Disease-Induced Microbial Shifts in Citrus Indicate Microbiome-Derived Responses to Huanglongbing Across the Disease Severity Spectrum

Abstract

Plant microbiomes are critical components to plant health and can influence disease outcomes. We provide empirical data describing disease-induced shifts within the citrus microbiome at different levels of Huanglongbing (HLB) disease severity. HLB is associated with an invasive phloem-limited bacterium, Candidatus Liberibacter asiaticus (CLas), that is introduced into the aerial portions of the tree by an insect vector. Disease manifests as above ground foliar and fruit symptoms and significant root decline below ground. During the early phase of disease, there were depletions of putative keystone taxa in leaves and roots, followed by enrichments of putative beneficial taxa suggesting a microbially-derived immune response involved in plant protection that is ancillary to immune components encoded in the plant’s genome. In the late phase of disease, we observed enrichments of parasitic and saprophytic microorganisms particularly in the roots. The community shifts within the root compartment are emblematic of a disease-induced dysbiosis where pathogens other than CLas begin to dominate the community. Furthermore, we define key taxa enriched in trees with a slower rate of disease development, referred to as survivor trees, that are hallmarks of those found in trees in the early phase of disease that may be drivers of the survivor tree phenotype. We propose a disease ecology model that illustrates the relationship between the pathogen, the microbiome and the host plant that highlights microorganisms that may serve as disease facilitators or antagonists.

Microbiome and Metagenome Analysis Reveals Huanglongbing Affects the Abundance of Citrus Rhizosphere Bacteria Associated with Resistance and Energy Metabolism

“…We identified 16 bacterial phyla in citrus root endophytes and rhizosphere, of which Proteobacteria, Actinobacteria, and Acidobacteria were the top three most abundant phyla, which is in line with previous studies [32][33][34]. This indicates that these three bacterial phyla may play important roles in the environmental acclimation in citrus roots, and possibly their abundance may not be easily affected by geographical location and citrus variety.…”

Plant Genotype Shapes the Bacterial Microbiome of Fruits, Leaves, and Soil in Olive Plants

“…For example, the abiotic environment has been reported to strongly drive the composition of the plant microbiome, including soil [ 1 , 2 , 3 ], atmosphere [ 4 ], geography [ 5 , 6 ], and many others. In addition, the plant microbiome is under the influence of many biotic factors, some of them exogenous like herbivory [ 1 , 7 ] or plant diseases [ 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 ], some others are instead driven by the plant itself. Indeed, previous studies reported variation in the structure of plant microbiomes according to compartment (e.g., root, leaf, fruit, flower) [ 18 ], but also within the same compartment, for example between different parts of flowers and fruits, or between internal and external tissues [ 18 , 19 ].…”

Arbuscular mycorrhizal fungal composition across US citrus orchards, management strategies, and disease severity spectrum

“…These symptoms are caused by carbon sequestration in the aboveground tissues and poor belowground translocation of photoassimilates leading to root carbohydrate starvation (63) and likely results in a disturbance of the symbiosis with AMF. In parallel, the mycorrhizal decline was also coupled with a significant increase in parasitic fungi and oomycetes (i.e., Fusarium and Phytophthora ) of the host rhizosphere and this enrichment of root-associated parasites was proposed to contribute to the root decline and hasten the decline of trees impacted with HLB (22). Several studies have highlighted the instrumental role of AMF in delaying disease onset or reducing symptoms against the soilborne pathogens Fusarium and Phytophthora in several pathosystems (64, 65) including citrus (24, 25).…”

“…Samples were collected similarly in Florida and lyophilized prior to shipment to UCR under USDA permit #P526P-16-00352 on dry ice. DNA extraction, library construction and sequencing: DNA was extracted from roots according to published protocols (22). Frozen and freeze-dried roots were crushed into small pieces (<0.5 cm) with sterile stainless-steel spatulas on dry-ice, and 100 mg of freeze-dried tissue was transferred to 2-ml microcentrifuge tubes (Eppendorf Safe-Lock tubes; Eppendorf, Hamburg, Germany) containing a single 4-mm stainless-steel grinding ball (SPEX SamplePrep, Metuchen, NJ, U.S.A.).…”