Nutrient and Transcriptome Analyses of Citrus Plants with Distinct Performances in Response to Huanglongbing

Citrus Huanglongbing (HLB), caused by 'Candidatus Liberibacter asiaticus', is currently the most devastating citrus disease worldwide. Interestingly, citrus groves with different performances, good production with lower HLB symptoms (good performance) and poor production with severe HLB symptoms (poor performance), have been observed. Here, we investigated the mechanism underlying this phenomenon. We analyzed 14 sweet orange groves consisting of seven good performance and seven poor performance groves. We analyzed the nutrient contents of approximately 1-year-old asymptomatic leaf tissue, root tissue, and soil samples. Higher concentrations of Mg, P, or S were observed in leaves of good performance groves than in those of poor performance groves. In roots, higher concentrations of N, S, and Mn and lower concentrations of K and Zn were observed in good performance groves than in poor performance groves. Higher concentration of soil organic matter was observed in good performance groves than in poor ones. Our data suggest that good performance groves have better uptake of nutrients than poor performance groves. We also conducted an RNA sequencing analysis of bark tissues of branches with (GS) or without (GA) HLB symptoms from a good performance grove and branches with HLB symptoms (PS) from a poor performance grove. Most differentially expressed NLR, RLCK, and CNGC genes (P < 0.05) were downregulated in GA but upregulated in GS and PS, indicating induced immune response in symptomatic tissues. Auxin-related genes were mostly upregulated in asymptomatic GA but downregulated in symptomatic GS and PS samples. Ethylene-related genes were mostly downregulated in GA and GS but mostly upregulated in PS. Most phloem-specific genes were expressed more in GA compared with GS and PS. Taken together, this study provides valuable information regarding the effects soil organic matter and overall nutrient uptake on citrus health in response to HLB and the molecular mechanism underlying the differential performances of citrus in response to HLB.