Failure of Parastrongyloides trichosuri daf-7 to complement a Caenorhabditis elegans daf-7 (e1372) mutant: implications for the evolution of parasitism

Abstract

DAF-7 is the ligand of the TGF-β pathway that, in conjunction with the insulin-like and guanylyl cyclase pathways, controls entry into dauer development in Caenorhabditis elegans. Proposed orthologues of Ce-daf-7 have been identified in several species of parasitic nematodes and demonstrate an expression pattern that is consistent between parasitic nematode genera but different to that of Ce-daf-7. This variation in expression pattern is consistent with the current paradigm in evolutionary developmental biology: that regulatory rather than functional change is the primary source of phenotypic diversity. In this work we investigated the proposed orthology of a daf-7 like sequence obtained from Parastrongyloides trichosuri, Pt-daf-7, to Ce-daf-7 via transformation rescue of a C. elegans daf-7 mutant with Pt-daf-7 coding regions. We also investigated further the difference in expression pattern of Pt-daf-7 both by fusing a Pt-daf-7 promoter to a Ce-daf-7 coding region and to a gfp reporter gene. We found that Pt-daf-7 was unable to complement a C. elegans daf-7 mutant, even when reduced to the smallest functional TGF-β unit possible, the ligand domain, and that this failure appears to be the result of gene silencing. Furthermore, we show that although the Pt-daf-7 promoter is active later in development than the Ce-daf-7 promoter and most likely active in the correct neurons, a Ce-daf-7 coding region under control of a Pt-daf-7 promoter failed to rescue. Together, these results suggest that, if the free-living nematode developmental pathways, such as the DAF-7 TGF- β pathway, have been co-opted during the evolution of parasitism, this co-option has been both at the protein level and in the control of their transcription.