AOBPreview originally published online on February 5, 2008
Annals of Botany 2008 101(6):825-832; doi:10.1093/aob/mcm331
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Allopolyploidization-accommodated Genomic Sequence Changes in Triticale
1 Department of Agronomy, University of Missouri-Columbia, MO 65211, USA
2 USDA-ARS, Plant Genetics Research Unit, University of Missouri-Columbia, MO 65211, USA
* For correspondence. E-mail Perry.Gustafson{at}ars.usda.gov
Received: 12 September 2007 Returned for revision: 7 November 2007 Accepted: 10 December 2007 Published electronically: 5 February 2008
 |
ABSTRACT |
|---|
Background: Allopolyploidization is one of the major evolutionary modes of plant speciation. Recent interest in studying allopolyploids has provided significant novel insights into the mechanisms of allopolyploid formation. Compelling evidence indicates that genetic and/or epigenetic changes have played significant roles in shaping allopolyploids, but rates and modes of the changes can be very different among various species. Triticale (x Triticosecale) is an artificial species that has been used to study the evolutionary course of complex allopolyploids due to its recent origin and availability of a highly diversified germplasm pool.
Scope: This review summarizes recent genomics studies implemented in hexaploid and octoploid triticales and discusses the mechanisms of the changes and compares the major differences between genomic changes in triticale and other allopolyploid species.
Conclusions: Molecular studies have indicated extensive non-additive sequence changes or modifications in triticale, and the degree of variation appears to be higher than in other allopolyploid species. The data indicate that at least some sequence changes are non-random, and appear to be a function of genome relations, ploidy levels and sequence types. Specifically, the rye parental genome demonstrated a higher level of changes than the wheat genome. The frequency of lost parental bands was much higher than the frequency of gained novel bands, suggesting that sequence modification and/or elimination might be a major force causing genome variation in triticale. It was also shown that 68 % of the total changes occurred immediately following wide hybridization, but before chromosome doubling. Genome evolution following chromosome doubling occurred more slowly at a very low rate and the changes were mainly observed in the first five or so generations. The data suggest that cytoplasm and relationships between parental genomes are key factors in determining the direction, amount, timing and rate of genomic sequence variation that occurred during inter-generic allopolyploidization in this system.
Key words: Triticale, wheat, rye, allopolyploid, genome evolution, sequence elimination
|
INTRODUCTION |
|---|
Allopolyploidy is a major process involved in plant speciation, which occurs naturally by joining two or more different, but usually closely related, genomes into the same nucleus through wide hybridization between different species (or genera). Genome-wide gene redundancy not only enables allopolyploids to tolerate more genome variation compared with their progenitors, but also provides novel opportunities to generate functional diversification between homoeologous genes and genomes (Adams and Wendel, 2005; De Bodt et al., 2005). Increased fitness is also provided by loss of self-incompatibility and gain of asexual reproduction and higher levels of heterozygosity, most of which can be fixed, in allopolyploids (Comai, 2005). Therefore, allopolyploidization can increase plant fitness and this may have contributed to the widespread occurrence of allopolyploids (Wendel, 2000), accounting for 30–70 % of plant species. Indeed it has been estimated that up to 100 % of angiosperms may be considered polyploids if paleopolyploids are included (Wolfe, 2001; Liu and Wendel, 2002). Support for this latter hypothesis has recently been provided by Cui et al. (2006), and was clearly demonstrated in cereals, which had encountered an ancient polyploidization event about 70 million years ago, before divergence of the major cereals (Paterson et al., 2004).
However, gene and genome duplication often cause genome instabilities, chromosome imbalances, regulatory incompatibilities, and reproductive failures (Chen, 2007). Therefore, newly formed allopolyploids must establish a compatible relationship between alien cytoplasm and nuclei and between two divergent genomes to be successfully adapted in nature (Chen, 2007). It was suggested that allopolyploid genomes have experienced both revolutionary (instant) and evolutionary (accumulating) changes (Feldman and Levy, 2005), which cover a variety of genetic as well as epigenetic interactions (Comai, 2000; Chen, 2007; Paun et al., 2007). These evolutionary forces have shaped allopolyploids, facilitating adaptive evolution and obscuring the polyploid nature of many paleopolyploids such as arabidopsis (Arabidopsis Genome Initiative, 2000), maize (Zea mays; Gaut, 2001), soybean (Glycine max; Grant et al., 2000) and rice (Oryza sativa; Guyot and Keller, 2004).
To understand early evolutionary events, newly synthesized allopolyploids have been used to investigate early genetic changes contributing to the diploidization process of allopolyploids which cannot be revealed in the natural counterparts (Song et al., 1995). This strategy has been widely used in many species including newly synthesized wheat (Triticum spp.) where molecular studies have revealed sequence elimination and gene expression changes shortly after allopolyploid formation (Feldman and Levy, 2005).
