B Chromosomes - Plants and Crops Science
INTRODUCTION
The earliest record of B chromosomes in plants comes from Anne Lutz in 1916 who found them in Oenothera, and referred to them as ‘‘diminutive chromosomes.’’ Later, they also became known as accessories or extra fragment chromosomes. The term B chromosomes is credited to Randolph, who used this name in 1928 to describe certain additional chromosomes found in some plants of maize and to distinguish them from those of the regular chromosome complement (2n = 2x = 20), which are the A chromosomes. B chromosomes is now the universally accepted term and can be conveniently shortened to B or Bs.
DISCUSSION
The special feature of Bs, which makes them so fascinating and enigmatic, is that they are only found in some individuals of a species and are completely absent from others: In other words, they are dispensable. We may look upon them as optional extras, which is a puzzling idea. It would not be puzzling was it not for the fact that Bs are not rarities at all, but are known in more than one thousand plants and several hundred animals. Bs are part of the genome in those species that carry them, but not an obligatory part like the basic set of A chromosomes. The standard reference that covers all aspects of Bs through the 1980s is by Jones and Rees; two other recent reviews update the story. The photos of Bs in rye (Secale cereale) in Fig. 1 are representative of how we see them in many plant species. In general terms we can profile them as follows:. At mitosis, Bs are morphologically distinct from the As in size (usually smaller), centromere position, and status of chromatin (often more heavily heterochromatic), which is how we first recognize them and distinguish them from extra copies of the As. . Their diagnostic feature is that they show no homology with any of the As and never pair or recombine with them—they follow their own evolutionary pathway. . They display non-Mendelian modes of inheritance due to their presence in variable numbers in different individuals and their special property of ‘‘selfishness’’ in terms of their numerical increase over generations. . In high numbers they reduce the vigor and fitness of plants. . Their phenotypic effects are of a quantitative nature, and they lack genes with major effects.
OCCURRENCE
The latest estimate gives the number of flowering plants with Bs as 1372, of which 12 are conifers and 1360 angiosperms. A few examples are known in ferns and fungi. Among flowering plants they occur in 738 monocots and 622 dicots, and they are found in polyploids as well as diploids. Their presence among families varies enormously, but this variation cannot be interpreted to fit any special pattern. The only thing we can say with any certainty is that they are most often seen in species favored for chromosome studies, such as the Liliaceae and Gramineae.
INHERITANCE
The non-Mendelian mode of transmission of Bs occurs because their number is variable, and meiosis is irregular due to complexities in pairing. In addition, there are systems of mitotic drive in some species (especially Gramineae) based on nondisjunction in gametophytes. In rye there is directed nondisjunction at the first pollen grain (Fig. 1) and first egg cell mitosis; this leads to an unreduced number of Bs being directed into the gametes. In maize the nondisjunction takes place at the second pollen mitosis, followed by preferential fertilization of the egg by the Bcarrying sperm, and likewise constitutes a selfish drive mechanism that causes the Bs to spread in natural populations. Equilibrium frequencies of Bs are reached when the forces of accumulation are balanced by those of meiotic loss and reduced fitness.
PHENOTYPIC EFFECTS
In general the phenotypic effects of Bs are either neutral (when they are present in low numbers) or harmful (when they are found in high numbers). These effects are manifested in all characters in a quantitative manner, but with some intriguing and unexplained differences depending on their occurrence in odd- or even-numbered combinations. Fertility is especially affected in a negative way by high B-numbers. There are some special diploidizing effects on meiosis in hybrid polyploid grass species, which has led to some optimism that Bs may have practical applications.
B chromosomes of rye (2n = 2x = 14+Bs) at mitosis and meiosis.
(a) c-metaphase in a root meristem cell in a plant with 2 Bs (arrowed).
(b) Metaphase I of meiosis shows 7 A-chromosome bivalents and a single unpaired B. The single B will divide at anaphase I and undergo loss at anaphase II. When 2 Bs are present they form a bivalent in most cells, but with higher numbers, multivalents are formed and meiosis is irregular.
(c) First mitosis of the pollen grain, showing a single B (arrowed) undergoing directed nondisjunction to the generative nucleus. The two chromatids of the B remain joined at sensitive sticking sites on each side of the centromere, and these receptors receive a signal from a genetic element near the end of the long arm of the B. When this element is deleted the Bs disjoin regularly. The spindle at first pollen grain mitosis is asymmetrical, with the equator nearest to the generative pole; it is thought that the sticking of the B chromatids delays their separation long enough for them to be passively included in the generative nucleus as the nuclear membrane encloses them at telophase.
(d) c-metaphase in a root meristem cell of a plant with 2 Bs after fluorescent in situ hybridization (FISH) with probes made from the D1100 and E3900 B-specific sequences.
NATURAL POPULATIONS
Large issues in terms of effects are to what extent B chromosomes are of adaptive significance and to what extent their natural polymorphisms are selfishly generated by mitotic drive, where this exists. There are two schools of thought, according to the system being investigated. In rye—one of the most intensely studied of all plant species—the situation is clear enough and was resolved by a computer simulation model.
This model demonstrated that the drive process based on nondisjunction in the gametophytes is strong enough to overcome all negative effects of the Bs on vigor and reproductive fitness and that the only factor that can negate the Bs is their own failure to pair and to segregate well at meiosis. The argument then becomes more esoteric and involves the antagonism and coevolutionary dynamics of Bs and anti-B genes in A chromosomes. We enter the dimension of host-parasite interactions, where we find the plants as hosts and the Bs as genome parasites.
The B-drive in maize is less strong than in rye, but the outcome is essentially the same and resolves the issue of how Bs come to exist so extensively in natural or seminatural populations. In maize, as in rye, Bs are not found in modern cultivars of these crops, and this is because of heavy selection for high fertility that quickly eliminates the B chromosomes. Chives (Allium schoenoprasum 2n = 2x = 16 + 0– 20 Bs) have Bs in natural populations, and tell a different story.
There is no obvious method of accumulation of the Bs in this species. In fact, they are transmitted at a mean of 0.39 in some populations, which is lower than the Mendelian rate of 0.5, and there is a net loss in progenies compared with their parents. Furthermore, their presence in high numbers reduces the fitness of the carriers, and this prompts the question of how they are maintained in nature. The hypothesis that is proposed, based on greenhouse experiments, is that there is differential selection operating at the seedling stage (based on drought tolerance) and that Bs confer some selective advantage in this respect.
CONCLUSION
In the final analysis, Bs remain enigmatic and intriguing. There is a wealth of data about their occurrence in populations, but a serious deficiency of understanding of the dynamics of their natural world. The glimpses we have been able to glean suggest a rich harvest of population genetics still awaits to be gathered before we even begin to close the book on this story. To complete the narrative we will also need more sequence data and a view of their mode of origin, which is missing at the present time.