Metabolomic Analysis Revealed Distinct Physiological Responses of Leaves and Roots to Huanglongbing in a Citrus Rootstock

Huanglongbing (HLB) is an obstinate disease in the citrus industry. No resistant citrus resources were currently available, but various degrees of Huanglongbing tolerance exist in different germplasm. Citrus junos is emerging as one of the popular rootstocks widely used in the citrus production. However, its responses to the HLB causal agent, Candidatus Liberibacter asiaticus (CLas), were still elusive. In the current study, we investigated the physiological, anatomical, and metabolomic responses of a C. junos rootstock 'Pujiang Xiangcheng' by a controlled CLas grafting inoculation. The summer flushes and roots were impaired at 15 weeks after inoculation, although typical leaf symptomatic phenotypes were not obvious. The chlorophyll pigments and the photosynthetic rate were compromised. The phloem sieve tubes were still working, despite the fact that the callose was deposited and the starch granules were accumulated in the phloem cells. A wide, targeted metabolomic analysis was carried out to explore the systematic alterations of the metabolites at this early stage of infection in the leaves and root system. The differentially accumulated metabolites in the CLas-affected leaves and roots compared with the mock-inoculation control tissues revealed that distinct responses were obvious. Besides the commonly observed alteration of sugar and amino acids, the active break down of starch in the roots was discovered. The different types of fatty acids were altered in the two tissues, with a more pronounced content decline in the roots. Our results not only provided fundamental knowledge about the response of the C. junos rootstock to the HLB disease, but also presented new insights into the host-pathogen interaction in the early stages.