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Michael D Purugganan

Publications and source records attributed to Michael D Purugganan.

At least 19 recordsLinked to original sources

Genomic variation in rice: genesis of highly polymorphic linkage blocks during domestication.

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.

Agriculture↗

Evolutionary patterns in the antR-Cor gene in the dwarf dogwood complex (Cornus, Cornaceae).

The evolutionary pattern of the myc-like anthocyanin regulatory gene antR-Cor was examined in the dwarf dogwood species complex (Cornus Subgenus Arctocrania) that contains two diploid species (C. canadensis and C. suecica), their putative hybrids with intermediate phenotypes, and a tetraploid derivative (C. unalaschkensis). Full-length sequences of this gene ( approximately 4 kb) were sequenced and characterized for 47 dwarf dogwood samples representing all taxa categories from 43 sites in the Pacific Northwest. Analysis of nucleotide diversity indicated departures from neutral evolution, due most likely to local population structure. Neighbor-joining and haplotype network analyses show that sequences from the tetraploid and diploid intermediates are much more strongly diverged from C. suecica than from C. canadensis, and that the intermediate phenotypes may represent an ancestral group to C. canadensis rather than interspecific hybrids. Seven amino acid mutations that are potentially linked to myc-like anthocyanin regulatory gene function correlate with petal colors differences that characterize the divergence between two diploid species and the tetraploid species in this complex. The evidence provides a working hypothesis for testing the role of the gene in speciation and its link to the petal coloration. Sequencing and analysis of additional nuclear genes will be necessary to resolve questions about the evolution of the dwarf dogwood complex.

Alaska↗

Selection under domestication: evidence for a sweep in the rice waxy genomic region.

Rice (Oryza sativa) was cultivated by Asian Neolithic farmers >11,000 years ago, and different cultures have selected for divergent starch qualities in the rice grain during and after the domestication process. An intron 1 splice donor site mutation of the Waxy gene is responsible for the absence of amylose in glutinous rice varieties. This mutation appears to have also played an important role in the origin of low amylose, nonglutinous temperate japonica rice varieties, which form a primary component of Northeast Asian cuisines. Waxy DNA sequence analyses indicate that the splice donor mutation is prevalent in temperate japonica rice varieties, but rare or absent in tropical japonica, indica, aus, and aromatic varieties. Sequence analysis across a 500-kb genomic region centered on Waxy reveals patterns consistent with a selective sweep in the temperate japonicas associated with the mutation. The size of the selective sweep (>250 kb) indicates very strong selection in this region, with an inferred selection coefficient that is higher than similar estimates from maize domestication genes or wild species. These findings demonstrate that selection pressures associated with crop domestication regimes can exceed by one to two orders of magnitude those observed for genes under even strong selection in natural systems.

Agriculture↗

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.

Cyanobacteria↗

High-diversity genes in the Arabidopsis genome.

High-diversity genes represent an important class of loci in organismal genomes. Since elevated levels of nucleotide variation are a key component of the molecular signature for balancing selection or local adaptation, high-diversity genes may represent loci whose alleles are selectively maintained as balanced polymorphisms. Comparison of 4300 random shotgun sequence fragments of the Arabidopsis thaliana Ler ecotype genome with the whole genomic sequence of the Col-0 ecotype identified 60 genes with putatively high levels of intraspecific variability. Eleven of these genes were sequenced in multiple A. thaliana accessions, 3 of which were found to display elevated levels of nucleotide polymorphism. These genes encode the myb-like transcription factor MYB103, a putative soluble starch synthase I, and a homeodomain-leucine zipper transcription factor. Analysis of these genes and 4-7 flanking genes in 14-20 A. thaliana ecotypes revealed that two of these loci show other characteristics of balanced polymorphisms, including broad peaks of nucleotide diversity spanning multiple linked genes and an excess of intermediate-frequency polymorphisms. Scanning genomes for high-diversity genomic regions may be useful in approaches to adaptive trait locus mapping for uncovering candidate balanced polymorphisms.

Alleles↗

The evolutionary dynamics of plant duplicate genes.

