Introduction

B chromosomes have been a subject of interest since they were first discovered in the plant bug insect Metapodius, by Wilson in 1906, 1907 [214, 215]. Wilson referred to them as supernumerary chromosomes, and listed their essential properties which we still recognise today as being their main diagnostic features: namely, may be present or absent, do not pair with the standard A chromosome set, no obvious effect on the phenotype, no relationship with environmental factors, and non-essential to their host organism. Their significance increased once they were discovered in maize, and named as B chromosomes (Bs) by Randolph in 1928 [163]. Their presence in rye [75] also stimulated fascination in their enigmatic properties in plants, and research in their properties grew steadily in both plants and animals as new cases were discovered. The significance of their role in the genome has been tracked through a number of reviews up to the present time, and a selection of the most recent significant publications are listed in Table 1, although it has to be said that in most cases we only know of their occurrence, and there is a blank canvas about their properties and biological significance. We have now reached the point where examples are coming to notice of a few species where Bs have functional genes (Table 1), although it still remains to be discovered what these B-genes actually do to account for the manifold effects on the phenotype of their hosts.

Table 1 Selected reviews on B chromosomes since 1980
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The present manuscript does not attempt to review the history of B chromosomes. The purpose is to update the number of species known to have Bs since the last such list was published in 1982 [93], and to add some comments on the diversity of newly discovered species since 1980. The B Chromosome Atlas in the B-book of 1982 [93] listed 1007 angiosperms, 9 gymnosperms and 263 animals known to carry Bs, a total of 1279 species. To compile this data a hard copy (reprints and photocopies) collection was made of 1373 papers of the world literature that could be traced over a period of ten years. Clearly it was not possible to trace every publication citing Bs during this time, and number of 1279 is therefore an underestimate.

The purpose of the current exercise is to augment this 1982 list based on a collection of publications produced since 1980, and to identify all new species with Bs recorded up to the present time (2017). This list is of necessity also an underestimate, since some papers are not available, and certain journals do not give open access, and cannot be used.

Materials and methods

The materials consist of the collection of the 900 publications used the compile the data in Table 2, and the method is the process of reading this extensive literature and extracting the names of the new species with B chromosomes from these papers.

Table 2 Full list of new species found with Bs since 1980
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Results

The data are recorded in detail in Table 2 which shows 13 species of fungi, 136 plants and 257 animals, giving a total of 406 new species with Bs. Together with the 1980 data we reach a total of 1685 +B species known at the present time. A summary of the data in Table 2 is given in Table 3, and is discussed here in comparison with the 1982 lists.

Table 3 Summary of new species with Bs since 1980
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Discussion

The first noticeable feature for the species listed in Table 2 is the presence of the 13 species of fungi with Bs, whereas none were listed in 1982. The fungi are listed separately from the plants since they are taxonomically distinct and their chromosomes are not studied in the same way using light microscopy. It is also a controversial matter as to whether we can truly call them Bs, as discussed in details by Covert [47]. Their tiny chromosomes are studied by separating them using gel electrophoresis. The studies are mostly done on pathogenic species affecting crop plants, and a basic set can be identified as well as a number of additional small dispensable chromosomes which are the Bs (sometimes called minichromosomes). It is also a feature that some of the extra chromosomes in fungi have genes that encoding detectable phenotypes, as recently noted in the wheat pathogen Mycosphaerella graminicola which has 8 dispensable chromosomes carrying 17 genes, compared to the 770 genes on the essential ones [184].

The 27 species in four families of gymnosperms with Bs are reviewed by Muratova [135], while there were 9 cases in five families in 1980. Muratova described the Bs in mitotic tissues, on the basis of their smaller size and distinctive structural properties, although aspects of their behaviour at meiosis are known from other works. It is noteworthy that most species have only one or two Bs, and higher numbers are rare. Tashev [187] considers that the distribution the Bs in Picea abies is related with the geographic factors, and has a possible adaptive role. Precisely how this adaptation works is conjectural.

