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Focus on polyploidy

2010; Wiley; Volume: 186; Issue: 1 Linguagem: Inglês

10.1111/j.1469-8137.2010.03215.x

1469-8137

Malika L. Aïnouche, Eric Jenczewski,

Plant Pathogens and Resistance

Polyploidy (whole-genome duplication) has played a pervasive role in the evolution of fungi and animals, and is particularly prominent in plants (Wendel & Doyle, 2005; Cui et al., 2006; Otto, 2007; Wood et al., 2009). This important evolutionary phenomenon has attracted renewed and growing interest from the scientific community in the last decade since it was discovered that even the smallest plant genomes considered to be 'diploid' (e.g. Arabidopsis thaliana, reviewed in Henry et al., 2006) have incurred at least one round of whole-genome duplication, possibly predating the origins of the angiosperms (Soltis et al., 2009). Polyploidy is an important speciation mechanism for all eukaryotes and has profound impacts on biodiversity dynamics and ecosystem functioning. Newly formed polyploids, and particularly those of hybrid origin (allopolyploids), frequently exhibit rapid range expansion (Ainouche et al., 2009), and over long periods of evolutionary time, polyploidy has increased morphological complexity and probably reduced the risk of species extinction (Fawcett et al., 2009). Last, but not least, genome duplication has often provided the raw material for plant domestication (e.g. wheat, Dubkovsky & Dvorak, 2007) and thus has had a major impact on human societies and the development of an agrarian lifestyle. '... there are reasons to ask whether genome multiplication represents an evolutionary advantage per se.' Why polyploids have been so successful is a question that has generated important research activity in the last decade (reviewed in Wendel, 2000; Osborn et al., 2003; Chen, 2007; Doyle et al., 2008; Van de Peer et al., 2009), accompanied by increasing national and international collaborative efforts through funded networks and international meetings. The International Polyploidy Conference held in London in April 2003 (Leitch et al., 2004) provided an opportunity to evaluate the progress made during the 25 years since the first International Conference, Polyploidy: Biological Relevance (Lewis, 1980) held in 1979 in St Louis, MI, USA. Significant advances have continued to be made towards an understanding of polyploid genome functioning and evolution over both the short-term (in young or neo-polyploids) and long-term (in paleopolyploids). The importance of recent findings from this timely and fast-evolving area was no more evident than at the latest gathering, the International Conference on Hybridization, Polyploidy and Biodiversity that was held in Saint-Malo (France), 17–20 May 2009 (http://www.icphb2009.univ-rennes1.fr/). In this special issue, New Phytologist recognizes these advances by bringing together current ideas and findings about plant polyploidy in a series of research reviews and accompanying original research articles. Polyploid species may be formed through a diversity of mechanisms in natural populations (unique or multiple origins, via one-step or stepwise) involving one progenitor species (i.e. autopolyploids) or divergent parental lineages (i.e. allopolyploids). Although autopolyploidy has long been considered as less prevalent than allopolyploidy, there are reasons to ask whether genome multiplication represents an evolutionary advantage per se (Parisod et al., this issue, pp. 5–17). Likewise, although estimating the time of origin of polyploid species is an important evolutionary issue, current procedures need to be handled with caution to avoid spurious conclusions (reviewed in Doyle & Egan, pp. 73–85). Once formed, neopolyploid plants face an immediate challenge during meiosis: the different sets of chromosomes are usually sufficiently similar to one another that recombination may lead to complex meiotic configurations which are prone to generate unbalanced gametes, aneuploid progenies (Mestiri et al., pp. 86–101) and chromosome re-arrangements (Szadkowski et al., pp. 102–112), and hence to impair fertility (reviewed by Gaeta & Pires, pp. 18–28). Precise control of meiotic crossovers (an important facet of meiotic recombination) is therefore a prerequisite for meiotic and reproductive stability in polyploids. This can be achieved either through random processes, accelerated by subfunctionalization (partitioning of homeologous gene expression in different tissues or developmental stages) or neofunctionalization (when one of the homeologous gene copies evolves a new function with a selective advantage) (Le Comber et al., pp. 113–122) or through the involvement of genes that contribute to the cytological diploidization of autopolyploid and allopolyploid species (Cifuentes et al., pp. 29–36). Interestingly, none of these processes necessarily impair the occurrence of noncrossover (i.e. the second product of meiotic recombination), as detected in synthetic and natural allotetraploid cotton (Salmon et al., pp. 123–134). The merger of divergent genomes in allopolyploids also represents a form of 'genomic shock' that may cause increased transposable element (TE) activity (reviewed in Parisod et al., this issue, pp. 37–45). Emerging evidence suggests that amplification of TEs during the first generations following polyploidy may be