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1.  Local Evolution of Seed Flotation in Arabidopsis 
PLoS Genetics  2014;10(3):e1004221.
Arabidopsis seeds rapidly release hydrophilic polysaccharides from the seed coat on imbibition. These form a heavy mucilage layer around the seed that makes it sink in water. Fourteen natural Arabidopsis variants from central Asia and Scandinavia were identified with seeds that have modified mucilage release and float. Four of these have a novel mucilage phenotype with almost none of the released mucilage adhering to the seed and the absence of cellulose microfibrils. Mucilage release was modified in the variants by ten independent causal mutations in four different loci. Seven distinct mutations affected one locus, coding the MUM2 β-D-galactosidase, and represent a striking example of allelic heterogeneity. The modification of mucilage release has thus evolved a number of times independently in two restricted geographical zones. All the natural mutants identified still accumulated mucilage polysaccharides in seed coat epidermal cells. Using nuclear magnetic resonance (NMR) relaxometry their production and retention was shown to reduce water mobility into internal seed tissues during imbibition, which would help to maintain seed buoyancy. Surprisingly, despite released mucilage being an excellent hydrogel it did not increase the rate of water uptake by internal seed tissues and is more likely to play a role in retaining water around the seed.
Author Summary
Seeds of the model plant Arabidopsis release sticky mucilage on imbibition that is constituted of complex polysaccharides. In this study, we have identified and characterised natural Arabidopsis variants that do not release mucilage and found that their seeds float. The accumulation of unreleased polysaccharides in the seed coat reduced water uptake rates on imbibition and would maintain buoyancy. We subsequently identified additional floating natural variants where mucilage is released, but is not attached to the seed, apparently due to defective cellulose production. The different variants arise from at least ten independent unique mutations and were collected from two discrete geographical areas. Arabidopsis seed flotation has thus evolved several times due to modifications in mucilage release. Released mucilage was found to retain water, but did not improve imbibition of internal seed tissues, indicating a role in maintaining seeds hydrated. These findings highlight the physical and potential physiological effects of mucilage production by the seed coat.
doi:10.1371/journal.pgen.1004221
PMCID: PMC3953066  PMID: 24625826
2.  Insights into the Dekkera bruxellensis Genomic Landscape: Comparative Genomics Reveals Variations in Ploidy and Nutrient Utilisation Potential amongst Wine Isolates 
PLoS Genetics  2014;10(2):e1004161.
The yeast Dekkera bruxellensis is a major contaminant of industrial fermentations, such as those used for the production of biofuel and wine, where it outlasts and, under some conditions, outcompetes the major industrial yeast Saccharomyces cerevisiae. In order to investigate the level of inter-strain variation that is present within this economically important species, the genomes of four diverse D. bruxellensis isolates were compared. While each of the four strains was shown to contain a core diploid genome, which is clearly sufficient for survival, two of the four isolates have a third haploid complement of chromosomes. The sequences of these additional haploid genomes were both highly divergent from those comprising the diploid core and divergent between the two triploid strains. Similar to examples in the Saccharomyces spp. clade, where some allotriploids have arisen on the basis of enhanced ability to survive a range of environmental conditions, it is likely these strains are products of two independent hybridisation events that may have involved multiple species or distinct sub-species of Dekkera. Interestingly these triploid strains represent the vast majority (92%) of isolates from across the Australian wine industry, suggesting that the additional set of chromosomes may confer a selective advantage in winery environments that has resulted in these hybrid strains all-but replacing their diploid counterparts in Australian winery settings. In addition to the apparent inter-specific hybridisation events, chromosomal aberrations such as strain-specific insertions and deletions and loss-of-heterozygosity by gene conversion were also commonplace. While these events are likely to have affected many phenotypes across these strains, we have been able to link a specific deletion to the inability to utilise nitrate by some strains of D. bruxellensis, a phenotype that may have direct impacts in the ability for these strains to compete with S. cerevisiae.
