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1.  Meiotic adaptation to genome duplication in Arabidopsis arenosa 
Current biology : CB  2013;23(21):10.1016/j.cub.2013.08.059.
Whole genome duplication (WGD) is a major factor in the evolution of multicellular eukaryotes, yet by doubling the number of homologs, WGD severely challenges reliable chromosome segregation [1, 2, 3], a process conserved across kingdoms [4]. Despite this, numerous genome-duplicated (polyploid) species persist in nature, indicating early problems can be overcome [1, 2]. Little is known about which genes are involved – only one has been molecularly characterized [5]. To gain new insights into the molecular basis of adaptation to polyploidy, we investigated genome-wide patterns of differentiation between natural diploids and tetraploids of Arabidopsis arenosa, an outcrossing relative of A. thaliana [6, 7]. We first show that diploids are not preadapted to polyploid meiosis. We then use a genome scanning approach to show that while polymorphism is extensively shared across ploidy levels, there is strong ploidy-specific differentiation in 39 regions spanning 44 genes. These are discrete, mostly single-gene peaks of sharply elevated differentiation. Among these peaks are eight meiosis genes whose encoded proteins coordinate a specific subset of early meiotic functions, suggesting these genes comprise a polygenic solution to WGD-associated chromosome segregation challenges. Our findings indicate that even conserved meiotic processes can be capable of nimble evolutionary shifts when required.
PMCID: PMC3859316  PMID: 24139735
2.  Activation of the Arabidopsis thaliana Immune System by Combinations of Common ACD6 Alleles 
PLoS Genetics  2014;10(7):e1004459.
A fundamental question in biology is how multicellular organisms distinguish self and non-self. The ability to make this distinction allows animals and plants to detect and respond to pathogens without triggering immune reactions directed against their own cells. In plants, inappropriate self-recognition results in the autonomous activation of the immune system, causing affected individuals to grow less well. These plants also suffer from spontaneous cell death, but are at the same time more resistant to pathogens. Known causes for such autonomous activation of the immune system are hyperactive alleles of immune regulators, or epistatic interactions between immune regulators and unlinked genes. We have discovered a third class, in which the Arabidopsis thaliana immune system is activated by interactions between natural alleles at a single locus, ACCELERATED CELL DEATH 6 (ACD6). There are two main types of these interacting alleles, one of which has evolved recently by partial resurrection of a pseudogene, and each type includes multiple functional variants. Most previously studies hybrid necrosis cases involve rare alleles found in geographically unrelated populations. These two types of ACD6 alleles instead occur at low frequency throughout the range of the species, and have risen to high frequency in the Northeast of Spain, suggesting a role in local adaptation. In addition, such hybrids occur in these populations in the wild. The extensive functional variation among ACD6 alleles points to a central role of this locus in fine-tuning pathogen defenses in natural populations.
Author Summary
Plants and their pathogens are engaged in an endless evolutionary battle. The invention of new strategies by pathogens pushes plants to continuously update their defenses. This in turn leads the pathogens to circumvent these new defenses, and so on. Given the abundance of potential enemies, it is therefore not surprising that genes involved in defense against pathogens are among the most variable in plants. A drawback of this extreme variation in pathogen-recognition mechanisms is that at times the plant mistakes itself for an enemy, leading to autonomous activation of defense responses in the absence of pathogens. Conventional models for this phenomenon, called hybrid necrosis, require the interaction between two different genes. Here we show instead that hybrid necrosis can be triggered by interactions between variants of a single gene, ACD6 (ACCELERATED CELL DEATH 6). Several of these variants are common in natural Arabidopsis thaliana populations and can interact to give different levels of activation of the immune system. Our results provide important information into the evolution and operation of the plant defense system. Moreover, the abundant presence of ACD6 functional variation suggests a major role for this gene in modulating plant defenses in nature.
PMCID: PMC4091793  PMID: 25010663
3.  Cheaters divide and conquer 
eLife  2014;3:e03371.
Three ‘killer genes’ in one species of fission yeast act selfishly and keep it reproductively isolated from a closely related species.
