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1.  Sociogenomics of self vs. non-self cooperation during development of Dictyostelium discoideum 
BMC Genomics  2014;15(1):616.
Dictyostelium discoideum, a microbial model for social evolution, is known to distinguish self from non-self and show genotype-dependent behavior during chimeric development. Aside from a small number of cell-cell recognition genes, however, little is known about the genetic basis of self/non-self recognition in this species. Based on the key hypothesis that there should be differential expression of genes if D. discoideum cells were interacting with non-clone mates, we performed transcriptomic profiling study in this species during clonal vs. chimeric development. The transcriptomic profiles of D. discoideum cells in clones vs. different chimeras were compared at five different developmental stages using a customized microarray. Effects of chimerism on global transcriptional patterns associated with social interactions were observed.
We find 1,759 genes significantly different between chimera and clone, 1,144 genes associated significant strain differences, and 6,586 genes developmentally regulated over time. Principal component analysis showed a small amount of the transcriptional variance to chimerism-related factors (Chimerism: 0.18%, Chimerism × Timepoint: 0.03%). There are 162 genes specifically regulated under chimeric development, with continuous small differences between chimera vs. clone over development. Almost 60% of chimera-associated differential genes were differentially expressed at the 4 h aggregate stage, which corresponds to the initial transition of D. discoideum from solitary life to a multicellular phase.
A relatively small proportion of over-all variation in gene expression is explained by differences between chimeric and clonal development. The relatively small modifications in gene expression associated with chimerism is compatible with the high level of cooperation observed among different strains of D. discoideum; cells of distinct genetic backgrounds will co-aggregate indiscriminately and co-develop into fruiting bodies. Chimeric development may involve re-programming of the transcriptome through small modifications of the developmental genetic network, which may also indicate that response to social interaction involves many genes with individually small transcriptional effect.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2164-15-616) contains supplementary material, which is available to authorized users.
PMCID: PMC4118049  PMID: 25048306
Social cooperation; Chimera; Multicellularity; Transcriptome
2.  Regional modulation of a stochastically expressed factor determines photoreceptor subtypes in the Drosophila retina 
Developmental cell  2013;25(1):93-105.
Stochastic mechanisms are sometimes utilized to diversify cell fates, especially in nervous systems. In the Drosophila retina, stochastic expression of the PAS-bHLH transcription factor Spineless (Ss) controls photoreceptor subtype choice. In one randomly distributed subset of R7 photoreceptors, Ss activates Rhodopsin4 (Rh4) and represses Rhodopsin3 (Rh3); counterparts lacking Ss express Rh3 and repress Rh4. In the dorsal third region of the retina, the Iroquois Complex transcription factors induce Rh3 in Rh4-expressing R7s. Here, we show that Ss levels are controlled in a binary On/Off manner throughout the retina, yet are attenuated in the dorsal third region to allow Rh3 co-expression with Rh4. Whereas the sensitivity of rh3 repression to differences in Ss levels generates stochastic and regionalized patterns, the robustness of rh4 activation ensures its stochastic expression throughout the retina. Our findings show how stochastic and regional inputs are integrated to control photoreceptor subtype specification in the Drosophila retina.
PMCID: PMC3660048  PMID: 23597484
3.  Possible Loss of the Chloroplast Genome in the Parasitic Flowering Plant Rafflesia lagascae (Rafflesiaceae) 
Molecular Biology and Evolution  2014;31(4):793-803.
Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ∼350× sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2×) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp, ndh, pet, psa, psb, rbcL), ribosomal RNA genes (rrn16, rrn23), ribosomal protein genes (rps7, rps11, rps16), transfer RNA genes, as well as matK, accD, ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ∼33% of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50% bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches—despite success in identifying and developing a draft assembly of the much larger mitochondrial genome—suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if present is found in cryptic form at very low levels.
PMCID: PMC3969568  PMID: 24458431
holoparasite; Tetrastigma; plastid; gene loss; horizontal gene transfer; NUPTs
4.  Molecular relationships between Australian annual wild rice, Oryza meridionalis, and two related perennial forms 
Rice  2013;6(1):26.
