Most cited article - PubMed ID 17562679
Recent natural hybridization between two allopolyploid wheatgrasses (Elytrigia, Poaceae): ecological and evolutionary implications
Genome or genomic dominance (GD) is a phenomenon observed in hybrids when one parental genome becomes dominant over the other. It is manifested by the replacement of chromatin of the submissive genome by that of the dominant genome and by biased gene expression. Nucleolar dominance (ND) - the functional expression of only one parental set of ribosomal genes in hybrids - is another example of an intragenomic competitive process which, however, concerns ribosomal DNA only. Although GD and ND are relatively well understood, the nature and extent of their potential interdependence is mostly unknown. Here, we ask whether hybrids showing GD also exhibit ND and, if so, whether the dominant genome is the same. To test this, we used hybrids between Festuca and Lolium grasses (Festulolium), and between two Festuca species in which GD has been observed (with Lolium as the dominant genome in Festulolium and F. pratensis in interspecific Festuca hybrids). Using amplicon sequencing of ITS1 and ITS2 of the 45S ribosomal DNA (rDNA) cluster and molecular cytogenetics, we studied the organization and expression of rDNA in leaf tissue in five hybrid combinations, four generations and 31 genotypes [F. pratensis × L. multiflorum (F1, F2, F3, BC1), L. multiflorum × F. pratensis (F1), L. multiflorum × F. glaucescens (F2), L. perenne × F. pratensis (F1), F. glaucescens × F. pratensis (F1)]. We have found that instant ND occurs in Festulolium, where expression of Lolium-type rDNA reached nearly 100% in all F1 hybrids and was maintained through subsequent generations. Therefore, ND and GD in Festulolium are manifested by the same dominant genome (Lolium). We also confirmed the concordance between GD and ND in an interspecific cross between two Festuca species.
- Keywords
- Festuca, Lolium, fluorescent in situ hybridization, genome dominance, genomic in situ hybridization, internal transcribed spacer, nucleolar dominance, ribosomal DNA,
- Publication type
- Journal Article MeSH
BACKGROUND: Interspecific hybridisation resulting in polyploidy is one of the major driving forces in plant evolution. Here, we present data from the molecular cytogenetic analysis of three cytotypes of Elytrigia ×mucronata using sequential fluorescence (5S rDNA, 18S rDNA and pSc119.2 probes) and genomic in situ hybridisation (four genomic probes of diploid taxa, i.e., Aegilops, Dasypyrum, Hordeum and Pseudoroegneria). RESULTS: The concurrent presence of Hordeum (descended from E. repens) and Dasypyrum + Aegilops (descended from E. intermedia) chromosome sets in all cytotypes of E. ×mucronata confirmed the assumed hybrid origin of the analysed plants. The following different genomic constitutions were observed for E. ×mucronata. Hexaploid plants exhibited three chromosome sets from Pseudoroegneria and one chromosome set each from Aegilops, Hordeum and Dasypyrum. Heptaploid plants harboured the six chromosome sets of the hexaploid plants and an additional Pseudoroegneria chromosome set. Nonaploid cytotypes differed in their genomic constitutions, reflecting different origins through the fusion of reduced and unreduced gametes. The hybridisation patterns of repetitive sequences (5S rDNA, 18S rDNA, and pSc119.2) in E. ×mucronata varied between and within cytotypes. Chromosome alterations that were not identified in the parental species were found in both heptaploid and some nonaploid plants. CONCLUSIONS: The results confirmed that both homoploid hybridisation and heteroploid hybridisation that lead to the coexistence of four different haplomes within single hybrid genomes occur in Elytrigia allopolyploids. The chromosomal alterations observed in both heptaploid and some nonaploid plants indicated that genome restructuring occurs during and/or after the hybrids arose. Moreover, a specific chromosomal translocation detected in one of the nonaploids indicated that it was not a primary hybrid. Therefore, at least some of the hybrids are fertile. Hybridisation in Triticeae allopolyploids clearly and significantly contributes to genomic diversity. Different combinations of parental haplomes coupled with chromosomal alterations may result in the establishment of unique lineages, thus providing raw material for selection.
