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

Abstract

Plant-parasitic nematodes (PPNs) cause tremendous yield losses worldwide in almost all economically important crops. The agriculturally most important PPNs belong to a small group of root-infecting sedentary endoparasites that includes cyst and root-knot nematodes. Both cyst and root-knot nematodes induce specialized long-term feeding structures in root vasculature from which they obtain their nutrients. A specialized cell layer in roots called the endodermis, which has cell walls reinforced with suberin deposits and a lignin-based Casparian strip (CS), protects the vascular cylinder against abiotic and biotic threats. To date, the role of the endodermis, and especially of suberin and the CS, during plant-nematode interactions was largely unknown. Here, we analyzed the role of suberin and CS during interaction between Arabidopsis plants and two sedentary root-parasitic nematode species, the cyst nematode Heterodera schachtii and the root-knot nematode Meloidogyne incognita. We found that nematode infection damages the endodermis leading to the activation of suberin biosynthesis genes at nematode infection sites. Although feeding sites induced by both cyst and root-knot nematodes are surrounded by endodermis during early stages of infection, the endodermis is degraded during later stages of feeding site development, indicating periderm formation or ectopic suberization of adjacent tissue. Chemical suberin analysis showed a characteristic suberin composition resembling peridermal suberin in nematode-infected tissue. Notably, infection assays using Arabidopsis lines with CS defects and impaired compensatory suberization, revealed that the CS and suberization impact nematode infectivity and feeding site size. Taken together, our work establishes the role of the endodermal barrier system in defence against a soil-borne pathogen.

The Arabidopsis R2R3 MYB Transcription Factor MYB15 Is a Key Regulator of Lignin Biosynthesis in Effector-Triggered Immunity

“…suggesting that lignin is associated with the Casparian strip-like structure, as lignin and CASPs were known to be the main components of the Casparian strip, a diffusion barrier in the root endodermis (Roppolo et al, 2011;Naseer et al, 2012;Lee et al, 2013). In fact, the endodermal Casparian strip in roots was shown to play a role in defense against root-parasitic nematode species, the cyst nematode Heterodera schachtii and the root-knot nematode Meloidogyne incognita (Holbein et al, 2019).These results suggest that the Casparian strip may also function in defense against soilborne pathogens. Table 1.…”

Molecular insights into the compatible and incompatible interactions between sugar beet and the beet cyst nematode

“…Induction of a gene encoding a casparian strip membrane domain protein (CASP)-like protein, belonging to "uncharacterized protein family UPF0497" was detected in the infected resistant roots compared to the uninfected resistant plants and to the susceptible plants at 4 dai. CASPs mediate Casparian strip formation, composed of a lignin polymer and acting as para-cellular barrier for selective nutrient uptake and stress resistance, also against nematodes [72]. It also plays a role in the activation of hormone signaling pathways [73][74][75][76].…”

Plant Immune Responses to Parasitic Nematodes

“…The RKN Meloidogyne naasi induces callose deposition at an early infection stage, and suberin accumulation at a later stage in the resistant grass plant Aegilops variabilis (Balhadère and Evans, 1995a; Balhadère and Evans, 1995b). Infection of Arabidopsis by RKN or CN also induces transcriptional activation of suberin biosynthesis genes at the site of infection (Holbein et al, 2019). Overexpression of the transcription factor RAP2.6 in Arabidopsis leads to enhanced callose deposition at syncytia and results in higher resistance to CN (Ali et al, 2013).…”

“…RKNs are not able to directly cross the endodermis because of the reinforcement of cell walls by suberin lamellae and casparian strips (Wyss et al, 1992; Abad et al, 2009). Indeed, Arabidopsis mutants defective in casparian strips are more susceptible to RKNs (Holbein et al, 2019).…”