The transition to self-compatibility in Arabidopsis thaliana and evolution within S-haplotypes over 10 Myr

A recent investigation found evidence that the transition of Arabidopsis thaliana from ancestral self-incompatibility (SI) to full self-compatibility occurred very recently and suggested that this occurred through a selective fixation of a nonfunctional allele (PsiSCR1) at the SCR gene, which determines pollen specificity in the incompatibility response. The main evidence is the lack of polymorphism at the SCR locus in A. thaliana. However, the nearby SRK gene, which determines stigma specificity in self-incompatible Brassicaceae species, has extremely high sequence diversity, with 3 very divergent SRK haplotypes, 2 of them present in multiple strains. Such high diversity is extremely unusual in this species, and it suggests the possibility that multiple, different SRK haplotypes may have been preserved from A. thaliana's self-incompatible ancestor. To study the evolution of S-haplotypes in the A. thaliana lineage, we searched the 2 most closely related Arabidopsis species Arabidopsis lyrata and Arabidopsis halleri, in which most populations have retained SI, and found SRK sequences corresponding to all 3 A. thaliana haplogroup sequences. Our molecular evolutionary analyses of these 3 S-haplotypes provide an independent estimate of the timing of the breakdown of SI and again exclude an ancient transition to selfing in A. thaliana. Comparing sequences of each of the 3 haplogroups between species, we find that 2 of the 3 SRK sequences (haplogroups A and B) are similar throughout their length, suggesting that little or no recombination with other SRK alleles has occurred since these species diverged. The diversity difference between the SCR and SRK loci in A. thaliana, however, suggests crossing-over, either within SRK or between the SCR and SRK loci. If the loss of SI involved fixation of the PsiSCR1 sequence, the exchange must have occurred during its fixation. Divergence between the species is much lower at the S-locus, compared with reference loci, and we discuss two contributory possibilities. Introgression may have occurred between A. lyrata and A. halleri and between their ancestral lineage and A. thaliana, at least for some period after their split. In addition, the coalescence times of sequences of individual S-haplogroups are expected to be less than those of alleles at non-S-loci.     

The glucosinolate-myrosinase system in an ecological and evolutionary context

Functional analysis of natural variation in the model species Arabidopsis thaliana has enabled the cloning of many glucosinolate biosynthesis and hydrolysis genes. Variation in these genes is central to understanding the ecological role of the glucosinolate-myrosinase defense system, and allows us to dissect the evolutionary and ecological forces that shape polymorphism at underlying loci. These same genes are also variable in other crucifer species, suggesting the presence of recurring selection, possibly mediated by insects. By utilizing the genomic tools available in A. thaliana to investigate these loci fully, it might be possible to generate detailed evolutionary or ecological models to apply to other species.     

Evolution of microsatellites in Arabis petraea and Arabis lyrata, outcrossing relatives of Arabidopsis thaliana

We examined microsatellite variation in two diploid, outcrossing relatives of Arabidopsis thaliana, Arabis petraea and Arabis lyrata. The primer sequences were derived from A. thaliana. About 50% (14 loci) of the A. thaliana primers could successfully amplify microsatellites in the related species. Analysis of microsatellite structure in the related species showed that there had been large changes in the microsatellites: there were large differences in repeat numbers and many of the A. thaliana simple repeats were shorter in the related species. For the loci we compared, the related species had a much lower level of variability at the microsatellites than Japanese wild populations of A. thaliana. This is presumably related to the different microsatellite structures, because allozyme data showed that the outcrossing relatives were highly polymorphic compared to other outcrossing herbaceous species. Use of microsatellites in assessing variability or phylogenetic relationships between different species requires caution, because changes in microsatellite structure may alter evolutionary rates.      