PMCID: PMC4066436  PMID: 24963143
speciation; meiotic drive; chromosomal rearrangements; recombination; S. pombe
4.  Cytological techniques to analyze meiosis in Arabidopsis arenosa for investigating adaptation to polyploidy 
Arabidopsis arenosa is a close relative of the model plant A. thaliana, and exists in nature as stable diploid and autotetraploid populations. Natural tetraploids have adapted to whole genome duplication and do not commonly show meiotic errors such as multivalent and univalent formation, which can lead to chromosome non-disjunction and reduced fertility. A genome scan for genes strongly differentiated between diploid and autotetraploid A. arenosa identified a subset of meiotic genes that may be responsible for adaptation to polyploid meiosis. To investigate the mechanisms by which A. arenosa adapted to its polyploid state, and the functionality of the identified potentially adaptive polymorphisms, a thorough cytological analysis is required. Therefore, in this chapter we describe methods and techniques to analyze male meiosis in A. arenosa, including optimum plant growth conditions, and immunocytological and cytological approaches developed with the specific purpose of understanding meiotic adaptation in an autotetraploid. In addition we present a meiotic cytological atlas to be used as a reference for particular stages and discuss observations arising from a comparison of meiosis between diploid and autotetraploid A. arenosa.
PMCID: PMC3879461  PMID: 24427164
Arabidopsis arenosa; polyploidy; cytology; immunolocalization; meiosis; recombination; synaptonemal complex
5.  Genetic Adaptation Associated with Genome-Doubling in Autotetraploid Arabidopsis arenosa 
PLoS Genetics  2012;8(12):e1003093.
Genome duplication, which results in polyploidy, is disruptive to fundamental biological processes. Genome duplications occur spontaneously in a range of taxa and problems such as sterility, aneuploidy, and gene expression aberrations are common in newly formed polyploids. In mammals, genome duplication is associated with cancer and spontaneous abortion of embryos. Nevertheless, stable polyploid species occur in both plants and animals. Understanding how natural selection enabled these species to overcome early challenges can provide important insights into the mechanisms by which core cellular functions can adapt to perturbations of the genomic environment. Arabidopsis arenosa includes stable tetraploid populations and is related to well-characterized diploids A. lyrata and A. thaliana. It thus provides a rare opportunity to leverage genomic tools to investigate the genetic basis of polyploid stabilization. We sequenced the genomes of twelve A. arenosa individuals and found signatures suggestive of recent and ongoing selective sweeps throughout the genome. Many of these are at genes implicated in genome maintenance functions, including chromosome cohesion and segregation, DNA repair, homologous recombination, transcriptional regulation, and chromatin structure. Numerous encoded proteins are predicted to interact with one another. For a critical meiosis gene, ASYNAPSIS1, we identified a non-synonymous mutation that is highly differentiated by cytotype, but present as a rare variant in diploid A. arenosa, indicating selection may have acted on standing variation already present in the diploid. Several genes we identified that are implicated in sister chromatid cohesion and segregation are homologous to genes identified in a yeast mutant screen as necessary for survival of polyploid cells, and also implicated in genome instability in human diseases including cancer. This points to commonalities across kingdoms and supports the hypothesis that selection has acted on genes controlling genome integrity in A. arenosa as an adaptive response to genome doubling.
Author Summary
Duplication of an entire set of chromosomes is a dramatic mutation disruptive to core cellular functions. Genome duplication and the genomic instability that generally follows can cause problems with fertility and viability, and in mammals is associated with cancer and spontaneous abortion. Yet, established polyploids occur naturally in both plants and animals. How do these organisms overcome these early problems and ultimately stabilize? The genetic basis of the adaptive response to polyploidy has remained almost completely unknown. We took advantage of modern genomic approaches to gain insight into this using a stable polyploid plant, Arabidopsis arenosa. We found evidence of selection in genes that control core genome maintenance processes. These overlap with genes or functions shown in yeast to be necessary for survival of polyploid cells and in humans implicated in cancer. Our results identify genes controlling core genome maintenance functions that may have undergone compensatory adaptation after genome doubling.
PMCID: PMC3527224  PMID: 23284289
6.  Horizontal transfer of expressed genes in a parasitic flowering plant 
BMC Genomics  2012;13:227.
