Abstract
There have been efforts to develop citrus cultivars that are tolerant of Huanglongbing (HLB), a catastrophic phloem-limited disease. Previous studies demonstrated that continuous plant growth with phloem regeneration is one of the major characteristics of HLB tolerance. In this study, the metabolic mechanisms of HLB tolerance in citrus were elucidated using a multiple pathway-targeted metabolomic approach. Comparative analysis of healthy and infected HLB-tolerant and HLB-sensitive mandarin cultivars (Citrus reticulata) revealed differentially expressed metabolic responses among different groups. Pathway enrichment analysis indicated aspartate and glutamate metabolism, purine metabolism, and biosynthesis of plant hormones were upregulated in the tolerant group, except salicylic acid signaling. Catabolic pathways linked to energy-yielding metabolism were also upregulated in the tolerant group. These metabolisms and pathways were interconnected with each other, unveiling a pivotal metabolic network associated with HLB tolerance. In the network, auxins and cytokinins, the plant hormones responsible for plant growth and phloem regeneration, were accumulated. In addition, purine metabolites serving as energy carriers and nitrogen sources of plants were increased. Only salicylic acid-related metabolites for plant defense responses were decreased in the tolerant group. Our findings may evidence the strategy of HLB-tolerant cultivars that sustain plant growth and phloem formation rather than displaying direct plant defense to overcome the disease.
Highlights
Huanglongbing (HLB), called citrus greening, is one of the most destructive diseases of citrus, presumably caused by phloem-limited bacteria named Candidatus Liberibacter asiaticus (CaLas), which is transmitted to the host by Asian citrus psyllids (Diaphorina citri) (Jagoueix et al, 1994; Bové, 2006)
Rapid replacement of phloem could compensate for the old disrupted phloem caused by the infection. These results suggest that sustaining plant growth, with lower levels of phloem damage and greater phloem regeneration, is a key element that contributes to HLB tolerance (Fan et al, 2013; Deng et al, 2019)
Healthy and CaLas-infected Sugar Belle R mandarin (HLBtolerant group) and ‘Murcott’ mandarin (HLB-sensitive group) trees were selected from the greenhouse at the University of Florida’s Citrus Research and Education Center (Lake Alfred, FL, USA)
Summary
Huanglongbing (HLB), called citrus greening, is one of the most destructive diseases of citrus, presumably caused by phloem-limited bacteria named Candidatus Liberibacter asiaticus (CaLas), which is transmitted to the host by Asian citrus psyllids (Diaphorina citri) (Jagoueix et al, 1994; Bové, 2006). HLB symptoms include leaf vein yellowing, foliar blotchy mottle, and asymmetrical chlorosis, followed by tree decline, leaf loss, and premature fruit drop. HLB has decimated millions of citrus trees, with a decrease in fruit quality and yield, resulting in a significant impact on global citrus production (Kramer et al, 2020; USDA, 2020). In the USA, HLB is prevalent in Florida where more than 95% of citrus groves are infected. Identify HLB-Tolerance Using Metabolomics by CaLas (Kramer et al, 2020). The production of oranges is less than one-third of what it was 20 years ago, leading to severe economic losses to the citrus industry (USDA, 2020)
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