Meiotic drive of female-inherited supernumerary chromosomes in a pathogenic fungus

Abstract

Meiosis is a key cellular process of sexual reproduction that includes pairing of homologous sequences. In many species however, meiosis can also involve the segregation of supernumerary chromosomes, which can lack a homolog. How these unpaired chromosomes undergo meiosis is largely unknown. In this study we investigated chromosome segregation during meiosis in the haploid fungus Zymoseptoria tritici that possesses a large complement of supernumerary chromosomes. We used isogenic whole chromosome deletion strains to compare meiotic transmission of chromosomes when paired and unpaired. Unpaired chromosomes inherited from the male parent as well as paired supernumerary chromosomes in general showed Mendelian inheritance. In contrast, unpaired chromosomes inherited from the female parent showed non-Mendelian inheritance but were amplified and transmitted to all meiotic products. We concluded that the supernumerary chromosomes of Z. tritici show a meiotic drive and propose an additional feedback mechanism during meiosis, which initiates amplification of unpaired female-inherited chromosomes.

Extraordinary Genome Instability and Widespread Chromosome Rearrangements During Vegetative Growth

“…While beneficial effects, even if they are comparably small, might explain the maintenance of accessory chromosomes in Z. tritici populations, negative effects as observed in this study and reported by Habig et al (2017) raise the question why these chromosomes have not been lost over time, especially as they can easily be lost during meiosis and mitosis. Accessory chromosome can be lost during meiosis ( Wittenberg et al 2009 ), but interestingly accessory chromosomes have also been shown to follow non-Mendelian segregation and to be transmitted at a significantly higher rate than expected, if one of the two mating partners lacks an accessory chromosome ( Fouché et al 2018 ; Habig et al , 2018 ). While there is no comprehensive mechanistic explanation yet, chromosome conservation by re-replication during meiosis may counteract the chromosome loss during vegetative growth and therefore maintain accessory chromosomes in pathogen populations.…”

Genome size evolution: towards new model systems for old questions

“…Further, even fewer of these present opportunity for experimentation which will lead to a deeper and more concrete understanding of the evolution of GS. Such an ambitious approach, which has been successfully employed in at least one pathogenic fungal species, revealed that accessory chromosomes which exhibit meiotic drive [123] are also associated with genome instability and an increase in virulence and fitness [124]. Here, I consider a further few promising model systems for testing the causality of these correlations through direct manipulation of both the environment and GS, to see the outcome on a phenotypic level.…”

Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria

“…The haploid genome of the reference isolate IPO323 comprises thirteen core and eight accessory chromosomes [23]. Some of these accessory chromosomes may encode traits that impact virulence of the fungus, however no gene encoded on an accessory chromosome has so far been described as a virulence or avirulence determinant [24][25][26][27][28][29]. Interestingly, the accessory chromosomes in Z. tritici show a low transcriptional activity in vitro as well as in planta [30,31].…”