Plant-parasitic nematode feeding tubes and plugs: new perspectives on function

Abstract

Sum m ary -Several structures associated with feeding by plant-parasitic nematodes have been described using two terms, feeding tubes and feeding plugs. However, both of these terms encompass multiple structures of independent evolution, some of which are functionally distinct. We have reviewed the literature on both structures and provide a new perspective on the function of intracellular feeding tubes to maintain the integrity and efficacy of the feeding site. We propose that they provide sufficient hydraulic resistance against the feeding site pressure to prevent it from collapsing during feeding. In addition, we propose that extracellular feeding tubes of migratory ectoparasites should be considered as the functional analogue of the stylet of all other plant-parasitic nematodes for withdrawal of host cell cytoplasm and, therefore, provide an example of convergent evolution. We also suggest that the main role of the feeding plug, irrespective of origin or composition, may be in adhesion.Keywords -biotrophic interactions, convergent evolution, hydraulic resistance, nematode feeding. Plant-parasitism by nem atodes encom passes a diverse array o f parasitism strategies. A w ide range and num ber o f species exist that are capable o f parasitising the roots, stem s or leaves o f plants. By far the m ost econom ically dam aging, and consequently the m ost studied, are those that parasitise roots. In general, root-parasitic ne m atodes can be broadly divided into tw o categories: those that spend their life cycle outside the host (ectoparasites), and those that spend part, if not all, o f their life w ithin the host (sem i-endoparasites and endoparasites). T he endoparasites include both m igratory and sedentary species, both o f w hich cause extensive dam age to root system architecture. M igratory endoparasites m ove destructively inside the root, feeding on cells that they disrupt. Seden tary endoparasites spend the m ajority o f their adult life inside the host; they re-program m e host root cells, by the secretion o f effectors, to create a highly m etabolically ac tive nutrient sink from w hich they feed for a num ber o f weeks. Plant-parasitic nem atodes, and the various m odes o f parasitism , are distributed across four o f the 12 clades o f the phylum N em atoda (van M egen et al., 2009) (Fig. 1). C lade 1 contains the m igratory ectoparasitic Trichodorus species, w hile C lade 2 contains the m igratory ectopara sitic Longidorus and Xiphinema species. Species o f two plant-parasitic genera, Bursaphelenchus (m igratory endoparasitic) and the foliar plant-parasitic Aphelenchoides, are found in C lade 10. T he m ajority o f plant-parasitic species, including the m ost econom ically im portant m i gratory endoparasitic and sedentary endoparasitic species,are found in C lade 12. In addition, it is generally ac cepted that, w ithin C lade 12, sedentary plant-parasitism has arisen on at least tw o separate occasions for the cyst and root-knot nem atodes, although given the range and diversity o f parasitic strate...

Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene

“…Hereafter, Clade 3 genes are thus referred to as GS-like effector genes. While it is highly unusual for a 100 kilodalton pathogen effector to be translocated to the host cell cytoplasm (GS-like effectors are obligate homo-dimers of 50 kDa per subunit, S4 Fig ), plant parasitic nematodes clearly have the ability to construct organelle-sized structures inside the host cell at the plasma membrane where it meets the stylet orifice (reviewed in [ 32 ]). The demonstrations that a native GS-like effector protein is secreted from the nematode, delivered into the host, translocated across the host plasma membrane, and localised within the host cell during parasitism are strong evidence of involvement in parasitism.…”

Potato cyst nematodes Globodera rostochiensis and G. pallida

“…The J2 feeds on the syncytium contents using a feeding tube that is produced during each feeding cycle. It has been suggested that this acts as a filter to prevent destruction of the feeding site, which the nematode must keep alive for the duration of the life cycle (Eves‐van den Akker, Lilley, Jones, et al., 2015). Once the feeding site is established and feeding has commenced, the nematode develops through a further three moults to the adult stage.…”

Parallel adaptations and common host cell responses enabling feeding of obligate and facultative plant parasitic nematodes

“…The delivery of pharyngeal gland secretions and extraction of assimilates by feeding nematodes occurs in repetitive cycles in which salivation and feeding phases are intermitted by a preparation phase marked by stylet retraction and reinsertion. For many lineages of plant parasitic nematodes, the salivation phase is associated with the formation of an intracellular feeding tube, the nature of which is not fully understood (Eves-van den Akker et al, 2015). However, it is thought that these feeding tubes function as molecular sieves enabling the selective uptake of small molecules from the host cell cytoplasm.…”