Similar genetic changes and epigenetic phenomena have been observed in other newly synthesized allopolyploids, such as arabidopsis, Brassica, cotton (Gossypium spp.) and triticale (x Triticosecale), and recently formed natural allopolyploids, Tragopogon miscellus and Spartina anglica (reviewed by Ma and Gustafson, 2005; Adams and Wendel, 2005; Chen, 2007). However, the rates, types and degrees of genetic and epigenetic changes are very different among various allopolyploid species (Ma and Gustafson, 2005). It is evident that genetic distance between the parental genomes combined in the polyploid nucleus and nuclear–cytoplasmic interactions play significant roles during allopolyploidization. Of the well-studied newly synthesized species, triticale is mostly characterized by its genome complexity, different ploidy levels of parental genomes and inter-generic hybridization. These features make the genomic changes of triticale more extensive than any of the other allopolyploid species studied. It has been suggested that, in triticale, cytoplasm and degree of relationship between the parental genomes were the key factors in determining the direction, amount, timing, and rate of genomic sequence variation occurring during intergeneric allopolyploidization, thus providing significant novel insights into the evolutionary mechanisms of allopolyploids (Ma et al., 2002, 2004; Ma and Gustafson, 2006). In this review, the observations obtained from triticale are summarized and the mechanisms of allopolyploidization discussed.
|
GENOME COMPLEXITY AND DIVERSIFICATION OF TRITICALE |
|---|
Triticale (x Triticosecale Wittmack) is an artificial species with a very short history of just over 100 years. It is a chromosome-doubled inter-generic hybrid between various wheat species (Triticum ssp., AA, AABB and AABBDD) and rye (Secale cereale, RR). Since the first attempt to produce an artificial hybrid (Wilson, 1876) and the first recognition of large-scale natural hybridization between wheat and rye (Meister, 1921), thousands of triticales have been synthesized in a variety of ploidy levels and genome constitutions, such as tetraploid (AARR), hexaploid (AABBRR) and octoploid (AABBDDRR). Furthermore, secondary triticale lines, which are the stable hexaploid derivatives obtained by intercrossing an octoploid triticale and/or hexaploid wheat with a hexaploid triticale, have been developed for cultivation. Compared with other allopolyploid species studied, triticale is very complex because of its high ploidy level, large genome size and the distant relationship between the wheat and rye genomes brought together into the polyploid nucleus. These features make triticale a very valuable species for analysing early genetic evolutionary events, which occur in a complex allopolyploid genome.
|
OVERALL GENOMIC SEQUENCE CHANGES IN TRITICALE |
|---|
 TOPABSTRACTINTRODUCTIONGENOME COMPLEXITY AND... OVERALL GENOMIC SEQUENCE CHANGES... TIME COURSE OF THE...GENE EXPRESSION CHANGES IN...NON-ADDITIVE AND NON-RANDOM...CONCLUSIONS AND PERSPECTIVESLITERATURE CITED |
|---|
The overall genomic sequence changes of triticale were studied using AFLP and RFLP profiles of two octoploid and two hexaploid triticales as well as their corresponding wheat and rye parents, F1 wheat–rye hybrids, and several early generations of the re-synthesized triticale lines (Ma et al., 2002, 2004; Ma and Gustafson, 2006). Large-scale AFLP studies were implemented using two kinds of primer combinations EcoRI–MseI and PstI–MseI to get an unbiased genome-wide estimation of genomic sequence variation that occurred in both repetitive and low-copy sequences. AFLP analysis provided an opportunity to investigate genomic sequence changes at a genome-wide level. However, how representative amplified sequences are of the entire genome depends on the restriction enzymes used in the study. A general factor affecting restriction enzyme cleavage is cytosine methylation, which is widespread in the genome. Cytosine methylation is predominately present at CpG or CpNpG sites (Gruenbaum et al., 1981), and in non-coding and repetitive sequences (Finnegan et al., 1998), whereas the coding sequences are usually not methylated. Compared with EcoRI, PstI is highly sensitive to the cytosine status in CpNpG sites because its recognition site (CTGCAG) involves two CpNpG trinucleotides. As a result, EcoRI–MseI primers mainly amplify repetitive sequences, whereas PstI–MseI primers predominantly target low-copy sequences (Ma et al., 2004). Although it is not a precise estimation of sequence types, these two kinds of AFLP markers fairly differentiated general sequence type distributions along chromosomes, in which EcoRI–MseI markers are evenly distributed, whereas most PstI–MseI markers are mainly present in the distal gene-rich regions (Young et al., 1999; Rodriguez Milla and Gustafson, 2001). Furthermore, coding sequence variation was investigated using cDNA-probed RFLP analyses (Ma et al., 2004). Overall estimations of the changes occurring in the three types of sequences in triticale are summarized from several studies (Ma et al., 2002, 2004; Ma and Gustafson, 2006) and presented in Table 1.
