Elucidating the Functional Role of Arabidopsis Fimbrins in Actin Cytoskeleton Rearrangements in Root-Knot Nematode Feeding Sites.

Abstract

The plant cytoskeleton undergoes extensive remodelling during the formation of Meloidogyne incognita-induced giant cells and plays a crucial role in their ontogenesis. Fimbrins (FIMs) are a conserved family of actin-bundling proteins that regulate cytoskeletal architecture and dynamics during diverse cellular processes. However, their functional contribution to giant cell development remains unknown. Here, we show that all five Arabidopsis thaliana FIM genes (FIM1-FIM5) are expressed in M. incognita-induced galls, with expression levels declining as giant cells mature. Loss of function of FIM2 or FIM3, as well as FIM2 overexpression, altered actin organisation and giant cell morphology, resulting in reduced cytoplasmic density and cell wall stubs. These defects were associated with changes in cell wall composition and vacuolar organisation. FIM2 overexpression increased the accumulation of low-methyl-esterified homogalacturonan in giant cell walls, whereas fim2 and fim3 mutants showed reduced accumulation, consistent with altered cell wall thickness. Increased vacuolar sizes in INT1-eGFP Arabidopsis galls following latrunculin B treatment further indicates that actin organisation is required to maintain vacuolar architecture in giant cells. Moreover, fim2, fim3 and FIM2OE lines showed enhanced resistance to M. incognita, with reduced gall formation and egg mass production. Together, our findings identify FIM2 and FIM3 as critical regulators of actin organisation, cell wall remodelling and vacuolar architecture during gall development, highlighting the importance of a balanced cytoskeleton dynamics for successful nematode parasitism.