A viral coat protein induces leaf yellowing by degrading ChlM to facilitate pollinator-mediated viral transmission

Abstract

Plant viral symptoms are not merely passive consequences of infection but can represent adaptive strategies for enhancing transmission. The molecular mechanisms and ecological consequences of such virus-induced symptoms, particularly in perennial crops such as kiwifruit, require exploration. Here, in field experiments, we discovered a kiwifruit infected with a novel virus, Actinidia yellow ringspot virus (AYRSpV), which exhibits severe yellowing symptoms and significantly increases the attractiveness of pollinating insects such as bees and aphids during the flowering season. Given that AYRSpV is pollen-transmissible, this visual manipulation may facilitate the pollinator-mediated spread of the virus. We further explored whether the AYRSpV coat protein (CP) is a key virulence determinant that interacts with and targets the chlorophyll metabolic enzyme magnesium protoporphyrin IX methyltransferase (ChlM) for degradation, leading to a significant reduction in chlorophyll content and systemic leaf yellowing. Knockout of kiwifruit ChlM recapitulated the yellowing phenotype and further enhanced plant susceptibility to AYRSpV. Our study elucidates a pathway whereby a viral CP protein directly disrupts chlorophyll biosynthesis to induce leaf yellowing. Furthermore, we reveal a strategy wherein the virus exploits this symptom as a visual signal to manipulate pollinator behavior, thus creating a ‘symptom-mediated transmission’ loop. These findings provide a comprehensive understanding of the molecular and ecological mechanisms driving the spread of an emerging kiwifruit virus.