The root knot nematode effector MiEFF186 interacts with a splicing factor to reshape plant transcriptome

The root-knot nematode Meloidogyne incognita secretes specific effectors to manipulate root cells and induce their redifferentiation into multinucleate feeding ‘giant cells’, which are essential for its development. A dedicated screen identified the Meloidogyne incognita MiEFF186a effector as a regulator of alternative splicing, a crucial mechanism of transcriptional gene regulation whereby a single gene can produce multiple mature mRNA variants, in plants. EFF186 is expressed in the esophageal glands of nematode juveniles, and in planta , it localizes to the nucleus and accumulates in the nucleolus. A yeast two-hybrid approach identified the nucleolar G-patch protein GDP1/CIS2 as a MiEFF186a target in tomato and Arabidopsis. Transcriptomic analyses of Arabidopsis roots ectopically expressing MiEFF186a or impaired in GDP1/CIS2 function revealed changes in both gene expression and alternative splicing, with partially overlapping responses. Finally, alteration of GDP1/CIS2 expression by virus-induced gene silencing in Solanaceae or in Arabidopsis gdp1 mutants affects susceptibility to M. incognita . Together, these results identify GDP1/CIS2 as a host target of MiEFF186a and support a role for these proteins in the modulation of host RNA metabolism during nematode parasitism.