|
The data were classified as present (no change) and absent (loss) for each ploidy level (hexaploid vs. octoploid), because different triticale materials within the same ploidy level showed similar results for each marker type used in the studies, but sequence variations between different ploidy levels were significantly different. Results indicated that the degree of genomic sequence variation in triticale was much higher than that which occurred in wheat, where sequence changes involved up to 15 % of the genomic DNA when the same method (AFLP) was used to investigate genome-wide sequence changes (Shaked et al., 2001). In addition, the majority of changes in triticale resulted from band loss rather than by gaining novel bands, implying potential sequence elimination, which has been well documented in a series of allopolyploid wheat studies (Feldman and Levy, 2005). The wheat and rye parental genomes demonstrated dramatic differences regarding sequence changes that had accumulated in the triticales. To investigate the effects of each factor influencing the rate of sequence change further, the data from Table 1 (except for the novel type) were re-formatted in Table 2 to clarify the parental effects, ploidy level effects and sequence type effects.
|
Parental effects: wheat vs. rye
Different parental effects controlling allopolyploid genome changes were observed in triticale with significantly more rye genomic changes than wheat (Fig. 1). As shown in Table 2, about 80 % of the wheat-specific bands but only 35 % of the rye-specific bands were retained in triticale and on average, 65 % of the rye bands were lost in triticale. It seems clear that, to be accommodated in a triticale background, the rye genome has undergone a much higher degree of genome adjustment than the wheat genome.
|
This high degree of directional genomic sequence changes in triticale is different from that reported in the wheat genome complex where specific sequence losses occurred about evenly from both parents (Feldman et al., 1997; Liu et al., 1998a, b; Ozkan et al., 2001). Nuclear–cytoplasmic interaction might explain the high degree of rye genomic changes observed in triticale. Since rye–wheat hybrids (i.e. rye used as the maternal parent) are extremely rare and unstable, all existing triticales have been derived from wheat–rye hybridization, which contain wheat cytoplasm. Gill (1991) hypothesized that the paternal genome may be more vulnerable to change in a newly formed hybrid, because it is exposed to the ‘hostile’ environment of maternal cytoplasm. Cytoplasm-caused directional sequence changes were clearly illustrated in Brassica when reciprocal inter-specific crosses were studied (Song et al., 1995).
In addition, since triticale comes from the hybridization between polyploid wheat and diploid rye, the wheat genome may be more adapted in a polyploid condition than the rye genome because the wheat genome has already experienced genetic and epigenetic changes during its allopolyploid evolution. This may, in part, explain why the changes in the wheat genome are less than in the rye genome in triticale.
Another notable difference was that the total amount of parental genome variation in triticale was much higher than that reported in the wheat complex, which could be due to the fact that the joined parental genomes of triticale are more distinctly related than those in wheat. It is plausible to speculate that hybrids between more distinctly related genomes would encounter a higher degree of evolutionary accommodation in order to achieve a balanced status (see also Song et al., 1995). It was also evident that, when a band was present in both wheat and rye parents, the frequency of that band being conserved in triticale was much higher than if it appeared in only one parent (Tables 1 and 2). Therefore, allopolyploids derived from closely related inter-specific crosses would be more likely to show small genome changes since their parents would share a higher percentage of common sequences.
Ploidy level effects: hexaploids vs. octoploids
Ploidy level was also shown to play a significant role in the extent of genomic changes in triticale. The relative frequency of sequence changes was similar within the same ploidy level, but significantly different between ploidy levels (Ma et al., 2002, 2004; Ma and Gustafson, 2006). Octoploid triticales (AABBDDRR) were more stable than hexaploid triticales (AABBRR). On average, about 30 % and 40 % of the parental bands were lost in octoploid and hexaploid triticales, respectively. The mechanism underlying this difference was not clear, but it could relate to the ratio of parental genome constitutions. The rye genome accounts for one-third of the triticale genome in hexaploid triticale, but it is only one-quarter of the triticale genome in octoploid triticale. Since the rye genome was more vulnerable to change, as discussed above, the higher ratio of rye genome content could increase overall genome instability in hexaploid triticale compared with octoploid triticale. A 9 % DNA content decrease was noted in octoploid triticale, but up to 28–30 % decrease was noted in hexaploid triticales (Boyko et al., 1984). This demonstrated the significant role of ploidy effects, and also implied that band losses mainly resulted from DNA content decrease or sequence elimination during the course of triticale formation.
There are few reports of ploidy level effects during allopolyploidization in other species because most of these studies have been implemented at the same ploidy level. The studies in the wheat complex included polyploidy levels from 4x to 8x, but there were no obvious differences in the overall genomic changes between different polyploidy levels (Ozkan et al., 2001).
