A century of B chromosomes in plants: so what?

BACKGROUND: Supernumerary B chromosomes (Bs) are a major source of intraspecific variation in nuclear DNA amounts in numerous species of plants. They favour large genomes, and create polymorphisms for DNA variation in natural populations. By studying Bs we can gain useful knowledge about the organization, function and evolution of genomes. There are also significant biological questions concerning the origin and structural organization of Bs, and the way in which these selfish elements can establish themselves by exploiting the replicative machinery of their host genome nucleus. SCOPE: It is a sine qua non that Bs originate from the A chromosomes, in a variety of ways. We can study their modes of drive and ask how it is that chromosomes which apparently lack genes can have control over their own drive process which leads to their survival in natural populations. Molecular cytogenetic studies are opening up new avenues of investigation. Population equilibria for B frequencies are determined by a balance between accumulation and harmful effects. Bs are also subject to meiotic loss due to polysomy and to elimination at meiosis as univalents. These balancing forces can be seen in the context of host/parasite interaction, based on a dissection of the genetic elements in both As and Bs (in maize) which interact to bring about a stable equilibrium, at least for a snapshot in time. CONCLUSIONS: Aside from their intrinsic enigmatic properties, B chromosomes make useful experimental tools to study genome organization. Thus far they have not been exploited for their applications, other than through the use of A-B translocations used for gene mapping in maize; but there are opportunities to use them to modulate the frequency and distribution of recombination, to diploidize allopolyploids, to study centromeres and to be developed as plant artificial chromosomes; given that they can be structurally modified and their inheritance stabilized.

Transcriptionally active heterochromatin in rye B chromosomes.

B chromosomes (Bs) are dispensable components of the genomes of numerous species. Thus far, there is a lack of evidence for any transcripts of Bs in plants, with the exception of some rDNA sequences. Here, we show that the Giemsa banding-positive heterochromatic subterminal domain of rye (Secale cereale) Bs undergoes decondensation during interphase. Contrary to the heterochromatic regions of A chromosomes, this domain is simultaneously marked by trimethylated H3K4 and by trimethylated H3K27, an unusual combination of apparently conflicting histone modifications. Notably, both types of B-specific high copy repeat families (E3900 and D1100) of the subterminal domain are transcriptionally active, although with different tissue type-dependent activity. No small RNAs were detected specifically for the presence of Bs. The lack of any significant open reading frame and the highly heterogeneous size of mainly polyadenylated transcripts indicate that the noncoding RNA may function as structural or catalytic RNA.

Phyletic hot spots for B chromosomes in angiosperms.

We determined whether supernumerary B chromosomes were nonrandomly distributed among major angiosperm lineages and among lineages within families, as well as the identity of lineages with unusually high B-chromosome frequencies (hot spots). The incidence of B chromosomes for each taxon was gathered from databases showing species with and without these chromosomes (among species with known chromosome numbers). Heterogeneity was found at all ranks above the species level. About 8% of monocots had B chromosomes versus 3% for eudicots; they were rare in nonmonocot basal angiosperms. Significant heterogeneity in B-chromosome frequency occurred among related orders, families within orders, and major taxa within families. There were many B-chromosome hot spots, including Liliales and Commelinales at the order level. At the family level, there was a trend suggesting that B-chromosome frequencies are positively correlated with genome size.

B chromosomes are more frequent in mammals with acrocentric karyotypes: support for the theory of centromeric drive.

The chromosomes of mammals tend to be either mostly acrocentric (having one long arm) or mostly bi-armed, with few species having intermediate karyotypes. The theory of centromeric drive suggests that this observation reflects a bias during female meiosis, favouring either more centromeres or fewer, and that the direction of this bias changes frequently over evolutionary time. B chromosomes are selfish genetic elements found in some individuals within some species. B chromosomes are often harmful, but persist because they drive (i.e. they are transmitted more frequently than expected). We predicted that species with mainly acrocentric chromosomes would be more likely to harbour B chromosomes than those with mainly bi-armed chromosomes, because female meiosis would favour more centromeres over fewer in species with one-armed chromosomes. Our results show that B chromosomes are indeed more common in species with acrocentric chromosomes, across all mammals, among rodents, among non-rodents and in a test of independent taxonomic contrasts. These results provide independent evidence supporting the theory of centromeric drive and also help to explain the distribution of selfish DNA across species. In addition, we demonstrate an association between the shape of the B chromosomes and the shape of the typical ('A') chromosomes.

A high-copy-number CACTA family transposon in temperate grasses and cereals.

A lineage of CACTA family transposons has been identified in temperate grasses and cereals, and a full-length representative of the subfamily from Lolium perenne has been sequenced. Both the size and internal organization of the L. perenne element are typical of other CACTA family elements but its high copy number and strong conservation are unexpected. Comparison with homologs in other species suggests that this lineage has adopted a distinct and novel evolutionary strategy, which has allowed it to maintain its presence in genomes over long periods of time.

The nature and destiny of translocated B-chromosome-specific satellite DNA of rye.

Translocations of A chromosome-specific and B chromosome-specific satellite DNA were tracked by fluorescence in situ hybridisation from an irradiated M1 generation of an experimental population of rye (Secale cereale L.) to its M2 progeny. Although high frequencies of large structural rearrangements were detected in root-tip meristems of M1 plants, none was present at meiosis or in somatic cells of their progeny. These results are interpreted in terms of efficient "filtering" of translocations during vegetative development, and not in the more usual terms of meiosis presenting a physical barrier to structural variants. These observations highlight the fact that B-A translocations are not tolerated, and may explain why this form of chromosome mutation is largely absent from natural populations.

B chromosomes in plants.

This review of supernumerary B chromosome systems in flowering plants deals mainly with work published in the last 15 yr, hut also includes older material which has not hitherto been presented systematically. The term B chromosome (B) is defined, and there is an introductory overview dealing with general characteristics and the significance of Bs as a widespread chromosome polymorphism. Detailed sections are then presented covering the occurrence of Bs in different taxa, their structure and molecular organization, their irregular modes of inheritance, their phenotypic effects, population dynamics and origin. Particular attention is paid to the research growth points in molecular analysis of the structure and genome organization of Bs, and to transmission genotypes in the context of their adaptive versus their selfish properties. Where appropriate, reference is also made to likely future lines of research, and also to the usefulness of B chromosomes in genetic analysis and as model systems to study general phenomena of genome organization and evolution, nuclear physiology and architecture, chromosome polymorphism and selfish DNA. CONTENTS Summary 411 I. Introduction 411 II. Occurrence 411 III. Structure and organization 415 IV. Inheritance 422 V. Phenotypic effects 426 VI. Populations 429 VII. Applications 430 VIII. Origin 430 Acknowiedgements 430 References 431.