The perennial, Oryza rufipogon distributed from Asia to Australia and the annual O. meridionalis indigenous to Australia are AA genome species in the Oryza. However, recent research has demonstrated that the Australian AA genome perennial populations have maternal genomes more closely related to those of O. meridionalis than to those found in Asian populations of O. rufipogon suggesting that the Australian perennials may represent a new distinct gene pool for rice.
Analysis of an Oryza core collection covering AA genome species from Asia to Oceania revealed that some Oceania perennials had organellar genomes closely related to that of O meridionalis (meridionalis-type). O. rufipogon accessions from New Guinea carried either the meridionalis-type or rufirpogon-type (like O. rufipogon) organellar genomes. Australian perennials carried only the meridionalis-type organellar genomes when accompanied by the rufipogon-type nuclear genome. New accessions were collected to better characterize the Australian perennials, and their life histories (annual or perennial) were confirmed by field observations. All of the material collected carried only meridionalis-type organellar genomes. However, there were two distinct perennial groups. One of them carried an rufipogon-type nuclear genome similar to the Australian O. rufipogon in the core collection and the other carried an meridionalis-type nuclear genome not represented in the existing collection. Morphologically the rufipogon-type shared similarity with Asian O. rufipogon. The meridionalis-type showed some similarities to O. meridionalis such as the short anthers usually characteristic of annual populations. However, the meridionalis-type perennial was readily distinguished from O. meridionalis by the presence of a larger lemma and higher number of spikelets.
Analysis of current accessions clearly indicated that there are two distinct types of Australian perennials. Both of them differed genetically from Asian O. rufipogon. One lineage is closely related to O. meridionalis and another to Asian O. rufipogon. The first was presumed to have evolved by divergence from O. meridionalis becoming differentiated as a perennial species in Australia indicating that it represents a new gene pool. The second, apparently derived from Asian O. rufipogon, possibly arrived in Australia later.
PMCID: PMC3874672  PMID: 24280095
Genetic divergence; Australia; Perennial; Annual; Oryza rufipogon; Oryza meridionalis
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.
PMCID: PMC3764102  PMID: 24039603
6.  Different evolutionary histories of two cation/proton exchanger gene families in plants 
BMC Plant Biology  2013;13:97.
Gene duplication events have been proposed to be involved in the adaptation of plants to stress conditions; precisely how is unclear. To address this question, we studied the evolution of two families of antiporters. Cation/proton exchangers are important for normal cell function and in plants, Na+,K+/H+ antiporters have also been implicated in salt tolerance. Two well-known plant cation/proton antiporters are NHX1 and SOS1, which perform Na+ and K+ compartmentalization into the vacuole and Na+ efflux from the cell, respectively. However, our knowledge about the evolution of NHX and SOS1 stress responsive gene families is still limited.
In this study we performed a comprehensive molecular evolutionary analysis of the NHX and SOS1 families. Using available sequences from a total of 33 plant species, we estimated gene family phylogenies and gene duplication histories, as well as examined heterogeneous selection pressure on amino acid sites. Our results show that, while the NHX family expanded and specialized, the SOS1 family remained a low copy gene family that appears to have undergone neofunctionalization during its evolutionary history. Additionally, we found that both families are under purifying selection although SOS1 is less constrained.
We propose that the different evolution histories are related with the proteins’ function and localization, and that the NHX and SOS1 families are examples of two different evolutionary paths through which duplication events may result in adaptive evolution of stress tolerance.
PMCID: PMC3726471  PMID: 23822194
7.  Longitudinal trends in climate drive flowering time clines in North American Arabidopsis thaliana 
Ecology and Evolution  2012;2(6):1162-1180.
