Copper microRNAs govern the formation of giant feeding cells induced by the root knot nematode Meloidogyne incognita in Arabidopsis thaliana

Abstract miR408 and miR398 are two conserved microRNAs which expression is activated by the SPL7 transcription factor in response to copper starvation. We identified these two microRNAs families as upregulated in Arabidopsis thaliana and Solanum lycopersicum roots infected by root-knot nematodes. These endoparasites induce the dedifferentiation of a few root cells and the reprogramming of their gene expression to generate giant feeding cells. By combining functional approaches, we deciphered the signaling cascade involving these microRNAs, their regulator and their targets. MIR408 expression was located within nematode-induced feeding cells in which it co-localised with SPL7 expression and was regulated by copper. Moreover, infection assays with mir408 and spl7 KO mutants or lines expressing targets rendered resistant to cleavage by miR398 demonstrated the essential role of the SPL7/MIR408/MIR398 module in the formation of giant feeding cells. Our findings reveals how perturbation of plant copper homeostasis, via the SPL7/MIR408/MIR398 module, governs the formation of nematode-induced feeding cells.