Genome evolution in allopolyploid wheat-a revolutionary reprogramming followed by gradual changes

Allopolyploidy accelerates genome evolution in wheat in two ways： 1） allopolyploidization triggers rapid genome alterations （revolutionary changes） through the instantaneous generation of a variety of cardinal genetic and epigenetic changes, and 2） the allopolyploid condition facilitates sporadic genomic changes during the life of the species （evolutionary changes） that are not attainable at the diploid level. The revolutionary alterations, occurring during the formation of the allopolyploid and leading to rapid cytological and genetic diploidization, facilitate the successful establishment of the newly formed allopolyploid in nature. On the other hand, the evolutionary changes, occurring during the life of the allopolyploids, increase the intra-specific genetic diversity, and consequently, increased fimess, adaptability and competitiveness. These phenomena, emphasizing the dynamic plasticity of the allopolyploid wheat genome with regards to both structure and function, are described and discussed in this review.     

山羊草属异源多倍体植物基因组进化的ISSR分析

使用31个ISSR引物对山羊草属Aegilops多倍体植物及其祖先二倍体（共23种）的基因组进行了分析,结果表明：与其二倍体祖先种相比,异源多倍体物种的基因组发生了很大变化。在含U基因组的异源多倍体物种中,U基因组相对而言变化很小,而其他基因组则发生了不同程度的变化。这表明当U基因组与其他基因组共存于多倍体物种中时,U基因组表现出较强的“同化效应”。对这些基因组的进化进行了讨论。     

Nonadditive changes in genome size during allopolyploidization in the wheat (aegilops-triticum) group

Interspecific or intergeneric hybridization, followed by chromosome doubling, can lead to the formation of new allopolyploid species. Recent studies indicate that allopolyploid formation is associated with genetic and epigenetic changes. Despite these studies, it is not yet clear whether the C value of an allopolyploid is the sum of its diploid parents. To address this question, six newly synthesized wheat allopolyploids and their parental plants were investigated. It was found that allopolyploids have a genome size significantly smaller than the expected value. The reduction of the nuclear genome size in the synthetic allotetraploids and allohexaploids was 2 pg DNA at 2C. It was also found that changes in the genome size already existed in the first generation amphiploids, indicating that the change was a rapid event. There was no difference in the reduction of nuclear genome size between the allotetraploid and the allohexaploid. These data clearly show that genome differentiation in allopolyploids was not related to the ploidy level. The data obtained clearly suggested that the nonadditive change in genome size that occurred during allopolyploidization may represent a preprogrammed adaptive response to genomic stress caused by hybridization and allopolyploidy, which serves to stabilize polyploid genomes.     

Natural variation and persistent developmental instabilities in geographically diverse accessions of the allopolyploid Arabidopsis suecica

Allopolyploids arise from the hybridization of two species concomitant to genome doubling. While established allopolyploids are common in nature and vigorous in growth, early generation allopolyploids are often less fertile than their progenitors and display frequent phenotypic instabilities. It is commonly assumed that new allopolyploid species must pass through a bottleneck from which only those lines emerge that have reconciled genomic incompatibilities inherited from their progenitors in their combined genome, yet little is known about the processes following allopolyploidization over evolutionary time. To address the question if a single allopolyploidization event leads to a single new homogeneous species or may result in diverse offspring lines, we have investigated 13 natural accessions of Arabidopsis suecica, a relatively recent allopolyploid derived from a single hybridization event. The studied accessions display low genetic diversity between lines, yet show evidence of heritable phenotypic diversity of traits, some of which may be adaptive. Furthermore, our data show that contrary to the notion that unstable phenotypes in neoallopolyploids are eliminated rapidly in the new species, some instabilities are carried along throughout the species' evolution, persisting in the established allopolyploid. In summary, our results suggest that a single allopolyploidization event may lay the foundation for diverse populations of the new allopolyploid species.     

