Metabolomic analysis elucidates how shade conditions ameliorate the deleterious effects of greening (Huanglongbing) disease in citrus

Abstract

Summary Under tropical and subtropical environments, citrus leaves are exposed to excess sunlight, inducing photoinhibition. Huanglongbing (HLB, citrus greening), a devastating phloem‐limited disease putatively caused by Candidatus Liberibacter asiaticus, exacerbates this challenge with additional photosynthetic loss and excessive starch accumulation. A combined metabolomics and physiological approach was used to elucidate whether shade alleviates the deleterious effects of HLB in field‐grown citrus trees, and to understand the underlying metabolic mechanisms related to shade‐induced morpho‐physiological changes in citrus. Using metabolite profiling and multinomial logistic regression, we identified pivotal metabolites altered in response to shade. A core metabolic network associated with shade conditions was identified through pathway enrichment analysis and metabolite mapping. We measured physio‐biochemical responses and growth and yield characteristics. With these, the relationships between metabolic network and the variables measured above were investigated. We found that moderate‐shade alleviates sink limitation by preventing excessive starch accumulation and increasing foliar sucrose levels. Increased growth and fruit yield in shaded compared with non‐shaded trees were associated with increased photosystem II efficiency and leaf carbon fixation pathway metabolites. Our study also shows that, in HLB‐affected trees under shade, the signaling of plant hormones (auxins and cytokinins) and nitrogen supply were downregulated with reducing new shoot production likely due to diminished needs of cell damage repair and tissue regeneration under shade. Overall, our findings provide the first glimpse of the complex dynamics between cellular metabolites and leaf physiological functions in citrus HLB pathosystem under shade, and reveal the mechanistic basis of how shade ameliorates HLB disease.

Nontargeted metabolomics-based multiple machine learning modeling boosts early accurate detection for citrus Huanglongbing

“…Overall, most of the metabolites in the pathway of carbon fixation in photosynthetic organisms were downregulated, and those distributed in other pathways were upregulated (see Figure 2 and Supplementary Data S3 ). This result is quite consistent with the previous reports [ 19 , 39 – 45 ].…”

“…Wei et al [ 40 ] also reported that the number of differentially expressed genes (DEGs) related to photosynthesis detected in “Valencia” orange ( C. sinensis ) at one and five days of post- Ca Las-infected psyllid infection was greatly less than that of healthy psyllid infection. Suh et al’s [ 19 ] research indicated the obvious downregulation of metabolites involved in carbon fixation in photosynthetic organisms in the leaves of four-year-old “Hamlin” orange ( C. sinensis ) trees naturally infected by Ca Las before experiments.…”

“…As the end products of cellular processes and genetic or environmental information processing, metabolites are directly linked to the phenotypes of plants, and their levels can be regarded as the ultimate response of biological systems to genetic or environmental changes [ 18 ]. In the presence of disease, the abundances of some metabolites in plants are significantly altered compared to the healthy states [ 19 ]. However, metabolites own a wide range of diverse chemical structures and are also highly dynamic in time and space, raising the challenges for analytical techniques in measuring them as a whole [ 20 ].…”

Individual Protective Covers (IPCs) Improve Yield and Quality of Citrus Fruit under Endemic Huanglongbing (HLB)

“…It was not clear if this advantage conferred by IPCs is the result of maintaining trees free from HLB, shading effect, or both combined. Shading can promote tree growth in citrus and improve photosynthesis [14] and may ameliorate HLB symptoms [15]. This possibility merits further evaluation, which is currently being performed in our labs.…”

Single-cell transcriptome sequencing revealing the difference in photosynthesis and carbohydrate metabolism between epidermal cells and non-epidermal cells of Gracilariopsis lemaneiformis (Rhodophyta)

“…In plants, photoassimilates are produced in source tissues (photosynthetically active tissues, such as leaves) and then allowed to be transported to support the growth of sink tissues such as fruits or roots which themselves are unable to produce assimilates or the assimilates produced by themselves are not enough to support their own needs ( Hofius and Börnke, 2007 ; Albacete et al., 2014 ; Suh et al., 2021 ).…”