Recent studies have shown that plant genomes have potentially undergone rampant horizontal gene transfer (HGT). In plant parasitic systems HGT appears to be facilitated by the intimate physical association between the parasite and its host. HGT in these systems has been invoked when a DNA sequence obtained from a parasite is placed phylogenetically very near to its host rather than with its closest relatives. Studies of HGT in parasitic plants have relied largely on the fortuitous discovery of gene phylogenies that indicate HGT, and no broad systematic search for HGT has been undertaken in parasitic systems where it is most expected to occur.
We analyzed the transcriptomes of the holoparasite Rafflesia cantleyi Solms-Laubach and its obligate host Tetrastigma rafflesiae Miq. using phylogenomic approaches. Our analyses show that several dozen actively transcribed genes, most of which appear to be encoded in the nuclear genome, are likely of host origin. We also find that hundreds of vertically inherited genes (VGT) in this parasitic plant exhibit codon usage properties that are more similar to its host than to its closest relatives.
Our results establish for the first time a substantive number of HGTs in a plant host-parasite system. The elevated rate of unidirectional host-to- parasite gene transfer raises the possibility that HGTs may provide a fitness benefit to Rafflesia for maintaining these genes. Finally, a similar convergence in codon usage of VGTs has been shown in microbes with high HGT rates, which may help to explain the increase of HGTs in these parasitic plants.
PMCID: PMC3460754  PMID: 22681756
Rafflesia; Transcriptome; Phylogenomics; Horizontal gene transfer; Codon usage
7.  Complex Evolutionary Events at a Tandem Cluster of Arabidopsis thaliana Genes Resulting in a Single-Locus Genetic Incompatibility 
PLoS Genetics  2011;7(7):e1002164.
Non-additive interactions between genomes have important implications, not only for practical applications such as breeding, but also for understanding evolution. In extreme cases, genes from different genomic backgrounds may be incompatible and compromise normal development or physiology. Of particular interest are non-additive interactions of alleles at the same locus. For example, overdominant behavior of alleles, with respect to plant fitness, has been proposed as an important component of hybrid vigor, while underdominance may lead to reproductive isolation. Despite their importance, only a few cases of genetic over- or underdominance affecting plant growth or fitness are understood at the level of individual genes. Moreover, the relationship between biochemical and fitness effects may be complex: genetic overdominance, that is, increased or novel activity of a gene may lead to evolutionary underdominance expressed as hybrid weakness. Here, we describe a non-additive interaction between alleles at the Arabidopsis thaliana OAK (OUTGROWTH-ASSOCIATED PROTEIN KINASE) gene. OAK alleles from two different accessions interact in F1 hybrids to cause a variety of aberrant growth phenotypes that depend on a recently acquired promoter with a novel expression pattern. The OAK gene, which is located in a highly variable tandem array encoding closely related receptor-like kinases, is found in one third of A. thaliana accessions, but not in the reference accession Col-0. Besides recruitment of exons from nearby genes as promoter sequences, key events in OAK evolution include gene duplication and divergence of a potential ligand-binding domain. OAK kinase activity is required for the aberrant phenotypes, indicating it is not recognition of an aberrant protein, but rather a true gain of function, or overdominance for gene activity, that leads to this underdominance for fitness. Our work provides insights into how tandem arrays, which are particularly prone to frequent, complex rearrangements, can produce genetic novelty.
Author Summary
While intraspecific hybrids are vitally important in modern agriculture because they often perform better than their inbred parents, certain hybrid combinations fail to develop normally and are inferior to their parents. We have identified an Arabidopsis thaliana hybrid with several aberrant growth phenotypes that are caused by divergence at a single locus encoding the receptor-like kinase OUTGROWTH-ASSOCIATED PROTEIN KINASE (OAK). OAK belongs to a group of similar genes arranged in a tandem cluster that varies substantially between A. thaliana strains. OAK originated through duplication within the cluster with concurrent recruitment of coding sequences from nearby genes to form a new promoter with a novel expression pattern. Kinase activity of OAK is required for its effects, indicating that it is not recognition of an aberrant protein but rather a true gain of function that leads to the incompatibility. Most of the incompatibility seems to come from divergence within the extracellular ligand-binding domain of the OAK protein, indicating that heterodimers of OAK may have higher affinity for a natural substrate compared to either homodimer. Finally, mis-expression of the incompatible OAK alleles from the promoter present in the reference strain of A. thaliana also leads to genetic incompatibility, but with different phenotypic outcomes.