Size matters in Triticeae polyploids: larger genomes have higher remodeling

Polyploidization is one of the major driving forces in plant evolution and is extremely relevant to speciation and diversity creation. Polyploidization leads to a myriad of genetic and epigenetic alterations that ultimately generate plants and species with increased genome plasticity. Polyploids are the result of the fusion of two or more genomes into the same nucleus and can be classified as allopolyploids (different genomes) or autopolyploids (same genome). Triticeae synthetic allopolyploid species are excellent models to study polyploids evolution, particularly the wheat-rye hybrid triticale, which includes various ploidy levels and genome combinations. In this review, we reanalyze data concerning genomic analysis of octoploid and hexaploid triticale and different synthetic wheat hybrids, in comparison with other polyploid species. This analysis reveals high levels of genomic restructuring events in triticale and wheat hybrids, namely major parental band disappearance and the appearance of novel bands. Furthermore, the data shows that restructuring depends on parental genomes, ploidy level, and sequence type (repetitive, low copy, and (or) coding); is markedly different after wide hybridization or genome doubling; and affects preferentially the larger parental genome. The shared role of genetic and epigenetic modifications in parental genome size homogenization, diploidization establishment, and stabilization of polyploid species is discussed.     

Allopolyploidization-accommodated genomic sequence changes in triticale

Background: Allopolyploidization is one of the major evolutionary modesof plant speciation. Recent interest in studying allopolyploidshas provided significant novel insights into the mechanismsof allopolyploid formation. Compelling evidence indicates thatgenetic and/or epigenetic changes have played significant rolesin shaping allopolyploids, but rates and modes of the changescan be very different among various species. Triticale (x Triticosecale)is an artificial species that has been used to study the evolutionarycourse of complex allopolyploids due to its recent origin andavailability of a highly diversified germplasm pool. Scope: This review summarizes recent genomics studies implemented inhexaploid and octoploid triticales and discusses the mechanismsof the changes and compares the major differences between genomicchanges in triticale and other allopolyploid species. Conclusions: Molecular studies have indicated extensive non-additive sequencechanges or modifications in triticale, and the degree of variationappears to be higher than in other allopolyploid species. Thedata indicate that at least some sequence changes are non-random,and appear to be a function of genome relations, ploidy levelsand sequence types. Specifically, the rye parental genome demonstrateda higher level of changes than the wheat genome. The frequencyof lost parental bands was much higher than the frequency ofgained novel bands, suggesting that sequence modification and/orelimination might be a major force causing genome variationin triticale. It was also shown that 68 % of the total changesoccurred immediately following wide hybridization, but beforechromosome doubling. Genome evolution following chromosome doublingoccurred more slowly at a very low rate and the changes weremainly observed in the first five or so generations. The datasuggest that cytoplasm and relationships between parental genomesare key factors in determining the direction, amount, timingand rate of genomic sequence variation that occurred duringinter-generic allopolyploidization in this system.     

Nuclear DNA amount and genome downsizing in natural and synthetic allopolyploids of the genera Aegilops and Triticum

Recent molecular studies in the genera Aegilops and Triticum showed that allopolyploidization (interspecific or intergeneric hybridization followed by chromosome doubling) generated rapid elimination of low-copy or high-copy, non-coding and coding DNA sequences. The aims of this work were to determine the amount of nuclear DNA in allopolyploid species of the group and to see to what extent elimination of DNA sequences affected genome size. Nuclear DNA amount was determined by the flow cytometry method in 27 natural allopolyploid species (most of which were represented by several lines and each line by several plants) as well as 14 newly synthesized allopolyploids (each represented by several plants) and their parental plants. Very small intraspecific variation in DNA amount was found between lines of allopolyploid species collected from different habitats or between wild and domesticated forms of allopolyploid wheat. In contrast to the constancy in nuclear DNA amount at the intraspecific level, there are significant differences in genome size between the various allopolyploid species, at both the tetraploid and hexaploid levels. In most allopolyploids nuclear DNA amount was significantly less than the sum of DNA amounts of the parental species. Newly synthesized allopolyploids exhibited a similar decrease in nuclear DNA amount in the first generation, indicating that genome downsizing occurs during and (or) immediately after the formation of the allopolyploids and that there are no further changes in genome size during the life of the allopolyploids. Phylogenetic considerations of the origin of the B genome of allopolyploid wheat, based on nuclear DNA amount, are discussed.     