Multilocus analysis of variation using a large empirical data set: phenylpropanoid pathway genes in Arabidopsis thaliana

Detecting the signature of adaptation on nucleotide variation is often difficult in species that like Arabidopsis thaliana might have a complex demographic history. Recent re-sequencing surveys in this species provided genome-wide information that would mainly reflect its demographic history. We have used a large empirical data set (LED) as well as multilocus coalescent simulations to analyse sequence variation at loci involved in the phenylpropanoid pathway of this species. We surveyed and examined DNA sequence variation at nine of these loci (about 19.7 kb) in 23 accessions of A. thaliana and one accession of its closely related species Arabidopsis lyrata . Nucleotide variation was lower at nonsynonymous sites than at silent sites in all loci, indicating generalized functional constraint at the protein level. No association between variation and position in the metabolic pathway was detected. When the data were contrasted against the standard neutral model, significant deviations for silent variation were detected with Tajima's D , Fu's F_S and Fay and Wu's H multilocus test statistics. These deviations were in the same direction than in previous large-scale multilocus analyses, suggesting a genome-wide effect. When the nine-locus data set was contrasted against the large empirical data set, the level (Watterson's θ) and pattern of variation (Tajima's D ) detected in these loci did not deviate either at the single-locus or multilocus level from the corresponding empirical distributions. These results would support an important role of the demographic history of A. thaliana in shaping nucleotide variation at the nine studied phenylpropanoid loci. The potential and limitations of the empirical distribution approach are discussed.     

A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers

A coalescent-based method was used to investigate the origins of the allotetraploid Arabidopsis suecica, using 52 nuclear microsatellite loci typed in eight individuals of A. suecica and 14 individuals of its maternal parent Arabidopsis thaliana, and four short fragments of genomic DNA sequenced in a sample of four individuals of A. suecica and in both its parental species A. thaliana and Arabidopsis arenosa. All loci were variable in A. thaliana but only 24 of the 52 microsatellite loci and none of the four sequence fragments were variable in A. suecica. We explore a number of possible evolutionary scenarios for A. suecica and conclude that it is likely that A. suecica has a recent, unique origin between 12,000 and 300,000 years ago. The time estimates depend strongly on what is assumed about population growth and rates of mutation. When combined with what is known about the history of glaciations, our results suggest that A. suecica originated south of its present distribution in Sweden and Finland and then migrated north, perhaps in the wake of the retreating ice.     

Duplication of centromeric histone H3 (HTR12) gene in Arabidopsis halleri and A. lyrata, plant species with multiple centromeric satellite sequences

Arabidopsis halleri and lyrata have three different major centromeric satellite sequences, a unique finding for a diploid Arabidopsis species. Since centromeric histones coevolve with centromeric satellites, these proteins would be predicted to show signs of selection when new centromere satellites have recently arisen. We isolated centromeric protein genes from A. halleri and lyrata and found that one of them, HTR12 (CENP-A), is duplicated, while CENP-C is not. Phylogenetic analysis indicates that the HTR12 duplication occurred after these species diverged from A. thaliana. Genetic mapping shows that HTR12 copy B has the same genomic location as the A. thaliana gene; the other copy (A, at the other end of the same chromosome) is probably the new copy. To test for selection since the duplication, we surveyed diversity at both HTR12 loci within A. lyrata. Overall, there is no strong evidence for an "evolutionary arms race" causing multiple replacement substitutions. The A. lyrata HTR12B sequences fall into three classes of haplotypes, apparently maintained for a long time, but they all encode the same amino acid sequence. In contrast, HTR12A has low diversity, but many variants are amino acid replacements, possibly due to independent selective sweeps within populations of the species.     

Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep

Morphological diversity is often caused by altered gene expression of key developmental regulators. However, the precise developmental trajectories through which morphologies evolved remain poorly understood. It is also unclear to what degree genetic changes contributing to morphological divergence were fixed by natural selection. Here we investigate these problems in the context of evolutionary developmental transitions that produced the simple unlobed leaf of the model species Arabidopsis thaliana. We demonstrate that A. thaliana leaf shape likely derived from a more complex lobed ancestral state that persists in extant Arabidopsis species. We also show that evolution of the unlobed leaf form in A. thaliana involved loss of expression of the knotted1-like homeobox gene SHOOTMERISTEMLESS (STM) in leaves and that cis-regulatory divergence contributed to this process. Further, we provide evidence for a selective sweep at the A. thaliana STM locus, indicating that loss of STM expression in A. thaliana leaves may have been fixed by positive selection. In summary, our data provide key information as to when and how the characteristic leaf form of A. thaliana evolved.     

Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history

Duplicated genes are important in the evolution and ecology of plant-defences because herbivore and pathogen attack can be countered via functional diversification at two levels: among duplicated loci and within loci. We explore molecular sequence variation for two members of a defence-related gene family, Arabidopsis thaliana trypsin inhibitors (ATTI), in A. thaliana and a closely related species, A. lyrata subspp. petraea. A worldwide sample of the inbreeding annual A. thaliana had less genetic variation at two ATTI loci (piTOTAL 相似文献   

Cross-species microsatellite markers for elucidating population genetic structure in Arabidopsis and Arabis (Brassicaeae)

Species closely related to model organisms present the opportunity to efficiently apply molecular and functional tools developed by a large research community to taxa with different ecological and evolutionary histories. We complied 42 microsatellite loci that amplify under common conditions in four closely related Arabidopsis: A. thaliana; A. halleri; A. lyrata ssp. lyrata; and A. lyrata ssp. petraea, as well as in one more distantly related crucifer; Arabis drummondii. Variation at these loci is amenable to a diversity of applications including population genetics, phylogeographical analyses, mapping of inter and intraspecific crosses, and recombination mapping. Our analysis of microsatellite variation illustrates significant differences in population genetic parameters among three Arabidopsis species. A population of A. thaliana, an inbreeding annual plant associated with disturbed habitats, was highly monomorphic (P = 8% percent polymorphic loci) and only 0.2% heterozygous for 648 locus-by-individual combinations. A population of the self-incompatible perennial herb, A. halleri, was more genetically variable (P = 71%) and had an excess of heterozygosity that may reflect a recent population bottleneck associated with human-mediated founder events. A population of the self-incompatible perennial herb, A. lyrata ssp. petraea, was even more genetically variable (P = 86%) and appeared to be at mutation-drift equilibrium. Population structure estimated from neutrally evolving loci provides an empirical expectation against which hypotheses of adaptive evolution at functional loci can be tested.     

Hybrid incompatibility in Arabidopsis is determined by a multiple-locus genetic network

The cross between Arabidopsis thaliana and the closely related species Arabidopsis arenosa results in postzygotic hybrid incompatibility, manifested as seed death. Ecotypes of A. thaliana were tested for their ability to produce live seed when crossed to A. arenosa. The identified genetic variation was used to map quantitative trait loci (QTLs) encoded by the A. thaliana genome that affect the frequency of postzygotic lethality and the phenotypes of surviving seeds. Seven QTLs affecting the A. thaliana component of this hybrid incompatibility were identified by crossing a Columbia × C24 recombinant inbred line population to diploid A. arenosa pollen donors. Additional epistatic loci were identified based on their pairwise interaction with one or several of these QTLs. Epistatic interactions were detected for all seven QTLs. The two largest additive QTLs were subjected to fine-mapping, indicating the action of at least two genes in each. The topology of this network reveals a large set of minor-effect loci from the maternal genome controlling hybrid growth and viability at different developmental stages. Our study establishes a framework that will enable the identification and characterization of genes and pathways in A. thaliana responsible for hybrid lethality in the A. thaliana × A. arenosa interspecific cross.     

Selection on rapidly evolving proteins in the Arabidopsis genome

Genes that have undergone positive or diversifying selection are likely to be associated with adaptive divergence between species. One indicator of adaptive selection at the molecular level is an excess of amino acid replacement fixed differences per replacement site relative to the number of synonymous fixed differences per synonymous site (omega = K(a)/K(s)). We used an evolutionary expressed sequence tag (EST) approach to estimate the distribution of omega among 304 orthologous loci between Arabidopsis thaliana and A. lyrata to identify genes potentially involved in the adaptive divergence between these two Brassicaceae species. We find that 14 of 304 genes (approximately 5%) have an estimated omega > 1 and are candidates for genes with increased selection intensities. Molecular population genetic analyses of 6 of these rapidly evolving protein loci indicate that, despite their high levels of between-species nonsynonymous divergence, these genes do not have elevated levels of intraspecific replacement polymorphisms compared to previously studied genes. A hierarchical Bayesian analysis of protein-coding region evolution within and between species also indicates that the selection intensities of these genes are elevated compared to previously studied A. thaliana nuclear loci.     

