The genome-wide meiotic recombination landscape in ciliates and its implications for crossover regulation and genome evolution

Meiotic recombination is essential for sexual reproduction and its regulation has been extensively studied in many taxa.However,genome-wide recombination landscape has not been reported in ciliates and it remains unknown how it is affected by the unique features of ciliates:the synaptonemal complex(SC)-independent meiosis and the nuclear dimorphism.Here,we show the recombination landscape in the model ciliate Tetrahymena thermophila by analyzing single-nucleotide polymorphism datasets from 38 hybrid progeny.We detect 1021 crossover(CO)events(35.8 per meiosis),corresponding to an overall CO rate of 9.9 cM/Mb.However,gene conversion by non-crossover is rare(1.03 per meiosis)and not biased towards G or C alleles.Consistent with the reported roles of SC in CO interference,we find no obvious sign of CO interference.CO tends to occur within germ-soma common genomic regions and many of the 44 identified CO hotspots localize at the centromeric or subtelomeric regions.Gene ontology analyses show that CO hotspots are strongly associated with genes responding to environmental changes.We discuss these results with respect to how nuclear dimorphism has potentially driven the formation of the observed recombination landscape to facilitate environmental adaptation and the sharing of machinery among meiotic and somatic recombination.

Crossover patterns under meiotic chromosome program

Repairing DNA double-strand breaks(DSBs)with homologous chromosomes as templates is the hallmark of meiosis.The critical outcome of meiotic homologous recombination is crossovers,which ensure faithful chromosome segregation and promote genetic diversity of progenies.Crossover patterns are tightly controlled and exhibit three characteristics:obligatory crossover,crossover interference,and crossover homeostasis.Aberrant crossover patterns are the leading cause of infertility,miscarriage,and congenital disease.Crossover recombination occurs in the context of meiotic chromosomes,and it is tightly integrated with and regulated by meiotic chromosome structure both locally and globally.Meiotic chromosomes are organized in a loop-axis architecture.Diverse evidence shows that chromosome axis length determines crossover frequency.Interestingly,short chromosomes show different crossover patterns compared to long chromosomes.A high frequency of human embryos are aneuploid,primarily derived from female meiosis errors.Dramatically increased aneuploidy in older women is the well-known“maternal age effect.”However,a high frequency of aneuploidy also occurs in young women,derived from crossover maturation inefficiency in human females.In addition,frequency of human aneuploidy also shows other age-dependent alterations.Here,current advances in the understanding of these issues are reviewed,regulation of crossover patterns by meiotic chromosomes are discussed,and issues that remain to be investigated are suggested.