In the flowering plants, a modest 18 new species with Bs are recorded for the dicotyledons, compared with 510 in 1980. Two new families appear in the data, namely Malpighiaceae, with two species, and the Stylidiaceae with just one. In general, most of the papers in this section deal mainly with the occurrence of Bs, their size variation, chromatic status and meiotic behaviour. Sharma et al. [178] describe the transmission of the additional chromosome in a triplo-4 individual of Plantago lagopus, which is significant since it later led to a novel hypothesis on the origin of the Bs in this species. Butea monosperma (Leguminosae) is one of those rare cases of B chromosomes in tree species [160], where the small euchromatic B was found in five out of 29 trees in a park in Lucknow in India. The presence of Bs in Acanthophyllum laxiusculum increases the chiasma frequency of the A chromosomes, but with an effect which is higher for plants with odd compared with even numbers of Bs [72]. This so-called odd–even effect is known in several plant and animal species and the mechanism of its action remains a mystery. The Australian daisy Brachycome dichromosomatica, 2n = 4, has only two As and from 0–3 Bs of two types [51, 105]. It is one the few plant species where detailed sequence analysis of plant B chromosomes has been undertaken, and a family of 176-bp tandem repeats specific to the B have been isolated and described [91].

The monocotyledons, in contrast with the 18 dicots have a larger number of 91 new species, but fewer than the 497 in listed in 1982. One reason for this difference could be that there are many species, such as those in the Liliaceae and Orchidaceae, which have large genomes that are attractive to cytologists, and which are therefore more intensively studied. It is also a truism that many species are investigated cytogenetically because they have not been previously studied, and there is opportunity to add to the chromosome knowledge base. Blagojević et al. [17] make the interesting point that B chromosomes should be regarded as a significant component of the eukaryote genetic system in organisms which carry them, since they are found in so many species at the population level. Chen et al. [37] noted no relationship between the presence of Bs and the ecological and climatic conditions in 21 natural populations of Agropyron cristatum and A. mongolicum. In Sorghum stipoideum the Bs are totally eliminated from stems and leaves [217].

In the animal kingdom, we are dealing with 257 new species with Bs, which is close to the 263 listed in 1982. In addition to that we have a large number of new entries (100) for fishes as well as one new entry for birds. There are also many new species of amphibia, reptiles and mammals. It is notable too how many orthoptera have been studied, no doubt on account of their large and amenable karyotypes.

The flat worm Polycelis nigra is a new species additional to the previous three [14]. This species is of interest since it can reproduce sexually or asexually, and has a complex mode of transmission. In the beetle Dichotomius geminatus the mapping of repetitive DNAs provided evidence of an association of 5S rRNA and histone H3 genes in insects, and there was also a similarity in repetitive DNA between the B and A chromosomes [26]. The arachnid Metagagrella tenuipes (2n = 18) was studied in 8 populations in Japan, and has up to 19 Bs [191]. All 19 Bs appear all be univalent at meiosis, and no correlation was found between the number of Bs and external morphologies or habitat type. In Drosophila subsilvestris a species-specific satellite DNA family (pSsP216) was found mainly on the Bs and at in the centromeric heterochromatin of the A chromosomes, and the authors suggest that the Bs may have been derived from the A chromosomes [79]. A SCAR marker was developed to show the presence of Bs in the stingless bee Partamona cupira [21]. Araujo et al. [6] have identified a mechanism in the haplodiploid wasp Trypoxylon albitarse whereby meiosis is regularised for limiting the number of Bs to one, thereby integrating the B as a regular member of the chromosome complement. In the acridid Aiolopus strepens there is an odd–even effect of the number of Bs on B pairing, and also on the number of macrospermatids, which are increased with odd numbers. Ruiz-Ruano et al. [167] investigated the origin of the B by analysing 27 families of satellite DNA, of which two of the families were found only on the B and many others on the A chromosomes as well. Detailed studies indicated a possible intraspecific origin of the B from the proximal third of the S8 autosome. The discovery of two types of Bs in five natural populations of Eyprepocnemis plorans opened up a whole new field of evolutionary studies in this species, as well as discovering effects on A chromosome chiasma frequency and distribution [28]. In contrast, there were no effects of Bs on chiasma frequency variation in Heteracris littoralis, although there was an increase in macrospermatids production [33].