Sequence type effects: repetitive vs. low-copy and coding sequences
The rate of genomic sequence changes among various DNA sequence types was also very different (Ma et al., 2002, 2004; Ma and Gustafson, 2006). Tentative repetitive sequences always underwent more extensive changes than tentative low-copy sequences, which were higher than coding sequences (Table 2). The pooled data from Table 2 indicate about 42 %, 31 % and 22 % of the bands were lost from tentative repetitive, tentative low-copy and coding sequences, respectively. This trend of sequence conservation suggests that fitness changes are more likely to occur in highly repetitive sequences. These differences may be driven by evolutionary forces, which select against potential detrimental changes in coding sequences, but are highly tolerant to changes in non-coding, repetitive sequences.
Sequence type effects were even more obvious when different ploidy levels and parental types were considered (Ma et al., 2002, 2004; Ma and Gustafson, 2006). For example, in hexaploid triticale, the percentage of wheat-specific bands maintained in triticale varied depending on sequence type (repetitive = 54·3 %, low-copy = 84·8 % and coding = 96·0 %; Table 1). In contrast, the percentage of rye-specific bands conserved in triticale ranged only 30–38 % and were not markedly affected by sequence type or ploidy level (i.e. hexaploid or octoploid).
|
TIME COURSE OF THE GENOMIC SEQUENCE CHANGES |
|---|
The time course of genomic sequence changes was investigated using re-synthesized triticales by crossing the exact same inbred wheat and rye parental lines as the existing triticales (Ma and Gustafson, 2006). The hybrids (F1) before chromosome doubling and three to five generations after chromosome doubling were obtained and used to study early genetic events during the course of triticale development with a subset of AFLP primers from the above studies to detect the amount of genome variation occurring before and after chromosome doubling (Ma et al., 2002, 2004; Ma and Gustafson, 2006). Most of the variation accumulated in existing triticales had already occurred in the F1 hybrids, indicating an immediate and dramatic response to the inter-generic crosses. Additional changes after chromosome doubling were relatively small and levelled off after several generations (Ma and Gustafson, 2006).
Changes in hybrid vs. triticale
The genomic sequence changes detected before and after chromosome doubling were re-formatted in Table 3 using data taken from Ma and Gustafson (2006). It was clear that different parental sequence types and ploidy levels played a role in determining the genomic sequence changes which occurred in the hybrids and existing triticales.
|
In the hybrids, differences were noted between the changes in the wheat-specific and rye-specific bands. The majority of wheat-specific bands lost in triticale were still present in the F1 hybrids. For the tentative repetitive sequences only about 10 % (9·4 % + 0·5 %, octoploid) and 22 % (19·9 % + 2·8 %, hexaploid) of the total wheat-specific bands were lost in the F1 hybrid. For tentative low-copy sequences even fewer bands were lost with only 3 % (1·7 % + 1·2 %) and 8 % (4·7 % + 2·8 %) of the total wheat-specific bands lost in octoploid and hexaploid F1 hybrids, respectively (Table 3).
However, for rye-specific bands, most were lost in the F1 hybrids, before chromosome doubling (Ma and Gustafson, 2006). The frequencies of changes in the F1 hybrids were very high, but at a similar level for different ploidy and/or sequence types, ranging from 45 % to 50 % of all rye-specific bands (Table 3). The data clearly indicate that the rye genome responds more extensively than the wheat genome to wide hybridization.
As expected, when a band was shared by both wheat and rye parents, the ratio of band losses in the hybrids was very low, about 5–10 % and 2–3 % of the total bands scored from repetitive and low-copy sequences, respectively. In all cases, there were always a few parental bands which were lost in the F1 hybrids, but re-appeared in the existing triticales, implying either epigenetic modifications or different changing events between the existing and the re-synthesized triticales. Moreover, band losses in the hybrids were generally more extensive in repetitive compared with low-copy sequences. Rapid and extensive changes in repetitive sequences may facilitate the overall compatibility between wheat and rye genomes in triticale (Ma and Gustafson, 2006).
Changes in different generations
Genomic changes following chromosome doubling were very small and appeared to be gradual (Ma and Gustafson, 2006). This process was hardly detected in the wheat parental genome because changes in wheat-specific bands were very rare after chromosome doubling (Ma et al., 2002, 2004; Ma and Gustafson, 2006). However, additional variation, mainly loss of rye-specific bands was detectable in the early-generations of triticales following chromosome doubling (Ma and Gustafson, 2006).
