Environmental sex determination in the cyst nematode Globodera pallida defaults to male development

Abstract

Environmental sex determination (ESD) enables organisms to adjust their sexual fate in response to external cues. Fluctuating sex ratios have long suggested the presence of ESD in populations of plant-parasitic nematodes. We show that in the potato cyst nematode Globodera pallida sex is regulated by nutritional cues. By manipulating sucrose availability to the host plant, we could steer the sex determination of G. pallida. Whereas high-sucrose medium promotes female development, low-sucrose medium promotes male development. Transcriptome analyses on the early stages of parasitism reveal that female development requires extensive transcriptional activation and post-transcriptional regulation. We identify Gp-lin-29, a transcription factor homologous to lin-29 in Caenorhabditis elegans, as a potential regulator of ESD. Small RNA sequencing uncovered the male-biased expression of Gp-let-7, a putative repressor of Gp-lin-29, and the female-biased expression of four miRNAs, including Gp-miR-100, located at the same genomic locus as Gp-let-7. Target prediction and enrichment analyses suggest that these female-biased miRNAs actively suppress male developmental programs. Together, our findings support a model in which G. pallida juveniles follow a default male developmental trajectory unless redirected by favourable environmental cues to become female. This study provides mechanistic insight into ESD in cyst nematodes and positions G. pallida as a tractable system for exploring epigenetic regulation of developmental plasticity.