Phloem-Limited Disease Impacts Citrus Carbohydrate Dynamics Distinctly from Source-Sink Manipulation

Abstract

Source-sink dynamics are defined by the interdependence of source and sink tissues and are key determinants of plant growth and productivity. This dynamic can, be altered by disease. One example is huanglongbing (HLB), a phloem-limited disease that impacts several economically important tree species by disrupting carbon partitioning and altering source-sink relationships. Though HLB is widespread in citrus, the specific mechanism in which phloem disruption impacts the co-regulation of carbon dynamics from source to sink has not been fully described. To address this, we took advantage of a natural study under field conditions, in which infected and uninfected trees were growing in the same field. After identifying trees that were uninfected, infected with symptoms, or infected without symptoms, we manipulated source:sink ratio by girdling branches and defoliating at 0%, 50%, and 75% of the original leaf area per fruit, while leaving a control treatment with no defoliation or girdling and used fruits as the sink of interest. We measured gas exchange, biomass, and non-structural carbohydrates in leaves, stems and fruits in response to these treatments. Our results show that leaf photosynthetic responses to HLB were primarily driven by stomatal regulation rather than biochemical limitations. HLB increased leaf dark respiration without altering the relationship between respiration and leaf soluble sugars. Among the plant organs, stem starch reserves were the most responsive to source-sink manipulation and were strongly correlated with multiple carbon pools and biomass in both fruits and leaves. Although HLB altered fruit carbon dynamics, it did not change fruit responses to source-sink manipulation. Overall, HLB affects source and sink tissues independently of the experimental source-sink manipulation. The stem serves as a transient carbon reserve and is sensitive to both HLB and source-sink manipulation. These findings raise further questions regarding total carbon fluxes and the importance of feedback inhibition of photosynthesis.