Twenty-nine new species of amphibia are recorded since 1980, when there were only ten species known. A review by Green [77] summarised the main features of the structure and evolution of the B chromosomes of 26 species of amphibians, including the earlier known cases. There is detailed information on the variation in structure, size and chromatic status, as well as the distribution pattern of their occurrence within and between species. They are generally large in size and amenable to study. The Pacific giant salamander, Dicamptodon tenebrosus has up to 10 Bs, but the number varies over different regions of the Pacific Northwest of North America [20]. The Bs in this species have been isolated by microdissection and their DNA hybridised to genomic DNA of a number of related species, and demonstrating that they originate from the standard A complement.

Only three species of reptiles with Bs were known by 1980, and this number has now increased up to 12. Bertolotto et al. [13] reviewed the system of Bs in lizards and described their structural variation, chromatic status and influence over the A chromosomes.

There were no fishes represented in the 1980 data. They made their first appearance in the 1980s/1990s, and then their numbers increased rapidly until they now account for more than 100 species, with many coming from studies in Brazil. The cyprinid fish Alburnus alburnus has some of the largest B chromosomes known in vertebrates. There are two morphological types, and only one or two Bs may be present with variable frequency in different populations. The Bs are completely heterochromatic, replicate their DNA late, and are composed of specific retrotransposable elements [174]. The large B represents 10% of the size of the genome size. Carvalho et al. [36] reviewed the occurrence of Bs neotropical fishes and pointed out that the greatest number occurred in the order Characiformes, with a lot of variation within as well as between species in their number, morphology and size, and tabulated the data for thirty-one species. In Astatotilapia latifasciata an investigation into the transcriptionally active repeated non-coding DNA (BncDNA) of the heterochromatic Bs found transcripts that are processed differentially in different tissues. This BncDNA potentially has actions which influence the maintenance of Bs in mitotic cells as well as meiotic drive in gametic cells [162]. Yosida et al. [225] sequenced a BAC clone from cichlid fishes in Lake Victoria and found several protein coding genes, suggesting that the Bs have a functional role, contrary to the widespread belief that they are simply selfish genetic elements. In this sense, the Bs in fishes have made highly significant contribution to the knowledge of Bs in the genetic system.

The first observation of B chromosomes in birds, in the zebra finch Taeniopygia guttate was recently described, in 1998 [155]. A single B was found in the germ cells of male and female, and described as being euchromatic in oocytes and strongly heterochromatic in spermatocyte.

An additional 53 mammals have now been described compared with the 19-species known in 1980, giving a total of 72. Silva and Yonenaga-Yassuda [180] reviewed the eight then known Brazilian rodents and found them to be heterogeneous in size, generally heterochromatic and late replicating.

Many of the publications simply deal with the discovery of Bs in particular species and a description of the Bs in term of their size variation (some are minute) and chromatic status. More detail is given in the review of Bs in mammals by Volobujev [206]. An analysis the DNA sequences in the marsupial Petauroides volans found the B to be composed of a heterogenous mixture of sequences, some unique to the B and others to the centromeric regions of the A chromosomes. [124].

Conclusions

The main findings of the current survey on new species discovered with Bs since 1980 are that organisms with these enigmatic chromosomes continue to be discovered on a regular basis, and they augment our knowledge base on this topic of growing interest. It should also be pointed out that certain species which are currently contributing much of the recent knowledge on the molecular organisation, origin and active genes in Bs were known before the discovery of the Bs listed in Table 2, and these will doubtless be reviewed in future publications.