Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Abstract

Plant-parasitic cyst nematodes induce hypermetabolic syncytial nurse cells in the roots of their host plants. Syncytia are their only food source. Cyst nematodes are sexually dimorphic, with their differentiation into male or female strongly influenced by host environmental conditions. Under favourable conditions with plenty of nutrients, more females develop, whereas mainly male nematodes develop under adverse conditions such as in resistant plants. Here, we developed and validated a method to predict the sex of beet cyst nematode (Heterodera schachtii) during the early stages of its parasitism in the host plant Arabidopsis thaliana. We collected root segments containing male-associated syncytia (MAS) or female-associated syncytia (FAS), isolated syncytial cells by laser microdissection, and performed a comparative transcriptome analysis. Genes belonging to categories of defence, nutrient deficiency, and nutrient starvation were over-represented in MAS as compared with FAS. Conversely, gene categories related to metabolism, modification, and biosynthesis of cell walls were over-represented in FAS. We used β-glucuronidase analysis, qRT-PCR, and loss-of-function mutants to characterize FAS-and MAS-specific candidate genes. Our results demonstrate that various plant-based factors, including immune response, nutrient availability, and structural modifications, influence the sexual fate of the cyst nematodes. K E Y W O R D S cyst nematodes, environmental sex determination, plant-nematode interaction, host-plant interaction

Possible stochastic sex determination in Bursaphelenchus nematodes

“…For example, the root-knot nematodes, Meloidogyne spp., and cyst nematodes, Heterodera spp./ Globodera spp. have been suggested to have ESD 49 – 51 . However, while it has been considered that sex is determined by the nutrient status of the host or under stress conditions in these nematodes, the molecular sex determination mechanisms are unknown.…”

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

“…Unusually for an animal, cyst nematode sex is determined during parasitism. It is understood that the sexually undetermined juvenile with access to ample nutrition (from a well-formed feeding site) will preferentially develop into a female, while those with limited nutrition preferentially develop into males, stop feeding, and regain motility and search for a mate 13 , 14 . The obligate sexual cyst nematode females will ultimately fill with eggs, their body wall will tan and harden, and the resultant cyst will drop off the root, and their eggs can remain dormant in the soil for several years.…”

The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5

“…Unusually for an animal, cyst nematode sex is determined during parasitism. It is understood that the sexually undetermined juvenile with access to ample nutrition (from a well-formed feeding site) will preferentially develop into a female, while those with limited nutrition preferentially develop into males, stop feeding, and regain motility and search for a mate (F. Grundler, Betka, and Wyss 1991;Anjam et al 2020). The obligate sexual cyst nematode females will ultimately fill with eggs, their body wall will tan and harden, and the resultant cyst will drop off the root, and their eggs can remain dormant in the soil for several years.…”