Ancient and recent polyploidy in angiospermsreview
Аннотация: One of the most startling results of recent genomics studies is the near ubiquity of polyploidy – even in organisms not suspected to have undergone genome doubling. The small genome of Arabidopsis may have been derived from three rounds of polyploidization (Vision et al., 2000; Bowers et al., 2003), and most other model plants are either ancient or recent polyploids (Blanc & Wolfe, 2004). Most recently, Oryza has been shown to have an anciently duplicated genome (Paterson et al., 2004; Wang et al., 2005; see also the commentary by Paterson, 2005), and it seems likely that all angiosperms are polyploid – the question is only one of scale. Of course, as stunning as these results are, plant biologists are not totally surprised: they have long recognized the importance of polyploidy as a speciation mechanism (e.g. Stebbins, 1950, 1966; Grant, 1971, 1981). However, the fact that yeast (Wolfe & Schields, 1997) and vertebrates (e.g. Ohno, 1970; Gu et al., 2002; McLysaght et al., 2002; Furlong & Holland, 2004) are also ancient polyploids is a bit more difficult for some to accept. Given the important role that polyploidy plays in plant evolution – and the decades of study devoted to polyploid plants – it seems likely that studies of recent polyploidy in targeted plant groups will provide clues to the causes and consequences of genome duplication. In this issue, Guo et al. (pp. 273–289) address the recurrent formation of polyploid lineages in Achillea, and Skalickáet al. (pp. 291–303) report rapid and repeated changes in genome content in synthetic allotetraploid tobacco. Both processes, (i) multiple origins of a polyploid 'species' from genetically different diploid parent individuals and (ii) rapid genomic change immediately after polyploid formation, may contribute to genetic diversity in polyploid plants, preventing their fate as 'evolutionary dead-ends' (Wagner, 1983). 'Analysis of the complete genome sequences of Arabidopsis and rice is forcing us to accept that probably all angiosperms – and maybe all plants – are polyploid to some extent' Although the mechanisms of polyploid formation are not entirely clear (see Ramsey & Schemske, 1998), the production of unreduced gametes is typically involved. Polyploid species that form through the combined processes of interspecific hybridization and chromosome doubling are considered allopolyploids, and those polyploids that arise within a single species are autopolyploids, which are much less common in nature. Polyploid complexes, such as the Achillea millefolium L. aggregate, may comprise diploid species, diploid hybrids, and auto- and allopolyploids of multiple ploidal levels (Guo et al.). Superimposed on this diversity is the fact that most polyploid species have formed recurrently from genetically distinct diploid progenitors, yielding a potentially large gene pool for the derivative polyploid. Over five decades ago, Ownbey and colleagues (Ownbey, 1950; Ownbey & McCollum, 1953, 1954) suggested that multiple populations of the allotetraploid Tragopogon mirus Ownbey had formed independently from local parental individuals of T. dubius Scop. and T. porrifolius L.; the same was proposed for the allotetraploid T. miscellus Ownbey and its progenitors, T. dubius and T. pratensis L. Ownbey and colleagues used a number of characteristics – morphological and cytogenetic – to infer multiple origins of each of these allotetraploid species. Unfortunately, such morphological and chromosomal signatures of multiple origins are not always evident, and several decades passed before the generality of Ownbey's observations was recognized. Landmark papers by Werth et al. (1985a, 1985b) elegantly used isozyme polymorphisms to document recurrent formation of polyploid species, and since then, increasingly sensitive genetic tools have been applied to polyploid systems to test hypotheses of recurrent formation. Nearly all polyploid species that have been examined using isozyme or DNA markers have formed recurrently, often dozens of times (for example, see reviews of Tragopogon, Soltis et al., 2004; Senecio, Abbott & Lowe, 2004; and the Arctic flora, Brochmann et al., 2004). Traditional models of allopolyploid formation predict a genetically uniform polyploid species that results from the genetic contributions of a single plant of each parental species. This mode of formation, coupled with the perceived buffering capacity of a duplicated genome, caused noted plant evolutionary biologists such as Stebbins and Wagner to consider polyploidy as an evolutionary dead-end: a genetically uniform species could not respond to a changing environment and would therefore face extinction when conditions changed. Current views of polyploid species, however, reveal instead genetic variability both among and, sometimes, within populations, due to the varied contributions of multiple parental individuals. Furthermore, crossing among genetically distinct individuals of separate origin may generate even greater genetic diversity through independent assortment. The result may be a pool of genetically different polyploid individuals that may respond differentially to various selection pressures, providing more opportunities for polyploid species to survive changing environments. Guo et al. present a staggering view of genetic and ploidal diversity in the Achillea millefolium species complex (Asteraceae). Decades of research, tracing back to Ehrendorfer's work in the 1950s, have documented numerous cases of polyploidy (2x–4x–6x–8x) and '… suggest that reticulate evolution is not only involved in recent radiations but must have been active already in the early diversification of Achillea.' Therefore, understanding more recent polyploid