Introduced species frequently show geographic differentiation, and when differentiation mirrors the ancestral range, it is often taken as evidence of adaptive evolution. The mouse-ear cress (Arabidopsis thaliana) was introduced to North America from Eurasia 150–200 years ago, providing an opportunity to study parallel adaptation in a genetic model organism. Here, we test for clinal variation in flowering time using 199 North American (NA) accessions of A. thaliana, and evaluate the contributions of major flowering time genes FRI, FLC, and PHYC as well as potential ecological mechanisms underlying differentiation. We find evidence for substantial within population genetic variation in quantitative traits and flowering time, and putatively adaptive longitudinal differentiation, despite low levels of variation at FRI, FLC, and PHYC and genome-wide reductions in population structure relative to Eurasian (EA) samples. The observed longitudinal cline in flowering time in North America is parallel to an EA cline, robust to the effects of population structure, and associated with geographic variation in winter precipitation and temperature. We detected major effects of FRI on quantitative traits associated with reproductive fitness, although the haplotype associated with higher fitness remains rare in North America. Collectively, our results suggest the evolution of parallel flowering time clines through novel genetic mechanisms.
PMCID: PMC3402192  PMID: 22833792
Arabidopsis; clines; ecological genomics; FRI; FLC; invasive species; parallel adaptation; PHYC
8.  Genome-Wide Patterns of Arabidopsis Gene Expression in Nature 
PLoS Genetics  2012;8(4):e1002662.
Organisms in the wild are subject to multiple, fluctuating environmental factors, and it is in complex natural environments that genetic regulatory networks actually function and evolve. We assessed genome-wide gene expression patterns in the wild in two natural accessions of the model plant Arabidopsis thaliana and examined the nature of transcriptional variation throughout its life cycle and gene expression correlations with natural environmental fluctuations. We grew plants in a natural field environment and measured genome-wide time-series gene expression from the plant shoot every three days, spanning the seedling to reproductive stages. We find that 15,352 genes were expressed in the A. thaliana shoot in the field, and accession and flowering status (vegetative versus flowering) were strong components of transcriptional variation in this plant. We identified between ∼110 and 190 time-varying gene expression clusters in the field, many of which were significantly overrepresented by genes regulated by abiotic and biotic environmental stresses. The two main principal components of vegetative shoot gene expression (PCveg) correlate to temperature and precipitation occurrence in the field. The largest PCveg axes included thermoregulatory genes while the second major PCveg was associated with precipitation and contained drought-responsive genes. By exposing A. thaliana to natural environments in an open field, we provide a framework for further understanding the genetic networks that are deployed in natural environments, and we connect plant molecular genetics in the laboratory to plant organismal ecology in the wild.
Author Summary
Plants in the real world are continuously exposed to multiple environmental signals and must respond appropriately to the dynamic conditions found in nature. Environmental signals can fluctuate during an individual's life cycle with varying degrees of predictability, and complex natural environments are where gene activity evolves. We grew two natural accessions of the model plant Arabidopsis thaliana in an open field in New York in the spring and examined genome-wide gene expression patterns in the wild. We find nearly 200 gene expression clusters in these field-grown plants, and many of these clusters were enriched in genes that had previously been shown to be associated with expression under various abiotic or biotic environmental stress conditions. Two major principal components of gene expression were associated with environmental fluctuations in temperature and rainfall, and we identified several genes (such as the thermoregulatory nucleosome occupancy gene ARP6 and the drought-sensitive hormone biosynthetic gene AAO3) that could be found in these principal components. By exploring genome-wide gene expression in plants in the wild, we were able to connect mechanistic aspects of plant molecular biology with ecological responses in nature and to begin to understand how organisms behave and adapt in their natural environments.
PMCID: PMC3330097  PMID: 22532807
9.  Levels and Patterns of Nucleotide Variation in Domestication QTL Regions on Rice Chromosome 3 Suggest Lineage-Specific Selection 
PLoS ONE  2011;6(6):e20670.
Oryza sativa or Asian cultivated rice is one of the major cereal grass species domesticated for human food use during the Neolithic. Domestication of this species from the wild grass Oryza rufipogon was accompanied by changes in several traits, including seed shattering, percent seed set, tillering, grain weight, and flowering time. Quantitative trait locus (QTL) mapping has identified three genomic regions in chromosome 3 that appear to be associated with these traits. We would like to study whether these regions show signatures of selection and whether the same genetic basis underlies the domestication of different rice varieties. Fragments of 88 genes spanning these three genomic regions were sequenced from multiple accessions of two major varietal groups in O. sativa—indica and tropical japonica—as well as the ancestral wild rice species O. rufipogon. In tropical japonica, the levels of nucleotide variation in these three QTL regions are significantly lower compared to genome-wide levels, and coalescent simulations based on a complex demographic model of rice domestication indicate that these patterns are consistent with selection. In contrast, there is no significant reduction in nucleotide diversity in the homologous regions in indica rice. These results suggest that there are differences in the genetic and selective basis for domestication between these two Asian rice varietal groups.