- Keywords
- Allopolyploidy, Chromosomal alterations, Elymus repens, FISH, GISH, Higher polyploids, Hybridisation, Thinopyrum intermedium,
- MeSH
- Cytogenetic Analysis MeSH
- DNA, Plant analysis MeSH
- Genotype * MeSH
- Hybridization, Genetic * MeSH
- In Situ Hybridization, Fluorescence MeSH
- In Situ Hybridization MeSH
- Poaceae genetics MeSH
- Polyploidy * MeSH
- RNA, Ribosomal, 18S analysis MeSH
- RNA, Ribosomal, 5S analysis MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Czech Republic MeSH
- Names of Substances
- DNA, Plant MeSH
- RNA, Ribosomal, 18S MeSH
- RNA, Ribosomal, 5S MeSH
The movement of nuclear DNA from one vascular plant species to another in the absence of fertilization is thought to be rare. Here, nonnative rRNA gene [ribosomal DNA (rDNA)] copies were identified in a set of 16 diploid barley (Hordeum) species; their origin was traceable via their internal transcribed spacer (ITS) sequence to five distinct Panicoideae genera, a lineage that split from the Pooideae about 60 Mya. Phylogenetic, cytogenetic, and genomic analyses implied that the nonnative sequences were acquired between 1 and 5 Mya after a series of multiple events, with the result that some current Hordeum sp. individuals harbor up to five different panicoid rDNA units in addition to the native Hordeum rDNA copies. There was no evidence that any of the nonnative rDNA units were transcribed; some showed indications of having been silenced via pseudogenization. A single copy of a Panicum sp. rDNA unit present in H. bogdanii had been interrupted by a native transposable element and was surrounded by about 70 kbp of mostly noncoding sequence of panicoid origin. The data suggest that horizontal gene transfer between vascular plants is not a rare event, that it is not necessarily restricted to one or a few genes only, and that it can be selectively neutral.
- Keywords
- Hordeum, Panicoideae, Triticeae, horizontal gene transfer, transposable elements,
- MeSH
- Cell Nucleus genetics MeSH
- Diploidy MeSH
- DNA, Plant chemistry genetics MeSH
- Phylogeny * MeSH
- Hordeum classification genetics MeSH
- Poaceae classification genetics MeSH
- DNA, Ribosomal Spacer chemistry genetics MeSH
- Evolution, Molecular MeSH
- Gene Transfer, Horizontal * MeSH
- DNA, Ribosomal chemistry genetics MeSH
- Genes, Plant genetics MeSH
- Sequence Analysis, DNA MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Plant MeSH
- DNA, Ribosomal Spacer MeSH
- DNA, Ribosomal MeSH
BACKGROUND: The wheat tribe Triticeae (Poaceae) is a diverse group of grasses representing a textbook example of reticulate evolution. Apart from globally important grain crops, there are also wild grasses which are of great practical value. Allohexaploid intermediate wheatgrass, Thinopyrum intermedium (2n = 6x = 42), possesses many desirable agronomic traits that make it an invaluable source of genetic material useful in wheat improvement. Although the identification of its genomic components has been the object of considerable investigation, the complete genomic constitution and its potential variability are still being unravelled. To identify the genomic constitution of this allohexaploid, four accessions of intermediate wheatgrass from its native area were analysed by sequencing of chloroplast trnL-F and partial nuclear GBSSI, and genomic in situ hybridization. RESULTS: The results confirmed the allopolyploid origin of Thinopyrum intermedium and revealed new aspects in its genomic composition. Genomic heterogeneity suggests a more complex origin of the species than would be expected if it originated through allohexaploidy alone. While Pseudoroegneria is the most probable maternal parent of the accessions analysed, nuclear GBSSI sequences suggested the contribution of distinct lineages corresponding to the following present-day genera: Pseudoroegneria, Dasypyrum, Taeniatherum, Aegilops and Thinopyrum. Two subgenomes of the hexaploid have most probably been contributed by Pseudoroegneria and Dasypyrum, but the identity of the third subgenome remains unresolved satisfactorily. Possibly it is of hybridogenous origin, with contributions from Thinopyrum and Aegilops. Surprising diversity of GBSSI copies corresponding to a Dasypyrum-like progenitor indicates either multiple contributions from different sources close to Dasypyrum and maintenance of divergent copies or the presence of divergent paralogs, or a combination of both. Taeniatherum-like GBSSI copies are most probably pseudogenic, and the mode of their acquisition by Th. intermedium remains unclear. CONCLUSIONS: Hybridization has played a key role in the evolution of the Triticeae. Transfer of genetic material via extensive interspecific hybridization and/or introgression could have enriched the species' gene pools significantly. We have shown that the genomic heterogeneity of intermediate wheatgrass is higher than has been previously assumed, which is of particular concern to wheat breeders, who frequently use it as a source of desirable traits in wheat improvement.
