Accessory genes in tropical race 4 contributed to the recent resurgence of the devastating disease of Fusarium wilt of banana

Abstract Fusarium wilt of banana, caused by Fusarium oxysporum f. sp. cubense ( Foc ), is one of the most damaging plant diseases recorded. Foc race 1 (R1) decimated the Gros Michel–based banana trade. Currently, tropical race 4 (TR4) is threatening the global production of its replacement cultivar, Cavendish banana. Population genomics and phylogenetics revealed that all Cavendish banana–infecting race 4 strains shared an evolutionary origin that is distinct from R1 strains. The TR4 genome lacks accessory or pathogenicity chromosomes, reported in other F. oxysporum genomes. Accessory genes—enriched for virulence and mitochondrial-related functions—are attached to ends of some core chromosomes. Meta-transcriptomics revealed the unique induction of the entire mitochondria-localized nitric oxide (NO) biosynthesis pathway upon TR4 infection. Empirically, we confirmed the unique induction of NO burst in TR4,suggesting the involvement of nitrosative pressure in its virulence. Targeted mutagenesis demonstrated the functional importance of accessory genes SIX1 and SIX4 as virulent factors.