Instability of chromosome number and DNA methylation variation induced by hybridization and amphidiploid formation between <Emphasis Type="Italic">Raphanus sativus</Emphasis> L. and <Emphasis Type="Italic">Brassica alboglabra</Emphasis>Bailey

Background  

Distant hybridization can result genome duplication and allopolyploid formation which may play a significant role in the origin and evolution of many plant species. It is unclear how the two or more divergent genomes coordinate in one nucleus with a single parental cytoplasm within allopolyploids. We used cytological and molecular methods to investigate the genetic and epigenetic instabilities associated with the process of distant hybridization and allopolyploid formation, measuring changes in chromosome number and DNA methylation across multiple generations.     

Allopolyploidy in wheat induces rapid and heritable alterations in DNA methylation patterns of cellular genes and mobile elements

Whereas accumulating recent evidences indicate that allopolyploid formation in plants is accompanied by rapid and non-Mendelian genomic changes, some other works showed genomic stasis in both nascent and natural allopolyploids. To further study the issue, we performed global DNA fingerprinting of a newly synthesized allohexaploid wheat and its natural counterpart, the common wheat, by AFLP analysis. It was found that ca. 20% bands showed deviation from parental additivity in both synthetic and the natural common wheat. Sequence analysis indicates that a majority of the changed bands represent known-function genes and transposable elements. DNA gel blot analysis showed that the main type of changes in the amphiploid is epigenetic in nature, i.e., alteration in DNA methylation patterns. Two types of alterations in methylation, random and non-random, were detected, and both types were stably inherited. Possible causes and implications of the epigenetic changes in allopolyploid genome evolution and speciation are discussed.     

Allopolyploidy in Wheat Induces Rapid and Heritable Alterations in DNA Methylation Patterns of Cellular Genes and Mobile Elements

Whereas accumulating recent evidences indicate that allopolyploid formation in plants is accompanied by rapid and non-Mendelian genomic changes, some other works showed genomic stasis in both nascent and natural allopolyploids. To further study the issue, we performed global DNA fingerprinting of a newly synthesized allohexaploid wheat and its natural counterpart, the common wheat, by AFLP analysis. It was found that ca. 20% bands showed deviation from parental additivity in both synthetic and natural common wheat. Sequence analysis indicates that a majority of the changed bands represent known-function genes and transposable elements. DNA gel blot analysis showed that the main type of changes in the amphiploid is epigenetic in nature, i.e., alteration in DNA methylation patterns. Two types of alterations in methylation, random and non-random, were detected, and both types were stably inherited. Possible causes and implications of the epigenetic changes in allopolyploid genome evolution and speciation are discussed.__________From Genetika, Vol. 41, No. 8, 2005, pp. 1089–1095.Original English Text Copyright © 2005 by Dong, Liu, Shan, Qiu, He, Liu.This text was submitted by the authors in English.     

Genome evolution of allopolyploids: a process of cytological and genetic diploidization

Allopolyploidy is a prominent mode of speciation in higher plants. Due to the coexistence of closely related genomes, a successful allopolyploid must have the ability to invoke and maintain diploid-like behavior, both cytologically and genetically. Recent studies on natural and synthetic allopolyploids have raised many discrepancies. Most species have displayed non-Mendelian behavior in the allopolyploids, but others have not. Some species have demonstrated rapid genome changes following allopolyploid formation, while others have conserved progenitor genomes. Some have displayed directed, non-random genome changes, whereas others have shown random changes. Some of the genomic changes have appeared in the F1 hybrids, which have been attributed to the union of gametes from different progenitors, while other changes have occurred during or after genome doubling. Although these observations provide significant novel insights into the evolution of allopolyploids, the overall mechanisms of the event are still elusive. It appears that both genetic and epigenetic operations are involved in the diploidization process of allopolyploids. Overall, genetic and epigenetic variations are often associated with the activities of repetitive sequences and transposon elements. Specifically, genomic sequence elimination and chromosome rearrangement are probably the major forces guiding cytological diploidization. Gene non-functionalization, sub-functionalization, neo-functionalization, as well as other kinds of epigenetic modifications, are likely the leading factors promoting genetic diploidization.     

