First Report of Bacterial Fruit Rot of Banana Caused by <i>Dickeya fangzhongdai</i> in China

Banana (Musa spp.), the fourth largest fruit globally, is extensively cultivated in tropical and subtropical regions. In October 2023, a soft rot disease occurred on green fruits of banana (Musa acuminata, AAA group, cultivar ‘Cavendish’) in a Plantation (23°13'3.72"N, 114°35'19.50"E) in Tiangang Village, Hengli Town, Huizhou City, Guangdong Province, China. The disease incidence of banana plants with 1-10 diseased fruits reached 20% across 33.33 hectares. Symptoms: Initially water-soaked black spots appear on the fruit peel, and after 24 hours, the lesion oozes black foul-smelling fluid. Within 72 hours, rot spread causing fruit cracking. After one week, the fruits are completely rotten, and the pathogen, harbored within the black fluid, spreads to adjacent fruits via the fluid, causing infection. To identify the causal agent, diseased fruits were collected in October and November 2023. 22 bacterial strains were isolated from 5 symptomatic fruits. Pathogenicity tests of 22 strains on banana fruits (3 fruits per strain, a total of 66 fruits were treated) revealed that 14 strains incited water-soaked black spots on inoculated banana fruits, indicating they were pathogenic; while 8 strains did not incited any symptoms on inoculated banana fruits, indicating they were non-pathogenic. Among the 12 strains inducing typical soft rot symptoms, strain BG43 caused the most severe rotting symptoms on inoculated banana fruits. All 12 strains displayed uniform colony morphology: creamy-white at 24 h transitioning to translucent at 72 h. The representative strain BG43 of 12 strains underwent 16S rRNA gene sequencing. BLAST analysis of the 16S rRNA gene sequence (GenBank accession number: PV741228) showed >99% identity with Dickeya fangzhongdai strains. The draft genome of BG43 was sequenced. Phylogenomic analysis (UBCG pipeline; Na et al., 2018) of 1,429 genomes across 28 phyla identified 92 single-copy core genes. A maximum-likelihood tree (RAxML v7.0.4, GTR model) placed BG43 closest to Chinese reference strain DSM 101947, confirming its novel classification as D. fangzhongdai. Inoculation of healthy bananas with BG43 induced typical soft rot symptoms within 48h, while LB-inoculated controls (n=3 fruits, 4 wounds per fruit) remained asymptomatic. Re-isolated pathogens were confirmed as D. fangzhongdai by 16S rRNA gene sequencing and phylogeny (MAFFT, MEGA-X ML, Bootstrap=1,000), clustering with D. fangzhongdai DSM 101947. The genome was deposited in NCBI GenBank (BioProject PRJNA1271973, SUB15366169). Gram staining of BG43 is negative, and it has biochemical properties such as the ability to secrete siderophore and pectinase. This is the first report of D. fangzhongdai causing banana fruit rot in China. This study provides the first conclusive evidence of D. fangzhongdai infecting banana fruits, expanding its known host ranges and damaged parts from banana leaves (Zhang et al., 2014), pseudostems (Guangdong), peduncles (Guangxi) (Yang et al., 2021), and pear trees (Chen et al., 2020) to banana fruits. Its host-jumping adaptation from ornamentals to fruit crops highlights emerging biosafety risks due to evolutionary plasticity. These findings underscore the urgent need for molecular epidemiological surveillance and transnational phytosanitary measures to prevent the global dissemination of this novel bacterial banana fruit rot in banana production regions.