Adaptive reduction of male gamete number in the selfing plant Arabidopsis thaliana.
Ontology highlight
ABSTRACT:
SUBMITTER: Tsuchimatsu T
PROVIDER: S-EPMC7280297 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundTransposable elements (TEs) are major contributors to genome evolution. One factor that influences their evolutionary dynamics is whether their host reproduces through selfing or through outcrossing. According to the recombinational spreading hypothesis, for instance, TEs can spread more easily in outcrossing species through recombination, and should thus be less abundant in selfing species. We here studied the distribution and evolutionary dynamics of TE families in the predominantly selfing plant Arabidopsis thaliana and its close outcrossing relative Arabidopsis lyrata on a genome-wide scale. We characterized differences in TE abundance between them and asked which, if any, existing hypotheses about TE abundances may explain these differences.ResultsWe identified 1,819 TE families representing all known classes of TEs in both species, and found three times more copies in the outcrossing A. lyrata than in the predominantly selfing A. thaliana, as well as ten times more TE families unique to A. lyrata. On average, elements in A. lyrata are younger than elements in A. thaliana. In particular, A. thaliana shows a marked decrease in element number that occurred during the most recent 10% of the time interval since A. thaliana split from A. lyrata. This most recent period in the evolution of A. thaliana started approximately 500,000 years ago, assuming a splitting time of 5 million years ago, and coincides with the time at which predominant selfing originated.ConclusionsOur results indicate that the mating system may be important for determining TE copy number, and that selfing species are likely to have fewer TEs.
| S-EPMC3292453 | biostudies-literature
Project description:Double fertilization in angiosperms involves several successive steps, including guidance and reception of the pollen tube and male-female gamete recognition. Each step entails extensive communication and interaction between two different reproductive cell or tissue types. Extensive research has focused on the pollen tube, namely, its interaction with the stigma and reception by maternal cells. Little is known, however, about the mechanism by which the gametes recognize each other and interact to form a zygote. We report that an ankyrin repeat protein (ANK6) is essential for fertilization, specifically for gamete recognition. ANK6 (At5g61230) was highly expressed in the male and female gametophytes before and during but not after fertilization. Genetic analysis of a T-DNA insertional mutant suggested that loss of function of ANK6 results in embryonic lethality. Moreover, male-female gamete recognition was found to be impaired only when an ank6 male gamete reached an ank6 female gamete, thereby preventing formation of homozygous zygotes. ANK6 was localized to the mitochondria, where it interacted with SIG5, a transcription initiation factor previously found to be essential for fertility. These results show that ANK6 plays a central role in male-female gamete recognition, possibly by regulating mitochondrial gene expression.
| S-EPMC3009778 | biostudies-literature
Project description:Seed plants vary tremendously in size and morphology; however, variation and covariation in plant traits may be governed, at least in part, by universal biophysical laws and biological constants. Metabolic scaling theory (MST) posits that whole-organismal metabolism and growth rate are under stabilizing selection that minimizes the scaling of hydrodynamic resistance and maximizes the scaling of resource uptake. This constrains variation in physiological traits and in the rate of biomass accumulation, so that they can be expressed as mathematical functions of plant size with near-constant allometric scaling exponents across species. However, the observed variation in scaling exponents calls into question the evolutionary drivers and the universality of allometric equations. We have measured growth scaling and fitness traits of 451 Arabidopsis thaliana accessions with sequenced genomes. Variation among accessions around the scaling exponent predicted by MST was correlated with relative growth rate, seed production, and stress resistance. Genomic analyses indicate that growth allometry is affected by many genes associated with local climate and abiotic stress response. The gene with the strongest effect, PUB4, has molecular signatures of balancing selection, suggesting that intraspecific variation in growth scaling is maintained by opposing selection on the trade-off between seed production and abiotic stress resistance. Our findings suggest that variation in allometry contributes to local adaptation to contrasting environments. Our results help reconcile past debates on the origin of allometric scaling in biology and begin to link adaptive variation in allometric scaling to specific genes.