radiations, such as the A. millefolium complex, may provide clues as to the processes and conditions that lead to both polyploid formation and persistence across geologic time. In their paper, Guo et al. used AFLP markers to tease apart historical patterns of hybridization and polyploidy in the A. millefolium complex. Hybridization across ploidal levels, the origins of several polyploid species, recurrent formation and patterns of worldwide migration of the complex were all detected with these sensitive markers (as demonstrated in other groups, for example by Hedrén et al., 2001). Although complex, the evolutionary patterns observed for A. millefolium and relatives are similar to those that have been reported for other complexes that have been studied in detail (e.g. Tragopogon, Soltis et al., 2004; Draba and other Arctic species, Brochmann et al., 2004; species of Glycine, Doyle et al., 2004; Veronica, D. Albach, University of Vienna, unpublished). With few exceptions, recurrent formation – resulting in genetically distinct derivative individuals – appears to characterize polyploid species of plants, and of other organisms as well. Views on the stability of the polyploid genome are also changing (see Matzke et al., 1999). Synthetic allotetraploids of Brassica napus L. (Song et al., 1995) and synthetic allopolyploids and diploid F1 hybrids of Aegilops and Triticum (Ozkan et al., 2001; Shaked et al., 2001; reviewed by Levy & Feldman, 2004) exhibited nonrandom genetic changes, including chromosome-specific and genome-specific gains and losses of loci. These genomic changes occurred rapidly, within a few generations of polyploid formation. Likewise, the naturally occurring Nicotiana tabacum L. (tobacco) has undergone genome reorganization (Kenton et al., 1993). However, not all polyploids display genomic rearrangement relative to their diploid progenitors: the recently formed polyploids of Tragopogon (Pires et al., 2004) and Spartina (Baumel et al., 2002) exhibit genome stability, as do older tetraploids in Gossypium (Liu et al., 2001) and Brassica juncea (L.) Czern. (and, interestingly, synthetic B. juncea; Axelsson et al., 2000). The small number of species examined for chromosomal repatterning makes it difficult at present to identify trends and form generalities, and more data are clearly needed. Skalickáet al. used an elegant approach to re-examine genomic rearrangements in tobacco. Although generation of synthetic polyploids of tobacco is difficult, success was obtained in 1973 (see Skalickáet al.) by crossing the parental diploid species N. sylvestris Speg. (maternal) and N. tomentosiformis Goodsp. (paternal), with chromosome doubling occurring in tissue culture, from which a single regenerated plant was obtained (the S0 generation). Repeated selfing of plants from this regenerant resulted in the S4 plants used by Skalickáet al.; these plants represent lines that were produced close to the time of polyploid formation and thus offer the potential to compare immediate genomic consequences of polyploidy with those observed in naturally occurring N. tabacum (Kenton et al., 1993). Repeated sequences derived from N. tomentosiformis (the paternal parent) were selectively eliminated from the synthetic S4 tobacco tetraploids. Furthermore, intergenomic translocation has occurred subsequent to polyploid formation. Both this translocation and the loss of N. tomentosiformis loci in these synthetic plants are similar to observations of natural tobacco, which exhibits an intergenomic translocation similar to that reported for the synthetics (along with several others; Kenton et al., 1993; Kitamura et al., 1997) and which showed less similarity to its paternal parent, N. tomentosiformis, than to the maternal parent, N. sylvestris, in Genome In Situ Hybridization studies (Kenton et al., 1993; Jakowitsch et al., 1998). These results demonstrate the remarkable facts that (i) genomic changes may occur very early – within the first few generations – in a polyploid lineage (as shown for B. napus, Aegilops, and wheat), and (ii) at least some of these genomic changes are repeatable, that is, they occurred in both synthetic and natural polyploid derivatives. Understanding the 'rules' of genetic and genomic change in polyploids is one of the next great frontiers in the study of polyploidy. The last five years have witnessed a reawakening in the study of polyploidy. The complete genome sequences of Arabidopsis and rice have revealed multiple and complex episodes of genome duplication during the diversification of the angiosperms, forcing us to accept that probably all angiosperms – and maybe all plants – are polyploid to some extent. This recognition brings with it new questions. How do polyploids form? What happens to their duplicate gene copies? Are there 'rules' that govern the behavior of homoeologous genes and chromosomes when united in a single nucleus? How does the genetic diversity observed in recent polyploids of multiple origin relate to the diversity observed in ancient polyploids? The papers by Guo et al. and Skalickáet al. attempt to bridge this gap through comparisons and inferences of ancient vs recent polyploid events. More such studies will be welcome additions to the rapidly accumulating data on genetic and genomic diversity of polyploid plants. I thank the US National Science Foundation for support and Doug Soltis for comments on an earlier draft of this manuscript.
Год издания: 2005
Авторы: Pamela S. Soltis
Издательство: Wiley
Источник: New Phytologist
Ключевые слова: Chromosomal and Genetic Variations, Plant Disease Resistance and Genetics, Plant tissue culture and regeneration
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Том: 166
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Страницы: 5–8