Non-Mendelian transmission of accessory chromosomes in fungi

Abstract

Non-Mendelian transmission has been reported for various genetic elements, ranging from small transposons to entire chromosomes. One prime example of such a transmission pattern are B chromosomes in plants and animals. Accessory chromosomes in fungi are similar to B chromosomes in showing presence/absence polymorphism and being non-essential. How these chromosomes are transmitted during meiosis is however poorly understood-despite their often high impact on the fitness of the host. For several fungal organisms, a non-Mendelian transmission or a mechanistically unique meiotic drive of accessory chromosomes have been reported. In this review, we provide an overview of the possible mechanisms that can cause the non-Mendelian transmission or meiotic drives of fungal accessory chromosomes. We compare processes responsible for the non-Mendelian transmission of accessory chromosomes for different fungal eukaryotes and discuss the structural traits of fungal accessory chromosomes affecting their meiotic transmission. We conclude that research on fungal accessory chromosomes, due to their small size, ease of sequencing, and epigenetic profiling, can complement the study of B chromosomes in deciphering factors that influence and regulate the non-Mendelian transmission of entire chromosomes.

Keywords: Accessory chromosomes; Disomy; Fungi; Meiotic drive; Non-Mendelian transmission.

Fig. 1

a Life cycle of Z. tritici as an example of an Ascomycete life cycle containing both asexual and sexual reproduction. Asexual reproduction results in pycnidiospores (asexual haploid spores), produced by asexual fruiting body (pycnidia) in infected wheat leaves (adapted from Ponomarenko 2011). The asexual cycle is assumed to only contain haploid cells. Sexual reproduction in Z. tritici results in ascospores (sexual haploid spores) produced in the sexual fruiting body (pseudothecium). Here, two specialized haploid cells fuse to form a diploid zygote which undergoes two meiotic cell divisions and one mitotic cell division to produce eight haploid ascospores contained in a sac-like structure (ascus). b Example pictures of asexual fruiting body (pycnidia) formed by Z. tritici on necrotic leaf tissue lesion carrying asexual pycnidiospores on a wheat leaf infected with Z. tritici. c Example picture of in vitro growth of Z. tritici growing on xylose minimum medium. d–e Models for losses and disomies of fungal accessory chromosomes due to nondisjunction of d homologous chromosomes or e sister chromatids during meiotic cell divisions. d Homologous accessory chromosomes fail to segregate at first meiotic division which leads to their disomy in half of the progeny and the absence of respective homologous accessory chromosomes in the remaining half of ascospores. e Nondisjunction of sister chromatids during the second meiotic division causes loss and disomy of accessory chromosomes. In contrast to disomic progeny from d, disomic accessory chromosomes are identical and chromosomes are absent in 25% of the progeny. For the sake of clarity, no recombination events are depicted

Fig. 2

Meiotic drive of accessory chromosomes in Z. tritici. a Accessory chromosomes show presence/absence polymorphisms among individuals in populations and thus can be unpaired during meiosis. The chromosomal drive during meiosis in Z. tritici is restricted to female-inherited and unpaired accessory chromosomes (light blue) and causes an overrepresentation of female-inherited unpaired accessory chromosomes in the progeny. b Male-inherited unpaired accessory chromosomes (light blue) show Mendelian segregation as well as the paired accessory chromosomes (light green and dark green). The potential mechanism of the meiotic drive of accessory chromosomes likely involves additional replication that can happen either c prior to the fusion of two haploid gametes or d in the diploid zygote. If c is true, all chromosomes in the female haploid gamete should be amplified (red arrow), and in the zygote, the additional copies of paired accessory chromosomes must be deleted (red cross). Alternatively, d the unpaired female-inherited accessory chromosomes are amplified in the zygote. For simplicity, recombination events are not shown