The Impact of Polyploidy on Grass Genome Evolution
Year: 2002
Type: review
Abstract: Polyploidy is an evolutionary process whereby two or more genomes are brought together into the same nucleus, usually by hybridization followed by chromosome doubling. As a result, the new polyploid is genetically isolated from its diploid progenitor(s) and a new species is formed. The importance of polyploidy was recognized early in the 20th century and for the past decades many studies have addressed the different categories of polyploids, their mode of formation, their cytogenetic behavior, the ecological implications, the impact of polyploidy on various population genetics aspects such as heterozygosity, mating mode, buffering of mutations, etc. (Stebbins, 1950, 1971). In the past few years, molecular and computational tools have provided new ways to probe the history of genomes, leading to the discovery that polyploidy is even more widespread than previously thought. The once controversial proposal that evolution moves forward through whole genome duplication (Ohno, 1970) is gaining recognition thanks to sequence analysis that is more sensitive than the traditional methods (chromosome counting, analysis of meiotic chromosome pairing, and marker-based mapping) that have been used to assess polyploidy. Accumulating evidence shows that genome duplications occurred in the lineage of all vertebrates (Wolfe, 2001, and refs. therein), including humans (Homo sapiens), whose genome might have been shaped by two rounds of duplication, suggesting octopolyploidy. Recent studies provide strong indications that even yeast (Saccharomyces cerevisiae), with its compact genome, is in fact an ancient tetraploid (Wong et al., 2002). In plants, polyploidy was proposed to have occurred in the lineage of at least 70% of angiosperms (Masterson, 1994) and in 95% of pteridophytes (Grant, 1981). Moreover, the first two species whose genomes have been fully sequenced, Arabidopsis (Arabidopsis Genome Initiative, 2000) and rice (Oryza sativa; Goff et al., 2002), were chosen principally because of their small genome. Therefore, it came as a surprise when sequence analysis revealed that these particular species, considered as classical diploids, are apparently ancient polyploids (paleopolyploids).Paleopolyploids are ancient polyploids which have a disomic inheritance and whose progenitors cannot be identified by cytological tools or DNA markers. Paleopolyploidy is detected by rather sophisticated bioinformatics tools that reveal similarity and colinearity between genes which diverged tens of millions of years ago (see Gaut, 2001 as example). If these minigenome “diploids” are in fact paleopolyploids, then it is reasonable to assume that many more, if not all, higher plant species, considered as diploids because of their genetic and cytogenetic behavior, are ancient polyploids that underwent a process of extensive diploidization. Thus, polyploidy is one of the major processes that has driven and shaped the evolution of higher organisms. The ubiquitous role of genome duplication in evolution is one of the important discoveries from the post-genomic era, explaining the renewed interest in polyploidy. Several reviews have been written recently on polyploidy in plants, covering various aspects such as the impact of polyploidy on speciation, genome structure, and gene expression (Leitch and Bennett, 1997; Comai, 2000;Soltis and Soltis, 2000; Wendel, 2000;Pikaard, 2001). This review will focus mainly on the effect of polyploidy on genome evolution in grasses—a family that has contributed some of the best models to the study of polyploidy. It will review the accumulating evidence of polyploidy as a trigger and/or facilitator for accelerated genome evolution in this family. Overall, we will try to learn from the grasses the causes for the formidable evolutionary success of polyploidy in nature. The grass family, Poaceae (=Gramineae) is one of the largest families of flowering plants, including approximately 10,000 species classified into 600 to 700 genera that diverged from an ancestral progenitor 50 to 70 million years ago (mya; Kellogg, 2001; Huang et al., 2002). As discussed below, most, if not all, grasses are polyploids; all major types of polyploids, namely autopolyploids, segmental allopolyploids, and allopolyploids, can be found in this family. Autopolyploids contain multiple sets (>2) of the same or similar genomes in their nucleus. They originated mostly from intraspecific crosses followed by chromosome doubling because of unreduced gametes and their chromosomes may form multivalents during meiosis and exhibit a multisomic inheritance. One advantage of autopolyploidy is the capacity to maintain high levels of heterozygosity, with multiple alleles per locus, or more rarely, to reach homozygosity with multiple dosage of a given allele. On the other hand, the formation of multivalents during meiosis is often associated with sterility. Therefore, it is not surprising that many autopolyploids are perennial species that also propagate vegetatively. Segmental allopolyploids contain both homologous and homoeologous chromosomal segments and, therefore, exhibit both bivalents and multivalents during meiosis. As a result, they have a mixed disomic/polysomic inheritance. Allopolyploids (or amphiploids) contain two or more diverged—homoeologous— genomes. They were derived from interspecific or intergeneric hybridization between species with diverged genomes. The resulting hybrid is sterile but fertility is obtained after chromosome doubling. Allopolyploids are characterized by bivalent pairing, full fertility, and disomic inheritance. Most allopolyploid grasses are annual species. Allopolyploidy enables the permanent fixing