PMCID: PMC3108957  PMID: 21674010
10.  Variation, Sex, and Social Cooperation: Molecular Population Genetics of the Social Amoeba Dictyostelium discoideum 
PLoS Genetics  2010;6(7):e1001013.
Dictyostelium discoideum is a eukaryotic microbial model system for multicellular development, cell–cell signaling, and social behavior. Key models of social evolution require an understanding of genetic relationships between individuals across the genome or possibly at specific genes, but the nature of variation within D. discoideum is largely unknown. We re-sequenced 137 gene fragments in wild North American strains of D. discoideum and examined the levels and patterns of nucleotide variation in this social microbial species. We observe surprisingly low levels of nucleotide variation in D. discoideum across these strains, with a mean nucleotide diversity (π) of 0.08%, and no strong population stratification among North American strains. We also do not find any clear relationship between nucleotide divergence between strains and levels of social dominance and kin discrimination. Kin discrimination experiments, however, show that strains collected from the same location show greater ability to distinguish self from non-self than do strains from different geographic areas. This suggests that a greater ability to recognize self versus non-self may arise among strains that are more likely to encounter each other in nature, which would lead to preferential formation of fruiting bodies with clonemates and may prevent the evolution of cheating behaviors within D. discoideum populations. Finally, despite the fact that sex has rarely been observed in this species, we document a rapid decay of linkage disequilibrium between SNPs, the presence of recombinant genotypes among natural strains, and high estimates of the population recombination parameter ρ. The SNP data indicate that recombination is widespread within D. discoideum and that sex as a form of social interaction is likely to be an important aspect of the life cycle.
Author Summary
Theories on the evolution of cooperation sometimes hinge on knowledge of genetic relatedness between individuals. Dictyostelium discoideum has been a model for the study of key biological phenomena, including the evolution and ecology of social cooperation, but the nature of genetic variation within this species is largely unknown. We determine the levels and patterns of molecular variation in this social species. We find a preference of genetically identical cells to cooperate with each other in forming fruiting bodies, a phenomenon known as kin discrimination. Kin discrimination, however, does not appear to be correlated with overall DNA divergence of the strains. Instead, familiarity appears to breed contempt, as strains from the same geographic location (which possibly encounter each other) show higher levels of kin discrimination than strains found further apart. We also show that sex, which is rarely observed in the laboratory, appears to be widespread in the wild—an interesting finding given that sex in D. discoideum is also associated with cooperation between numerous single cells to feed the developing cannibalistic zygote. The finding that sex may occur more frequently in the wild opens the possibility of conducting controlled laboratory matings and developing D. discoideum as a genetic model system.
PMCID: PMC2895654  PMID: 20617172
11.  A Multiparent Advanced Generation Inter-Cross to Fine-Map Quantitative Traits in Arabidopsis thaliana 
PLoS Genetics  2009;5(7):e1000551.
Identifying natural allelic variation that underlies quantitative trait variation remains a fundamental problem in genetics. Most studies have employed either simple synthetic populations with restricted allelic variation or performed association mapping on a sample of naturally occurring haplotypes. Both of these approaches have some limitations, therefore alternative resources for the genetic dissection of complex traits continue to be sought. Here we describe one such alternative, the Multiparent Advanced Generation Inter-Cross (MAGIC). This approach is expected to improve the precision with which QTL can be mapped, improving the outlook for QTL cloning. Here, we present the first panel of MAGIC lines developed: a set of 527 recombinant inbred lines (RILs) descended from a heterogeneous stock of 19 intermated accessions of the plant Arabidopsis thaliana. These lines and the 19 founders were genotyped with 1,260 single nucleotide polymorphisms and phenotyped for development-related traits. Analytical methods were developed to fine-map quantitative trait loci (QTL) in the MAGIC lines by reconstructing the genome of each line as a mosaic of the founders. We show by simulation that QTL explaining 10% of the phenotypic variance will be detected in most situations with an average mapping error of about 300 kb, and that if the number of lines were doubled the mapping error would be under 200 kb. We also show how the power to detect a QTL and the mapping accuracy vary, depending on QTL location. We demonstrate the utility of this new mapping population by mapping several known QTL with high precision and by finding novel QTL for germination data and bolting time. Our results provide strong support for similar ongoing efforts to produce MAGIC lines in other organisms.
