the capacity of organisms to develop embryos from unfertilized eggs. When parthenogenesis is coupled with unreduced gamete formation (apomeiosis),...
PREMISE
Parthenogenesis is the capacity of organisms to develop embryos from unfertilized eggs. When parthenogenesis is coupled with unreduced gamete formation (apomeiosis), genetically maternal progeny result. Genetic elucidation of this form of reproduction in plants, apomixis, has important agronomic implications. However, genetic characterization of apomeiosis and parthenogenesis has been problematic in part because the traits usually co-occur and are restricted to polyploids. In this work, the inheritance of parthenogenetic embryo development, by itself, was studied at the diploid level.
METHODS
Progeny resulting from a cross between a diploid (2n = 18), heterozygous, parthenogenetic pollen donor, and a diploid, wildtype, sexual seed parent were evaluated. Paternity was tested with conserved orthologous sequence (COS) markers, reproductive development of F1s was evaluated with microscopy of cleared ovules, and an amplified fragment length polymorphism (AFLP) marker (Eagc × Macg.615) co-segregating with parthenogenesis was characterized at the sequence level.
RESULTS
Of 102 diploid biparental progeny, 47 exhibited parthenogenetic embryo and endosperm development, and 55 lacked development of the egg and central cell. This result is consistent with Mendelian inheritance for a single locus (P = 0.43). Isolation and sequencing of the AFLP marker indicates that it is likely a portion of a Ty-Gypsy retrotransposon. Attempts to develop a sequence-characterized amplified region marker from the AFLP were unsuccessful.
CONCLUSIONS
This work shows that parthenogenesis can be transmitted simply at the diploid level. This advance is key in the development of a tractable system in Erigeron aimed at the identification of the parthenogenesis locus using genetic mapping strategies.
Topics: Diploidy; Erigeron; Amplified Fragment Length Polymorphism Analysis; Magnoliopsida; Parthenogenesis; Embryonic Development
PubMed: 36112611
DOI: 10.1002/ajb2.16071 -
Proceedings of the National Academy of... Mar 2000In this paper, we investigate the coevolution of diploid sexual reproduction and cell senescence (i.e., cell aging). We use probability analysis, computer simulation,...
In this paper, we investigate the coevolution of diploid sexual reproduction and cell senescence (i.e., cell aging). We use probability analysis, computer simulation, and exact numerical computation to analyze the impacts of deleterious recessive mutations on sexual and asexual reproduction. The main conclusion is that, without cell senescence, the evolutionary advantages of sexual reproduction cannot be realized in unicellular organisms that reproduce both sexually and asexually. Also, cell senescence is found to be useful in the maintenance of sexual reproduction. This result suggests that diploid sexual reproduction was unlikely to establish itself as a widespread reproduction mechanism without the complementary process of cell senescence.
Topics: Biological Evolution; Cellular Senescence; Diploidy; Genome; Reproduction
PubMed: 10737794
DOI: 10.1073/pnas.97.7.3330 -
BMC Plant Biology Apr 2024Whole-genome doubling leads to cell reprogramming, upregulation of stress genes, and establishment of new pathways of drought stress responses in plants. This study...
Whole-genome doubling leads to cell reprogramming, upregulation of stress genes, and establishment of new pathways of drought stress responses in plants. This study investigated the molecular mechanisms of drought tolerance and cuticular wax characteristics in diploid and tetraploid-induced Erysimum cheiri. According to real-time PCR analysis, tetraploid induced wallflowers exhibited increased expression of several genes encoding transcription factors (TFs), including AREB1 and AREB3; the stress response genes RD29A and ERD1 under drought stress conditions. Furthermore, two cuticular wax biosynthetic pathway genes, CER1 and SHN1, were upregulated in tetraploid plants under drought conditions. Leaf morphological studies revealed that tetraploid leaves were covered with unique cuticular wax crystalloids, which produced a white fluffy appearance, while the diploid leaves were green and smooth. The greater content of epicuticular wax in tetraploid leaves than in diploid leaves can explain the decrease in cuticle permeability as well as the decrease in water loss and improvement in drought tolerance in wallflowers. GC‒MS analysis revealed that the wax components included alkanes, alcohols, aldehydes, and fatty acids. The most abundant wax compound in this plant was alkanes (50%), the most predominant of which was C29. The relative abundance of these compounds increased significantly in tetraploid plants under drought stress conditions. These findings revealed that tetraploid-induced wallflowers presented upregulation of multiple drought-related and wax biosynthesis genes; therefore, polyploidization has proved useful for improving plant drought tolerance.
