GENOME INFORMED COMPARATIVE CHARACTERIZATION OF A BANANA FUSARIUM WILT PATHOGEN IN HAWAI’I AND SCREENING BANANA GERMPLASM FOR DISEASE RESISTANCE

Date
2022
Authors
Shipman, Aaron Keith
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Tian, Miaoying
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Tropical Plant Pathology
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Bananas are one of the most popular fruits, being crucial to global food and economic security. Fusarium wilt of banana, also known as Panama wilt, is a major threat to banana production worldwide. The disease is caused by several pathogens in distinct lineages of the Fusarium oxysporum species complex (FOSC). Fusarium oxysporum f. sp. cubense (FOC) refers to a polyphyletic group of FOSC pathogens that are specialized for attacking bananas, which all cause vascular wilt disease. Few lineages of FOC are well understood regarding evolutionary relatedness, virulence, and pathogenic host range on different types of bananas. A strain of the pathogen was recently isolated during a survey for Fusarium wilt of banana in the State of Hawaii. A comparative study was performed by whole genome sequencing and by evaluating the responses of a diverse panel of 26 banana species, subspecies, and domesticated varieties of banana. The Hawaii isolate was pathogenic to 18 of these accessions, of which 8 were highly susceptible to disease. ‘Gros Michel’, the banana variety differentiating race 1 pathogenicity was highly susceptible while, ‘Cavendish’, the race 4 differential was highly resistant. Very interestingly, ‘Bluggoe’ the variety differentiating race 2 pathogenicity was only moderately resistant. All the major banana cultivars grown in Hawaii were affected by this disease. Phylogenetic analysis of the TEF-1α (translation elongation factor), the RPB1 (largest subunit of DNA-dependent RNA polymerase II), and the RPB2 (second largest subunit of DNA-dependent RNA polymerase II) barcoding regions classified this Hawaii isolate to an understudied FOC lineage undergoing geographical range expansion and genetic diversification in Asia, which was proposed to be named Fusarium grosmichelii in 2019. More recent advances into the systematics of FOSC in 2020 suggested that all FOSC diversity should be classified into three phylogenetic species. Through further phylogenetic analysis based on seven genomic loci and the conserved coding sequences of whole genomes, multiple lineages of FOC were shown, including the Hawaii isolate, to be nestled within a larger species proposed as Fusarium oxysporum sensu stricto by the 2020 study, while other FOC lineages were classified into the two other species. This is the first study showing FOC is classified into the three species delimited within the Fusarium oxysporum species complex. Furthermore, whole genome phylogenies suggested that the lineage of Fusarium grosmichelii is more closely related to FOSC isolates pathogenic to pea and watermelon than to other lineages pathogenic to banana. Screening of a 99.7% complete de novo genome assembly as indicated by analysis with BUSCO software found a unique profile of secreted in xylem (SIX) genes, composed of two different copies of SIX1 and SIX9 each and a copy of SIX13, with SIX4 and SIX6 absent. This is the first report of this FOC lineage outside of Asia, and the first report of an isolate of this lineage lacking homologs of SIX4 and SIX6. This study also reports the first formal description of a pathogen found causing Fusarium wilt of banana in Hawaii, and to our knowledge, produced the first publicly available whole genome assembly representing this lineage of FOC. These findings are presented alongside the differential pathogenic host range and virulence of this Hawaii isolate on a large diverse set of banana germplasm, which the dual approach of de novo genome assembly and large disease assay is unavailable for most lineages. These findings serve to further basic knowledge on this lineage of FOC regarding pathogenicity and evolutionary systematics. The implications of this study could guide banana breeding and cultivar deployment in Hawaii and beyond.
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Agriculture, Plant sciences, Pathology, avirulence gene, banana, disease management, Fusarium oxysporum f. sp. cubense, pathogen virulence, SIX effectors
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87 pages
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