Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Mendy, Badou; Wang’ombe, Mary Wanjiku; Radakovic, Zoran S.; Holbein, Julia; Ilyas, Muhammad; Chopra, Divykriti; Holton, Nicholas; Zipfel, Cyril; Grundler, Florian M. W.; Siddique, Shahid

doi:10.1371/journal.ppat.1006284

Cited by 146 publications

(152 citation statements)

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“…Invasion of the root by nematodes, and subsequent migration towards the vascular cylinder, cause cellular damage and activate plant defence responses (Holbein, Grundler, & Siddique, ; Mendy et al, ). Nematodes use their stylets to secrete a variety of molecules (effectors) that suppress the defence responses in infected plant cells, leading to the formation of a functional feeding site (Juvale & Baum, ).…”

Section: Discussionmentioning

confidence: 99%

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Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Anjam

Shah

Matera

et al. 2020

Plant Cell & Environment

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Plant-parasitic cyst nematodes induce hypermetabolic syncytial nurse cells in the roots of their host plants. Syncytia are their only food source. Cyst nematodes are sexually dimorphic, with their differentiation into male or female strongly influenced by host environmental conditions. Under favourable conditions with plenty of nutrients, more females develop, whereas mainly male nematodes develop under adverse conditions such as in resistant plants. Here, we developed and validated a method to predict the sex of beet cyst nematode (Heterodera schachtii) during the early stages of its parasitism in the host plant Arabidopsis thaliana. We collected root segments containing male-associated syncytia (MAS) or female-associated syncytia (FAS), isolated syncytial cells by laser microdissection, and performed a comparative transcriptome analysis. Genes belonging to categories of defence, nutrient deficiency, and nutrient starvation were over-represented in MAS as compared with FAS. Conversely, gene categories related to metabolism, modification, and biosynthesis of cell walls were over-represented in FAS. We used β-glucuronidase analysis, qRT-PCR, and loss-of-function mutants to characterize FAS-and MAS-specific candidate genes. Our results demonstrate that various plant-based factors, including immune response, nutrient availability, and structural modifications, influence the sexual fate of the cyst nematodes. K E Y W O R D S cyst nematodes, environmental sex determination, plant-nematode interaction, host-plant interaction

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Section: Discussionmentioning

confidence: 99%

“…* using the MAS5 algorithm. Statistical analysis of microarray data was performed as described previously (Mendy et al, ). The gene set enrichment analysis of FAS and MAS data was performed using PlantGSEA tool kit as described previously (Yi, Du, & Su, ).…”

Section: Methodsmentioning

confidence: 99%

Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Anjam

Shah

Matera

et al. 2020

Plant Cell & Environment

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“…Meloidogyne incognita was propagated and eggs were extracted as described previously (Mendy et al ., ). To separate freshly extracted eggs from soil particles, the eggs were suspended in a 35% (w/v) sucrose solution and centrifuged.…”

Section: Methodsmentioning

confidence: 97%

“…To separate freshly extracted eggs from soil particles, the eggs were suspended in a 35% (w/v) sucrose solution and centrifuged. Eggs and freshly hatched J2s were surface sterilized as described previously (Mendy et al ., ). The roots of 10‐ to 12‐day‐old plants were inoculated with 90–100 sterile J2s and the plants were stored under standard growth conditions in darkness (see above).…”

Section: Methodsmentioning

confidence: 97%

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

et al. 2019

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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.

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“…ROS production was measured on a 96-well illuminometer (Mithras LB 940; Berthold Technologies) according to Mendy et al (2017). Briefly, leaf disks 0.5 cm in diameter were cut from 12-day-old Arabidopsis plants and incubated in ddH 2 O for 12 h in the dark.…”

Section: Oxidative Burst Assaymentioning

confidence: 99%

Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii

Radakovic

Anjam

Escobar

et al. 2017

Preprint

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SummarySedentary plant-parasitic cyst nematodes are obligate biotrophs that infect the roots of their host plant. Their parasitism is based on modification of root cells to form a hypermetabolic syncytium from which the nematodes draw their nutrients. The aim of this study was to identify nematode susceptibility genes in Arabidopsis thaliana and to characterize their roles in supporting the parasitism of Heterodera schachtii. By selecting genes that were most strongly upregulated in response to cyst nematode infection, we identified HIPP27 (HEAVY METAL-ASSOCIATED ISOPRENYLATED PLANT PROTEIN 27) as a host susceptibility factor required for beet cyst nematode infection and development. Detailed expression analysis revealed that HIPP27 is a cytoplasmic protein and that HIPP27 is strongly expressed in leaves, young roots and nematode-induced syncytia. Loss-of-function Arabidopsis hipp27 mutants exhibited severely reduced susceptibility to H. schachtii and abnormal starch accumulation in syncytial and peridermal plastids. Our results suggest that HIPP27 is a susceptibility gene in Arabidopsis whose loss-of-function reduces plant susceptibility to cyst nematode infection without increasing susceptibility to other pathogens or negatively affecting plant phenotype.

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Arabidopsis leucine-rich repeat receptor–like kinase NILR1 is required for induction of innate immunity to parasitic nematodes

Cited by 146 publications

References 50 publications

Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana

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

Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii

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