Author Summary
The yeast D. bruxellensis is of great importance in biofuel and fermented beverage industries, largely as a contaminant and/or spoilage organism. Its lifestyle is not unlike that of the wine/brewing/baking yeast S. cerevisiae, with independent evolutionary pathways having led to this convergence; these species are phylogenetically very distant. Unlike S. cerevisiae, D. bruxellensis is highly intractable in the laboratory; it is difficult to mate and to transform, making even the most basic genetic analysis very difficult. Thus we still have a great deal to learn about this economically important yeast. The latest gene sequencing technologies are, however, providing a means of addressing these limitations. The current manuscript describes a comparative genomics approach to providing insights into inter-strain variations that shape the genomic landscape of D. bruxellensis. Like other industrial yeasts, it has a diploid core genome, but there are also triploid isolates which possess the core diploid complement with an additional, more distantly related, full set of chromosomes. Evidence presented in this paper suggests that this form of triploidy has arisen more than once in the evolutionary history of D. bruxellensis, and it confers a selective advantage for strains of this yeast isolated from wineries.
doi:10.1371/journal.pgen.1004161
PMCID: PMC3923673  PMID: 24550744
3.  Comparative Evolutionary and Developmental Dynamics of the Cotton (Gossypium hirsutum) Fiber Transcriptome 
PLoS Genetics  2014;10(1):e1004073.
The single-celled cotton (Gossypium hirsutum) fiber provides an excellent model to investigate how human selection affects phenotypic evolution. To gain insight into the evolutionary genomics of cotton domestication, we conducted comparative transcriptome profiling of developing cotton fibers using RNA-Seq. Analysis of single-celled fiber transcriptomes from four wild and five domesticated accessions from two developmental time points revealed that at least one-third and likely one-half of the genes in the genome are expressed at any one stage during cotton fiber development. Among these, ∼5,000 genes are differentially expressed during primary and secondary cell wall synthesis between wild and domesticated cottons, with a biased distribution among chromosomes. Transcriptome data implicate a number of biological processes affected by human selection, and suggest that the domestication process has prolonged the duration of fiber elongation in modern cultivated forms. Functional analysis suggested that wild cottons allocate greater resources to stress response pathways, while domestication led to reprogrammed resource allocation toward increased fiber growth, possibly through modulating stress-response networks. This first global transcriptomic analysis using multiple accessions of wild and domesticated cottons is an important step toward a more comprehensive systems perspective on cotton fiber evolution. The understanding that human selection over the past 5,000+ years has dramatically re-wired the cotton fiber transcriptome sets the stage for a deeper understanding of the genetic architecture underlying cotton fiber synthesis and phenotypic evolution.
Author Summary
Ever since Darwin biologists have recognized that comparative study of crop plants and their wild relatives offers a powerful framework for generating insights into the mechanisms that underlie evolutionary change. Here, we study the domestication process in cotton, Gossypium hirsutum, an allopolyploid species (containing two different genomes) which initially was domesticated approximately 5000 years ago, and which primarily is grown for its single-celled seed fibers. Strong directional selection over the millennia was accompanied by transformation of the short, coarse, and brown fibers of wild plants into the long, strong, and fine white fibers of the modern cotton crop plant. To explore the evolutionary genetics of cotton domestication, we conducted transcriptome profiling of developing cotton fibers from multiple accessions of wild and domesticated cottons. Comparative analysis revealed that the domestication process dramatically rewired the transcriptome, affecting more than 5,000 genes, and with a more evenly balanced usage of the duplicated copies arising from genome doubling. We identify many different biological processes that were involved in this transformation, including those leading to a prolongation of fiber elongation and a reallocation of resources toward increased fiber growth in modern forms. The data provide a rich resource for future functional analyses targeting crop improvement and evolutionary objectives.
doi:10.1371/journal.pgen.1004073
PMCID: PMC3879233  PMID: 24391525
4.  Selection on Plant Male Function Genes Identifies Candidates for Reproductive Isolation of Yellow Monkeyflowers 
PLoS Genetics  2013;9(12):e1003965.
Understanding the genetic basis of reproductive isolation promises insight into speciation and the origins of biological diversity. While progress has been made in identifying genes underlying barriers to reproduction that function after fertilization (post-zygotic isolation), we know much less about earlier acting pre-zygotic barriers. Of particular interest are barriers involved in mating and fertilization that can evolve extremely rapidly under sexual selection, suggesting they may play a prominent role in the initial stages of reproductive isolation. A significant challenge to the field of speciation genetics is developing new approaches for identification of candidate genes underlying these barriers, particularly among non-traditional model systems. We employ powerful proteomic and genomic strategies to study the genetic basis of conspecific pollen precedence, an important component of pre-zygotic reproductive isolation among yellow monkeyflowers (Mimulus spp.) resulting from male pollen competition. We use isotopic labeling in combination with shotgun proteomics to identify more than 2,000 male function (pollen tube) proteins within maternal reproductive structures (styles) of M. guttatus flowers where pollen competition occurs. We then sequence array-captured pollen tube exomes from a large outcrossing population of M. guttatus, and identify those genes with evidence of selective sweeps or balancing selection consistent with their role in pollen competition. We also test for evidence of positive selection on these genes more broadly across yellow monkeyflowers, because a signal of adaptive divergence is a common feature of genes causing reproductive isolation. Together the molecular evolution studies identify 159 pollen tube proteins that are candidate genes for conspecific pollen precedence. Our work demonstrates how powerful proteomic and genomic tools can be readily adapted to non-traditional model systems, allowing for genome-wide screens towards the goal of identifying the molecular basis of genetically complex traits.
