The Impact of Polyploidy on Grass Genome Evolution

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 veg