Author Summary
Most traits of economic and evolutionary interest vary quantitatively and have multiple genes affecting their expression. Dissecting the genetic basis of such traits is crucial for the improvement of crops and management of diseases. Here, we develop a new resource to identify genes underlying such quantitative traits in Arabidopsis thaliana, a genetic model organism in plants. We show that using a large population of inbred lines derived from intercrossing 19 parents, we can localize the genes underlying quantitative traits better than with existing methods. Using these lines, we were able to replicate the identification of previously known genes that affect developmental traits in A. thaliana and identify some new ones. This paper also presents all the necessary biological and computational material necessary for the scientific community to use these lines in their own research. Our results suggest that the use of lines derived from a multiparent advanced generation inter-cross (MAGIC lines) should be very useful in other organisms.
PMCID: PMC2700969  PMID: 19593375
12.  Genome-Wide Patterns of Nucleotide Polymorphism in Domesticated Rice 
PLoS Genetics  2007;3(9):e163.
Domesticated Asian rice (Oryza sativa) is one of the oldest domesticated crop species in the world, having fed more people than any other plant in human history. We report the patterns of DNA sequence variation in rice and its wild ancestor, O. rufipogon, across 111 randomly chosen gene fragments, and use these to infer the evolutionary dynamics that led to the origins of rice. There is a genome-wide excess of high-frequency derived single nucleotide polymorphisms (SNPs) in O. sativa varieties, a pattern that has not been reported for other crop species. We developed several alternative models to explain contemporary patterns of polymorphisms in rice, including a (i) selectively neutral population bottleneck model, (ii) bottleneck plus migration model, (iii) multiple selective sweeps model, and (iv) bottleneck plus selective sweeps model. We find that a simple bottleneck model, which has been the dominant demographic model for domesticated species, cannot explain the derived nucleotide polymorphism site frequency spectrum in rice. Instead, a bottleneck model that incorporates selective sweeps, or a more complex demographic model that includes subdivision and gene flow, are more plausible explanations for patterns of variation in domesticated rice varieties. If selective sweeps are indeed the explanation for the observed nucleotide data of domesticated rice, it suggests that strong selection can leave its imprint on genome-wide polymorphism patterns, contrary to expectations that selection results only in a local signature of variation.
Author Summary
Domesticated Asian rice is one of the oldest and most important crops in the world. Two main rice evolutionary lineages have been identified, and are thought to have been independently domesticated in Asia. We have examined patterns of DNA sequence variation in the genomes of rice and its wild ancestor to make inferences about the origin of domesticated rice. Population bottlenecks (a reduction in the size of the founding population) in the evolutionary transition from wild to cultivated species has long been thought to be the dominant force shaping patterns of molecular evolution during domestication. We find that the nucleotide variation patterns in rice are inconsistent with a simple bottleneck model. Rice genetic variation, however, can be explained by either a model that incorporates both a bottleneck and migration among rice variety groups, or a model that incorporates a bottleneck and multiple rounds of artificial selection on rice. Selection by humans is believed to have played an important role during crop domestication, and these results may suggest that strong, recurrent selection can leave a signal that can be observed throughout the genomes of domesticated species.
PMCID: PMC1994709  PMID: 17907810
13.  Genomic Variation in Rice: Genesis of Highly Polymorphic Linkage Blocks during Domestication 
PLoS Genetics  2006;2(11):e199.