Author Summary
Barriers to reproduction are necessary for generating new species. Little is known about the genes underlying reproductive barriers, particularly those that function prior to fertilization, but their identity is of great interest as they offer insight into the genetic mechanisms and evolutionary forces generating biological diversity. In this work, we use an emerging plant model system for speciation studies (yellow monkeyflowers, species of Mimulus) to identify genes that might influence the relative competitive abilities of male pollen from the same versus different species within the maternal flower's style. This is a common reproductive barrier among plant taxa known as conspecific pollen precedence (CPP), and is analogous to sperm competition during animal fertilization. We first identify the pollen proteins that are found within the style where pollen competition occurs, and then screen these for evidence that may indicate which genes have been targets of pollen competition (a form of sexual selection among individuals of a population) or adaptive diversification among species of yellow monkeyflowers (a common feature of genes underlying reproductive barriers). Our evolutionary analyses identify 159 candidates that may function in reproductive isolation of yellow monkeyflowers, and provide some of the first broad perspectives on evolution of plant reproductive genes.
doi:10.1371/journal.pgen.1003965
PMCID: PMC3854799  PMID: 24339787
5.  Plasticity Regulators Modulate Specific Root Traits in Discrete Nitrogen Environments 
PLoS Genetics  2013;9(9):e1003760.
Plant development is remarkably plastic but how precisely can the plant customize its form to specific environments? When the plant adjusts its development to different environments, related traits can change in a coordinated fashion, such that two traits co-vary across many genotypes. Alternatively, traits can vary independently, such that a change in one trait has little predictive value for the change in a second trait. To characterize such “tunability” in developmental plasticity, we carried out a detailed phenotypic characterization of complex root traits among 96 accessions of the model Arabidopsis thaliana in two nitrogen environments. The results revealed a surprising level of independence in the control of traits to environment – a highly tunable form of plasticity. We mapped genetic architecture of plasticity using genome-wide association studies and further used gene expression analysis to narrow down gene candidates in mapped regions. Mutants in genes implicated by association and expression analysis showed precise defects in the predicted traits in the predicted environment, corroborating the independent control of plasticity traits. The overall results suggest that there is a pool of genetic variability in plants that controls traits in specific environments, with opportunity to tune crop plants to a given environment.
Author Summary
Plants can dramatically alter their development in order to cope with new environmental conditions. Such plasticity is especially evident in the root system since it adopts a particular architecture under one condition, but can change architecture by altering the extent of lateral root branching in a different condition. To explore the extent of root plasticity to the critical nutrient nitrogen we analyzed a natural population of the model plant Arabidopsis in both nitrogen-limiting and nitrogen-rich environments. This revealed that root architecture plasticity appears to be the combined effect of many individual root responses to the environment that are independently modulated. Each aspect, such as lateral root length, number, or density seems to be turned on or off separately, giving the whole system flexibility. We then identified specific genes that control these individual component responses by exploring the genetic variation across the natural population in combination with analyzing which genes respond to nitrogen. Together the results help us gain insights into how the environment shapes plant development. This knowledge can be used to better understand how the growth of our existing crop species might change as the climate varies, and identify new crop varieties that will be robust to such variation.
doi:10.1371/journal.pgen.1003760
PMCID: PMC3764102  PMID: 24039603
6.  Hard Selective Sweep and Ectopic Gene Conversion in a Gene Cluster Affording Environmental Adaptation 
PLoS Genetics  2013;9(8):e1003707.
