Current Genomics - Volume 3, Issue 6, 2002

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.

Many of the proteins involved in meiotic recombination are conserved among eukaryotes, and here we discuss those recombination proteins that have been identified in plants. In addition, we summarize some of the differences in crossover regulation between plants and budding yeast (the primary model for molecular studies of recombination in eukaryotes). We also discuss factors that influence the distribution of crossovers including chromosome, chromatin and genomic structure. Different methods have been used for mapping recombination in plants including genetic linkage maps, cytogenetic maps (e.g., chiasmata and recombination nodules), and physical maps (DNA sequence and contigs). Progress has been made in integrating the different types of maps to provide a more complete understanding of genome structure and function in plants, including the control of meiotic recombination.

Telomeres and centromeres are the most important functional elements in plant chromosomes, as in other eukaryotic chromosomes. Both elements are in general composed of repetitive DNA sequences, and binding or associated proteins. Recent findings showed that the telomere DNA sequences are conserved among all plant species except Allium and related species, and that they form high-order complexes together with special proteins for maintaining the functions. Although centromere-specific DNA sequences have been isolated in a wide range of plant species, almost no conservation was found in their DNA sequences. Exceptions are cereal centromeres, which contain common Ty3 / gypsy-type retrotransposon-like sequences. Recently, homologues to the genes encoding mammalian centromere proteins (CENPs) have been identified in maize and A. thaliana. This indicates that high-order structures of centromeres or kinetochore assemblies are conserved among eukaryotic organisms. The 180-bp centromeric repeat family of Arabidopsis thaliana is strongly suggested to play important roles for centromere functions. Since the organization of this family is similar to that of human alpha-satellite family, it is likely to be possible to build Arabidopsis thaliana artificial chromosomes (AtAC) with the same strategies used for constructing mammalian artificial chromosomes.

The application of DNA-based phylogenies to the study of chromosome evolution has allowed the direction of many of the changes that give rise to the chromosome variation to be analysed objectively for the first time. Dysploid changes in chromosome number, differences in the degree of karyotype symmetry, the loss or gain of chromosome bands, changes in genome size and variation in the number of ribosomal RNA gene clusters can all be shown to undergo a variety of changes, suggesting that there are no universal rules governing karyotype evolution. Phylogenetic studies as well as chromosome mapping and the analysis of chromosome pairing patterns using genomic in situ hybridization also demonstrate that cryptic or ancient polyploids may be more widespread in angiosperms than previously thought.

In land plants (Embryophyta), comprising bryophytes, pteridophytes, gymnosperms and angiosperms, DNA Cvalue data has increased significantly in recent years. Estimates are available for over 3,800 species, ranging over 2000- fold (1C = 0.06 - 127.4 pg). Evaluating the phylogenetic component of this variation is essential to understand its evolutionary significance. Consequently, C-value data were superimposed onto well-supported phylogenies. This showed: (1) Most angiosperms (52%) had small C-values (defined as 1C ≤ 3.5 pg) within five times the mode (0.6 pg). Very large C-values (1C ≥ 35.0 pg) occurred in only two distantly related groups (monocots and Santalales) suggesting that ancestral angiosperms had small genomes, and that very large genomes represented a derived condition that arose independently at least twice. (2) In contrast, extant gymnosperms (sister to angiosperms) typically had larger genomes whose modal Cvalue (15.8 pg) was over 20 times greater than angiosperms. Large C-values (≥14.0 pg) were even typical in extant cycads (mean 1C = 14.7 pg), regarded as the basal group of gymnosperms. Thus within extant seed plants (gymnosperms and angiosperms), possession of a small genome seems unique to angiosperms. (3) C-value data in pteridophytes and bryophytes are still too sparse to permit analysis of evolutionary trends. However, low C-values (1C = 0.06 - 2.1 pg) in lycophytes, a pteridophyte group sister to all other extant vascular plants, suggest that first vascular plants had small genomes. Further, the narrow range and small size of C-values in bryophytes and Selaginella and Lycopodium (0.06 - 2.1 pg) seem likely to be under tight nucleotypic control. Nucleotypic correlations between cell size and nuclear DNA Cvalues in fossil plants may reveal major trends of plant genome size evolution over geological time. Knowledge of genome size, its origin and consequences will further unify our understanding of the evolutionary processes, structural components and DNA sequences responsible for plant genome diversity.

Nucleolar dominance is an enigma. The puzzle of differential amphiplasty has remained unresolved since it was first recognised and described in Crepis hybrids by Navashin in 1934. Here we review the body of knowledge that has grown out of the many models that have tried to find the genetic basis for differential rRNA gene expression in hybrids, and present a new interpretation. We propose and discuss a chromatin imprinting model which re-interprets differential amphiplasty in terms of two genomes of differing size occupying a common space within the nucleus, and with heterochromatin as a key player in the scenario. Difference in size between two parental genomes induces an inherited epigenetic mark in the hybrid that allows patterns of chromatin organization to have positional effects on the neighbouring domains. This chromatin imprinting model can be also used to explain complex genomic interactions which transcend nucleolar dominance and which can account for the overall characteristics of hybrids. Gene expression in hybrids, relative to parentage, is seen as being based on the nuclear location of the sequences concerned within their genomic environment, and where the presence of particular repetitive DNA sequences are ‘sensed’, and render silent the adjacent information.

Wheat is the most consumed grain crop in the world. It is also an excellent model of allopolyploid inheritance. Genomic analysis of wheat is essential for understanding the genetic mechanisms underlying allopolyploid evolution and speciation as well as the biology of agronomically important traits influencing production. In spite of the large genome and polyploidy, researchers have devised novel strategies for in depth structural and functional analysis of the wheat genome. Beginning with the 1920s, wheat has been a model crop for cytogenetic studies, and a plethora of cytogenetic stocks of various types have been developed. Today, a combined cytogenetic and molecular approach has greatly advanced wheat genome analysis. The comparison of physical maps of wheat chromosomes based on chromosome deletion mapping with molecular genetic linkage maps led to the notion that genes were not distributed at random throughout the wheat genome, but rather exist in gene-rich recombination hot spots along the chromosomes. Recent construction and sequencing of local BAC contigs has verified this hypothesis, suggesting that most genes in wheat are amenable to positional cloning. Wheat is now moving into the functional genomics era as researchers focus on the expressed portion of the wheat genome. A database of expressed sequence tags (ESTs) is growing rapidly as researchers work to assign gene function. High-throughput production and identification of mutants will be necessary for the assignment of function to the many genes being discovered in wheat.