PMCID: PMC3136440  PMID: 21779175
8.  Arabidopsis and relatives as models for the study of genetic and genomic incompatibilities 
The past few years have seen considerable advances in speciation research, but whether drift or adaptation is more likely to lead to genetic incompatibilities remains unknown. Some of the answers will probably come from not only studying incompatibilities between well-established species, but also from investigating incipient speciation events, to learn more about speciation as an evolutionary process. The genus Arabidopsis, which includes the widely used Arabidopsis thaliana, provides a useful set of model species for studying many aspects of population divergence. The genus contains both self-incompatible and incompatible species, providing a platform for studying the impact of mating system changes on genetic differentiation. Another important path to plant speciation is via formation of polyploids, and this can be investigated in the young allotetraploid species A. arenosa. Finally, there are many cases of intraspecific incompatibilities in A. thaliana, and recent progress has been made in discovering the genes underlying both F1 and F2 breakdown. In the near future, all these studies will be greatly empowered by complete genome sequences not only for all members of this relatively small genus, but also for many different individuals within each species.
PMCID: PMC2871890  PMID: 20439283
speciation; Arabidopsis; hybrid incompatibility; self-incompatibility; polyploid speciation
9.  Genetic Architecture of Flowering-Time Variation in Arabidopsis thaliana 
Genetics  2011;188(2):421-433.
The onset of flowering is an important adaptive trait in plants. The small ephemeral species Arabidopsis thaliana grows under a wide range of temperature and day-length conditions across much of the Northern hemisphere, and a number of flowering-time loci that vary between different accessions have been identified before. However, only few studies have addressed the species-wide genetic architecture of flowering-time control. We have taken advantage of a set of 18 distinct accessions that present much of the common genetic diversity of A. thaliana and mapped quantitative trait loci (QTL) for flowering time in 17 F2 populations derived from these parents. We found that the majority of flowering-time QTL cluster in as few as five genomic regions, which include the locations of the entire FLC/MAF clade of transcription factor genes. By comparing effects across shared parents, we conclude that in several cases there might be an allelic series caused by rare alleles. While this finding parallels results obtained for maize, in contrast to maize much of the variation in flowering time in A. thaliana appears to be due to large-effect alleles.
PMCID: PMC3122318  PMID: 21406681
10.  Progress and Promise in using Arabidopsis to Study Adaptation, Divergence, and Speciation 
Fundamental questions remain to be answered on how lineages split and new species form. The Arabidopsis genus, with several increasingly well characterized species closely related to the model system A. thaliana, provides a rare opportunity to address key questions in speciation research. Arabidopsis species, and in some cases populations within a species, vary considerably in their habitat preferences, adaptations to local environments, mating system, life history strategy, genome structure and chromosome number. These differences provide numerous open doors for understanding the role these factors play in population divergence and how they may cause barriers to arise among nascent species. Molecular tools available in A. thaliana are widely applicable to its relatives, and together with modern comparative genomic approaches they will provide new and increasingly mechanistic insights into the processes underpinning lineage divergence and speciation. We will discuss recent progress in understanding the molecular basis of local adaptation, reproductive isolation and genetic incompatibility, focusing on work utilizing the Arabidopsis genus, and will highlight several areas in which additional research will provide meaningful insights into adaptation and speciation processes in this genus.
PMCID: PMC3244966  PMID: 22303263
11.  Local-Scale Patterns of Genetic Variability, Outcrossing, and Spatial Structure in Natural Stands of Arabidopsis thaliana 
PLoS Genetics  2010;6(3):e1000890.
As Arabidopsis thaliana is increasingly employed in evolutionary and ecological studies, it is essential to understand patterns of natural genetic variation and the forces that shape them. Previous work focusing mostly on global and regional scales has demonstrated the importance of historical events such as long-distance migration and colonization. Far less is known about the role of contemporary factors or environmental heterogeneity in generating diversity patterns at local scales. We sampled 1,005 individuals from 77 closely spaced stands in diverse settings around Tübingen, Germany. A set of 436 SNP markers was used to characterize genome-wide patterns of relatedness and recombination. Neighboring genotypes often shared mosaic blocks of alternating marker identity and divergence. We detected recent outcrossing as well as stretches of residual heterozygosity in largely homozygous recombinants. As has been observed for several other selfing species, there was considerable heterogeneity among sites in diversity and outcrossing, with rural stands exhibiting greater diversity and heterozygosity than urban stands. Fine-scale spatial structure was evident as well. Within stands, spatial structure correlated negatively with observed heterozygosity, suggesting that the high homozygosity of natural A. thaliana may be partially attributable to nearest-neighbor mating of related individuals. The large number of markers and extensive local sampling employed here afforded unusual power to characterize local genetic patterns. Contemporary processes such as ongoing outcrossing play an important role in determining distribution of genetic diversity at this scale. Local “outcrossing hotspots” appear to reshuffle genetic information at surprising rates, while other stands contribute comparatively little. Our findings have important implications for sampling and interpreting diversity among A. thaliana accessions.
