Plant parasitic nematode proteins and the host–parasite interaction

Rosane H. C. Curtis This review focuses on the proteins and secretions of sedentary plant parasitic nematodes potentially important for plant^ nematode interactions. These nematodes are well equipped for parasitism of plants. Having acquired the ability to manipulate fundamental aspects of plant biology, they are able to hijack host-cell development to make their feeding site. They feed exclusively from feeding sites as they complete their life cycle, satisfying their nutritional demands for development and reproduction. Biochemical and genomic approaches have been used successfully to identify a number of nematode parasitism genes. So far, 65 204 expressed sequence tags (ESTs) have been generated for six Meloidogyne species and sequencing projects, currently in progress, will underpin genomic comparisons of Meloidogyne spp. with sequences of other pathogens and generate genechip microarrays to undertake profiling studies of up- and down-regulated genes during the infection process. RNA interference provides a molecular genetic tool to study gene function in parasitism. These methods should provide new data to help our understanding of how parasitic nematodes infect their hosts, leading to the identification of novel pathogenicity genes. - BACKGROUND Currently, plant parasitic nematodes are a major limitation on crop yield and quality causing estimated losses of $70 billion per annum [1]. The sedentary plant parasitic root-knot nematodes (Meloidogyne spp.) and cyst nematodes (Globodera spp. and Heterodera spp.) are amongst the worlds most damaging agricultural pests attacking a wide range of crops. Due to their economic importance and their intimate hostparasite relationship, this review focuses on these nematodes. Current approaches to combat agricultural losses are the use of nematicides, cultural techniques and resistant varieties that may be used in an integrated manner. Nematicides include some of the most hazardous compounds used in agriculture and alternative control is required urgently, because of health and environmental concerns over their use. The complex nematode life cycle consists of eggs and a distinct free living pre-parasitic stage in the soil and parasitic stages inside the root tissue. Once hatched from eggs, the second-stage juvenile (J2) of cyst and root-knot nematodes does not feed in soil and thus must have a behavioural strategy that makes efficient use of its lipid reserves to find a host plant; if these reserves are depleted by more than 65% of the original level the juvenile is unable to invade plants and establish a feeding site [2]. Therefore, to establish a successful parasitic relationship with plants, nematodes rely on behavioural strategies based on their well developed nervous system, including specific sense cells and also on special structures (such as the stylet and large pharyngeal glands) for efficient root-cell penetration and modification, and food withdrawal and digestion. Biology of cyst and root-knot nematodes The J2s of cyst forming nematodes are attracted to, and penetrate, plant roots to migrate intracellularly towards the vascular cylinder, where they establish an intimate nutritional relationship with their host through the development of syncytial feeding sites. Rosane H. C. Curtis, Nematode Interactions Unit, Division of Plant-Pathogen Interactions, Rothamsted-Research, Harpenden, AL5 2JQ, Hertfordshire, UK. E-mail: Rosane H. C. Curtis works in Rothamsted-Research within the Nematology group studying host recognition processes, the focus of her research is the identification of nematode molecules important for plant-nematode interactions. During nematode development, the syncytium continuously increases in volume by incorporation of neighbouring cells through cell wall breakdown. The syncytium becomes a large multinucleated hypertrophied cell generated by the fusion of as many as 200 neighbouring protoplasts after partial cell wall dissolution [3]. The juveniles undergo three additional moults before reaching the adult stage. When feeding commences, the juvenile body grows and becomes saccate and immobile (Figure 1A and B). The vermiform males regain their mobility and leave the root to migrate in the soil, where they are attracted to the females by a pheromone and fertilization occurs. The fertilized females produce eggs, most of which remain inside their bodies. They become a protective cyst, when they die and under favourable conditions the J2 will hatch and migrate towards a new host root [3]. In contrast, J2 of root-knot nematodes after penetrating the root epidermis migrate intercellularly between cortical cells until they find a suitable root cell to form their feeding site. Root cells around the nematodes head are stimulated to go through repeated rounds of mitosis uncoupled from cytokinesis, leading to multinucleated giant cells [4]. The juveniles moult three times and although males can be formed, reproduction of most root-knot nematodes is by parthenogenesis. Eggs are deposited outside the female body and stay in a protective proteinaceous matrix secreted by the female until they are ready to hatch as J2 and then continue the nematodes life-cycle which takes approximately 2530 days from eggs to adults. Syncytium and giant cell maintenance require repeated stimulation from the nematode and cyst, and root-knot nematodes depend entirely on functional feeding cells to complete their life cycles. Nematode invasion of roots and their migration to their feeding sites results in changed root architecture and significant reductions in nutrient and water uptake and consequent crop yields. The hostparasite relationship is governed by a complex network of interactions and in susceptible interactions there is a subtle interplay between parasite survival strategies and host defense mechanisms. Understanding the complexity of the molecular signal exchange and response during infection of plants is important to identify vulnerable points in the life cycle of the parasite, which can be used to target disruption of nematodehostrecognition, nematode migration and feeding inside root tissue. This information will be useful in defining those processes that are essential for pathogenesis by the nematode. Nematode signals potentially important for the plant^nematode relationship Feeding cell formation is presumably initiated in response to signal molecules released by the parasitic J2, but the nature of the primary stimulus is unknown, as is the host target for the presumed nematode ligand(s), which must be transduced to elicit the feeding site. The most widely held hypothesis is that the necessary metabolic re-programming of root cells is triggered by specific nematode secretions, which presumably interact with membrane or cytoplasmic receptors in the plant to switch on cascades of gene expression that alter cell development [57]. As nematodes set up their feeding site they alter plant gene expression, leadin (...truncated)