The generation series involving the newly created triticale lines provided a clear picture with similar tendencies of genomic sequence changes for EcoRI–MseI and PstI–MseI primers in all four sets of triticale lineages studied (Ma and Gustafson, 2006). In this review, only data from the ‘Chinese Spring’ x ‘Imperial’ lineage are discussed because it is the only hybrid selfed up to five generations after chromosome doubling. The EcoRI–MseI and PstI–MseI data were pooled for each generation of the ‘Chinese Spring’ x ‘Imperial’ lines and plotted in Fig. 2.
|
The data show that the proportion of lost bands increased in the first five generations, reaching the highest level at the C5 generation, which explained 8·1 % of the total rye band losses accumulated in existing triticale. All together, the first five generations following chromosome doubling accounted for 17·4 % of the total band losses (Fig. 2). The remaining 14 % represented the accumulated losses of more than 30 generations after C5 (Ma and Gustafson, 2006). The data imply that the amount of genomic change following chromosome doubling reached its highest point at C5, or soon after, and then levelled off. This observation is unexpected as we speculated that the greatest amount of genome change after chromosome doubling would occur in the first allopolyploid generation after chromosome doubling (Ma and Gustafson, 2006). The reason for this unexpected tendency in early generations is not clear.
A similar tendency of genomic changes was also seen in re-synthesized Brassica napus (Lukens et al., 2006; Gaeta et al., 2007). The studies only detected rare genetic changes in the first generation (S0), but these became much more frequent in the S5 generation (Lukens et al., 2006; Gaeta et al., 2007). Cytosine methylation changes were observed to be frequent in S0 and most of the S0 methylation status remained fixed in their S5 progeny, although some reversions and new methylation patterns were also observed (Gaeta et al., 2007). It is noted that the S5 changes detected by Gaeta et al. (2007) might involve accumulated changes of several early generations. The study also indicated that the genetic changes in Brassica were mainly due to homoeologous nonreciprocal transpositions because DNA fragment losses often occurred at linked marker loci, and most fragment losses co-occurred with intensification of signal from homoeologous markers (Gaeta et al., 2007). However, in triticale, the band loss was rarely associated with band intensification, and the overall frequency of losing bands were much higher than gaining novel bands.
Time courses of genomic sequence changes were also studied in the wheat complex for natural and non-natural occurring allopolyploid combinations (Ozkan et al., 2001). Here it was found that the pattern, rate and time of elimination of various chromosome and genome-specific sequences were affected by the genomic combination of the allopolyploid, with rapid elimination occurring in combinations that existed in nature (Ozkan et al., 2001). The rapidity of processes in natural allopolyploid combinations may facilitate their successful establishment. Triticale is a man-made species, although natural wheat–rye hybridizations have been reported. However, the overall genomic changes are very large and occurred very rapidly, indicating a highly imbalanced state of the combined wheat and rye genomes in triticale.
|
GENE EXPRESSION CHANGES IN TRITICALE |
|---|
Overall, we conclude that a large degree of non-additive genomic sequence changes have occurred during the course of triticale evolution. However, how gene expression has been affected is still elusive. Due to its high genome complexity, molecular studies on gene expression lag behind other allopolyploid model species, but changes in gene expression in triticale, compared with parents, have been reported (Lacadena et al., 1984; Somers and Gustafson, 1994; Gustafson and Flavell, 1996; Viegas et al., 1996; Houchins et al., 1997; Neves et al., 1997; Rozynek et al., 1998; Voylokov and Tikhenko, 2002; Leonova et al., 2005). Studies showing variations in cDNA-probed RFLP banding profiles also imply changes in gene expression (Tables 1 and 2). A very high level of expressed sequence changes was also reported in the early generation of an octoploid triticale (Han et al., 2003). Gene expression changes induced by allopolyploidization have been widely observed in other species (Chen, 2007). It is not surprising that gene expression changes are often associated with other genetic events, including sequence deletion, interchromosomal exchanges and rearrangements, and transposon activation; thus, extensive genomic banding variation will undoubtedly affect parental gene expression in allopolyploid triticale. It is possible that changes in gene expression may lead to increased fitness and the successful establishment of the triticale genome.
|
NON-ADDITIVE AND NON-RANDOM GENOME CHANGES AND MECHANISMS OF ALLOPOLYPLOIDIZATION |
|---|
Non-additive phenomena and non-random genome changes have been widely observed in allopolyploids (Liu and Wendel, 2002; Feldman and Levy, 2005) and these changes have shaped the evolutionary processes of allopolyploids. As discussed, the triticale genome has undergone a remarkable degree of non-additive sequence changes which are non-random, but are a function of the relationship between the parental genomes, ploidy level and sequence type. A typical observation of the non-random changes in triticale was the large number of bands lost from the rye parental genome. Independent occurrences of losing the same bands were observed among three sister lines of each generation of newly synthesized triticale lineages (Ma and Gustafson, 2006), indicating at least some of these events were non-random. Band loss or sequence elimination is believed to be a major evolutionary force driving the successful establishment of allopolyploid wheat (Feldman and Levy, 2005) and agrees with studies on C-values of polyploids showing that genome downsizing, or loss of DNA following polyploidization, might be a widespread phenomenon shaping allopolyploids (Leitch and Bennett, 2004). Indeed polyploidy and segmental duplication followed by gene loss are likely to have occurred extensively during the evolution of all flowering plants (Bennetzen, 2007).
