Occurrence of prophage and historical perspectives associated with the dissemination of huanglongbing in mainland China

Authors: FU, SHIMIN - Southwest University; BAI, ZIQIN - Southwest University; SU, HUANAN - Southwest University; LIU, JINXIANG - Southwest University; Hartung, John; ZHOU, CHANGYONG - Southwest University; WANG, XUEFENG - Southwest University

Submitted to: Plant Pathology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/16/2019
Publication Date: 9/24/2019
Citation: Fu, S., Bai, Z., Su, H., Liu, J., Hartung, J.S., Zhou, C., Wang, X. 2019. Occurrence of prophage and historical perspectives associated with the dissemination of huanglongbing in mainland China. Plant Pathology. 69:132-138. https://doi.org/10.1111/ppa.13100.
DOI: https://doi.org/10.1111/ppa.13100

Interpretive Summary: Huanglongbing (HLB) is the most serious disease of citrus in the world today. HLB, also known as citrus greening, originated in China and has devastated the citrus industry in Florida since its introduction there in 2005 and currently threatens to spread out of the Los Angeles basin where it is very widespread and into the San Joaquin Valley and Ventura county to threaten the California citrus industry. The history of HLB in China is long, but poorly documented both within china and for the world outside of china which is now acutely interested in the disease. We carried out an extensive review of literature and unpublished records in China related to the spread of HLB in China from its original description in Fujian province in 1919 to the present. The records show that although the disease had been known for at least 30 years by the time it was described in 1919 it had not spread widely. Then the disease appeared to spread steadily from that point on until it is present wherever citrus is grown in China. The initial spread was due to ignorance of the cause and in some regions dissemination of bud wood and trees, that appeared to be healthy but were infected with HLB. In other regions distribution of infected bud wood and trees was less of a problem than the spread of the insect that transmits the disease. We also used original molecular assays of current HLB samples collected across China to show that there are apparently three strains of the pathogen that are widespread in China. One is present in hot and humid regions at low elevation, another at cooler and higher elevation regions and a third in both areas. This is consistent with a separate origin of the strain found at higher elevations in Sichuan and Yunnan provinces rather than simple spread from the original Fujian outbreak. The different forms of HLB are associated with different viruses that are part of the pathogens genome. Our work will be of interest to the research and regulatory communities primarily in China, but also in the world outside of China, because the global citrus industry is threatened by HLB.

Technical Abstract: Although huanglongbing (HLB) is the most destructive citrus diseases, the history of the dissemination of HLB in mainland China is not well understood. The history of local incursions into previously disease free provinces and the dynamics of both HLB and psyllid introductions were modeled by reviewing and organizing local documents, personal notes and published papers. Three factors contributed to the spread of HLB within China: The origin of the disease within China, the dissemination diseased seedlings and the spread of psyllids. Guangdong has been generally recognized as the site of the origin of HLB but both Yunnan and Sichuan were proposed as the possible origins. The introduction of HLB in Fujian, Guangxi, Jiangxi, Hunan and Zhejiang provinces was likely due to the introduction of diseased seedlings, mostly from Guangdong. However, the spread of psyllids probably led to the introduction of HLB in Guangxi and Guizhou. CLas populations from high altitude regions (HAR), mainly Yunnan and Sichuan, and low altitude regions (LAR) were preferentially associated with SC1 and SC2 prophage, respectively. CLas from HAR possess higher prophage activity and genome plasticity. The molecular evidence support the hypotheses above.