Xanthomonas citri pv. citri findings in imported citrus fruit consignments in the Netherlands

Citrus bacterial canker (CBC), caused by Xanthomonas citri pv. citri and pv. aurantifolii, presents a major risk to the Mediterranean citrus producing areas of the European Union (EU). The commercial trade of citrus fruit is recognized as one of the seven significant X. citri pv. citri introduction pathways, however, under the current EU phytosanitary measures the likelihood of introduction of X. citri pv. citri and X. citri pv. aurantifolii in the Mediterranean region with infected fruit is rated unlikely. In order to closely monitor the commercial trade flow of citrus fruit, all imported consignments from outside the EU from 2013-2022 have undergone visual inspection for the presence of CBC symptoms upon entering the Netherlands. Consignments that contained citrus fruits with symptoms that could indicate a X. citri pv citri or X. citri pv. aurantifolii infection were quarantined and a sample of symptomatic fruits per consignment was sent to the laboratory for official analysis. The number of consignments containing such symptomatic citrus fruits increased from only 8 in 2013 to 136 in 2022. Survey results revealed the presence of only X. citri pv. citri in 97 infected consignments in the period 2013-2022. Remarkably, 48 consignments were infected with X. citri pv. citri in 2022 alone, representing a 35.3% of the consignments containing symptomatic citrus fruit, matching the expected CBC symptoms. These X. citri pv. citri infected consignments in the period 2013-2022 primarily referred to fruits of C. latifolia (64), C. hystrix (17) and C. grandis (11) and from several countries in South and Southeast Asia as well as in South America. The increasing number of intercepted consignments containing symptomatic citrus fruits due to the presence of viable and highly pathogenic X citri pv citri strains entering the Netherlands raises concerns about the effectiveness of the post-harvest chemical disinfection treatment implemented in the citrus fruit exporting countries. It additionally puts the role of citrus fruit in the long distance dispersal of X. citri pv. citri under debate. Appropriate monitoring of the citrus fruit trade flow by visual inspections for the presence of CBC symptoms and subsequent laboratory testing remains a significant tool in reducing the potential risk of the long distance dispersal of X. citri pv. citri.

由野油菜黄单胞菌柑橘致病变种（Xanthomonas citri pv. citri）与野油菜黄单胞菌橙致病变种（pv. aurantifolii）引发的柑橘细菌性溃疡病（Citrus bacterial canker, CBC），对欧盟（European Union, EU）地中海柑橘产区构成重大威胁。商用柑橘果品贸易被认定为野油菜黄单胞菌柑橘致病变种的七大主要传入途径之一，但依据欧盟现行植物检疫措施，受感染果品携带该病菌及橙致病变种传入地中海地区的可能性被评定为低风险。为严密监测柑橘果品的商业贸易流向，2013至2022年间，所有从欧盟境外进口的货批在入境荷兰时均需接受柑橘细菌性溃疡病症状的目视检查。凡检出疑似野油菜黄单胞菌柑橘致病变种或橙致病变种感染症状的柑橘果品货批，均予以隔离检疫，并从每批带症状果品中抽取样品送至实验室开展官方检测。此类带症状柑橘果品的货批数量从2013年的仅8批，增长至2022年的136批。2013至2022年的调查结果显示，仅在97批受感染货批中检出野油菜黄单胞菌柑橘致病变种。值得注意的是，仅2022年就有48批货批感染该病菌，占同期带症状柑橘果品货批的35.3%，与预期的柑橘细菌性溃疡病症状特征相符。2013至2022年间检出的野油菜黄单胞菌柑橘致病变种感染货批，主要涉及来自南亚、东南亚及南美洲多国的C. latifolia（64批）、C. hystrix（17批）与C. grandis（11批）果品。入境荷兰的携带活性且高致病性野油菜黄单胞菌柑橘致病变种菌株的带症状柑橘果品货批数量持续攀升，这引发了业界对柑橘果品出口国所采用的采后化学消毒处理措施有效性的担忧，同时也使柑橘果品在野油菜黄单胞菌柑橘致病变种长距离传播中所扮演的角色受到广泛质疑。通过目视检查柑橘果品是否存在溃疡病症状，并辅以后续实验室检测的常规监测手段，仍是降低野油菜黄单胞菌柑橘致病变种长距离传播潜在风险的重要防控工具。