Plant-parasitic root-knot and cyst nematodes are microscopic worms that cause severe damage to crops and induce major agricultural losses worldwide. These parasites penetrate into host roots and induce the formation of specialized feeding structures, which supply the resources required for nematode development. Root-knot nematodes induce the redifferentiation of five to seven root cells into giant multinucleate feeding cells, whereas cyst nematodes induce the formation of a multinucleate syncytium by targeting a single root cell. Transcriptomic analyses have shown that the induction of these feeding cells by nematodes involves an extensive reprogramming of gene expression within the targeted root cells. MicroRNAs are small noncoding RNAs that act as key regulators of gene expression in eukaryotes by inducing the posttranscriptional silencing of protein coding genes, including many genes encoding transcription factors. A number of microRNAs (miRNAs) displaying changes in expression in root cells in response to nematode infection have recently been identified in various plant species. Modules consisting of miRNAs and the transcription factors they target were recently shown to be required for correct feeding site formation. Examples include miR396 and GRF in soybean syncytia and miR159 and MYB33 in Arabidopsis giant cells. Moreover, some conserved miRNA/target modules seem to have similar functions in feeding site formation in different plant species. These miRNAs may be master regulators of the reprogramming of expression occurring during feeding site formation. This review summarizes current knowledge about the role of these plant miRNAs in plant–nematode interactions.
Root-knot nematodes (RKNs) are among the most damaging pests of agricultural crops. Meloidogyne is an extremely polyphagous genus of nematodes that can infect thousands of plant species. A few genes for resistance (R-genes) to RKN suitable for use in crop breeding have been identified, but virulent strains and species of RKN have emerged that render these R-genes ineffective. Secretion of RKN effectors targeting plant functions mediates the reprogramming of root cells into specialized feeding cells, the giant cells, essential for RKN development and reproduction. Conserved targets among plant species define the more relevant strategies for controlling nematode infection. The EFFECTOR18 (EFF18) protein from M. incognita interacts with the spliceosomal small nuclear ribonucleoprotein (snRNP) D1 (SmD1) in Arabidopsis (Arabidopsis thaliana), disrupting its function in alternative splicing regulation and modulating the giant cell transcriptome. We show here that EFF18 is a conserved RKN-specific effector that targets this conserved spliceosomal SmD1 protein in Solanaceae. This interaction modulates alternative splicing events produced by tomato (Solanum lycopersicum) in response to M. incognita infection. The alteration of SmD1 expression by virus-induced gene silencing (VIGS) in Solanaceae affects giant cell formation and nematode development. Thus, our work defines a promising conserved SmD1 target gene to develop broad resistance for the control of Meloidogyne spp. in plants.
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