Among the rare colonizers of heavy-metal rich toxic soils, Arabidopsis halleri is a compelling model extremophile, physiologically distinct from its sister species A. lyrata, and A. thaliana. Naturally selected metal hypertolerance and extraordinarily high leaf metal accumulation in A. halleri both require Heavy Metal ATPase4 (HMA4) encoding a PIB-type ATPase that pumps Zn2+ and Cd2+ out of specific cell types. Strongly enhanced HMA4 expression results from a combination of gene copy number expansion and cis-regulatory modifications, when compared to A. thaliana. These findings were based on a single accession of A. halleri. Few studies have addressed nucleotide sequence polymorphism at loci known to govern adaptations. We thus sequenced 13 DNA segments across the HMA4 genomic region of multiple A. halleri individuals from diverse habitats. Compared to control loci flanking the three tandem HMA4 gene copies, a gradual depletion of nucleotide sequence diversity and an excess of low-frequency polymorphisms are hallmarks of positive selection in HMA4 promoter regions, culminating at HMA4-3. The accompanying hard selective sweep is segmentally eclipsed as a consequence of recurrent ectopic gene conversion among HMA4 protein-coding sequences, resulting in their concerted evolution. Thus, HMA4 coding sequences exhibit a network-like genealogy and locally enhanced nucleotide sequence diversity within each copy, accompanied by lowered sequence divergence between paralogs in any given individual. Quantitative PCR corroborated that, across A. halleri, three genomic HMA4 copies generate overall 20- to 130-fold higher transcript levels than in A. thaliana. Together, our observations constitute an unexpectedly complex profile of polymorphism resulting from natural selection for increased gene product dosage. We propose that these findings are paradigmatic of a category of multi-copy genes from a broad range of organisms. Our results emphasize that enhanced gene product dosage, in addition to neo- and sub-functionalization, can account for the genomic maintenance of gene duplicates underlying environmental adaptation.
Author Summary
Existing genetic diversity reflects evolutionary history, but it has rarely been possible to probe for footprints of selection at loci known to functionally govern adaptive traits. Both naturally selected metal hypertolerance and extraordinary leaf metal accumulation of the extremophile Arabidopsis halleri require strongly enhanced transcript levels of Heavy Metal ATPase4 (HMA4) encoding a PIB-type ATPase that pumps Zn2+ and Cd2+ out of specific cells. By comparison to the metal-sensitive A. thaliana, highly elevated HMA4 expression results from a combination of gene copy number expansion and cis-regulatory modifications. But how do these findings, which were based on a single accession, relate to species-wide HMA4 sequence diversity in A. halleri? Addressing this question, we detect positive selection in the promoter regions of three tandem A. halleri HMA4 paralogs, which are uniformly cis-activated. The accompanying hard selective sweep, however, is segmentally eclipsed as a consequence of recurrent ectopic gene conversion among HMA4 protein-coding sequences, which undergo concerted evolution. Together, this constitutes an unexpectedly complex profile of polymorphism as a result of natural selection. Our observations can serve as a blueprint for future analyses of duplicated genes that have undergone selection for more of the same gene product.
doi:10.1371/journal.pgen.1003707
PMCID: PMC3749932  PMID: 23990800
7.  Divergent Selection Drives Genetic Differentiation in an R2R3-MYB Transcription Factor That Contributes to Incipient Speciation in Mimulus aurantiacus 
PLoS Genetics  2013;9(3):e1003385.
Identifying the molecular genetic basis of traits contributing to speciation is of crucial importance for understanding the ecological and evolutionary mechanisms that generate biodiversity. Despite several examples describing putative “speciation genes,” it is often uncertain to what extent these genetic changes have contributed to gene flow reductions in nature. Therefore, considerable interest lies in characterizing the molecular basis of traits that actively confer reproductive isolation during the early stages of speciation, as these loci can be attributed directly to the process of divergence. In Southern California, two ecotypes of Mimulus aurantiacus are parapatric and differ primarily in flower color, with an anthocyanic, red-flowered morph in the west and an anthocyanin-lacking, yellow-flowered morph in the east. Evidence suggests that the genetic changes responsible for this shift in flower color have been essential for divergence and have become fixed in natural populations of each ecotype due to almost complete differences in pollinator preference. In this study, we demonstrate that a cis-regulatory mutation in an R2R3-MYB transcription factor results in differential regulation of enzymes in the anthocyanin biosynthetic pathway and is the major contributor to differences in floral pigmentation. In addition, molecular population genetic data show that, despite gene flow at neutral loci, divergent selection has driven the fixation of alternate alleles at this gene between ecotypes. Therefore, by identifying the genetic basis underlying ecologically based divergent selection in flower color between these ecotypes, we have revealed the ecological and functional mechanisms involved in the evolution of pre-mating isolation at the early stages of incipient speciation.