Author Summary
The popular model plant Arabidopsis thaliana is increasingly used to investigate questions in evolution and ecology. Thus it is important to understand the dynamics of wild populations at a scale relevant to single plants. We analyzed over 1,000 individuals from 77 ecologically diverse stands near Tübingen in Southwestern Germany. By assaying hundreds of independent markers in their genomes, we generated an unprecedentedly detailed view of local relatedness and recombination patterns. As has been observed previously for Arabidopsis thaliana and other self-compatible plants, even closely neighboring stands were strongly differentiated. Nevertheless, individuals tended to be most closely related to near neighbors, and footprints of recent recombination events were apparent. Structure was evident within stands, suggesting short dispersal ranges and the potential for nearest neighbor mating to reduce heterozygosity. We also observed differences between stands in rural and urban settings: stands in species-rich rural sites had higher average genetic diversity and presented more evidence of past and ongoing outcrossing than their species-poor urban counterparts. Thus novel combinations of genes may primarily arise in a subset of stands that act as “outcrossing hotspots,” while others contribute little to increasing genetic diversity.
PMCID: PMC2845663  PMID: 20361058
12.  Autoimmune Response as a Mechanism for a Dobzhansky-Muller-Type Incompatibility Syndrome in Plants 
PLoS Biology  2007;5(9):e236.
Epistatic interactions between genes are a major factor in evolution. Hybrid necrosis is an example of a deleterious phenotype caused by epistatic interactions that is observed in many intra- and interspecific plant hybrids. A large number of hybrid necrosis cases share phenotypic similarities, suggesting a common underlying mechanism across a wide range of plant species. Here, we report that approximately 2% of intraspecific crosses in Arabidopsis thaliana yield F1 progeny that express necrosis when grown under conditions typical of their natural habitats. We show that several independent cases result from epistatic interactions that trigger autoimmune-like responses. In at least one case, an allele of an NB-LRR disease resistance gene homolog is both necessary and sufficient for the induction of hybrid necrosis, when combined with a specific allele at a second locus. The A. thaliana cases provide insights into the molecular causes of hybrid necrosis, and serve as a model for further investigation of intra- and interspecific incompatibilities caused by a simple epistatic interaction. Moreover, our finding that plant immune-system genes are involved in hybrid necrosis suggests that selective pressures related to host–pathogen conflict might cause the evolution of gene flow barriers in plants.
Author Summary
Hybridization brings together genetic material from different genomes. Sometimes, the novel combinations of genes are deleterious in the offspring, even though the genes were innocuous, or even beneficial, in their parents. Such “genetic incompatibilities” have been observed in crosses within and between species in plants, animals, and fungi, and could contribute to the maintenance of population or species boundaries. We have investigated a highly deleterious genetic incompatibility called hybrid necrosis that is observed in many plant taxa. Using different wild strains of Arabidopsis thaliana as a model, we show that hybrid necrosis is often associated with inappropriate activation of the plant immune system—effectively plant autoimmunity. We identified a gene in one strain that triggers necrosis when combined with a second locus from another strain. The product of this gene is an NB-LRR protein, the most common type of plant disease resistance protein. This finding raises the possibility that selective pressure exerted by pathogens can promote rapid evolution of gene variants that might provide benefits to the parent lineage but can cause serious problems for hybrid progeny.
Sometimes, genes that are innocuous in the parents are deleterious when combined in the offspring. Here, some genes involved in hybrid necrosis in plants have been identified.
PMCID: PMC1964774  PMID: 17803357

Results 1-12 (12)