Given the prevalence of duplicate genes and genomes in plant species, the study of their evolutionary dynamics has been a focus of study in plant evolutionary genetics over the past two decades. The past few years have been a particularly exciting time because recent theoretical and experimental investigations have led to a rethinking of the classic paradigm of duplicate gene evolution. By combining recent advances in genomic analysis with a new conceptual framework, researchers are determining the contributions of single-gene and whole-genome duplications to the diversification of plant species. This research provides insights into the roles that gene and genome duplications play in plant evolution.

Evolution, Molecular↗

RETRACTED: Darwinian selection on a selfing locus.

The shift to self-pollination is one of the most prevalent evolutionary transitions in flowering plants. In the selfing plant Arabidopsis thaliana, pseudogenes at the SCR and SRK self-incompatibility loci are believed to underlie the evolution of self-fertilization. Positive directional selection has driven the evolutionary fixation of pseudogene alleles of SCR, leading to substantially reduced nucleotide variation. Coalescent simulations indicate that this adaptive event may have occurred very recently and is possibly associated with the post-Pleistocene expansion of A. thaliana from glacial refugia. This suggests that ancillary morphological innovations associated with self-pollination can evolve rapidly after the inactivation of the self-incompatibility response.

Alleles↗

Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait.

Epistatic gene interactions are believed to be a major factor in the genetic architecture of evolutionary diversification. In Arabidopsis thaliana, the FRI and FLC genes mechanistically interact to control flowering time, and here we show that this epistatic interaction also contributes to a latitudinal cline in this life history trait within the species. Two major FLC haplogroups (FLC(A) and FLC(B)) are associated with flowering time variation in A. thaliana in field conditions, but only in the presence of putatively functional FRI alleles. Significant differences in latitudinal distribution of FLC haplogroups in Eurasia and North Africa also depend on the FRI genotype. There is significant linkage disequilibrium between FRI and FLC despite their location on separate chromosomes. Although no nonsynonymous polymorphisms differentiate FLC(A) and FLC(B), vernalization induces the expression of an alternatively spliced FLC transcript that encodes a variant protein with a radical amino acid replacement associated with the two FLC haplogroups. Numerous polymorphisms differentiating the FLC haplogroups also occur in intronic regions implicated in the regulation of FLC expression. The features of the regulatory gene interaction between FRI and FLC in contributing to the latitudinal cline in A. thaliana flowering time are consistent with the maintenance of this interaction by epistatic selection. These results suggest that developmental genetic pathways and networks provide the molecular basis for epistasis, contributing to ecologically important phenotypic variation in natural populations and to the process of evolutionary diversification.

Alternative Splicing↗

Molecular population genetics of redundant floral-regulatory genes in Arabidopsis thaliana.

Functional redundancy between duplicated genes is predicted to be transitory, as one gene either loses its function or gains a new function, or both genes accrue degenerative, yet complimentary mutations. Yet there are many examples where functional redundancy has been maintained between gene duplicates. To determine whether selection is acting on functionally redundant gene duplicates, we performed molecular evolution and population genetic analyses between two pairs of functionally redundant MADS-box genes from the model plant Arabidopsis thaliana: SEPALLATA1 (SEP1) and SEPALLATA2 (SEP2), involved in floral organ identity, and SHATTERPROOF1 (SHP1) and SHATTERPROOF2 (SHP2), involved in seed shattering. We found evidence for purifying selection acting to constrain functional divergence between paralogous genes. The protein evolution of both pairs of duplicate genes is functionally constrained, as evidenced by Ka/Ks ratios of 0.16 between paralogs. This functional constraint is stronger in the highly conserved DNA-binding and protein-binding MIK region than in the C-terminal region. We also assayed the evolutionary forces acting between orthologs of the SEP and SHP genes in A. thaliana and the closely related species, Arabidopsis lyrata. Heterogeneity analyses of the polymorphism-to-divergence ratio indicate selective sweeps have occurred within the transcriptional unit of SHP1 and the promoter of SHP2 in the A. thaliana lineage. Similar analyses identified a significant reduction in polymorphism within the SEP1 locus, spanning the 3' region of intron 1 to exon 3, that may represent an intragenic sweep within the SEP1 locus. We discuss whether the evolutionary forces acting on SEP1 and SEP2 versus SHP1 and SHP2 vary according to their position in the floral developmental pathway, as found with other floral-regulatory genes.