| S-EPMC5879651 | biostudies-literature
Project description:Evolution of chromosome complements can be resolved by genome sequencing, comparative genetic mapping, and comparative chromosome painting. Previously, comparison of genetic maps and gene-based phylogenies suggested that the karyotypes of Arabidopsis thaliana (n = 5) and of related species with six or seven chromosome pairs were derived from an ancestral karyotype with eight chromosome pairs. To test this hypothesis, we applied multicolor chromosome painting using contiguous bacterial artificial chromosome pools of A. thaliana arranged according to the genetic maps of Arabidopsis lyrata and Capsella rubella (both n = 8) to A. thaliana, A. lyrata, Neslia paniculata, Turritis glabra, and Hornungia alpina. This approach allowed us to map the A. lyrata centromeres as a prerequisite to defining a putative ancestral karyotype (n = 8) and to elucidate the evolutionary mechanisms that shaped the karyotype of A. thaliana and its relatives. We conclude that chromosome "fusions" in A. thaliana resulted from (i) generation of acrocentric chromosomes by pericentric inversions, (ii) reciprocal translocation between two chromosomes (one or both acrocentric), and (iii) elimination of a minichromosome that arose in addition to the "fusion chromosome." Comparative chromosome painting applied to N. paniculata (n = 7), T. glabra (n = 6), and H. alpina (n = 6), for which genetic maps are not available, revealed chromosomal colinearity between all species tested and allowed us to reconstruct the evolution of their chromosomes from a putative ancestral karyotype (n = 8). Although involving different ancestral chromosomes, chromosome number reduction followed similar routes as found within the genus Arabidopsis.
| S-EPMC1458822 | biostudies-literature
Project description:The DEMETER (DME) DNA glycosylase initiates active DNA demethylation via the base-excision repair pathway and is vital for reproduction in Arabidopsis thaliana DME-mediated DNA demethylation is preferentially targeted to small, AT-rich, and nucleosome-depleted euchromatic transposable elements, influencing expression of adjacent genes and leading to imprinting in the endosperm. In the female gametophyte, DME expression and subsequent genome-wide DNA demethylation are confined to the companion cell of the egg, the central cell. Here, we show that, in the male gametophyte, DME expression is limited to the companion cell of sperm, the vegetative cell, and to a narrow window of time: immediately after separation of the companion cell lineage from the germline. We define transcriptional regulatory elements of DME using reporter genes, showing that a small region, which surprisingly lies within the DME gene, controls its expression in male and female companion cells. DME expression from this minimal promoter is sufficient to rescue seed abortion and the aberrant DNA methylome associated with the null dme-2 mutation. Within this minimal promoter, we found short, conserved enhancer sequences necessary for the transcriptional activities of DME and combined predicted binding motifs with published transcription factor binding coordinates to produce a list of candidate upstream pathway members in the genetic circuitry controlling DNA demethylation in gamete companion cells. These data show how DNA demethylation is regulated to facilitate endosperm gene imprinting and potential transgenerational epigenetic regulation, without subjecting the germline to potentially deleterious transposable element demethylation.
| S-EPMC5338364 | biostudies-literature
Project description:Although the contribution of cytonuclear interactions to plant fitness variation is relatively well documented at the interspecific level, the prevalence of cytonuclear interactions at the intraspecific level remains poorly investigated. In this study, we set up a field experiment to explore the range of effects that cytonuclear interactions have on fitness-related traits in Arabidopsis thaliana To do so, we created a unique series of 56 cytolines resulting from cytoplasmic substitutions among eight natural accessions reflecting within-species genetic diversity. An assessment of these cytolines and their parental lines scored for 28 adaptive whole-organism phenotypes showed that a large proportion of phenotypic traits (23 of 28) were affected by cytonuclear interactions. The effects of these interactions varied from slight but frequent across cytolines to strong in some specific parental pairs. Two parental pairs accounted for half of the significant pairwise interactions. In one parental pair, Ct-1/Sha, we observed symmetrical phenotypic responses between the two nuclear backgrounds when combined with specific cytoplasms, suggesting nuclear differentiation at loci involved in cytonuclear epistasis. In contrast, asymmetrical phenotypic responses were observed in another parental pair, Cvi-0/Sha. In the Cvi-0 nuclear background, fecundity and phenology-related traits were strongly affected by the Sha cytoplasm, leading to a modified reproductive strategy without penalizing total seed production. These results indicate that natural variation in cytoplasmic and nuclear genomes interact to shape integrative traits that contribute to adaptation, thereby suggesting that cytonuclear interactions can play a major role in the evolutionary dynamics ofA. thaliana.
| S-EPMC4822599 | biostudies-literature
Project description:Over the past 20 y, many studies have examined the history of the plant ecological and molecular model, Arabidopsis thaliana, in Europe and North America. Although these studies informed us about the recent history of the species, the early history has remained elusive. In a large-scale genomic analysis of African A. thaliana, we sequenced the genomes of 78 modern and herbarium samples from Africa and analyzed these together with over 1,000 previously sequenced Eurasian samples. In striking contrast to expectations, we find that all African individuals sampled are native to this continent, including those from sub-Saharan Africa. Moreover, we show that Africa harbors the greatest variation and represents the deepest history in the A. thaliana lineage. Our results also reveal evidence that selfing, a major defining characteristic of the species, evolved in a single geographic region, best represented today within Africa. Demographic inference supports a model in which the ancestral A. thaliana population began to split by 120-90 kya, during the last interglacial and Abbassia pluvial, and Eurasian populations subsequently separated from one another at around 40 kya. This bears striking similarities to the patterns observed for diverse species, including humans, implying a key role for climatic events during interglacial and pluvial periods in shaping the histories and current distributions of a wide range of species.