Author Summary
A fundamental goal of evolutionary biology is to identify the genetic changes and evolutionary mechanisms involved in speciation. Knowledge of the genes allows us to address important unresolved questions about the genetics of speciation, such as what role does ecologically based natural selection play during the process of divergence? We characterize the evolutionary processes and genetic changes that influence the early stages of speciation between divergent populations of the wildflower Mimulus aurantiacus. Populations with different flower colors attract different animal pollinators, resulting in a prominent reproductive barrier that reduces gene exchange between populations. We provide multiple lines of corroborating evidence to verify the functional role of the major gene responsible for this flower color shift, including genetic mapping, gene expression analyses, and gene knockdown approaches. We then use molecular population genetic techniques to show a remarkably tight association between genetic variants in this gene and the geographic shift in flower color, which reflects a history of divergent natural selection on flower color between these populations. These results provide a striking demonstration of how adaptation to different environments can result in the early stages of divergence and the evolution of reproductive isolation between populations.
doi:10.1371/journal.pgen.1003385
PMCID: PMC3605050  PMID: 23555295
8.  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.
doi:10.3389/fpls.2013.00546
PMCID: PMC3879461  PMID: 24427164
Arabidopsis arenosa; polyploidy; cytology; immunolocalization; meiosis; recombination; synaptonemal complex
9.  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.
doi:10.1371/journal.pgen.1003093
PMCID: PMC3527224  PMID: 23284289
10.  Genome-Wide Association Studies Identify Heavy Metal ATPase3 as the Primary Determinant of Natural Variation in Leaf Cadmium in Arabidopsis thaliana 
PLoS Genetics  2012;8(9):e1002923.
Understanding the mechanism of cadmium (Cd) accumulation in plants is important to help reduce its potential toxicity to both plants and humans through dietary and environmental exposure. Here, we report on a study to uncover the genetic basis underlying natural variation in Cd accumulation in a world-wide collection of 349 wild collected Arabidopsis thaliana accessions. We identified a 4-fold variation (0.5–2 µg Cd g−1 dry weight) in leaf Cd accumulation when these accessions were grown in a controlled common garden. By combining genome-wide association mapping, linkage mapping in an experimental F2 population, and transgenic complementation, we reveal that HMA3 is the sole major locus responsible for the variation in leaf Cd accumulation we observe in this diverse population of A. thaliana accessions. Analysis of the predicted amino acid sequence of HMA3 from 149 A. thaliana accessions reveals the existence of 10 major natural protein haplotypes. Association of these haplotypes with leaf Cd accumulation and genetics complementation experiments indicate that 5 of these haplotypes are active and 5 are inactive, and that elevated leaf Cd accumulation is associated with the reduced function of HMA3 caused by a nonsense mutation and polymorphisms that change two specific amino acids.
Author Summary
Cadmium (Cd) is a potentially toxic metal pollutant that threatens food quality and human health in many regions of the world. Plants have evolved mechanisms for the acquisition of essential metals such as zinc and iron from the soil. Though often quite specific, such mechanisms can also lead to the accumulation of Cd by plants. Understanding natural variation in the processes that contribute to Cd accumulation in food crops could help minimize the human health risk posed. We have discovered that DNA sequence changes at a single gene, which encodes the Heavy Metal ATPase 3 (HMA3), drives the variation in Cd accumulation we observe in a world-wide sample of Arabidopsis thaliana. We identified 10 major HMA3 protein variants, of which five contribute to reduce Cd accumulation in leaves of A. thaliana.
doi:10.1371/journal.pgen.1002923
PMCID: PMC3435251  PMID: 22969436
11.  Horizontal transfer of expressed genes in a parasitic flowering plant 
BMC Genomics  2012;13:227.
Background
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.
Results
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.
Conclusions
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.
doi:10.1186/1471-2164-13-227
PMCID: PMC3460754  PMID: 22681756
Rafflesia; Transcriptome; Phylogenomics; Horizontal gene transfer; Codon usage
12.  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.
doi:10.1371/journal.pgen.1002164
PMCID: PMC3136440  PMID: 21779175
13.  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.
doi:10.1098/rstb.2009.0304
PMCID: PMC2871890  PMID: 20439283
speciation; Arabidopsis; hybrid incompatibility; self-incompatibility; polyploid speciation
14.  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.
doi:10.1534/genetics.111.126607
PMCID: PMC3122318  PMID: 21406681
15.  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.
doi:10.1199/tab.0138
PMCID: PMC3244966  PMID: 22303263
16.  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.
doi:10.1371/journal.pgen.1000890
PMCID: PMC2845663  PMID: 20361058
17.  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.
doi:10.1371/journal.pbio.0050236
PMCID: PMC1964774  PMID: 17803357

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