Citrus yellow vein clearing virus infection triggers phloem remobilization of iron- and zinc-nicotianamine in citrus

Abstract Citrus yellow vein clearing virus (CYVCV) is a worldwide and highly destructive disease of citrus, but the mechanisms involved in CYVCV-inhibited plant growth are not well understood. This study examined nutrient levels and their cellular distribution in different organs of healthy and CYVCV-affected citrus (Citrus reticulata ‘Kanpei’) plants. We found that CYVCV-infected plants exhibit characteristic symptoms, including a significant reduction in iron (Fe) and other elemental nutrients in the shoots. Our data suggest that CYVCV-induced chlorosis in citrus leaf veins is primarily due to iron deficiency, leading to reduced chlorophyll synthesis. Further analysis revealed a marked decrease in iron concentration within the pith and xylem of citrus petioles post-CYVCV infection, contrasting with increased Fe and zinc (Zn) concentrations in the phloem. Moreover, a substantial accumulation of starch granules was observed in the pith, xylem, and phloem vessels of infected plants, with vessel blockage due to starch accumulation reaching up to 81%, thus significantly obstructing Fe transport in the xylem. Additionally, our study detected an upregulation of genes associated with nicotinamide metabolism and Fe and Zn transport following CYVCV infection, leading to increased levels of nicotinamide metabolites. This suggests that CYVCV-infected citrus plants may induce nicotinamide synthesis in response to Fe deficiency stress, facilitating the transport of Fe and Zn in the phloem as nicotinamide-bound complexes. Overall, our findings provide insight into the mechanisms of long-distance Fe and Zn transport in citrus plants in response to CYVCV infection and highlight the role of nutritional management in mitigating the adverse effects of CYVCV, offering potential strategies for cultivating CYVCV-resistant citrus varieties.