of heterozygosity between homoeoalleles, even in self-pollinating species. Grass crops such as wheat (Triticum spp.), maize (Zea mays), and rice are well-studied genetic systems, each corresponding to a prototype polyploid (allopolyploid, segmental allopolyploid, and paleopolyploid, respectively); all types of synthetic polyploids can be readily made, enabling one to mimic and study the genetic and epigenetic events that occurred early on at the onset of polyploidy. All the above makes grasses one of the best systems to study polyploidy. Most, if not all, grasses are polyploids: Based on the assumption that all genera and families, which have a basic chromosome number of x = 12, are derivatives of lines that underwent genome duplication at some time during their evolutionary history (Stebbins, 1971), and because all the primitive grass subfamilies, namely Anomochlooideae, Pharoideae, and Puelioideae (Grass Phylogeny Working Group, http://www.ftg.fiu.edu/grass/gpwg/) have a basic chromosome number of x = 12, this would imply that the ancestor of the grasses was itself a polyploid. In accordance, all the diploid Poaceae species would be paleopolyploids. The family also contains a large number of species (>60%), distributed in all the clades, that are classified as polyploids (Goldblatt, 1980), i.e. based on the above hypothesis, underwent an additional cycle of chromosome doubling (neopolyploids). In these species, the duplicated genomes did not diverge much from their “diploid” progenitors and chromosome number and cytological behavior are still indicative of genome duplication. Most of these neopolyploids (>65%) were derived from distant interspecific or intergeneric hybridizations, giving rise to new allopolyploid species and the remaining derived from intraspecific or close interspecific hybridizations giving rise to new autopolyploid cytotypes (Stebbins, 1971). Prototype polyploid grasses are as follows. Bread wheat (Triticum aestivum) represents one of the best-characterized examples of evolution through allopolyploidy. It is an allohexaploid (genome BBAADD) containingn = 21 chromosomes that arose from hybridization, followed by chromosome doubling, between a tetraploid (genome BBAA,n = 14) and a diploid (genome DD, n = 7) species about 9,500 callibrated years ago (Feldman, 2001). Two of its three diploid progenitors have been identified: Triticum urartu (genome AA) and Aegilops tauschii (genome DD) (Feldman, 2001). The origin of the B genome remains elusive. The diploid species whose genome is the closest to the B genome is Aegilops speltoides. In a pioneering tour de force, Sears (1954) classified the 21 pairs of bread wheat chromosomes into seven homoeologous groups based on the ability of a tetrasome (four doses of a given chromosome) to compensate for the absence of each of the other two chromosomes of the same group. This work was the first evidence for syntenic relationships among the grass genomes. Despite their genetic relatedness, homoeologous wheat chromosomes do not pair under normal conditions. However, in the absence of the homoeologous pairing suppressor genePh1, pairing and recombination between homoeologs can occur (Sears, 1976). Suppressing inter-genomic pairing is important in maintaining the disomic inheritance and, as a consequence, the fertility of wheat, as well as facilitating permanent heterozygosity between homoeoalleles. Maize is thought to be an ancient segmental allotetraploid (Gaut and Doebley, 1997). The evidence for this is based on chromosome number and molecular analysis: Maize has n = 10 chromosomes, compared with n = 5 for species in its tribe (Andropogoneae). Moreover, sequence analysis of 14 pairs of duplicated genes revealed two sets of gene pairs: those that diverged approximately 20 mya and those that diverged approximately 11 mya. A likely explanation for such data is a segmental allotetraploid origin, whereby some chromosomes did not recombine in the early stages of polyploidy and duplicated sequences on these chromosomal segments have the age of the common ancestor (approximately 20 mya), whereas on chromosomes that did recombine, the duplicated sequences have the age of the polyploid formation (approximately 11 mya). This analysis has been extended to a large number of loci (from the UMC98 map) using new computational approaches (Gaut, 2001). It reveals that up to 80% of the maize genome remains organized in colinear regions. Rice is the best characterized paleopolyploid in the grasses (Goff et al., 2002): >2,000 duplicated cDNAs were plotted by chromosomal regions and the extent of genome duplications were defined. This analysis showed that, with the exception of a large segment shared between chromosomes 11 and 12, the duplicated segments were relatively small, suggesting that many translocations had occurred since the original genome duplication event. The rate of amino acid substitution was used to estimate the time that duplicated genes had diverged. A peak of duplication events was found 40 to 50 mya, the putative time of whole genome duplication. Finally, we do not have enough molecular data for other “diploid grasses” but it is likely that sorghum (Sorghum bicolor) and barley (Hordeum vulgare), which have several duplicated loci, might also be paleopolyploids. Polyploidy in grasses as an ongoing process. The estimated number of years (Age) since polyploidy occurred is shown for various grass species. Another recent allopolyploidy event that had dramatic consequences for humankind is the formation of bread wheat (genome BBAADD), approximately 9,500 calibrated years ago. When domesticated tetraploid wheat (genome BBAA) was brought to western Iran, where Ae. tauschii, the diploid donor of the D genome grew, hybridization