Slipped-strand mispairing: a major mechanism for DNA sequence evolution

Simple repetitive DNA sequences are a widespread and abundant feature of genomic DNA. The following several features characterize such sequences: (1) they typically consist of a variety of repeated motifs of 1-10 bases--but may include much larger repeats as well; (2) larger repeat units often include shorter ones within them; (3) long polypyrimidine and poly-CA tracts are often found; and (4) tandem arrangements of closely related motifs are often found. We propose that slipped-strand mispairing events, in concert with unequal crossing- over, can readily account for all of these features. The frequent occurrence of long tandem repeats of particular motifs (polypyrimidine and poly-CA tracts) appears to result from nonrandom patterns of nucleotide substitution. We argue that the intrahelical process of slipped-strand mispairing is much more likely to be the major factor in the initial expansion of short repeated motifs and that, after initial expansion, simple tandem repeats may be predisposed to further expansion by unequal crossing-over or other interhelical events because of their propensity to mispair. Evidence is presented that single-base repeats (the shortest possible motifs) are represented by longer runs in mammalian introns than would be expected on a random basis, supporting the idea that SSM may be a ubiquitous force in the evolution of the eukaryotic genome. Simple repetitive sequences may therefore represent a natural ground state of DNA unselected for coding functions.      

Slipped-strand mispairing can function as a phase variation mechanism in Escherichia coli

Slipped-strand mispairing (SSM) has not been identified as a mechanism of phase variation in Escherichia coli. Using a reporter gene, we show that sequences that cause phase variation by SSM in Haemophilus influenzae also lead to phase variation when introduced onto the chromosome of E. coli, and the frequencies of switching are in the biologically relevant range. Thus, the absence of SSM-mediated phase variation in E. coli does not appear to be due to a mechanistic constraint.     

Slipped-strand mispairing at noncontiguous repeats in Poecilia reticulata: a model for minisatellite birth

The standard slipped-strand mispairing (SSM) model for the formation of variable number tandem repeats (VNTRs) proposes that a few tandem repeats, produced by chance mutations, provide the "raw material" for VNTR expansion. However, this model is unlikely to explain the formation of VNTRs with long motifs (e.g., minisatellites), because the likelihood of a tandem repeat forming by chance decreases rapidly as the length of the repeat motif increases. Phylogenetic reconstruction of the birth of a mitochondrial (mt) DNA minisatellite in guppies suggests that VNTRs with long motifs can form as a consequence of SSM at noncontiguous repeats. VNTRs formed in this manner have motifs longer than the noncontiguous repeat originally formed by chance and are flanked by one unit of the original, noncontiguous repeat. SSM at noncontiguous repeats can therefore explain the birth of VNTRs with long motifs and the "imperfect" or "short direct" repeats frequently observed adjacent to both mtDNA and nuclear VNTRs.     

Attribute correlations in the Poaceae (grasses)

Investigation of correlations between a number of two-state attributes for a sample of grass genera revealed that a high proportion of the correlations were statistically significant. There were proportionately more correlations between attributes from the same organ than between attributes from different organS. Furthermore, attributes associated with the fruit and leaf were found to be more closely correlated with attributes other than those of the flower and spikelet, thereby indicating fruit and leaf attributes to be important in the classification of the grasseS. It is considered that the correlations have arisen in part as a result of the phylogenetic origins of the genera and in part as a response to natural selection determining distribution of genera adapted to present-day habitats.     

The biogeography of grasses (Poaceae)

The grasses are the most important plant family for food production. Despite the domestication of Oryza sativa L. (rice), Triticum aestivum L. (wheat), Zea mays L. (corn), Hordeum vulgare L.(barely), Secale cereale L. (rye), Avena sativa L. (oats), Sorghum bicolor (L.) Moench (sorghum), Saacharum officinarum L. (sugar cane), Pennisetum glaucum (L.) R. Br. (pearl millet), Panicum virgatum L. (switchgrass), Eleusine coracana (L.) Gaertn (finger millet.) and Eragrostis tef (Zucc.) Trotter (tef), the family has not been widely studied biogeographically (Bouchenak-Khelladi et al.,2010). Other notable economic uses of grasses include landscaping, construction (primarily bamboos), and biofuel production (Miscanthus x giganteus J.M. Greef & Deuter ex Hodk. & Renvoize, Panicum L., and Zea L.).     