- MeSH
- Phylogeny MeSH
- Genome, Plant * MeSH
- Polyploidy MeSH
- Triticum genetics MeSH
- Plant Proteins genetics MeSH
- Starch Synthase genetics MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- granule-bound starch synthase I MeSH Browser
- Plant Proteins MeSH
- Starch Synthase MeSH
BACKGROUND: Hieracium s.str. is a complex species-rich group of perennial herbs composed of few sexual diploids and numerous apomictic polyploids. The existence of reticulation and the near-continuity of morphological characters across taxa seriously affect species determination, making Hieracium one of the best examples of a 'botanist's nightmare'. Consequently, its species relationships have not previously been addressed by molecular methods. Concentrating on the supposed major evolutionary units, we used nuclear ribosomal (ETS) and chloroplast (trnT-trnL) sequences in order to disentangle the phylogenetic relationships and to infer the origins of the polyploids. RESULTS: Despite relatively low interspecific variation, the nuclear data revealed the existence of two major groups roughly corresponding to species with a Western or Eastern European origin. Extensive reticulation was mainly inferred from the character additivity of parental ETS variants. Surprisingly, many diploid species were of hybrid origin whilst several polyploid taxa showed no evidence of reticulation. Intra-individual ETS sequence polymorphism generally exceeded interspecific variation and was either independent of, or additional to, additive patterns accounted for by hybrid origin. Several ETS ribotypes occurred in different hybrid taxa, but never as the only variant in any species analyzed. CONCLUSION: The high level of intra-individual ETS polymorphism prevented straightforward phylogenetic analysis. Characterization of this variation as additive, shared informative, homoplasious, or unique made it possible to uncover the phylogenetic signal and to reveal the hybrid origin of 29 out of 60 accessions. Contrary to expectation, diploid sexuals and polyploid apomicts did not differ in their molecular patterns. The basic division of the genus into two major clades had not previously been intimated on morphological grounds. Both major groups are thought to have survived in different glacial refugia and to have hybridized as a result of secondary contact. Several lines of evidence suggest the data is best explained by the presence of an extinct range of variation and a larger diversity of ancestral diploids in former times rather than by unsampled variation. Extinct diversity and extensive reticulation are thought to have largely obscured the species relationships. Our study illustrates how multigene sequences can be used to disentangle the evolutionary history of agamic complexes or similarly difficult datasets.
- MeSH
- Asteraceae classification genetics MeSH
- Bayes Theorem MeSH
- Diploidy MeSH
- DNA, Chloroplast genetics MeSH
- DNA, Plant genetics MeSH
- Species Specificity MeSH
- Phylogeny * MeSH
- Hybridization, Genetic * MeSH
- DNA, Ribosomal Spacer genetics MeSH
- Evolution, Molecular * MeSH
- Polymorphism, Genetic MeSH
- Polyploidy MeSH
- Likelihood Functions MeSH
- Sequence Analysis, DNA MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA, Chloroplast MeSH
- DNA, Plant MeSH
- DNA, Ribosomal Spacer MeSH