Topics: Diploidy; Drought Resistance; Gene Expression Profiling; Gene Expression Regulation, Plant; Plant Epidermis; Plant Leaves; Tetraploidy; Waxes
PubMed: 38664602
DOI: 10.1186/s12870-024-05007-6 -
Genome Research 2022Recent advancements in long-read sequencing have enabled the telomere-to-telomere (complete) assembly of a human genome and are now contributing to the...
Recent advancements in long-read sequencing have enabled the telomere-to-telomere (complete) assembly of a human genome and are now contributing to the haplotype-resolved complete assemblies of multiple human genomes. Because the accuracy of read mapping tools deteriorates in highly repetitive regions, there is a need to develop accurate, (detecting potential assembly errors), and e (distinguishing different haplotypes) tools for read mapping in complete assemblies. We describe the first accurate, error-exposing, and partially diploid-aware VerityMap tool for long-read mapping to complete assemblies.
Topics: Humans; Sequence Analysis, DNA; High-Throughput Nucleotide Sequencing; Genome, Human; Repetitive Sequences, Nucleic Acid; Diploidy
PubMed: 36379716
DOI: 10.1101/gr.276871.122 -
GigaScience Dec 2020Plums are one of the most economically important Rosaceae fruit crops and comprise dozens of species distributed across the world. Until now, only limited genomic...
BACKGROUND
Plums are one of the most economically important Rosaceae fruit crops and comprise dozens of species distributed across the world. Until now, only limited genomic information has been available for the genetic studies and breeding programs of plums. Prunus salicina, an important diploid plum species, plays a predominant role in modern commercial plum production. Here we selected P. salicina for whole-genome sequencing and present a chromosome-level genome assembly through the combination of Pacific Biosciences sequencing, Illumina sequencing, and Hi-C technology.
FINDINGS
The assembly had a total size of 284.2 Mb, with contig N50 of 1.78 Mb and scaffold N50 of 32.32 Mb. A total of 96.56% of the assembled sequences were anchored onto 8 pseudochromosomes, and 24,448 protein-coding genes were identified. Phylogenetic analysis showed that P. salicina had a close relationship with Prunus mume and Prunus armeniaca, with P. salicina diverging from their common ancestor ∼9.05 million years ago. During P. salicina evolution 146 gene families were expanded, and some cell wall-related GO terms were significantly enriched. It was noteworthy that members of the DUF579 family, a new class involved in xylan biosynthesis, were significantly expanded in P. salicina, which provided new insight into the xylan metabolism in plums.
CONCLUSIONS
We constructed the first high-quality chromosome-level plum genome using Pacific Biosciences, Illumina, and Hi-C technologies. This work provides a valuable resource for facilitating plum breeding programs and studying the genetic diversity mechanisms of plums and Prunus species.
Topics: Chromosomes; Diploidy; Humans; Phylogeny; Plant Breeding; Prunus domestica
PubMed: 33300949
DOI: 10.1093/gigascience/giaa130 -
American Journal of Botany Dec 2020Hybridization plays a key role in introgressive adaptation, speciation, and adaptive radiation as a source of evolutionary innovation. Hybridization is considered common...
PREMISE
Hybridization plays a key role in introgressive adaptation, speciation, and adaptive radiation as a source of evolutionary innovation. Hybridization is considered common in Arctostaphylos, yet species boundaries are retained in stands containing multiple species. Arctostaphylos contains diploids and tetraploids, and recent phylogenies indicate two clades; we hypothesize combinations of these traits limit or promote hybridization rates.
METHODS
We statistically analyzed co-occurrence patterns of species by clade membership and ploidy level from 87 random 0.1 ha plots. We sampled multiple sites to analyze for percent hybridization based on morphology. Finally, phenophases were analyzed by scoring herbarium sheets for a large number of taxa from both clades as well as tetraploids, and second, surveying three field sites over two years for divergence in phenological stages between co-occurring taxa.
RESULTS
Most taxa in Arctostaphylos are allopatric relative to other congenerics. When two taxa co-occur, the patterns are a diploid with a tetraploid, or two diploids from different clades. When three taxa co-occur, the pattern is two diploids from different clades and a tetraploid. Field and herbarium data both indicate flowering phenology is displaced between diploids from the two clades; one of the diploid clades and tetraploids overlap considerably.
CONCLUSIONS
The two deep clades in Arctostaphylos are genetically distant, with hybrids rare or non-existent when taxa co-occur. Reproductive isolation between clades is enhanced by displaced flowering phenology for co-occurring species. Within clades, taxa appear to have few reproductive barriers other than an allopatric distribution or different ploidy levels.