Low-copy sequence elimination has been well studied in newly synthesized wheat allopolyploids (Feldman and Levy, 2005) and there are now reports of repetitive sequence elimination in allopolyploids. For example, studies in wheat (Han et al., 2005) and tobacco (Skalicka et al., 2005) have shown that copies of certain repeats were eliminated rapidly and preferentially in a genome-specific manner. The elimination process was reproducible and continuously targeted the same repeat sequence in several consecutive generations (Han et al., 2005). It was also observed that elimination of the same repeat sequence was reproducible among different individuals derived from a single cross (Skalicka et al., 2005) or even among different allopolyploids synthesized from different parental species (Han et al., 2005). More importantly, at least some (Skalicka et al., 2005) or all (Han et al., 2005) of the genome changes showed concordance with changes that presumably occurred during evolution of their natural counterparts, indicating non-random, selective elimination of the repeats.
Chromosomal translocations and nonreciprocal transpositions are believed to be a major cause of genomic sequence changes in Tragopogon miscellus and Brassica napus (Song et al., 1995; Tate et al., 2006; Gaeta et al., 2007). It was suggested that exchanges among homoeologous chromosomes were a major mechanism in creating novel allele combinations and phenotypic variation in newly formed B. napus polyploids (Gaeta et al., 2007). Recent comparative genomics studies have uncovered an even higher level of genomic rearrangement than originally observed in grass species (Bennetzen, 2007). Small rearrangements (mostly tiny deletions), which are caused by illegitimate recombination, are exceedingly abundant in grasses (Bennetzen, 2007). Transposon activity has also played a significant role in plant speciation (Chen, 2007; Bennetzen, 2007), and their role in polyploid evolution is also suggested from studies by Kashkush et al. (2003). They showed that allopolyploidization in wheat lead to activation of retroelements resulting in changes in gene expression. In triticale, disappearance of retrotransposon sequences has also been reported (Han et al., 2003).
Epigenetic changes are widely observed in newly created allopolyploids and are the major phenomena observed in cotton and arabidopsis allopolyploids (Adams et al., 2003; Wang et al., 2006). The current research did not provide direct data supporting epigenetic changes, but an earlier study showed that the wheat genome composition did change rye gene expression in triticale (Houchins et al., 1997).
|
CONCLUSIONS AND PERSPECTIVES |
|---|
Overall, significant genomic sequence changes have been detected in triticales and the extent of these changes is much greater than that observed in any other allopolyploid species studied. The genomic changes in triticale are mainly observed as AFLP and RFLP band losses in the F1 hybrids, with most losses occurring from the rye genome. The frequency of band losses in hexaploid triticales is much higher than that in octoploid triticale; and it is also higher in tentative repetitive sequences than in low-copy sequences. These observations, together with the reported genome size decrease (Boyko et al., 1984), suggests that rapid and extensive sequence elimination is a major process involved in the evolution of triticale.
Although a large-scale genomic profile study has been initiated in triticale, more molecular work is needed to uncover genetic and epigenetic events during triticale formation. Understanding the nature, extent and consequences of gene expression changes and epigenetic modifications are worthy goals to increase understanding into the evolutionary process involved in generating allopolyploids.
|
FOOTNOTES |
|---|
Present address: Ceres Inc., Thousand Oaks, CA 91320, USA. 
|
LITERATURE CITED |
|---|
-
Adams KL, Wendel JF. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology (2005) 8:135–141.[CrossRef][Web of Science][Medline]
Adams KL, Cronn R, Percifield R, Wendel JF. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. In: Proceedings of the National Academy of Sciences of the USA (2003) 100:4649–4654.
Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature (2000) 408:796–815.[CrossRef][Medline]
Bennetzen JL. Patterns in grass genome evolution. Current Opinion in Plant Biology (2007) 10:176–181.[CrossRef][Web of Science][Medline]
Boyko EV, Badaev NS, Maximov NG, Zelenin AV. Does DNA content change in the course of triticale breeding? Cereal Research Communications (1984) 12:99–100.[Web of Science]
Chen ZJ. Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annual Review of Plant Biology (2007) 58:377–406.[CrossRef][Medline]
Comai L. Genetic and epigenetic interactions in allopolyploid plants. Plant Molecular Biology (2000) 43:387–399.[CrossRef][Web of Science][Medline]
Comai L. The advantages and disadvantages of being polyploidy. Nature Reviews Genetics (2005) 6:836–846.[CrossRef][Web of Science][Medline]
Cui L, Wall PK, Leebens-Mack JH, Lindsay BG, Soltis DE, Doyle JJ, et al. Widespread genome duplications throughout the history of flowering plants. Genome Research (2006) 16:738–749.
