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Rewiring the Sex-Determination Pathway During the Evolution of Self-Fertility
Yongquan Shen1, Shin-Yi Lin1, Jonathan Harbin1
1Department of Molecular Biology, Rowan-Virtua School of Translational Biomedical Engineering and Science, Rowan-Virtua School of Osteopathic Medicine, Stratford, NJ 08084, USA.
Abstract:
Although evolution is driven by changes in how regulatory pathways control development, we know little about the molecular details underlying these transitions. The TRA-2 domain that mediates contact with TRA-1 is conserved in Caenorhabditis. By comparing the interaction of these proteins in two species, we identified a striking change in how sexual development is controlled. Identical mutations in this domain promote oogenesis in Caenorhabditis elegans but promote spermatogenesis in Caenorhabditis briggsae. Furthermore, the effects of these mutations involve the male-promoting gene fem-3 in C. elegans but are independent of fem-3 in C. briggsae. Finally, reciprocal mutations in these genes show that C. briggsae TRA-2 binds TRA-1 to prevent expression of spermatogenesis regulators. By contrast, in C. elegans TRA-1 sequesters TRA-2 in the germ line, allowing FEM-3 to initiate spermatogenesis. Thus, we propose that the flow of information within the sex determination pathway has switched directions during evolution. This result has important implications for how evolutionary change can occur.
Insights
Evolutionary changes in sex determination pathways were uncovered by comparing Caenorhabditis nematodes. A conserved protein interaction switches function, impacting oogenesis versus spermatogenesis, revealing novel insights into developmental evolution.
Area of Science:
- Developmental biology
- Evolutionary genetics
- Molecular biology
Background:
- Evolutionary transitions in development are driven by changes in regulatory pathways.
- The molecular mechanisms underlying these developmental shifts remain largely unknown.
- The TRA-2 domain, crucial for TRA-1 interaction, is conserved across Caenorhabditis species.
Purpose of the Study:
- To investigate the molecular basis of evolutionary changes in sex determination pathways.
- To compare the function of the TRA-2/TRA-1 interaction in Caenorhabditis elegans and Caenorhabditis briggsae.
- To elucidate how alterations in protein interactions drive evolutionary transitions in development.
Main Methods:
- Comparative analysis of TRA-2 and TRA-1 protein interactions across two Caenorhabditis species.
- Introduction of identical mutations in the TRA-2 domain in both species.
- Examination of the effects of these mutations on oogenesis and spermatogenesis.
- Investigation of the role of the fem-3 gene in C. elegans sex determination.
Main Results:
- Identical mutations in the TRA-2 domain differentially regulate sexual development: promoting oogenesis in C. elegans and spermatogenesis in C. briggsae.
- The effects of these mutations are dependent on the fem-3 gene in C. elegans but independent in C. briggsae.
- Reciprocal mutations reveal that C. briggsae TRA-2 inhibits spermatogenesis regulators, while C. elegans TRA-1 sequesters TRA-2, enabling spermatogenesis initiation.
Conclusions:
- The direction of information flow within the sex determination pathway has likely switched during evolution between C. elegans and C. briggsae.
- This study provides a molecular example of how changes in conserved protein interactions can lead to significant evolutionary shifts in developmental processes.
- Understanding these molecular switches is key to comprehending the broader mechanisms of evolutionary change.
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