Nuclear transfer of a beneficial fungal effector-host target complex via the NTF2 pathway underpins symbiont-induced plant immunity.

The symbiotic fungus Serendipita indica confers broad-spectrum beneficial effects on diverse plant hosts. Its key effector SIE141 elicits immunity against Phytophthora and salt tolerance by binding and relocalizing thioredoxin CDSP32 from chloroplast to the nucleus. Here, we show that this functionally essential nuclear transfer process of the SIE141-CDSP32 complex is mediated by the host NTF2 proteins. NTF2 family proteins are direct targets of SIE141, whose knockdown abolished nuclear accumulation of both SIE141 and CDSP32, leading to their rendered accumulation to chloroplasts. The glutamine residue at position 40 of NbNTF2A is critical for its interaction with both SIE141 and Ran GTPase 1. SIE141 modulates NbNTF2-NbRan1 interaction in a dose-dependent manner, without impairing nuclear accumulation of NbRan1 and the NTF2-mediated positive immune function of Ran1. Our results reveal a previously unknown mechanism where a beneficial symbiotic fungal effector utilizes the conserved NTF2 rather than other core nuclear import machinery components to traffic an immune complex and enhance disease resistance. These findings provide a potential strategy for engineering plant immunity by manipulating NTF2-RanGTPase dependent nucleocytoplasmic transport.