The molecular basis of how cyst nematodes coordinate their life cycle with their host

Plant-parasitic nematodes cause huge damage to global agriculture. In the UK, the potato cyst nematodes (PCN) are the most important pests of potato and an absence of effective control measures for PCN causes major problems for potato growers. A key point in the PCN life cycle is a dormant survival stage - the second stage juvenile - which remains unhatched and protected in the eggs. As PCN cannot infect other crops the unhatched nematode remains dormant until chemical cues are detected from the roots of growing potato plants. In our previous work we have identified an annexin protein present in the eggshell of PCN. We have shown that this annexin is required by the nematode to maintain the normal function of the eggshell and that the protein undergoes a change in the presence of the chemical cues present in root diffusates. These data suggest that this protein plays a key role in allowing the nematode to respond to the presence of host plants. Annexins are calcium dependent lipid binding proteins. In this project we aim to determine how the annexin responds to the presence of host chemical cues and calcium to control changes in the permeability of the lipid layers in the eggshell and thus provides a link between the nematode life cycle and the presence of a host plant.

This project will determine the molecular basis by which this protein links hatch of PCN to the presence of host root diffusates. Our preliminary data have allowed the identification of an eggshell localised annexin, which contains a unique (to this specific annexin in PCN) an insertion in one of the predicted calcium binding sites of the protein. We have confirmed that this annexin binds lipids in a calcium-dependent manner and that it undergoes a conformational change in the presence of calcium that is lost in the presence of host root diffusates. Silencing of the gene encoding this annexin disrupts the ability of the nematode to control the permeability of the eggshell. Collectively these data suggest a critical role for the annexin in linking activation of the nematode life cycle to the presence of host derived chemical cues. In this project we will determine the structural and biochemical basis by which the annexin responds to compounds present in root diffusates and changes the permeability of the nematode eggshell.

Cyst nematodes are devastating crop pathogens and the majority have a restricted host range. In the UK, the potato cyst nematode (PCN) species Globodera rostochiensis and G. pallida cause extensive damage to potato crops, valued in excess of £50 million per annum in the UK alone (Jones et al., 2017, Global Change Biology 23, 4497-4507). A lack of resistance (particularly against G. pallida) in commercially viable cultivars, coupled with the withdrawal of many effective nematicides due to potential environmental concerns, has led to the AHDB listing PCN as the most important pest faced by potato growers in the UK (https://potatoes.ahdb.org.uk/agronomy/plant-health-weed-pest-disease-management/pcn). New infestations into previously clean land threatens the future of the seed industry in Scotland. In addition, PCN has been reported in several sub-Sharan African countries where potato is a major food and cash crop for smallholder farmers and is causing huge yield losses in this region. New control strategies for PCN therefore offer the potential for major societal impact.
The proposed work described here offers the potential for scientific advances in terms of our understanding of the interaction between plants and pathogens as well as the development of new knowledge that could underpin development of new control strategies for these devastating pathogens. The proposed work will provide the starting point for new chemical control agents that specifically target the function of this protein. This protein represents an attractive control target as it is specific to pest species of nematode and can be targeted in the dormant stage of the nematode. These features contrast with current chemical control strategies which have broad off-target effects and are effective only against the juvenile stage which is active for a very short time in the soil. The unique opportunity for development of new cyst nematode control tools presented by this protein is recognised by Syngenta, who have provided a letter of support confirming their willingness to further exploit the findings derived from this project.