Using Arabidopsis to explore zinc tolerance and hyperaccumulation

Identifying the particular gene or genes underlying a specific adaptation is a major challenge in modern biology. Currently, the study of naturally occurring variation in Arabidopsis thaliana provides a bridge between functional genetics and evolutionary analyses. Nevertheless, the use of A. thaliana to study adaptation is limited to those traits that have undergone selection. Therefore, to understand fully the genetics of adaptation, the vast arsenal of genetic resources developed in A. thaliana must be extended to other species that display traits absent in this model species. Here, we discuss how A. thaliana resources can significantly enhance the study of heavy-metal tolerance and hyperaccumulation in the wild species Arabidopsis halleri.     

Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae)

We analyzed sequence variation for chalcone synthase (CHS:) and alcohol dehydrogenase (ADH:) loci in 28 species in the genera ARABIDOPSIS: and ARABIS: and related taxa from tribe Arabideae. CHS: was single-copy in nearly all taxa examined, while ADH: duplications were found in several species. Phylogenies constructed from both loci confirmed that the closest relatives of Arabidopsis thaliana include Arabidopsis lyrata, Arabidopsis petraea, and Arabidopsis halleri (formerly in the genus CARDAMINOPSIS:). Slightly more distant are the North American n = 7 Arabis (BOECHERA:) species. The genus ARABIS: is polyphyletic-some unrelated species appear within this taxonomic classification, which has little phylogenetic meaning. Fossil pollen data were used to compute a synonymous substitution rate of 1.5 x 10 substitutions per site per year for both CHS: and Adh. Arabidopsis thaliana diverged from its nearest relatives about 5 MYA, and from Brassica roughly 24 MYA. Independent molecular and fossil data from several sources all provide similar estimates of evolutionary timescale in the Brassicaceae.     

Comparison of a Brassica oleracea genetic map with the genome of Arabidopsis thaliana

Brassica oleracea is closely related to the model plant, Arabidopsis thaliana. Despite this relationship, it has been difficult to both identify the most closely related segments between the genomes and determine the degree of genome replication within B. oleracea relative to A. thaliana. These difficulties have arisen in part because both species have replicated genomes, and the criteria used to identify orthologous regions between the genomes are often ambiguous. In this report, we compare the positions of sequenced Brassica loci with a known position on a B. oleracea genetic map to the positions of their putative orthologs within the A. thaliana genome. We use explicit criteria to distinguish orthologous from paralogous loci. In addition, we develop a conservative algorithm to identify collinear loci between the genomes and a permutation test to evaluate the significance of these regions. The algorithm identified 34 significant A. thaliana regions that are collinear with >28% of the B. oleracea genetic map. These regions have a mean of 3.3 markers spanning 2.1 Mbp of the A. thaliana genome and 2.5 cM of the B. oleracea genetic map. Our findings are consistent with the hypothesis that the B. oleracea genome has been highly rearranged since divergence from A. thaliana, likely as a result of polyploidization.     

Comparative genomics in the Brassicaceae: a family-wide perspective

Comparative genomics of Arabidopsis relatives has great potential to improve our understanding of molecular function and evolutionary processes. Recent studies of phylogenetic relationships within Brassicaceae and the publication of a new tribal classification scheme provide an important framework for comparative genomics research. Comparative linkage mapping and chromosome painting in the close relatives of Arabidopsis have inferred an ancestral karyotype of these species. In addition, comparative mapping to Brassica has identified genomic blocks that have been maintained since the divergence of the Arabidopsis and Brassica lineages. Several analyses of conserved non-coding regions have identified putative cis-regulatory sequences, and have highlighted the need for comparative sequencing at greater evolutionary distances. The development of new model species with novel physiological and ecological traits allows analysis of phenotypes that are not available in A. thaliana. Looking towards the future, we suggest a prioritized research agenda for comparative genomics in the Brassicaceae.     

Partial shotgun sequencing of the Boechera stricta genome reveals extensive microsynteny and promoter conservation with Arabidopsis

