Abstract
Huanglongbing (HLB) is the most devastating and widespread citrus disease. All commercial citrus varieties are susceptible to the HLB-associated bacterium, Candidatus Liberibacter asiaticus (CLas), which resides in the phloem. The phloem is part of the plant vascular system and is involved in sugar transport. To investigate the plant response to CLas, we enriched for proteins surrounding the phloem in an HLB susceptible sweet orange variety, Washington navel (Citrus sinensis (L) Osbeck). Quantitative proteomics revealed global changes in the citrus proteome after CLas inoculation. Plant metabolism and translation were suppressed, whereas defense-related proteins such as peroxidases, proteases and protease inhibitors were induced in the vasculature. Transcript accumulation and enzymatic activity of plant peroxidases in CLas infected sweet orange varieties under greenhouse and field conditions were assessed. Although peroxidase transcript accumulation was induced in CLas infected sweet orange varieties, peroxidase enzymatic activity varied. Specific serine proteases were up-regulated in Washington navel in the presence of CLas based on quantitative proteomics. Subsequent activity-based protein profiling revealed increased activity of two serine proteases, and reduced activity of one protease in two C. sinensis sweet orange varieties under greenhouse and field conditions. The observations in the current study highlight global reprogramming of the citrus vascular proteome and differential regulation of enzyme classes in response to CLas infection. These results open an avenue for further investigation of diverse responses to HLB across different environmental conditions and citrus genotypes.
Highlights
Huanglongbing (HLB) is the most devastating and widespread citrus disease
The sweet orange cultivar Washington navel (Citrus sinensis (L) Osbeck), which is susceptible to HLB, was graft inoculated or mock inoculated with Candidatus Liberibacter asiaticus (CLas) positive budwood
Uninfected samples had an average of 1259 protein identifications and infected samples had an average of 1152 protein identifications across all four biological replicates. 329 (24%) proteins were significantly up-regulated and 363 (27%) proteins were down-regulated in infected samples
Summary
Highlights HLB is the most devastating citrus disease associated with the pathogen CLas. Proteases and peroxidases accumulated in plant vascular tissue after CLas infection. To investigate the plant response to CLas, we enriched for proteins surrounding the phloem in an HLB susceptible sweet orange variety, Washington navel (Citrus sinensis (L) Osbeck). CLas induces plant defense responses in leaf tissue, including the transcription of pathogenesis-related (PR) genes, chitinases, callose synthases, and defense-related WRKY transcription factors [11, 31, 33, 35, 36] Consistent with these observations, infected C. sinensis midveins exhibit callose and starch accumulation in the sieve tubes that lead to phloem plugging and collapse [33, 34, 37]. This study advances our understanding of vascular changes and highlights the important role of peroxidases and proteases during CLas infection
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