The phytochrome gene family in grasses (Poaceae): a phylogeny and evidence that grasses have a subset of the loci found in dicot angiosperms

The phytochrome nuclear gene family encodes photoreceptor proteins that mediate developmental responses to red and far red light throughout the life of the plant. From studies of the dicot flowering plant Arabidopsis, the family has been modeled as comprising five loci, PHYA- PHYE. However, it has been shown recently that the Arabidopsis model may not completely represent some flowering plant groups because additional PHY loci related to PHYA and PHYB of Arabidopsis apparently have evolved independently several times in dicots, and monocot flowering plants may lack orthologs of PHYD and PHYE of Arabidopsis. Nonetheless, the phytochrome nucleotide data were informative in a study of organismal evolution because the loci occur as single copy sequences and appear to be evolving independently. We have continued our investigation of the phytochrome gene family in flowering plants by sampling extensively in the grass family. The phytochrome nuclear DNA data were cladistically analyzed to address the following questions: (1) Are the data consistent with a pattern of differential distribution of phytochrome genes among monocots and higher dicots, with homologs of PHYA, B, C, D, and E present in higher dicots, but of just PHYA, B, and C in monocots, and (2) what phylogenetic pattern within Poaceae do they reveal? Results of these analyses, and of Southern blot experiments, are consistent with the observation that the phytochrome gene family in grasses comprises the same subset of loci detected in other monocots. Furthermore, for studies of organismal phylogeny in the grass family, the data are shown to provide significant support for relationships that are just weakly resolved by other data sets.      

Complex evolution in Arundinarieae (Poaceae: Bambusoideae): incongruence between plastid and nuclear GBSSI gene phylogenies

The monophyly of tribe Arundinarieae (the temperate woody bamboos) has been unequivocally recovered in previous molecular phylogenetic studies. In a recent phylogenetic study, 10 major lineages in Arundinarieae were resolved based on eight non-coding plastid regions, which conflicted significantly with morphological classifications both at the subtribal and generic levels. Nevertheless, relationships among and within the 10 lineages remain unclear. In order to further unravel the evolutionary history of Arundinarieae, we used the nuclear GBSSI gene sequences along with those of eight plastid regions for phylogenetic reconstruction, with an emphasis on Chinese species. The results of the plastid analyses agreed with previous studies, whereas 13 primary clades revealed in the GBSSI phylogeny were better resolved at the generic level than the plastid phylogeny. Our analyses also revealed many inconsistencies between the plastid DNA and the nuclear GBSSI trees. These results implied that the nuclear genome and the plastid genome had different evolutionary trajectories. The patterns of incongruence suggested that lack of informative characters, incomplete lineage sorting, and/or hybridization (introgression) could be the causes. Seven putative hybrid species were hypothesized, four of which are discussed in detail on the basis of topological incongruence, chromosome numbers, morphology, and distribution patterns, and those taxa probably resulted from homoploid hybrid speciation. Overall, our study indicates that the tribe Arundinarieae has undergone a complex evolution.     

Allotetraploid origin and divergence in Eleusine (Chloridoideae, Poaceae): evidence from low-copy nuclear gene phylogenies and a plastid gene chronogram

Background and Aims Eleusine

(Poaceae) is a small genus of the subfamily Chloridoideae exhibiting considerable morphological and ecological diversity in East Africa and the Americas. The interspecific phylogenetic relationships of Eleusine are investigated in order to identify its allotetraploid origin, and a chronogram is estimated to infer temporal relationships between palaeoenvironment changes and divergence of Eleusine in East Africa.

