Persistence

Some animals have evolved to withstand the assault of extreme environmental conditions over long periods when a suitable food source is not available. Plant parasitic nematodes, more specifically the cyst nematodes, are good examples of this. These microscopic animals live in the soil and are dependent on specific species of host plants as food sources. Currently the control of these obligate parasites represents the largest variable cost to growers of crops such as potatoes. The potato cyst nematodes, which can only infect Solanaceous plants, exhibit remarkable persistence and can survive dormant in the soil for decades before emerging to infect crops. Encysted eggs retained in the hardened body wall of the female are the survival stage that is able to persist in the absence of a host plant and survive adverse soil temperature and moisture. This ability to survive long periods in the soil underlies their status as agriculturally important global pathogens.

We have recently identified UK populations of potato cyst nematode that vary in their longevity in the field i.e. their viability in the absence of a potato crop declines at different rates. Importantly, we have also found that the rate at which nematode viability declines in the soil can be very much slower than previously described. This finding has important implications for management and control of potato cyst nematode, especially given the dwindling chemical control options available to UK growers. The specific molecular and biochemical mechanisms that allow this extraordinary longevity remain unanswered. These newly-identified long-lived populations offer a unique opportunity to understand the basic processes that protect the animal across a wide range of extreme environmental conditions.
Cumulative damage to biological macromolecules including DNA, RNA, proteins and lipids occurs in cells during prolonged periods of dormancy. There is thus strong selection pressure to ensure that extending lifespan in dormancy does not compromise subsequent vigour. We hypothesise that, similar to desiccation-tolerant seeds, cyst nematodes have evolved powerful protection and repair mechanisms. Recent advances by co-I West have revealed crucial roles for genome maintenance pathways in the extended survival of seeds in the quiescent state. These features are shared widely amongst anhydrobiotic organisms and provide an exciting new target for understanding and attenuating the nematode lifecycle.

This project will combine a range of techniques to reveal how nematodes have adapted to survive for extended periods in the soil. We will assess how much and what types of cellular damage accumulate during nematode dormancy. We have collections of stored nematode cysts that span a 30 year period of dormancy so we can analyse these to determine if cellular damage increases over time and when it reaches a critical point that affects survival. We will also determine the activity of DNA repair mechanisms that act in genome maintenance pathways after potato cyst nematode eggs rehydrate and are released from dormancy. We predict that cyst nematodes will require mechanisms to provide enhanced protection from damage during and after dormancy. We will analyse and compare global gene expression in dormant, rehydrated and hatched nematodes to identify the predominant stresses associated with these states and the mitigation strategies that protect and repair any damage. Finally, we will use our main findings to correlate the unexpected extreme longevity of recently discovered populations of potato cyst nematode with activity of molecular protect and repair mechanisms. This will provide the first evidence for the molecular basis of nematode longevity in the soil, fundamental to the development of a new suite of control measures.

Potato cyst nematode parasites (PCN) cause great economic losses across the potato sector worldwide. Encysted eggs retained in the hardened body wall of the female are the survival stage in the soil. They exhibit remarkable longevity with dormant juveniles able to remain viable for more than 20 years. This ability contributes significantly to the economic importance of cyst nematodes. The driver for this proposal was our recent survey of PCN across England: we found that some PCN field populations exhibit far higher persistence than previously described. This offers a unique opportunity to investigate the basic processes that protect the animal during dormancy and understand how such extreme longevity may arise. These processes may be analogous to those that allow seeds to remain viable in the soil for many years. Consequently this application brings together experts in organisms from both the plant and animal kingdoms to determine the molecular and biochemical mechanisms that underlie the extraordinary longevity of PCN. Cyst nematodes must have incredibly efficient systems to counteract the cumulative damage to biological macromolecules that will occur during prolonged dormancy. We will investigate the extent to which damage accumulates over time in dormant eggs of the PCN Globodera pallida, which molecules are most severely compromised and the specific characteristics of that damage. A transcriptomic approach will identify key cellular factors associated with enhanced longevity in the dormant stage and damage response factors expressed on rehydration where our focus will be on DNA damage and genome maintenance. We will investigate the role played by key genes using RNAi. The new knowledge will be synthesised to correlate the extreme persistence of some PCN populations with activity of protect and repair mechanisms thereby discovering molecular signatures of extreme longevity in G. pallida.