Comparative Genomics of Fov (Fusarium oxysporum f. sp. vasinfectum) in US Cotton Provides Insights into Race-Specific Regions Related to Pathogenicity and Evolution

Fusarium wilt disease of cotton, caused by soil-borne fungal pathogen Fusarium oxysporum f. sp. vasinfectum (Fov), is a continuing problem causing cotton losses worldwide. The upland U.S. cotton industry is currently facing a strategic threat by reason of the expansion of Fov Race 4 (Fov4) from the San Joaquin Valley of California in 2003 into Texas and New Mexico in 2017. There is an incumbent need to understand the extent of genetic diversity and pathogenicity of different Fov isolates in the field. While Race1 requires root knot nematode to effectively cause infection in cotton, Race4 is independent of root knot nematode. The differences in behavior of between these two races is unknown.

Lineage-specific chromosomes have been reported to determine host specific pathogenicity in Fusarium oxysporum species but there is no report of lineage specific chromosomes in Fov and its function. We deployed long read whole genome sequencing and captured Race-specific (RS) regions unique to Race1 and Race4 Fov genomes. These RS regions were more enriched in GC, repetitive sequences, transposons and effectors compared to the core regions of all four genomes sequenced. It is well known that fungal avirulence genes encode virulence factors called effectors which play major role in virulence. RS regions amassed more secreted effectors with transmembrane domain and extracellular localization in contrast with the core chromosome regions. Genes and transposon elements enriched in these Race-specific regions might have strong correlation with pathogenicity and explain the different behavior of CA10 (Race 1) isolates compared to CA14 (Race 4) isolates. We also show several gene duplication events only observed in the Race-specific regions of the Fov genomes which plays an important role in the evolution of Fov. This is the first report of compartmentalization and identification of Race-specific regions with several events of gene duplication in the Fov genome.