Cytoskeleton reorganization,a key process in root-knot nematode-induced giant cell ontogenesis

Root-knot nematodes are plant parasitic worms that establish and maintain an intimate relationship with their host plants. RKN induce the redifferentiation of root cells into multinucleate and hypertrophied giant cells essential for nematode growth and reproduction. Major rearrangements of the cytoskeleton occur during giant cell formation. We characterized the first plant candidate genes implicated in giant cell actin and microtubule cytoskeleton reorganization. We showed previously that formins may regulate giant cell isotropic growth by controlling the assembly of actin cables. Recently we demonstrated that a Microtubule-Associated Protein, MAP65-3, is essential for giant cell development. In the absence of functional MAP65-3, giant cells started to develop but failed to fully differentiate and were eventually destroyed. In developing giant cells, MAP65-3 was associated with a novel kind of cell plate—the giant cell mini cell plate—that separates daughter nuclei. Despite karyokinesis occurs without cell division in giant cell, we demonstrated that cytokinesis is initiated and required for successful pathogen growth and development.Key words: cytoskeleton, microfilament, formin, microtubule, microtubule-associated protein, giant cells, nematodeRoot-knot nematodes (RKN) Meloidogyne spp. is one of the most damaging plant pathogen worldwide.¹ Their potential host range encompasses more than 2,000 plant species. During a compatible interaction, these obligate biotrophic pathogen have evolved an ability to manipulate host functions to their own benefit.^2–6 At the onset of parasitism, the infective second stage juveniles (J2) penetrate the root tip and migrate intercellularly to reach the root vascular cylinder. Each J2 then induces the redifferentiation of five to seven parenchymatic root cells into hypertrophied and multinucleate cells, named giant cells. Giant cells result from synchronous repeated karyokinesis without cell division.⁷ Despite lack of complete cytokinesis, we demonstrated that cytokinesis is initiated and essential for giant cell ontogenesis.⁸ Fully differentiated giant cells reach a final size about four hundred times that of root vascular cells and contain more than a hundred polyploid nuclei. Giant cell nuclei show an increase in DNA, possibly reflecting endoreduplication.⁹ These “feeding” giant cells constitute the exclusive source of nutrients for the nematode until reproduction. Giant cell development is accompanied by division and hypertrophy of surrounding cells, leading to a typical root gall formation, the primary visible symptom of infection.