restricted to a few TEs (e.g. young active elements), such as Tnt1 in synthetic allotetraploid Nicotiana tabacum (Petit et al., pp. 135–147), while most others are rapidly targeted by epigenetic changes following hybridization in allopolyploids (Parisod et al., 2009). Transposable element activity notably leads to the production of specific classes of small interfering RNAs (siRNAs) that are differently contributed by the maternal and paternal genomes and may lead to an epigenetic hybrid barrier (Martienssen, pp. 46–53). Of note, TEs are not the only repetitive sequences that are prone to rapid evolutionary changes, as demonstrated by the unexpected rate of satellite repeat replacement in allopolyploids of Nicotiana (Koukalova et al., pp. 148–160). Significant progress has been made in understanding changes of gene and genome expression in polyploids compared with their parents, including expression dominance from one parent, transgressive expression levels compared with parents, and modulation or silencing of transcriptional activity of homeologous subgenomes in nascent (e.g. Spartina, Chelaifa et al., pp. 161–174; and Tragopogon, Buggs et al., pp. 175–183) or long-evolved (e.g. Gossypium, Flagel & Wendel, pp. 184–193) polyploids. Interestingly, genome duplication per se (in autopolyploids) seems to have limited effects on global genome expression, although it may significantly impact less complex regulatory pathways (Pignatta et al., pp. 194–206). These observations are in agreement with the theory that the stoichiometry/connectivity of multisubunit complexes is a major determinant driving the ability of duplicated genes to evolve (Birchler & Veitia, pp. 54–62). There is also evidence that some changes in gene and genome expression are epigenetically controlled. For example, the down-regulation of microRNA (miRNA) biogenesis was shown to induce developmental changes in resynthesized Arabidopsis allotetraploids (Lackey et al., pp. 207–215). Likewise, small RNAs are likely candidates for explaining proteomic changes in resynthesized Brassica napus allotetraploids that otherwise exhibit mainly additive transcriptomes of their parents (Marmagne et al., pp. 216–227). Increasingly, data are documenting the link between the regulation of gene expression and phenotypic changes following allopolyploid speciation. Evolution of tandem gene duplications at the Flowering LocusC (FLC) and the divergence of corresponding putative regulatory upstream sequences have increased expression diversity and flowering time variation in Arabidopsis allotetraploids (Nah & Chen, pp. 228–238). Transcriptional changes of floral gene regulators were found to be associated with photoperiod-dependent floral reversion in the natural allotetraploid A. thaliana, thus increasing the plasticity of this species (McCullough et al., pp. 239–250). Increased plasticity of mating systems was also demonstrated in natural and synthetic allohexaploid Senecio cambrensis (Brennan & Hiscock, pp. 251–261). Finally, the importance of gene flow across ploidy levels causing increases in phenotypic variation and adaptation in natural populations is revisited and shown to occur in Senecio (reviewed in Chapman & Abbott, pp. 63–71). As data accumulate from different biological systems, much progress is being made towards understanding the respective impacts of hybridization (i.e. genome merger), genome duplication (polyploidy per se) and subsequent evolution following allopolyploid and autopolyploid speciation. Experimentally resynthesized polyploids from model systems in a known genetic context, and comparisons with their corresponding natural species, are providing invaluable insight into the nature and tempo of the mechanisms involved. The rapidly evolving tools (e.g. next-generation sequencing technologies), allowing large-scale investigations of genomes, epigenomes and transcriptomes, offer promising opportunities to extend our knowledge in natural populations of previously under-explored wild species from various plant lineages, thus providing both a precise and a broader picture of the important evolutionary process of polyploidy. The 'International Conference on Polyploidy, Hybridization and Biodiversity' (ICPHB) was organized following the initiative of the Polyploidy Consortium 'Polyploidy and Biodiversity' funded by the French National Research Agency (ANR) and animated by M.L. Ainouche, A-M. Chèvre, E. Jenczewski, K. Alix, H. Thiellement, B. Chalhoub, J. Jahier and M-A. Grandbastien. The meeting was held with contribution and support from the US NSF-funded Polyploidy group (coordinated by L. Comai). A. Leitch is thanked for particular help in the organization process. We acknowledge support from University of Rennes 1, CNRS, INRA, AgroParisTech, CIRAD, Genopole Evry, Biogenouest, Region Bretagne-Pays de Loire and the Conseil General d'Ille et Vilaine, New Phytologist Trust, the French Genetics Society and the Systematics Association (London). This special issue of New Phytologist was coordinated by M.L. Ainouche and edited by R. Abbott, L. Galloway, M.D. Rausher, P.S. Soltis and S.H. Strauss. Thanks are due to H. Slater and N.J. Hetherington for their assistance in coordinating the issue and also to the many contributing Authors and Reviewers involved. We hope that you, our Readers, will enjoy and take inspiration from this special issue.