took place in a farmer's field and gave rise to bread wheat, an allohexaploid that does not exist in the wild. Wild emmer wheat (Triticum turgidum subsp. dicoccoides; genome BBAA), the progenitor of macaroni wheat (Triticum turgidum subsp. durum; genome BBAA), was presumably formed a few hundred thousand years ago, whereas Triticum timopheevii (genome GGAA), another allotetraploid wheat, appeared later, about 50,000 to 300,000 years ago (Mori et al., 1995; Huang et al., 2002). Maize and rice were probably formed approximately 11 mya and approximately 40 to 50 mya ago, respectively, as discussed above. Altogether, these data indicate that polyploidy is an ongoing process that has been occurring millions of years ago and is still occurring now, giving rise to new species at a rapid rate. The fact that polyploidy in the grasses is an ongoing process and is widespread suggests that it may also occur recurrently from independent events. Recent studies indicate that many polyploid taxa are of multiple origin (Soltis and Soltis, 2000, and refs. therein). Such an origin can widen the genetic basis of the polyploid species, promoting its adaptation to a variety of new habitats and increasing its capability to compete successfully with other species. However, the indications for multiple origins of several grass polyploids are not strongly substantiated. In the wheat (Aegilops spp.-Triticum spp.) group, the only allopolyploid species that might have originated from two independent events is Ae. triuncialis (genome UUCC), having one subspecies that contains the U cytoplasm and another that contains the C cytoplasm (Ogihara and Tsunewaki, 1988). Such a polymorphism, however, could also be derived from hybridization between the allopolyploid and the paternal diploid parent of the allopolyploid, now as a female, and introgression of the cytoplasm via backcrossing the triploid hybrid to the allopolyploid. Moreover, there is not sufficient evidence for multiple origin of tetraploid and hexaploid wheat. On the contrary, studies of chloroplast and mitochondrial DNA revealed little, if any, variation in their plastotypes (Miyashita et al., 1994), indicating a single origin of these allopolyploids. It is surprising that despite the sympatric distribution of the diploid parents of polyploid wheat, there exist only a few successful allopolyploidization events. Therefore, it is not clear to what extent multiple independent origins have been a major in the of these under polyploidy. from an ancestral species, which can be diploid or paleopolyploid, species with genomes. In the genome A is to and the chromosomes of A and can still pair in an A and similarity with some chromosomes that can pair and other chromosomes that are more diverged and do not A and B are more distant and, therefore, their chromosome cannot pair and the hybrid is chromosome doubling, and rise to an a segmental allopolyploid, or a allopolyploid, (see for A of genetic and epigenetic occur in the early of the hybrid and/or after chromosome doubling on evolutionary the genomes of the polyploids and the similarity to their diploid progenitors but can still be detected by cytological that at this gene between species is in polyploids that one genome. the of the original genome duplication can be detected only by a sequence the of this new or paleopolyploid, genomes are formed. is the common and process that can rise to a new species in one makes such a process an evolutionary success is that genome doubling is probably a It the of of gene with genome the of multiple and different genomes, and pairing between pairing between The of polyploidy and the fact that it is an ongoing process may that are to with of polyploidy. The new polyploid has to be with enabling it to with the of chromosome doubling, in the early stages of its formation, that it does not have and can compete with its parents as well as other species. review the various genetic and epigenetic events that occur in formed polyploids, some of which may to their evolutionary It was found recently that DNA of DNA sequences in the early stages of polyploidy et al., 1997). work on different interspecific and intergeneric of and between species and Triticum showed that in a as as in the hybrid and/or in the first after chromosome doubling and may up to of the DNA et al., 2001; et al., 2001). This was by different methods hybridization and using DNA with various including and and through with was only from one genome in tetraploid and from two genomes in therefore, one is to the between homoeologous A of this process is the of inter-genomic recombination and, The ability to DNA was with fertility and with the of pairing in the number of a DNA sequence that represents of the Ae. genome, was found in the first of having Ae. as a diploid parent et al., the of the the of in the formed in such as was also in the early stages of allopolyploid formation et al., The of these is not Finally, and in with the above molecular the of was than that for the genomes of its wheat and progenitors et al., 1988). a in DNA was found in the first of several wheat Another that may and, as a consequence, gene expression and chromosome pairing, is the in or new that was found for of the loci et al., 2001). important of rapid to duplicated dosage is through of gene In wheat, inter-genomic as by of was formation of a wheat allohexaploid (genome and was The of the tetraploid genomes. to genes from tetraploid to hexaploid wheat because of a suppressor gene that was to chromosome and Another well-studied of inter-genomic is the of genes in the of the wheat genome. is in this as by of the genes with and by the of et al., 1997). In to inter-genomic dosage for was also in of wheat with doses of