Methods

Two low-copy nuclear (LCN) markers, Pepc4 and EF-1α, were analysed using parsimony, likelihood and Bayesian approaches. A chronogram of Eleusine was inferred from a combined data set of six plastid DNA markers (ndhA intron, ndhF, rps16-trnK, rps16 intron, rps3, and rpl32-trnL) using the Bayesian dating method.

Key Results

The monophyly of Eleusine is strongly supported by sequence data from two LCN markers. In the cpDNA phylogeny, three tetraploid species (E. africana, E. coracana and E. kigeziensis) share a common ancestor with the E. indica–E. tristachya clade, which is considered a source of maternal parents for allotetraploids. Two homoeologous loci are isolated from three tetraploid species in the Pepc4 phylogeny, and the maternal parents receive further support. The A-type EF-1α sequences possess three characters, i.e. a large number of variations of intron 2; clade E-A distantly diverged from clade E-B and other diploid species; and seven deletions in intron 2, implying a possible derivation through a gene duplication event. The crown age of Eleusine and the allotetraploid lineage are 3·89 million years ago (mya) and 1·40 mya, respectively.

Conclusions

The molecular data support independent allotetraploid origins for E. kigeziensis and the E. africana–E. coracana clade. Both events may have involved diploids E. indica and E. tristachya as the maternal parents, but the paternal parents remain unidentified. The habitat-specific hypothesis is proposed to explain the divergence of Eleusine and its allotetraploid lineage.     

Molecular evolution and nucleotide diversity of nuclear plastid phosphoglycerate kinase (PGK) gene in Triticeae (Poaceae)

Levels of nucleotide divergence provide key evidence in the evolution of polyploids. The nucleotide diversity of 226 sequences of pgk1 gene in Triticeae species was characterized. Phylogenetic analyses based on the pgk1 gene were carried out to determine the diploid origin of polyploids within the tribe in relation to their A^u, B, D, St, Ns, P, and H haplomes. Sequences from the Ns genome represented the highest nucleotide diversity values for both polyploid and diploid species with π = 0.03343 and θ = 0.03536 for polyploid Ns genome sequences and π = 0.03886 and θ = 0.03886 for diploid Psathyrostachys sequences, while Triticum urartu represented the lowest diversity among diploid species at π = 0.0011 and θ = 0.0011. Nucleotide variation of diploid Aegilops speltoides (π = 0.2441, presumed the B genome donor of Triticum species) is five times higher than that (π = 0.00483) of B genome in polyploid species. Significant negative Tajima's D values for the St, A^u, and D genomes along with high rates of polymorphisms and low sequence diversity were observed. Origins of the A^u, B, and D genomes were linked to T. urartu, A. speltoides, and A. tauschii, respectively. Putative St genome donor was Pseudoroegneria, while Ns and P donors were Psathyrostachys and Agropyron. H genome diploid donor is Hordeum.     

An optimized chloroplast DNA extraction protocol for grasses (Poaceae) proves suitable for whole plastid genome sequencing and SNP detection

Background

Obtaining chloroplast genome sequences is important to increase the knowledge about the fundamental biology of plastids, to understand evolutionary and ecological processes in the evolution of plants, to develop biotechnological applications (e.g. plastid engineering) and to improve the efficiency of breeding schemes. Extraction of pure chloroplast DNA is required for efficient sequencing of chloroplast genomes. Unfortunately, most protocols for extracting chloroplast DNA were developed for eudicots and do not produce sufficiently pure yields for a shotgun sequencing approach of whole plastid genomes from the monocot grasses.

Methodology/Principal Findings

We have developed a simple and inexpensive method to obtain chloroplast DNA from grass species by modifying and extending protocols optimized for the use in eudicots. Many protocols for extracting chloroplast DNA require an ultracentrifugation step to efficiently separate chloroplast DNA from nuclear DNA. The developed method uses two more centrifugation steps than previously reported protocols and does not require an ultracentrifuge.