Genomic regions that are unusually divergent between closely related species or racial groups can be particularly informative about the process of speciation or the operation of natural selection. The two sequenced genomes of cultivated Asian rice, Oryza sativa, reveal that at least 6% of the genomes are unusually divergent. Sequencing of ten unlinked loci from the highly divergent regions consistently identified two highly divergent haplotypes with each locus in nearly complete linkage disequilibrium among 25 O. sativa cultivars and 35 lines from six wild species. The existence of two highly divergent haplotypes in high divergence regions in species from all geographical areas (Africa, Asia, and Oceania) was in contrast to the low polymorphism and low linkage disequilibrium that were observed in other parts of the genome, represented by ten reference loci. While several natural processes are likely to contribute to this pattern of genomic variation, domestication may have greatly exaggerated the trend. In this hypothesis, divergent haplotypes that were adapted to different geographical and ecological environments migrated along with humans during the development of domesticated varieties. If true, these high divergence regions of the genome would be enriched for loci that contribute to the enormous range of phenotypic variation observed among domesticated breeds.
The coexistence of high and low divergence regions in the genomes of two incipient species can be informative about the process of speciation. For example, it may indicate a long period of continual gene flow during species formation. In the conventional view of speciation by geographical separation, there is little intermingling in the process, and the level of divergence should be relatively uniform across the genome. Domesticated plants and animals are excellent materials for studying speciation because the process of domestication may often exaggerate the forces that drive speciation. These forces include selection (artificial rather than natural) and admixture among diverging varieties mediated by humans. In this study, the authors analyzed the whole genome sequences between the two subspecies of domesticated rice. These subspecies have developed partial reproductive isolation. By studying the entire genomic patterns, as well as the detailed population genetics of 20 loci among 60 lines of cultivars and wild rice, the authors observed regions of unusually high divergence, which occupy more than 6% of the whole genome. Hence, the formation of domesticated rice resembles a process in which previously divergent populations/races were brought together, sorted, and re-assembled. How much this process may echo the formation of species in nature is discussed.
PMCID: PMC1636696  PMID: 17112320
14.  Molecular Population Genetics and Phenotypic Diversification of Two Populations of the Thermophilic Cyanobacterium Mastigocladus laminosus 
We investigated the distributions of genetic and phenotypic variation for two Yellowstone National Park populations of the heterocyst-forming cyanobacterium Mastigocladus (Fischerella) laminosus that exhibit dramatic phenotypic differences as a result of environmental differences in nitrogen availability. One population develops heterocysts and fixes nitrogen in situ in response to a deficiency of combined nitrogen in its environment, whereas the other population does neither due to the availability of a preferred nitrogen source. Slowly evolving molecular markers, including the 16S rRNA gene and the downstream internal transcribed spacer, are identical among all laboratory isolates from both populations but belie considerable genetic and phenotypic diversity. The total nucleotide diversity at six nitrogen metabolism loci was roughly three times greater than that observed for the human global population. The two populations are genetically differentiated, although variation in performance on different nitrogen sources among genotypes could not be explained by local adaptation to available nitrogen in the respective environments. Population genetic models suggest that local adaptation is mutation limited but also that the populations are expected to continue to diverge due to low migratory gene flow.
PMCID: PMC1449082  PMID: 16597984
15.  Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS 
Nature Communications  2014;5:3651.
The onset of flowering, the change from vegetative to reproductive development, is a major life history transition in flowering plants. Recent work suggests that mutations in cis-regulatory mutations should play critical roles in the evolution of this (as well as other) important adaptive traits, but thus far there has been little evidence that directly links regulatory mutations to evolutionary change at the species level. While several genes have previously been shown to affect natural variation in flowering time in Arabidopsis thaliana, most either show protein-coding changes and/or are found at low frequency (<5%). Here we identify and characterize natural variation in the cis-regulatory sequence in the transcription factor CONSTANS that underlies flowering time diversity in Arabidopsis. Mutation in this regulatory motif evolved recently and has spread to high frequency in Arabidopsis natural accessions, suggesting a role for these cis-regulatory changes in adaptive variation of flowering time.
The transcription factor CONSTANS regulates the timing of flowering in Arabidopsis. Rosas et al. report that genetic variation in the cis-regulatory regions of this gene contributes to natural phenotypic variation in flowering time.
PMCID: PMC3997802  PMID: 24736505

Results 1-15 (15)