Nematode feeding sites: unique organs in plant roots

Kyndt, Tina; Vieira, Paulo; Gheysen, Godelieve; Almeida-Engler, Janice de

doi:10.1007/s00425-013-1923-z

Cited by 152 publications

(136 citation statements)

References 85 publications

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“…Microarray transcript abundance studies of laser-capture microdissected syncytium samples have indicated that Rhg1-mediated disease resistance is accompanied by a cellular stress profile that includes oxidative, cold, osmotic, and unfolded protein stresses (43). Additionally, the high metabolic demands and large-scale membrane reorganizations necessary to form the syncytium (16)(17)(18) may amplify cellular sensitivity to noncooperative α-SNAPs, even in cases where there may be a less significant shift in the ratio of resistance-type Rhg1 α-SNAPs to wild-type α-SNAPs. A study of virulent SCN populations that had recently evolved to reproduce on soybeans carrying high-copy Rhg1 haplotypes demonstrated allelic imbalance of a SNARE-like effector protein in the nematode (44).…”

Section: Discussionmentioning

confidence: 99%

“…Syncytium formation is a complex process involving plant cell-wall dissolution, endoreduplication, cell-cell fusion, and membrane reorganization, with the eventual incorporation of over 100 host root cells into one large multinucleate cell (15,16,18). Because egg-filled SCN cysts can persist in fields for many years and nematicides are often costly and environmentally damaging, the two core SCN control strategies are crop rotation to reduce inoculum load and use of SCN-resistant soybean varieties.…”

Section: Significancementioning

confidence: 99%

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Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

Bayless

Smith

Song

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

154

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α-SNAP [soluble NSF (N-ethylmaleimide–sensitive factor) attachment protein] and NSF proteins are conserved across eukaryotes and sustain cellular vesicle trafficking by mediating disassembly and reuse of SNARE protein complexes, which facilitate fusion of vesicles to target membranes. However, certain haplotypes of the Rhg1 (resistance to Heterodera glycines 1) locus of soybean possess multiple repeat copies of an α-SNAP gene (Glyma.18G022500) that encodes atypical amino acids at a highly conserved functional site. These Rhg1 loci mediate resistance to soybean cyst nematode (SCN; H. glycines), the most economically damaging pathogen of soybeans worldwide. Rhg1 is widely used in agriculture, but the mechanisms of Rhg1 disease resistance have remained unclear. In the present study, we found that the resistance-type Rhg1 α-SNAP is defective in interaction with NSF. Elevated in planta expression of resistance-type Rhg1 α-SNAPs depleted the abundance of SNARE-recycling 20S complexes, disrupted vesicle trafficking, induced elevated abundance of NSF, and caused cytotoxicity. Soybean, due to ancient genome duplication events, carries other loci that encode canonical (wild-type) α-SNAPs. Expression of these α-SNAPs counteracted the cytotoxicity of resistance-type Rhg1 α-SNAPs. For successful growth and reproduction, SCN dramatically reprograms a set of plant root cells and must sustain this sedentary feeding site for 2–4 weeks. Immunoblots and electron microscopy immunolocalization revealed that resistance-type α-SNAPs specifically hyperaccumulate relative to wild-type α-SNAPs at the nematode feeding site, promoting the demise of this biotrophic interface. The paradigm of disease resistance through a dysfunctional variant of an essential gene may be applicable to other plant–pathogen interactions.

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Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

Bayless

Smith

Song

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

154

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“…The role of ethylene in plant-nematode interactions is complex (reviewed in Kyndt et al, 2013). Although ethylene biosynthesis genes responded slightly faster to nematode infection in TOG5681 in comparison with 'Nipponbare', a complex pattern of repression and activation was observed in both the incompatible and compatible interactions.…”

