Citrus photosynthesis and morphology acclimate to phloem-affecting huanglongbing disease at the leaf and shoot levels

Abstract

Huanglongbing (HLB) is a phloem-affecting disease of citrus that reduces growth and has impacted global citrus production. 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. HLB induces feedback inhibition of photosynthesis by reducing foliar carbohydrate export. In this work we assessed the relationship of bacterial distribution within the foliage, foliar starch accumulation, and net CO2 assimilation (Anet). Because HLB impacts canopy morphology, we developed a chamber to measure whole-shoot Anet to test the effects of HLB at both leaf and shoot levels. Whole-shoot-level Anet saturated at high irradiance, and green stems had high photosynthetic rates compared to leaves. Starch accumulation was correlated with bacterial population, and starch was negatively correlated with Anet at the leaf level but not at the shoot level. Starch increased initially after 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, in association with reduced leaf size and greater relative contribution of stems to photosynthetic surface area. Although HLB-increased photosynthetic efficiency, total carbon fixed per shoot decreased because photosynthetic surface area was reduced. We conclude that the localized effects of infection on photosynthesis are mitigated by whole shoot morphological acclimation over time. Stems contribute important proportions of whole shoot Anet, and these contributions are likely increased by the morphological acclimation induced by HLB.