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Project description:Meiotic homologous recombination plays a central role in creating genetic variability, making it an essential biological process relevant to evolution and crop breeding. In this study, we used pollen-specific fluorescent tagged lines (FTLs) to measure male meiotic recombination frequency during the development of Arabidopsis thaliana. Interestingly, a subset of pollen grains consistently shows loss of fluorescence expression in tested lines. Using nine independent FTL intervals, the spatio-temporal dynamics of male recombination frequency was assessed during plant development, considering both shoot type and plant age as independent parameters. In most genomic intervals assayed, male meiotic recombination frequency is highly consistent during plant development, showing no significant change between different shoot types and during plant aging. However, in some genomic regions, such as I1a and I5a, a small but significant effect of either developmental position or plant age were observed, indicating that the meiotic CO frequency in those intervals varies during plant development. Furthermore, from an overall view of all nine genomic intervals assayed, both primary and tertiary shoots show a similar dynamics of increasing recombination frequency during development, while secondary and lateral shoots remain highly stable. Our results provide new insights in the dynamics of male meiotic recombination frequency during plant development.
| S-EPMC5304153 | biostudies-literature
Project description:A subset of genes in Arabidopsis thaliana is known to be up-regulated in response to a wide range of different environmental stress factors. However, not all of these genes are characterized as yet with respect to their functions. In this study, we used transgenic knockout, overexpression and reporter gene approaches to try to elucidate the biological roles of five unknown multiple-stress responsive genes in Arabidopsis. The selected genes have the following locus identifiers: At1g18740, At1g74450, At4g27652, At4g29780 and At5g12010. Firstly, T-DNA insertion knockout lines were identified for each locus and screened for altered phenotypes. None of the lines were found to be visually different from wildtype Col-0. Secondly, 35S-driven overexpression lines were generated for each open reading frame. Analysis of these transgenic lines showed altered phenotypes for lines overexpressing the At1g74450 ORF. Plants overexpressing the multiple-stress responsive gene At1g74450 are stunted in height and have reduced male fertility. Alexander staining of anthers from flowers at developmental stage 12-13 showed either an absence or a reduction in viable pollen compared to wildtype Col-0 and At1g74450 knockout lines. Interestingly, the effects of stress on crop productivity are most severe at developmental stages such as male gametophyte development. However, the molecular factors and regulatory networks underlying environmental stress-induced male gametophytic alterations are still largely unknown. Our results indicate that the At1g74450 gene provides a potential link between multiple environmental stresses, plant height and pollen development. In addition, ruthenium red staining analysis showed that At1g74450 may affect the composition of the inner seed coat mucilage layer. Finally, C-terminal GFP fusion proteins for At1g74450 were shown to localise to the cytosol.
| S-EPMC4619001 | biostudies-literature
Project description:In this study, we ask two questions: (1) Is reproductive success independent of parental genetic distance in predominately selfing plants? (2) In the absence of early inbreeding depression, is there substantial maternal and/or paternal variation in reproductive success in natural populations? Seed yield in single pollinations and proportion of seeds sired in mixed pollinations were studied in genetically defined accessions of the predominately selfing plant Arabidopsis thaliana by conducting two diallel crosses. The first diallel was a standard, single pollination design that we used to examine variance in seed yield. The second diallel was a mixed pollination design that utilized a standard pollen competitor to examine variance in proportion of seeds sired. We found no correlation between reproductive success and parental genetic distance, and self-pollen does not systematically differ in reproductive success compared to outcross pollen, suggesting that Arabidopsis populations do not experience embryo lethality due to early-acting inbreeding or outbreeding depression. We used these data to partition the contributions to total phenotypic variation from six sources, including maternal contributions, paternal contributions and parental interactions. For seed yield in single pollinations, maternal effects accounted for the most significant source of variance (16.6 %). For proportion of seeds sired in mixed pollinations, the most significant source of variance was paternal effects (17.9 %). Thus, we show that population-level genetic similarities, including selfing, do not correlate with reproductive success, yet there is still significant paternal variance under competition. This suggests two things. First, since these differences are unlikely due to early-acting inbreeding depression or differential pollen viability, this implicates natural variation in pollen germination and tube growth dynamics. Second, this strongly supports a model of fixation of pollen performance genes in populations, offering a focus for future genetic studies in differential reproductive success.
| S-EPMC3825607 | biostudies-literature