Section: Role Of Hormonal Pathways Is Complexmentioning

confidence: 99%

Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots

et al. 2017

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Background and Aims The root-knot nematode Meloidogyne graminicola is responsible for production losses in rice (Oryza sativa) in Asia and Latin America. The accession TOG5681 of African rice, O. glaberrima, presents improved resistance to several biotic and abiotic factors, including nematodes. The aim of this study was to assess the cytological and molecular mechanisms underlying nematode resistance in this accession.Methods Penetration and development in M. graminicola in TOG5681 and the susceptible O. sativa genotype 'Nipponbare' were compared by microscopic observation of infected roots and histological analysis of galls. In parallel, host molecular responses to M. graminicola were assessed by root transcriptome profiling at 2, 4 and 8 d postinfection (dpi). Specific treatments with hormone inhibitors were conducted in TOG5681 to assess the impact of the jasmonic acid and salicylic acid pathways on nematode penetration and reproduction.Key Results Penetration and development of M. graminicola juveniles were reduced in the resistant TOG5681 in comparison with the susceptible accession, with degeneration of giant cells observed in the resistant genotype from 15 dpi onwards. Transcriptome changes were observed as early as 2 dpi, with genes predicted to be involved in defence responses, phenylpropanoid and hormone pathways strongly induced in TOG5681, in contrast to 'Nipponbare'. No specific hormonal pathway could be identified as the major determinant of resistance in the ricenematode incompatible interaction. Candidate genes proposed as involved in resistance to M. graminicola in TOG5681 were identified based on their expression pattern and quantitative trait locus (QTL) position, including chalcone synthase, isoflavone reductase, phenylalanine ammonia lyase, WRKY62 transcription factor, thionin, stripe rust resistance protein, thaumatins and ATPase3.Conclusions This study provides a novel set of candidate genes for O. glaberrima resistance to nematodes and highlights the rice-M. graminicola pathosystem as a model to study plant-nematode incompatible interactions.

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“…These obligate parasites initiate a long period of biotic interactions with their host plants where formation of an operative feeding structure, the syncytium, is vital for nematode survival and development. The nematode provokes differentially terminated cells in the vascular root tissues to redifferentiate into a syncytium cell type, a dynamic process that involves changes in the expression of thousands of genes simultaneously (Hewezi and Baum, 2013;Kyndt et al, 2013;Hewezi, 2015). Though the mechanisms controlling gene expression changes in the syncytium remain ill defined, recent studies indicate that epigenetic mechanisms including noncoding small RNAs and DNA methylation may play fundamental roles (Hewezi and Baum, 2015).…”

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confidence: 99%

Cyst Nematode Parasitism Induces Dynamic Changes in the Root Epigenome

et al. 2017

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A growing body of evidence indicates that epigenetic modifications can provide efficient, dynamic, and reversible cellular responses to a wide range of environmental stimuli. However, the significance of epigenetic modifications in plant-pathogen interactions remains largely unexplored. In this study, we provide a comprehensive analysis of epigenome changes during the compatible interaction between the beet cyst nematode Heterodera schachtii and Arabidopsis (Arabidopsis thaliana). Whole-genome bisulfite sequencing was conducted to assess the dynamic changes in the methylome of Arabidopsis roots in response to H. schachtii infection. H. schachtii induced widespread hypomethylation of protein-coding genes and transposable elements (TEs), preferentially those adjacent to protein-coding genes. The abundance of 24-nt siRNAs was associated with hypermethylation of TEs and gene promoters, with influence observed for methylation context and infection time points. mRNA sequencing revealed a significant enrichment for the differentially methylated genes among the differentially expressed genes, specifically those with functions corresponding to primary metabolic processes and responses to stimuli. The differentially methylated genes overlapped with more than one-fourth of the syncytium differentially expressed genes and are of functional significance. Together, our results provide intriguing insights into the potential regulatory role of differential DNA methylation in shaping the biological interplay between cyst nematodes and host plants.

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Nematode feeding sites: unique organs in plant roots

Cited by 152 publications

References 85 publications

Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

Disease resistance through impairment of α-SNAP–NSF interaction and vesicular trafficking by soybean Rhg1

Transcriptomic and histological responses of African rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots

Cyst Nematode Parasitism Induces Dynamic Changes in the Root Epigenome

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