Convergent recognition of tobamovirus movement proteins by phylogenetically distinct NLR immune receptors

Abstract

The tobamovirus Tomato brown rugose fruit virus (ToBRFV) has rapidly emerged as a major threat to tomato production worldwide, overcoming the widely deployed Tm-22-mediated resistance and challenging current strategies for tobamovirus disease control. The tomato coiled-coil nucleotide-binding leucine-rich repeat (CC-NLR) immune receptor HREZ confers resistance to ToBRFV. However, the activation mechanism underlying HREZ recognition of ToBRFV remains unclear. Here, we show that HREZ is activated by the movement protein (MP) of ToBRFV and induces hypersensitive cell death. Upon activation, HREZ assembles into a higher-order oligomeric complex, with AlphaFold 3 modelling supporting a pentameric resistosome model. Phylogenetic analysis places HREZ in a CC-NLR lineage distinct from the canonical tobamovirus resistance receptor Tm-22, consistent with convergent evolution of tobamovirus MP recognition. Comparative analysis of eight MPs from the family Virgaviridae reveals that HREZ and Tm-22 have distinct recognition spectra. Four distinct tobamovirus MPs that activate HREZ also promote its assembly into a higher-order oligomeric complex. Together, these findings show how phylogenetically distinct CC-NLRs can converge on the same viral target while retaining distinct recognition breadth and provide a foundation for developing resistance strategies against current and emerging tobamoviruses.