Citrus photosynthesis and morphology acclimate to phloem-affecting huanglongbing disease at the leaf and shoot levels
Huanglongbing (HLB) is a phloem-affecting disease of citrus that reduces growth and has impacted citrus production in most global production regions. HLB is caused by a phloem-limited bacterium (Candidatus Liberibacter asiaticus; CLas). By inhibiting phloem function, HLB stunts sink growth, including reducing production of new shoots and leaves, and induces hyperaccumulation of foliar starch. Despite evidence that HLB induces feedback inhibition of photosynthesis by reducing foliar carbohydrate export, its effects on net CO2 assimilation (Anet) have not been reported. In this work we assessed the relationship of bacterial distribution within the foliage, foliar starch accumulation, and Anet. Because HLB impacts canopy morphology, we developed a chamber to measure whole shoot Anet, and tested the effects of HLB at both leaf and shoot levels. Starch accumulation was correlated with bacterial population, and starch was negatively correlated with Anet at the leaf but not at the shoot level. Starch increased between the uninfected group and the shortest duration of infection, then decreased progressively with increasing length of infection. HLB infection reduced Anet at the leaf level, but increased it at the whole shoot level. We attribute this enhancement of whole shoot Anet to the increased contribution of stem photosynthesis due to the altered shoot morphology induced by the disease. Despite the increased photosynthetic efficiency, total carbon fixation per shoot decreased because shoot size and leaf area were reduced. Overall, our results indicate a localized relationship of CLas distribution with negative impacts on foliar carbohydrate export and photosynthesis. Additionally, starch accumulation and Anet acclimate over time at the shoot level to the localized impacts of the disease. Stems contribute important proportions of whole shoot Anet, and these contributions are likely increased by the morphological acclimation induced by HLB. This study highlights the importance of temporal and spatial scale in assessing photosynthesis.