to for the chromosome et al., types of dosage can be in polyploids, as by the work of et have the of genes in a maize autopolyploidy of to and found dosage and In a recent analysis of the wheat of a wheat et found that were in one or both diploid progenitors and in the was by gene or gene but not all, of the genes were in the In of new was found in the corresponding to All the above rapid and genetic and epigenetic to polyploidy the of grass genomes. It is to that such is to the of the new species. In to the events that occur at the onset of the formation of the we the polyploid per in the that cannot be at the diploid and, the of genome and (see review by Wendel, and refs. have proposed that polyploidy the and, the of new This proposal has not been in an of the to study events on an evolutionary we a of evidence that this some such as inter-genomic of chromosomal or genes between the genomes, can occur in an allopolyploid inter-genomic translocations were found by in hybridization in allohexaploid and translocations can be species such as the that probably occurred early in the emmer wheat whereas several different translocations have originated in another tetraploid wheat and of the A genome by sequences from the B genome was detected in tetraploid wheat (genome BBAA) using in hybridization et al., The time of such is not The might be inter-genomic or gene between Another of evolution through allopolyploidy is that it enables recombination between genomes that would not occur at the diploid It was shown in tetraploid Aegilops that recombination can occur between homoeologous genomes B and in between that one genome and in the other and and Such a recombination may to the of genomes that cannot be formed at the diploid a diploid genome would be sterile in whereas an is only presumably because of the buffering effect of genome The B genome of wheat is thought to be such a genome (Feldman, 2001). In the of inter-genomic through or to be widespread in grasses and is a of allopolyploids that to their and enables to new genetic that are the of two genomes. Another is evolutionary processes that occur in diploids, such as and mutations, occur at a rate in polyploids compared with their diploid In of this are such as a of because of genetic in the polyploid and data of polyploids to compared with their diploid progenitors (Sears, despite these there is evidence that evolutionary processes are accelerated as a of polyploidy. could also to genetic by the recent in a bread wheat gene et al., however, there is evidence for a as a of polyploidy. in has shown that only a few have occurred since its formation et al., the of in the maize genome is estimated to have occurred during approximately the past mya ago, i.e. approximately mya after maize et al., Finally, of wheat was detected in a wheat polyploid et al., however, this was not associated with a of and Overall, there is a of evidence for an of evolutionary processes such as mutations, and as a of polyploidy. have we from polyploidy in the from the polyploidy is not an of a few species but it is an evolutionary successful by of the grasses from the of their formation to the It has a role in the evolution of the three important wheat, maize and each of which a to study segmental or what are the causes of its One might be the by such as the variety of genetic systems, namely disomic and/or multisomic inheritance with the on or of inter-genomic In to this the polyploid enables through inter-genomic of chromosomal segments and genes in a that could not in a diploid Moreover, an that be is the polyploid enables an of evolutionary processes that are also in diploids, such as mutations, or which may the variation on which can A and not for evolutionary success is that polyploid species to chromosome doubling because they with the rather dramatic event of that cannot we have to assume that there is a process that polyploidy has then there be of this and there will be of gene expression on a by leading to dosage on the other hand, to gene All we about these is that is also do not what the genes are whose or may to an in the polyploid. such as cytological are also in place to disomic chromosome in allopolyploids. have and of DNA a that the between homoeologs and, their of This of also suggests the is and we do not widespread such a is in the Another field of in polyploidy is the study of the of DNA and chromosome of the two genomes that the same nucleus. Finally, it will be of interest to some are successful and are it to the ability to to the of or to a ability between genomes of between it is that makes polyploid species grasses have It will more and new tools to what it the new tools to study polyploidy in grasses are new that provide a the and of duplications Gaut, 2001; et al., 2002). with to between homoeologs and, the types of loci that are by polyploidy are also This provide on an or a of in gene expression in to polyploidy. This may also to the genes in to polyploidy. The sequence of the rice genome, together with an for genome analysis in the will be an for this will also be to study the of genes on the of the genome to polyploidy. Finally, the will be to which of the genetic and epigenetic that occur as a of polyploidy or are In an recently to the and Genome Bennett, and on the DNA of species for which there is on The DNA for diploids is for for and for The in genome is not in with but rather it is than for This suggests that DNA polyploidy is widespread in the grass family. for and and for of the
Source: PLANT PHYSIOLOGY
DOI: 10.1104/pp.015727
Authors: Avraham A. Levy, Moshe Feldman
Institution: Weizmann Institute of Science
Language: English
Subfield: Genetics
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W2160970573