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

Abstract

SUMMARYParallel adaptations enabling the use of plant cells as the primary food source have occurred multiple times in distinct nematode clades. The hallmark of all extant obligate and facultative plant-feeding nematodes is the presence of an oral stylet, which is required for penetration of plant cell walls, delivery of pharyngeal gland secretions into host cells and selective uptake of plant assimilates. Plant parasites from different clades, and even within a single clade, display a large diversity in feeding behaviours ranging from short feeding cycles on single cells to prolonged feeding on highly sophisticated host cell complexes. Despite these differences, feeding of nematodes frequently (but certainly not always) induces common responses in host cells (e.g. endopolyploidization and cellular hypertrophy). It is thought that these host cell responses are brought about by the interplay of effectors and other biological active compounds in stylet secretions of feeding nematodes, but this has only been studied for the most advanced sedentary plant parasites. In fact, these responses are thought to be fundamental for prolonged feeding of sedentary plant parasites on host cells. However, as we discuss in this review, some of these common plant responses to independent lineages of plant parasitic nematodes might also be generic reactions to cell stress and as such their onset may not require specific inputs from plant parasitic nematodes. Sedentary plant parasitic nematodes may utilize effectors and their ability to synthesize other biologically active compounds to tailor these common responses for prolonged feeding on host cells.

Root endodermal barrier system contributes to defence against plant‐parasitic cyst and root‐knot nematodes

“…The induction of these feeding sites requires cellular reprogramming, which is achieved by a cocktail of proteinaceous and non‐proteinaceous compounds secreted by the J2s into the initial feeding cell. These secretions induce profound ultrastructural and physiological changes in both the initial feeding cell and adjoining tissue (Siddique et al ., ; Juvale and Baum, ; Smant et al ., ). CNs form syncytia by locally dissolving cell walls and fusing the protoplasts of neighbouring cells into single entities (Golinowski et al ., ; Sobczak et al ., ).…”

Phytoparasitic Nematode Control of Plant Hormone Pathways

“…Plant-parasitic nematodes are microscopically small animals that cause global annual crop losses of at least 80 billion dollars (Nicol et al, 2011). The evolution of nematodes into plant parasites occurred several times, resulting in diverse interaction modes with the plant (Smant et al, 2018). We will focus this review on the sedentary cyst nematodes (CN) and root-knot nematodes (RKN), as they are the foremost studied due to their economic importance (Jones et al, 2013) and fascinating liaison with plants in the form of nematode feeding sites (Box 1).…”

Plant biotic interactions: from conflict to collaboration

“…The authors propose working models to explain the role of these transporters in pathogen interactions, including the two hypotheses of "pathogen starvation" and "sugar signaling".Plant-microorganism interactions remain intensively studied, but host cell responses to organisms such as nematodes or insects are also garnering increasing attention. Smant et al (2018) discuss the molecular and physiological processes…”

“…Plant-microorganism interactions remain intensively studied, but host cell responses to organisms such as nematodes or insects are also garnering increasing attention. Smant et al (2018) discuss the molecular and physiological processes…”