Conclusions/Significance

The described method delivered chloroplast DNA of very high quality from two grass species belonging to highly different taxonomic subfamilies within the grass family (Lolium perenne, Pooideae; Miscanthus×giganteus, Panicoideae). The DNA from Lolium perenne was used for whole chloroplast genome sequencing and detection of SNPs. The sequence is publicly available on EMBL/GenBank.     

The system of grasses (Poaceae) and their evolution

Originally published in Russian as number 37 of Komarov Readings, 1987. Translated by Victoria V. Michaelova, Brigham Young University, Provo, Utah 84602. Translation edited by Arthur Cronquist, New York Botanical Garden, New York, and approved by the author. A few additions have been made to account for very recent literature.     

Evolution of Ac and Dsl elements in select grasses (Poaceae)

We present data on evolution of the Ac/Ds family of transposable elements in select grasses (Poaceae). An Ac-like element was cloned from a DNA library of the grass Pennisetum glaucum (pearl millet) and 2387 bp of it have been sequenced. When the pearl millet Ac-like sequence is aligned with the corresponding region of the maize Ac sequence, it is found that all sequences corresponding to intron II in maize Ac are absent in pearl millet Ac. Kimura's evolutionary distance between maize and pearl millet Ac sequences is estimated to be 0.429±0.020 nucleotide substitutions per site. This value is not significantly different from the average number of synonymous substitutions for coding regions of the Adh1 gene between maize and pearl millet, which is 0.395±0.051 nucleotide substitutions per site. If we can assume Ac and Adh1 divergence times are equivalent between maize and pearl millet, then the above calculations suggest Ac-like sequences have probably not been strongly constrained by natural selection. The level of DNA sequence divergence between maize and pearl millet Ac sequences, the estimated date when maize and pearl millet diverged (25–40 million years ago), coupled with their reproductive isolation/lack of current genetic exchange, all support the theory that Ac-like sequences have not been recently introduced into pearl millet from maize. Instead, Ac-like sequences were probably present in the progenitor of maize and pearl millet, and have thus existed in the grasses for at least 25 million years. Ac-like sequences may be widely distributed among the grasses. We also present the first 2 Dsl controlling element sequences from teosinte species: Zea luxurians and Zea perennis. A total of 10 Dsl elements had previously been sequenced from maize and a distant maize relative, Tripsacum. When a maximum likelihood network of genetic relationships is constructed for all 12 sequenced Dsl elements, the 2 teosinte Dsl elements are as distant from most maize Dsl elements and from each other, as the maize Dsl elements are from one another. Our new teosinte sequence data support the previous conclusion that Dsl elements have been accumulating mutations independently since maize and Tripsacum diverged. We present a scenario for the origin of Dsl elements.     

Biogeography of grasses (Poaceae) on islands of southwestern Australia

Abstract The number of native grass species and exotic grass species present on 129 offshore islands of southwestern Australia is best predicted by island area and island disturbance, respectively. Isolation of islands and gull activity on islands only slightly improved these predictions. Species turnover on a subset of 30 islands indicated that exotic grass species were more prone to local extinction and more likely to immigrate than native grass species. The major conservation implication of this study is that habitat disturbance on these islands should be minimized to reduce establishment of exotic grass species.     

Cleaning up the grasses dustbin: systematics of the Arundinoideae subfamily (Poaceae)

Among the 12 subfamilies currently considered in the systematics of Poaceae, the Arundinoideae have long been considered as a dustbin group, with a diversity of forms putatively hiding incertae sedis. Because this subfamily has been poorly investigated using molecular markers for the last two decades, the present study provides the first complete phylogeny of the Arundinoideae based on five plastid DNA loci sequenced for 12 genera, and analysed with and without plastome data from previous studies. The refined Arundinoideae appear to be a robust evolutionary lineage of Poaceae, divided into three tribes with some biogeographical patterns: (1) tribe Arundineae, the most heterogeneous tribe, including Eurasian Arundo, Australian Amphipogon and Monachather, and South African Dregeochloa; (2) tribe Crinipedeae (described here), including Crinipes, Elytrophorus, Styppeiochloa and Pratochloa (described here), with a South and East African distribution; and (3) tribe Molinieae, including Hakonechloa, Molinia and Phragmites, with a Eurasian distribution. Despite reduction in size, this small subfamily conserves a high diversity of morphological forms, with several small but highly differentiated genera. Finally, the molecular dating approach provides an evolutionary framework to understand the diversification of Arundinoideae, refuting Gondwanan vicariance between genera and suggesting capability for long distance dispersal.     