De Bodt S, Maere S, de Peer YV. Genome duplication and the origin of angiosperms. Trends in Ecology and Evolution (2005) 20:591–597.[CrossRef]
Feldman M, Levy AA. Allopolyploidy – a shaping force in the evolution of wheat genomes. Cytogenetic and Genome Research (2005) 109:250–258.[CrossRef][Web of Science][Medline]
Feldman M, Liu B, Segal G, Abbo S, Levy AA, Vega JM. Rapid elimination of low-copy DNA sequences in polyploid wheat: a possible mechanism for differentiation of homoeologous chromosomes. Genetics (1997) 147:1381–1387.[Abstract]
Finnegan EJ, Genger RK, Peacock WJ, Dennis ES. DNA methylation in plants. Annual Review of Plant Physiology and Plant Molecular Biology (1998) 49:223–247.[CrossRef][Web of Science]
Gaeta RT, Pires JC, Iniguez-Luy F, Leon E, Osborn TC. Genomic changes in resynthesized Brassica napus and their effect on gene expression and phenotype. Plant Cell Preview (2007) 10·1105/tpc.107·054346.
Gaut BS. Patterns of chromosomal duplication in maize and their implications for comparative maps of the grasses. Genome Research (2001) 11:55–66.
Gill BS. Nucleocytoplasmic interaction (NCI) hypothesis of genome evolution and speciation in polyploid plants. In: Proceedings of the Kihara Memorial International Symposium on Cytoplasmic Engineering in Wheat.—Sasakurma T, ed. (1991) Yokohama, Japan. 48–53.
Grant D, Cregan P, Shoemaker RC. Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. In: Proceedings of the National Academy of Sciences of the USA (2000) 97:4168–4173.
Gruenbaum Y, Naveh-Many T, Cedar H, Razin A. Sequence specificity of methylation in higher plant DNA. Nature (1981) 292:860–862.[CrossRef][Medline]
Gustafson JP, Flavell RB. Control of nucleolar expression in triticale. In: Triticale: today and tomorrow.—Guedes-Pinto H, et al, eds. (1996) Dordrecht, The Netherlands: Kluwer Academic Publisher. 119–126.
Guyot R, Keller B. Ancestral genome duplication in rice. Genome (2004) 47:610–614.[Medline]
Han F, Fedak G, Guo W, Liu B. Rapid and repeatable elimination of a parental genome-specific DNA repeat (pGc1R-1a) in newly synthesized wheat allopolyploids. Genetics (2005) 170:1239–1245.
Han FP, Fedak G, Ouellet T, Liu B. Rapid genomic changes in interspecific and intergeneric hybrids and allopolyploids of Triticeae. Genome (2003) 46:716–723.[Medline]
Houchins K, O'Dell M, Flavell RB, Gustafson JP. Cytosine methylation and nucleolar dominance in cereal hybrids. Molecular and General Genetics (1997) 255:294–301.[CrossRef]
Kashkush K, Feldman M, Levy AA. Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nature Genetics (2003) 33:102–106.[CrossRef][Web of Science][Medline]
Lacadena JR, Cermeno MC, Orellana J, Santos JL. Evidence for wheat-rye molecular competition (amphiplasty) in triticale by silver staining procedure. Theoretical and Applied Genetics (1984) 67:207–213.[CrossRef][Web of Science]
Leitch IJ, Bennett MD. Genome downsizing in polyploid plants. Biological Journal of the Linnean Society (2004) 82:651–663.[CrossRef][Web of Science]
Leonova IN, Dobrovol'skaia OB, Kminskaia LN, Adogina IG, Koren' LV, Khotyleva LV, et al. Molecular analysis of the triticale lines with different Vrn gene systems using microsatellite markers and hybridization in situ. Genetika (2005) 41:1236–43.[Medline]
Liu B, Wendel JF. Non-Mendelian phenomena in allopolyploid genome evolution. Current Genomics (2002) 3:489–505.[CrossRef]
Liu B, Vega MJ, Feldman M. Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. II. Changes in low-copy coding DNA sequences. Genome (1998) a 41:535–542.[Medline]
Liu B, Vega JM, Segal G, Abbo S, Rodova M, Feldman M. Rapid genomic changes in newly synthesized amphiploids of Triticum and Aegilops. I. Changes in low-copy noncoding DNA sequences. Genome (1998) b 41:272–277.
Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T. Patterns of sequence loss and cytosine methylation within a population of newly resynthesized Brassica napus allopolyploids. Plant Physiology (2006) 140:336–348.
Ma X-F, Gustafson JP. Genome evolution of allopolyploids: a process of cytological and genetic diploidization. Cytogenetic and Genome Research (2005) 109:236–249.[CrossRef][Web of Science][Medline]
Ma X-F, Gustafson JP. Timing and rate of genome variation in triticale following allopolyploidization. Genome (2006) 49:950–958.[Medline]
Ma X-F, Rodriguez Milla MA, Gustafson JP. AFLP-based genome studies of triticale following polyploidization. In: Proceedings of the 5th International Triticale Symposium—Aniol A, et al, eds. (2002) Vol. 1. Radzików, Poland. 89–94.