Arabidopsis↗

A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA.

A latitudinal cline in flowering time in accessions of Arabidopsis thaliana has been widely predicted because the environmental cues that promote flowering vary systematically with latitude, but evidence for such clines has been lacking. Here, we report evidence of a significant latitudinal cline in flowering time among 70 Northern European and Mediterranean ecotypes when grown under ecologically realistic conditions in a common garden environment. The detected cline, however, is found only in ecotypes with alleles of the flowering time gene FRIGIDA (FRI) that lack major deletions that would disrupt protein function, whereas there is no relationship between flowering time and latitude of origin among accessions with FRI alleles containing such deletions. Analysis of climatological data suggests that late flowering in accessions with putatively functional FRI was associated with reduced January precipitation at the site of origin, consistent with previous reports of a positive genetic correlation between water use efficiency and flowering time in Arabidopsis, and the pleiotropic effects of FRI of increasing water use efficiency. In accessions collected from Southern latitudes, we detected that putatively functional FRI alleles were associated with accelerated flowering relative to accessions with nonfunctional FRI under the winter conditions of our experiment. These results suggest that the ecological function of the vernalization requirement conferred by FRI differs across latitudes. More generally, our results indicate that by combining ecological and molecular genetic data, it is possible to understand the forces acting on life history transitions at the level of specific loci.

Arabidopsis↗

The evolution of molecular genetic pathways and networks.

There is growing interest in the evolutionary dynamics of molecular genetic pathways and networks, and the extent to which the molecular evolution of a gene depends on its position within a pathway or network, as well as over-all network topology. Investigations on the relationships between network organization, topological architecture and evolutionary dynamics provide intriguing hints as to how networks evolve. Recent studies also suggest that genetic pathway and network structures may influence the action of evolutionary forces, and may play a role in maintaining phenotypic robustness in organisms.

Animals↗

Epialleles via DNA methylation: consequences for plant evolution.

In plants, naturally occurring methylation of genes can affect the level of gene expression. Variation among individuals in the degree of methylation of a gene, termed epialleles, produces novel phenotypes that are heritable across generations. To date, ecologically important genes with methylated epialleles have been found to affect floral shape, vegetative and seed pigmentation, pathogen resistance and development in plants. Currently, the extent to which epiallelic variation is an important common contributor to phenotypic variation in natural plant populations and its fitness consequences are not known. Because epiallele phenotypes can have identical underlying DNA sequences, response to selection on these phenotypes is likely to differ from expectations based on traditional models of microevolution. Research is needed to understand the role of epialleles in natural plant populations. Recent advances in molecular genetic techniques could enable population biologists to screen for epiallelic variants within plant populations and disentangle epigenetic from more standard genetic sources of phenotypic variance, such as additive genetic variance, dominance variance, epistasis and maternal genetic effects.

Journal Article↗

Heterogeneous evolution of the Myc-like Anthocyanin regulatory gene and its phylogenetic utility in Cornus L. (Cornaceae).

Anthocyanin is a major pigment in vegetative and floral organs of most plants and plays an important role in plant evolution. The anthocyanin regulatory genes are responsible for regulating transcription of genes in the anthocyanin synthetic pathway. To assess evolutionary significance of sequence variation and evaluate the phylogenetic utility of an anthocyanin regulatory gene, we compared nucleotide sequences of the myc-like anthocyanin regulatory gene in the genus of dogwoods (Cornus: Cornaceae). Phylogenetic analyses demonstrate that the myc-like anthocyanin regulatory gene has potential as an informative phylogenetic marker at different taxonomic levels, depending on the data set considered (DNA or protein sequences) and regions applied (exons or introns). Pairwise nonsynonymous and synonymous substitution rate tests and codon-based substitution models were applied to characterize variation and to identify sites under diversifying selection. Mosaic evolution and heterogeneous rates among different domains and sites were detected.