Topics: Arctostaphylos; Diploidy; Hybridization, Genetic; Reproductive Isolation; Sympatry
PubMed: 33274449
DOI: 10.1002/ajb2.1576 -
GigaScience Mar 2022Cassava (Manihot esculenta) is an important clonally propagated food crop in tropical and subtropical regions worldwide. Genetic gain by molecular breeding has been...
BACKGROUND
Cassava (Manihot esculenta) is an important clonally propagated food crop in tropical and subtropical regions worldwide. Genetic gain by molecular breeding has been limited, partially because cassava is a highly heterozygous crop with a repetitive and difficult-to-assemble genome.
FINDINGS
Here we demonstrate that Pacific Biosciences high-fidelity (HiFi) sequencing reads, in combination with the assembler hifiasm, produced genome assemblies at near complete haplotype resolution with higher continuity and accuracy compared to conventional long sequencing reads. We present 2 chromosome-scale haploid genomes phased with Hi-C technology for the diploid African cassava variety TME204. With consensus accuracy >QV46, contig N50 >18 Mb, BUSCO completeness of 99%, and 35k phased gene loci, it is the most accurate, continuous, complete, and haplotype-resolved cassava genome assembly so far. Ab initio gene prediction with RNA-seq data and Iso-Seq transcripts identified abundant novel gene loci, with enriched functionality related to chromatin organization, meristem development, and cell responses. During tissue development, differentially expressed transcripts of different haplotype origins were enriched for different functionality. In each tissue, 20-30% of transcripts showed allele-specific expression (ASE) differences. ASE bias was often tissue specific and inconsistent across different tissues. Direction-shifting was observed in <2% of the ASE transcripts. Despite high gene synteny, the HiFi genome assembly revealed extensive chromosome rearrangements and abundant intra-genomic and inter-genomic divergent sequences, with large structural variations mostly related to LTR retrotransposons. We use the reference-quality assemblies to build a cassava pan-genome and demonstrate its importance in representing the genetic diversity of cassava for downstream reference-guided omics analysis and breeding.
CONCLUSIONS
The phased and annotated chromosome pairs allow a systematic view of the heterozygous diploid genome organization in cassava with improved accuracy, completeness, and haplotype resolution. They will be a valuable resource for cassava breeding and research. Our study may also provide insights into developing cost-effective and efficient strategies for resolving complex genomes with high resolution, accuracy, and continuity.
Topics: Alleles; Chromosomes; Diploidy; Haplotypes; Manihot; Plant Breeding; Sequence Analysis, DNA; Transcriptome
PubMed: 35333302
DOI: 10.1093/gigascience/giac028 -
Oncotarget Mar 2017Soft tissue sarcomas with complex genomics are very heterogeneous tumors lacking simple prognosis markers or targeted therapies. Overexpression of a subset of mitotic...
Soft tissue sarcomas with complex genomics are very heterogeneous tumors lacking simple prognosis markers or targeted therapies. Overexpression of a subset of mitotic genes from a signature called CINSARC is of bad prognosis, but the significance of this signature remains elusive. Here we precisely measure the cell cycle and mitosis duration of sarcoma cell lines and we found that the mitotic gene products overexpression does not reflect variation in the time spent during mitosis or G2/M. We also found that the CINSARC cell lines, we studied, are composed of a mixture of aneuploid, diploid, and tetraploid cells that are highly motile in vitro. After sorting diploid and tetraploid cells, we showed that the tetraploid cell clones do not possess a proliferative advantage, but are strikingly more motile and invasive than their diploid counterparts. This is correlated with higher levels of mitotic proteins overexpression. Owing that mitotic proteins are almost systematically degraded at the end of mitosis, we propose that it is the abnormal activity of the mitotic proteins during interphase that boosts the sarcoma cells migratory properties by affecting their cytoskeleton. To test this hypothesis, we designed a screen for mitotic or cytoskeleton protein inhibitors affecting the sarcoma cell migration potential independently of cytotoxic activities. We found that inhibition of several mitotic kinases drastically impairs the CINSARC cell invasive and migratory properties. This finding could provide a handle by which to selectively inhibit the most invasive cells.
Topics: Cell Line; Cell Movement; DNA, Neoplasm; Diploidy; Genetic Heterogeneity; Humans; Sarcoma; Tetraploidy
PubMed: 28035071
DOI: 10.18632/oncotarget.14291