Gibberellic acid mitigates Huanglongbing symptoms by reducing osmotic and oxidative stress in sweet orange

Abstract

Huanglongbing (HLB; citrus greening disease) is presumably caused by the bacterium Candidatus Liberibacter (CLas). Here, we present evidence in terms of physiological, carbohydrate, transcriptome, phytohormones, and key enzyme activities behind the beneficial effect of gibberellic acid (GA3) in mitigating biotic (CLas-infection) and abiotic (osmotic) stresses in HLB-affected ‘Valencia’ sweet orange. For two consecutive years, non-fruiting leaves of untreated control tress accumulated ≈ 8 % higher fructose whereas fruiting leaves accumulated ≈ 10 % higher fructose and glucose compared to GA3 treated trees. Control trees also had higher starch (≈ 25 %) and callose (≈ 15 %) content than GA3 trees, which are indicators for osmotic stress, and CLas-induced plasmodesmata closure resulting in anemic growth. In non-fruiting leaves of control trees, higher auxins and salicylic acid, and lower jasmonic acid content were found compared to GA3 trees. In fruiting leaves, higher abscisic acid was found in control trees than GA3 trees, suggesting water deficient conditions. In February, non-fruiting leaves of control versus GA3, differentially expressed genes (DEGs) related to response to stress, defense response, and carbohydrate metabolic process were upregulated, and those with stomatal movement and gibberellic acid mediated signaling pathway were downregulated. DEGs encoding sucrose synthase (provide UDP-glucose for callose synthesis) and invertase (sucrose to hexose conversion) were upregulated in control compared to GA3 trees, indicating a higher capacity to import assimilates thus attracting water as well as callose accumulation. Furthermore, osmotic stress induced key markers including DEGs encoding lactate dehydrogenase and hexokinase, and the acyl-CoA-binding protein transcription factor family were upregulated in control compared to GA3 trees, with a concomitant of higher enzymatic activity of alcohol dehydrogenase in control trees. Altogether, control trees indicate a higher carbohydrate tradeoff on defenses against biotic (CLas), and abiotic (osmotic) stresses than on growth. GA3 improves vegetative growth as indicated by greater leaf weight and area, stem length, leaf relative water content thus improving photosynthetic activity as well as gas exchange potential in leaves. Thus facilitating, and better carbohydrate translocation within the tree body leading to better fruit retention on tree and productivity in HLB-affected sweet orange.