Ma X-F, Fang P, Gustafson JP. Polyploidization-induced genome variation in triticale. Genome (2004) 47:839–848.[Medline]
Meister GK. Natural hybridization of wheat and rye in Russia. Journal of Heredity (1921) 12:467–470.
Neves N, Silva M, Heslop-Harrison JS, Viegas W. Nucleolar dominance in triticales: control by unlinked genes. Chromosome Research (1997) 5:125–131.[CrossRef][Web of Science][Medline]
Ozkan H, Levy AA, Feldman M. Allopolyploidy-induced rapid genome evolution in the wheat (Aegilops-Triticum) group. The Plant Cell (2001) 13:1735–1747.
Paterson AH, Bowers JE, Chapman BA. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. In: Proceedings of the National Academy of Sciences of the USA (2004) 101:9903–9908.
Paun O, Fay MF, Soltis DE, Chase MW. Genetic and epigenetic alterations after hybridization and genome doubling. Taxon (2007) 56:649–656.[Web of Science]
Rodriguez Milla MA, Gustafson JP. Genetic and physical characterization of the chromosome 4DL in wheat. Genome (2001) 44:883–892.[Medline]
Rozynek B, Guenther T, Hesemann CU. Gel electrophoretic investigations of prolamins in eu- and alloplasmatic octoploid primary triticale forms. Theoretical and Applied Genetics (1998) 96:46–51.[CrossRef][Web of Science]
Shaked H, Kashkush K, Ozkan H, Feldman M, Levy AA. Sequence elimination and cytosine methylation are rapid and reproducible responses of the genome to wide hybridization and allopolyploidy in wheat. The Plant Cell (2001) 13:1749–1759.
Skalicka K, Lim KY, Matyasek R, Matzke M, Leitch AR, Kovarik A. Preferential elimination of repeated DNA sequences from the paternal, Nicotiana tomentosiformis genome donor of a synthetic, allotetraploid tobacco. New Phytologist (2005) 166:291–303.[CrossRef][Web of Science][Medline]
Somers DJ, Gustafson JP. A review of wheat/rye genomic interactions and gene expression in triticale. Genetics (Life Science Advances) (1994) 13:57–63.
Song K, Lu P, Tang K, Osborn TC. Rapid genome change in synthetic polyploids of Brassica and its implications for polyploid evolution. In: Proceedings of the National Academy of Sciences of the USA (1995) 92:7719–7723.
Tate JA, Ni Z, Scheen A-C, Koh J, Gilbert CA, Lefkowitz D, et al. Evolution and expression of homeologous loci in Tragopogon miscellus (Asteraceae), a recent and reciprocally formed allopolyploid. Genetics (2006) 173:1599–1611.
Viegas W, Silva M, Neves N, Castilho A, Barao A, Queiroz A, et al. Expression of 1R rRNA loci in triticale: genetic and developmental controls. In: Triticale: today and tomorrow.—Guedes-Pinto H, et al, eds. (1996) Dordrecht The Netherlands: Kluwer Academic Publisher. 127–134.
Voylokov V, Tikhenko ND. Triticale as a model for study of genome interaction and genome evolution in allopolyploid plants. In: Proceedings of the 5th International Triticale Symposium—Aniol A, et al, eds. (2002) Vol. 1. Radzików, Poland. 63–70.
Wang J, Tian L, Lee H-S, Wei NE, Jiang H, Watson B, et al. Genomewide non-additive gene regulation in Arabidopsis allotetraploids. Genetics (2006) 172:507–517.
Wendel JF. Genome evolution in polyploids. Plant Molecular Biology (2000) 42:225–249.[CrossRef][Web of Science][Medline]
Wilson AS. Wheat and rye hybrids. Edinburgh Botanical Society Transactions (1876) 12:286–288.
Wolfe KH. Yesterday's polyploids and the mystery of polyploidization. Nature Reviews Genetics (2001) 2:333–341.[CrossRef][Web of Science][Medline]
Young WP, Schupp JM, Keim P. DNA methylation and AFLP marker distribution in the soybean genome. Theoretical and Applied Genetetics (1999) 99:785–792.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
Related articles in Ann Bot:
- ContentSnapshots
Ann Bot 2008 101: NP.[Extract] [Full Text]
This article has been cited by other articles:
|
|
 |
|
  N. Ishikawa, J. Yokoyama, and H. Tsukaya Molecular evidence of reticulate evolution in the subgenus Plantago (Plantaginaceae) Am. J. Botany, September 1, 2009; 96(9): 1627 - 1635. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 I. J. Leitch and M. F. Fay Plant Genome Horizons: Michael Bennett's Contribution to Genome Research Ann. Bot., April 1, 2008; 101(6): 737 - 746. [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||