1. Identification of BiP as a temperature sensor mediating temperature-induced germline sex reversal in C. elegans.
- Author
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Shi, Jing, Sheng, Danli, Guo, Jie, Zhou, Fangyuan, Wu, Shaofeng, and Tang, Hongyun
- Subjects
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TEMPERATURE-dependent sex determination , *SEX reversal , *SEX determination , *CAENORHABDITIS elegans , *HIGH temperatures , *GENETIC sex determination - Abstract
Sex determination in animals is not only determined by karyotype but can also be modulated by environmental cues like temperature via unclear transduction mechanisms. Moreover, in contrast to earlier views that sex may exclusively be determined by either karyotype or temperature, recent observations suggest that these factors rather co-regulate sex, posing another mechanistic mystery. Here, we discovered that certain wild-isolated and mutant C. elegans strains displayed genotypic germline sex determination (GGSD), but with a temperature-override mechanism. Further, we found that BiP, an ER chaperone, transduces temperature information into a germline sex-governing signal, thereby enabling the coexistence of GGSD and temperature-dependent germline sex determination (TGSD). At the molecular level, increased ER protein-folding requirements upon increased temperatures lead to BiP sequestration, resulting in ERAD-dependent degradation of the oocyte fate-driving factor, TRA-2, thus promoting male germline fate. Remarkably, experimentally manipulating BiP or TRA-2 expression allows to switch between GGSD and TGSD. Physiologically, TGSD allows C. elegans hermaphrodites to maintain brood size at warmer temperatures. Moreover, BiP can also influence germline sex determination in a different, non-hermaphroditic nematode species. Collectively, our findings identify thermosensitive BiP as a conserved temperature sensor in TGSD, and provide mechanistic insights into the transition between GGSD and TGSD. Synopsis: Temperature has long been known to modulate sex in various animals, but the mechanism for transducing temperature into a sex reversal signal is still a mystery. This work identifies BiP as a sensor that translates ambient temperature cues into the germline sex determination signal in C. elegans. Genotypic germline sex determination (GGSD) in wild-isolated and mutant C. elegans strains can be overridden by temperature changes. BiP sequestration for increased ER protein folding burden upon temperature elevation causes ERAD-mediated downregulation of the oocyte fate-driving factor, TRA-2. BiP's role in germline sex determination is conserved in a dioecious nematode species. Manipulation of BiP-dependent transduction allows switching between GGSD and temperature-dependent germline sex determination (TGSD). TGSD facilitates brood size maintenance in C. elegans hermaphrodites at elevated temperatures. Masculinization of the C. elegans germline in response to temperature elevation is mediated by BiP, which can override genotypic sex determination. [ABSTRACT FROM AUTHOR]
- Published
- 2024
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