Anthocyanins↗

Linkage disequilibrium mapping of Arabidopsis CRY2 flowering time alleles.

The selfing plant Arabidopsis thaliana has been proposed to be well suited for linkage disequilibrium (LD) mapping as a means of identifying genes underlying natural trait variation. Here we apply LD mapping to examine haplotype variation in the genomic region of the photoperiod receptor CRYPTOCHROME2 and associated flowering time variation. CRY2 DNA sequences reveal strong LD and the existence of two highly differentiated haplogroups (A and B) across the gene; in addition, a haplotype possessing a radical glutamine-to-serine replacement (AS) occurs within the more common haplogroup. Growth chamber and field experiments using an unstratified population of 95 ecotypes indicate that under short-day photoperiod, the AS and B haplogroups are both highly significantly associated with early flowering. Data from six genes flanking CRY2 indicate that these haplogroups are limited to an approximately 65-kb genomic region around CRY2. Whereas the B haplogroup cannot be delimited to <16 kb around CRY2, the AS haplogroup is characterized almost exclusively by the nucleotide polymorphisms directly associated with the serine replacement in CRY2; this finding strongly suggests that the serine substitution is directly responsible for the AS early flowering phenotype. This study demonstrates the utility of LD mapping for elucidating the genetic basis of natural, ecologically relevant variation in Arabidopsis.

Amino Acid Sequence↗

The early stages of duplicate gene evolution.

Gene duplications are one of the primary driving forces in the evolution of genomes and genetic systems. Gene duplicates account for 8-20% of the genes in eukaryotic genomes, and the rates of gene duplication are estimated at between 0.2% and 2% per gene per million years. Duplicate genes are believed to be a major mechanism for the establishment of new gene functions and the generation of evolutionary novelty, yet very little is known about the early stages of the evolution of duplicated gene pairs. It is unclear, for example, to what extent selection, rather than neutral genetic drift, drives the fixation and early evolution of duplicate loci. Analysis of recently duplicated genes in the Arabidopsis thaliana genome reveals significantly reduced species-wide levels of nucleotide polymorphisms in the progenitor and/or duplicate gene copies, suggesting that selective sweeps accompany the initial stages of the evolution of these duplicated gene pairs. Our results support recent theoretical work that indicates that fates of duplicate gene pairs may be determined in the initial phases of duplicate gene evolution and that positive selection plays a prominent role in the evolutionary dynamics of the very early histories of duplicate nuclear genes.

Arabidopsis↗

Patterns of nucleotide variation in homoeologous regulatory genes in the allotetraploid Hawaiian silversword alliance (Asteraceae).

Genome-wide duplication (polyploidization) is prevalent in a large number of eukaryotic organisms and is particularly widespread in flowering plants. Polyploid species appear to vary from their diploid progenitors in a variety of ecologically important traits, suggesting that genome duplications provide a mechanism for ecological diversification. Studies of nucleotide variation at duplicate genes that arise via polyploidization allow us to infer the evolutionary forces that act on these polyploid loci. In an effort to examine the evolutionary dynamics of homoeologous loci, molecular population genetic analyses were undertaken for duplicate regulatory genes in the allopolyploid Hawaiian silversword alliance, a premier example of adaptive radiation. The levels and patterns of nucleotide variation for the floral homeotic genes ASAPETALA1 (ASAP1) and ASAPETALA3/TM6 (ASAP3/TM6) were studied in two species representing different lineages within the Hawaiian silversword alliance: Argyroxiphium sandwicense ssp. macrocephalum and Dubautia ciliolata ssp. glutinosa. Homoeologueous copies of ASAP1 and ASAP3/TM6 show differing levels and patterns of nucleotide polymorphism. Duplicate ASAP1 copies have similar levels of nucleotide diversity and haplotype structure in both species; by contrast, duplicate ASAP3/TM6 genes display different levels and patterns of variation in D. ciliolata ssp. glutinosa. Additionally, D. ciliolata ssp. glutinosa appears to be segregating for a moderate frequency null allele in one ASAP3/TM6 homoeologue. These results suggest that differing evolutionary forces can affect duplicate loci arising from allopolyploidization.

Asteraceae↗