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

Gall-inducing insects and nematodes engage in sophisticated interactions with their host plants. These parasites can induce major morphological and physiological changes in host roots, leaves, and other tissues. Sedentary endoparasitic nematodes, root-knot and cyst nematodes in particular, as well as gall-inducing and leaf-mining insects, manipulate plant development to form unique organs that provide them with food from feeding cells. Sometimes, infected tissues may undergo a developmental switch resulting in the formation of aberrant and spectacular structures (clubs or galls). We describe here the complex interactions between these plant-reprogramming sedentary endoparasites and their infected hosts, focusing on similarities between strategies of plant manipulation. We highlight progress in our understanding of the host plant response to infection and focus on the nematode and insect molecules secreted in planta. We suggest thatlooking at similarities may identify convergent and conserved strategies and shed light on the promise they hold for the development of new management strategies in agriculture and forestry.

/pdf/gall-inducing-parasites-convergent-and-conserved-strategies-3bv1guw98m.pdf

Gall-Inducing Parasites: Convergent and Conserved Strategies of Plant Manipulation by Insects and Nematodes.

Sedentary plant-parasitic cyst nematodes are obligate biotrophs that infect the roots of their host plant. Their parasitism is based on the 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 the susceptibility to other pathogens or negatively affecting the plant phenotype.

https://bsppjournals.onlinelibrary.wiley.com/doi/pdf/10.1111/mpp.12668

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

The root-knot nematode Meloidogyne incognita secretes specific effectors (MiEFF) and induces the redifferentiation of plant root cells into enlarged multinucleate feeding 'giant cells' essential for nematode development. Immunolocalizations revealed the presence of the MiEFF18 protein in the salivary glands of M. incognita juveniles. In planta, MiEFF18 localizes to the nuclei of giant cells demonstrating its secretion during plant-nematode interactions. A yeast two-hybrid approach identified the nuclear ribonucleoprotein SmD1 as a MiEFF18 partner in tomato and Arabidopsis. SmD1 is an essential component of the spliceosome, a complex involved in pre-mRNA splicing and alternative splicing. RNA-seq analyses of Arabidopsis roots ectopically expressing MiEFF18 or partially impaired in SmD1 function (smd1b mutant) revealed the contribution of the effector and its target to alternative splicing and proteome diversity. The comparison with Arabidopsis galls data showed that MiEFF18 modifies the expression of genes important for giant cell ontogenesis, indicating that MiEFF18 modulates SmD1 functions to facilitate giant cell formation. Finally, Arabidopsis smd1b mutants exhibited less susceptibility to M. incognita infection, and the giant cells formed on these mutants displayed developmental defects, suggesting that SmD1 plays an important role in the formation of giant cells and is required for successful nematode infection.

The root-knot nematode effector MiEFF18 interacts with the plant core spliceosomal protein SmD1 required for giant cell formation

Plant parasitic nematodes are obligate parasites causing serious reduction in crop yields. Several economically important species parasitize various plant species, but the root knot and cyst nematodes belonging to the Heteroderidae family are especially dangerous. Plant parasitic nematodes result in crop losses of over $150 billion worldwide. This review gives an account of morpho-physiological and molecular events during parasitism of root-knot and cyst nematodes. It describes the transcriptomes and parasitomes of various nematodes indicating that the effector proteins are crucial for the compatible plant nematode interactions. Various sequencing techniques used in plant-nematode genomics and transcriptomics are discussed. Moreover, the dynamics of host transcriptomes in response to infection with different nematode species have been reported. The host transcriptomes have unrevealed many candidate genes, which are involved in both compatible and incompatible plant nematode interactions. The strategy of manipulation of expression of the genes induced and suppressed by the nematodes in the feeding sites has also been suggested for enhancement of resistance against nematodes. This review will provide the researchers with the information regarding transcriptional changes in the nematodes as well as host plants, which would be important for the induction of resistance against nematodes in different crop plants. © 2015 Friends Science Publishers

Plant-nematode interactions: from genomics to metabolomics.

Summary
Novel approaches for the control of agriculturally damaging nematodes are sorely needed. Endoparasitic nematodes complete their life cycle within the root vascular cylinder, inducing specialized feeding cells: giant cells for root-knot nematodes and syncytia for cyst nematodes. Both nematodes hijack parts of the transduction cascades involved in developmental processes, or partially mimic the plant responses to other interactions with microorganisms, but molecular evidence of their differences and commonalities is still under investigation. Transcriptomics has been used to describe global expression profiles of their interaction with Arabidopsis, generating vast lists of differentially expressed genes. Although these results are available in public databases and publications, the information is scattered and difficult to handle. Here, we present a rapid, visual, user-friendly and easy to handle spreadsheet tool, called NEMATIC (NEMatode–Arabidopsis Transcriptomic Interaction Compendium; http://www.uclm.es/grupo/gbbmp/english/nematic.asp). It combines existing transcriptomic data for the interaction between Arabidopsis and plant-endoparasitic nematodes with data from different transcriptomic analyses regarding hormone and cell cycle regulation, development, different plant tissues, cell types and various biotic stresses. NEMATIC facilitates efficient in silico studies on plant–nematode biology, allowing rapid cross-comparisons with complex datasets and obtaining customized gene selections through sequential comparative and filtering steps. It includes gene functional classification and links to utilities from several databases. This data-mining spreadsheet will be valuable for the understanding of the molecular bases subjacent to feeding site formation by comparison with other plant systems, and for the selection of genes as potential tools for biotechnological control of nematodes, as demonstrated in the experimentally confirmed examples provided.

/pdf/nematic-a-simple-and-versatile-tool-for-the-in-silico-15yg9wa3h8.pdf

NEMATIC: a simple and versatile tool for the in silico analysis of plant–nematode interactions

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NEMATIC: a simple and versatile tool for the in silico analysis of plant–nematode interactions