Phylogenetic signals in the realized climate niches of Chinese grasses (Poaceae)

Explaining relationships between species richness and biogeographical patterns over a broad geographic scale is a central issue of biogeography and macroecology. We document the realized climate niches for grasses in China’s nature reserves and discuss its formation mechanism using grass richness data combined with climatic, physiological, and phylogenetic data. Our results suggest that climate niche structure of grasses is phylogenetically conservative for BEP (Bambusoideae, Ehrhartoideae, and Pooideae) and PACMAD (Panicoideae, Arundinoideae, Chloridoideae, Micrairoideae, Aristidoideae, and Danthonioideae) clades along temperature gradients and for Chloridoideae and Panicoideae along precipitation gradients. At the national scale, the divergence patterns of climate niches between two major clades are more distinguishable than between C₃ and C₄ grasses. High rates of climate niche evolution are found in C₄ clades in the subtropical forest region. There appears to be a strong association between elevation gradients and grass diversity: the specific environmental conditions (e.g. energy) and the rapid shifts of climate conditions drive high grass diversification. Evolutionary conservatism of climate niches may be influenced by the specific adaptive ability to changing environmental conditions within NAD-ME/NADP-ME clades. Our results indicate that adaptations to major climate changes may be accomplished by C₄ grass nodes of high climate niche evolutionary rates in China’s nature reserves.     

Universal primers for the amplification of chloroplast microsatellites in grasses (Poaceae)

Attempts to design truly universal primers to amplify chloroplast microsatellites have met with limited success due to nonconservation of repeat loci across widely divergent taxa. We have used the complete chloroplast genome sequences of rice, maize and wheat to design five pairs of primers that amplify homologous mononucleotide repeats across the Poaceae (grasses). Sequencing confirmed conservation of repeat motifs across subfamilies and a preliminary study in Anthoxanthum odoratum revealed polymorphism at two loci with a haplotype diversity value of 0.495. These primers provide a valuable tool to study cytoplasmic diversity in this extensively studied and economically important range of taxa.     

Patterns of genetic diversification within the Adh gene family in the grasses (Poaceae).

We investigated the evolutionary dynamics of the Adh gene family within the grasses (Poaceae), with the goal of using molecular evolutionary tools to understand the process of gene family diversification. We analyzed 21 Adh sequences representing a broad array of grasses. Phylogenetic analyses suggested that Adh duplicated into Adh1 and Adh2 before the radiation of the grasses roughly 65 MYA. Gene structure, including intron length, has varied little over this period. Conservation of intron length prompted investigation into the dynamics of intron evolution, particularly the ability of intron sequences to form secondary structures. Intron sequences did not have an extremely high or low minimum free energy of folding relative to permuted sequences, suggesting that individual Adh introns do not evolve under secondary structural constraints. For coding sequences, the diversification of Adh1 and Adh2 was marked by a shift in third-position G + C content. This shift may reflect differential selection for codon use. Diversification between Adh1 and Adh2 was also typified by a shift in nonsynonymous nucleotide substitution rates, but there was no evidence that relatively fast nonsynonymous nucleotide substitution rates in the Adh2 clade were a product of diversifying selection. Gene conversion may have played a role in retarding diversification of Adh1 and Adh2 in rice, but there is no evidence of gene conversion between paralogs in other taxa. Although the reasons for retention of two functional Adh genes remain obscure, we propose that a shift in gene expression was important for the retention of the two Adh gene copies within the grasses.