Comparative genomics provides insight into the evolutionary dynamics that shape discrete sequences as well as whole genomes. To advance comparative genomics within the Brassicaceae, we have end sequenced 23,136 medium-sized insert clones from Boechera stricta, a wild relative of Arabidopsis (Arabidopsis thaliana). A significant proportion of these sequences, 18,797, are nonredundant and display highly significant similarity (BLASTn e-value < or = 10(-30)) to low copy number Arabidopsis genomic regions, including more than 9,000 annotated coding sequences. We have used this dataset to identify orthologous gene pairs in the two species and to perform a global comparison of DNA regions 5' to annotated coding regions. On average, the 500 nucleotides upstream to coding sequences display 71.4% identity between the two species. In a similar analysis, 61.4% identity was observed between 5' noncoding sequences of Brassica oleracea and Arabidopsis, indicating that regulatory regions are not as diverged among these lineages as previously anticipated. By mapping the B. stricta end sequences onto the Arabidopsis genome, we have identified nearly 2,000 conserved blocks of microsynteny (bracketing 26% of the Arabidopsis genome). A comparison of fully sequenced B. stricta inserts to their homologous Arabidopsis genomic regions indicates that indel polymorphisms >5 kb contribute substantially to the genome size difference observed between the two species. Further, we demonstrate that microsynteny inferred from end-sequence data can be applied to the rapid identification and cloning of genomic regions of interest from nonmodel species. These results suggest that among diploid relatives of Arabidopsis, small- to medium-scale shotgun sequencing approaches can provide rapid and cost-effective benefits to evolutionary and/or functional comparative genomic frameworks.     

Comparative evolution history of SINEs in Arabidopsis thaliana and Brassica oleracea: evidence for a high rate of SINE loss

Brassica oleracea and Arabidopsis thaliana belong to the Brassicaceae(Cruciferae) family and diverged 16 to 19 million years ago. Although the genome size of B. oleracea (approximately 600 million base pairs) is more than four times that of A. thaliana (approximately 130 million base pairs), their gene content is believed to be very similar with more than 85% sequence identity in the coding region. Therefore, this important difference in genome size is likely to reflect a different rate of non-coding DNA accumulation. Transposable elements (TEs) constitute a major fraction of non-coding DNA in plant species. A different rate in TE accumulation between two closely related species can result in significant genome size variations in a short evolutionary period. Short interspersed elements (SINEs) are non-autonomous retroposons that have invaded the genome of most eukaryote species. Several SINE families are present in B. oleracea and A. thaliana and we found that two of them (called RathE1 and RathE2) are present in both species. In this study, the tempo of evolution of RathE1 and RathE2 SINE families in both species was compared. We observed that most B. oleracea RathE2 SINEs are "young" (close to the consensus sequence) and abundant while elements from this family are more degenerated and much less abundant in A. thaliana. However, the situation is different for the RathE1 SINE family for which the youngest elements are found in A. thaliana. Surprisingly, no SINE was found to occupy the same (orthologous) genomic locus in both species suggesting that either these SINE families were not amplified at a significant rate in the common ancestor of the two species or that older elements were lost and only the recent (lineage-specific) insertions remain. To test this latter hypothesis, loci containing a recently inserted SINE in the A. thaliana col-0 ecotype were selected and characterized in several other A. thaliana ecotypes. In addition to the expected SINE containing allele and the pre-integrative allele (i.e. the "empty" allele), we observed in the different ecotypes, alleles with truncated portions of the SINE (up to the complete loss of the element) and of the immediate genomic flanking sequences. The absence of SINEs in orthologous positions between B. oleracea and A. thaliana and the presence in recently diverged A. thaliana ecotypes of alleles containing severely truncated SINEs suggest a very high rate of SINE loss in these species.     

Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe

Arabidopsis thaliana provides a useful model system for functional, evolutionary and ecological studies in plant biology. We have analysed natural genetic variation in A. thaliana in order to infer its biogeographical and historical distribution across Eurasia. We analysed 79 amplified fragment length polymorphism (AFLP) markers in 142 accessions from the species' native range, and found highly significant genetic isolation by distance among A. thaliana accessions from Eurasia and southern Europe. These spatial patterns of genetic variation suggest that A. thaliana colonized central and northern Europe from Asia and from Mediterranean Pleistocene refugia, a trend which has been identified in other species. Statistically significant levels of multilocus linkage disequilibrium suggest intermediate levels of disequilibrium among subsets of loci, and analysis of genetic relationships among accessions reveal a star or bush-like dendrogram with low bootstrap support. Taken together, it appears that there has been sufficient historical recombination in the A. thaliana genome such that accessions do not conform to a tree-like, bifurcating pattern of evolution - there is no 'ecotype phylogeny.' Nonetheless, significant isolation by distance provides a framework upon which studies of natural variation in A. thaliana may be designed and interpreted.