Current Genomics, 2002, 3, 000-000 1 1389-2029/02 $35.00+.00 © 2002 Bentham Science Publishers Ltd. Non-Mendelian Phenomena in Allopolyploid Genome Evolution Bao Liu 1 and Jonathan F. Wendel 2, * 1 Institute of Genetics & Cytology, Northeast Normal University, Changchun 130024, China and 2 Department of Botany, Bessey Hall, Iowa State University, Ames, IA 50011, USA Abstract: Perhaps all flowering plants have experienced one or more episodes of polyploidization at some time in their evolutionary history. Recent evidence indicates that this genome doubling may be accompanied by a variety of non- Mendelian phenomena, some of which operate during hybridization and polyploid formation while others manifest more gradually on an evolutionary timescale. Here we review these phenomena, drawing attention to recent paradigm shifts necessitated by new insights from model plant systems. Allopolyploid formation in some plant groups is associated with an unexplained and in some cases directed process of genomic alteration leading to non-additivity with respect to parental genomes. Novel intergenomic interactions become possible as a consequence of the merger of two previously isolated diploid genomes, variously leading to intergenomic colonization and/or homogenization of formerly diverged sequences. Several epigenetic processes may accompany nascent allopolyploidy, such as nucleolar dominance, gene silencing and mobile element activation, the latter also resulting in genetic change. These myriad phenomena do not characterize all polyploid systems, and some nascent allopolyploids appear to be genomically quiescent. Although a direct connection to adaptation remains to be established, the diversity of genetic responses to allopolyploid formation and their apparent high frequency suggest that non-Mendelian phenomena contribute directly to polyploid stabilization and diversification. I. INTRODUCTION Polyploidy, resulting from either duplication of a single but complete genome (autopolyploidy) or from combination of two or more differentiated genomes (allopolyploidy), is a prominent mode of speciation in plants [1-8], and has also been significant in the evolution of vertebrates and possibly many other eukaryotes, including humans [9-16]. It is difficult to overstate the importance of polyploidy in the evolutionary history of plants. While estimates vary regarding the proportion of angiosperms that have experienced one or more episodes of chromosome doubling at some point in their evolutionary history, it is at least 50% and may be higher than 70% [2,6]; perhaps 95% of pteridophytes have experienced at least one episode of polyploidization in their past [1,2]. Many important crop plants, including wheat, oat, coffee, potato, canola, soybean, sugarcane, tobacco and cotton are typical polyploids. Because most ancient polyploids have undergone an evolutionary process of chromosomal and perhaps genic “diploidization”, their polyploid history may be obscured at the cytological and classic genetics levels. Consequently, the polyploid nature of many plant genomes was not evident until the advent of comparative genomics and whole-genome sequencing. Recent and prominent examples include maize [17,18] and Arabidopsis [19-21] — both species were traditionally recognized as diploids, but in fact their genomes harbor compelling evidence of historical cycles of genome doubling. Given these and other recent examples from plants [e.g. 22,23-26], it is probably safe to state that there are no bona fide diploid species in the plant kingdom. *Address correspondence to this author at the Department of Botany, Bessey Hall, Iowa State University, Ames, IA 50011, USA; E-mail: jfw@iastate.edu Given the prominence of polyploidy in plants, it is not surprising that there has been a great deal of interest in its biological significance. Various aspects of polyploidy have attracted attention, including classification of the various types of polyploids, mode and frequency of formation, significance vis-à-vis adaptation and diversification, and correlations with life-history attributes and ecological parameters. These subjects have been thoroughly reviewed elsewhere [6-8,27-32] and will not be discussed here. More recently, attention has been focused on genetic and genomic attributes of polyploidy, including the immediate and long- term consequences of genome doubling [reviewed in 33]. Because of rapid progress in the field, there has been growing awareness of the diversity of phenomena associated with polyploidy, particularly its surprising non-Mendelian attributes (i.e., those not characterized by conventional transmission genetics). The present review is aimed at these phenomena, with the goal of providing a convenient entry into a rapidly expanding literature. We will revisit some of the central principles of polyploid genome evolution [cf. 33] as well as draw attention to recent paradigm shifts necessitated by new insights from model plant systems. Particular emphasis will be placed on the mysterious process of rapid and in some cases directed structural changes that occur in polyploid genomes upon their formation; novel intergenomic interactions that become possible as a consequence of the merger of two formerly isolated genomes; and epigenetic mechanisms that may accompany nascent allopolyploidy, such as nucleolar dominance, gene silencing and mobile element activation. These myriad phenomena do not characterize all polyploid systems, and in fact some nascent allopolyploids appear to be genomically quiescent in this respect. We will summarize experimental data from model polyploid systems, explore the possible mechanisms and biological significance of the various