Eberly College of Arts and Sciences
Turnovers of sex-determining systems represent important diversifying forces across eukary- otes. Shifts in sex chromosomes—but conservation of the master sex-determining genes— characterize distantly related animal lineages. Yet in plants, in which separate sexes have evolved repeatedly and sex chromosomes are typically homomorphic, we do not know whether such translocations drive sex-chromosome turnovers within closely related taxo- nomic groups. This phenomenon can only be demonstrated by identifying sex-associated nucleotide sequences, still largely unknown in plants. The wild North American octoploid strawberries (Fragaria) exhibit separate sexes (dioecy) with homomorphic, female heteroga- metic (ZW) inheritance, yet sex maps to three different chromosomes in different taxa. To characterize these turnovers, we identified sequences unique to females and assembled their reads into contigs. For most octoploid Fragaria taxa, a short (13 kb) sequence was observed in all females and never in males, implicating it as the sex-determining region (SDR). This female-specific “SDR cassette” contains both a gene with a known role in fruit and pollen production and a novel retrogene absent on Z and autosomal chromosomes. Phy- logenetic comparison of SDR cassettes revealed three clades and a history of repeated translocation. Remarkably, the translocations can be ordered temporally due to the capture of adjacent sequence with each successive move. The accumulation of the “souvenir” sequence—and the resultant expansion of the hemizygous SDR over time—could have been adaptive by locking genes into linkage with sex. Terminal inverted repeats at the inser- tion borders suggest a means of movement. To our knowledge, this is the first plant SDR shown to be translocated, and it suggests a new mechanism (“move-lock-grow”) for expan- sion and diversification of incipient sex chromosomes.
Digital Commons Citation
Tennessen, Jacob A.; Wei, Na; Straub, Shannon C.K.; Govindarajulu, Rajanikanth; Liston, Aaron; and Ashman, Tia-Lynn, "Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries" (2018). Faculty & Staff Scholarship. 1514.
Tennessen JA, Wei N, Straub SCK, Govindarajulu R, Liston A, Ashman T-L (2018) Repeated translocation of a gene cassette drives sex-chromosome turnover in strawberries. PLoS Biol 16(8): e2006062. https://doi.org/10.1371/ journal.pbio.2006062