Analysis of 5S rDNA changes in synthetic allopolyploids <Emphasis Type="Italic">Triticum</Emphasis> × <Emphasis Type="Italic">Aegilops</Emphasis>

Changes of 5S rDNA at the early stage of allopolyploidization were investigated in three synthetic allopolyploids: Aegilops sharonensis × Ae. umbellulata (2n = 28), Triticum urartu × Ae. tauschii (2n = 28), and T. dicoccoides × Ae. tauschii (2n = 42). Fluorescent in situ hybridization (FISH) revealed quantitative changes affecting separate loci of one of the parental genomes in S₃ plants of each hybrid combination. Southern hybridization with genomic DNA of the allopolyploid T. urartu × Ae. tauschii (TMU38 × TQ27) revealed a lower intensity of signals from Ae. tauschii fragments compared with those derived from T. urartu. This confirmed the signal reduction revealed for chromosome 1D of this hybrid by FISH. Neither Southern hybridization nor PCR testing of 5–15 plants of the S₂-S₃ generations revealed an appearance of new 5S rDNA fragments or a complete disappearance of parental fragments from the allopolyploids under study. No changes were found by aligning nine 5S rDNA sequences of the allopolyploid TMU38 × TQ27 with corresponding sequences of the parental species. The similarity between one of the synthetic allopolyploids examined and a natural allopolyploid with the same genome composition points to an early formation of the 5S rDNA organization unique for each allopolyploid.     

Genetic Basis for Spontaneous Hybrid Genome Doubling during Allopolyploid Speciation of Common Wheat Shown by Natural Variation Analyses of the Paternal Species

The complex process of allopolyploid speciation includes various mechanisms ranging from species crosses and hybrid genome doubling to genome alterations and the establishment of new allopolyploids as persisting natural entities. Currently, little is known about the genetic mechanisms that underlie hybrid genome doubling, despite the fact that natural allopolyploid formation is highly dependent on this phenomenon. We examined the genetic basis for the spontaneous genome doubling of triploid F₁ hybrids between the direct ancestors of allohexaploid common wheat (Triticum aestivum L., AABBDD genome), namely Triticum turgidum L. (AABB genome) and Aegilops tauschii Coss. (DD genome). An Ae. tauschii intraspecific lineage that is closely related to the D genome of common wheat was identified by population-based analysis. Two representative accessions, one that produces a high-genome-doubling-frequency hybrid when crossed with a T . turgidum cultivar and the other that produces a low-genome-doubling-frequency hybrid with the same cultivar, were chosen from that lineage for further analyses. A series of investigations including fertility analysis, immunostaining, and quantitative trait locus (QTL) analysis showed that (1) production of functional unreduced gametes through nonreductional meiosis is an early step key to successful hybrid genome doubling, (2) first division restitution is one of the cytological mechanisms that cause meiotic nonreduction during the production of functional male unreduced gametes, and (3) six QTLs in the Ae . tauschii genome, most of which likely regulate nonreductional meiosis and its subsequent gamete production processes, are involved in hybrid genome doubling. Interlineage comparisons of Ae . tauschii ’s ability to cause hybrid genome doubling suggested an evolutionary model for the natural variation pattern of the trait in which non-deleterious mutations in six QTLs may have important roles. The findings of this study demonstrated that the genetic mechanisms for hybrid genome doubling could be studied based on the intrinsic natural variation that exists in the parental species.