Genome sequence data reveal at least two distinct incursions of the tropical race 4 (TR4) variant ofFusariumwilt into South America

Abstract

The global banana industry is threatened by one of the most devastating diseases: Fusarium wilt (FWB). FWB is caused by the soil-borne fungus Fusarium oxysporum f. sp. cubense (Foc), which almost annihilated the banana production in the late 1950s. A new strain of Foc, known as tropical race 4 (TR4), attacks a wide range of banana varieties including Cavendish clones which are the source of 99% of banana exports. In 2019, Foc TR4 was reported in Colombia, and more recently (2021) in Peru. In this study, we sequenced three fungal isolates identified as Foc TR4 from La Guajira (Colombia) and compared them against 19 whole-genome sequences of Foc TR4 publicly available, including four genome sequences recently released from Peru. To understand the genetic relatedness of the Colombian Foc TR4 isolates and those from Peru, we conducted a phylogenetic analysis based on a genome-wide set of single nucleotide polymorphisms (SNPs). Additionally, we compared the genomes of the 22 available Foc TR4 isolates looking for the presence-absence of gene polymorphisms and genomic regions. Our results reveal that (i) the Colombian and Peruvian isolates are genetically distant, which could be better explained by independent incursions of the pathogen to the continent, and (ii) there is a high correspondence between the genetic relatedness and geographic origin of Foc TR4. The profile of present/absent genes and the distribution of missing genomic regions showed a high correspondence to the clades recovered in the phylogenetic analysis, supporting the results obtained by SNP-based phylogeny.

Uncontained spread of Fusarium wilt of banana threatens African food security

“… ( A ) Banana is a major food crop in tropical and subtropical regions, especially in sub-Saharan Africa. In most major banana-producing regions, TR4 incursions have been reported (green dots), and TR4 is spreading globally from its Asian center of origin to other banana-growing regions [ 8 , 19 – 27 ]. The colors of the countries on the global map indicate banana production in million tonnes per year.…”

“…Map downloaded from Natural Earth Data; https://www.naturalearthdata.com . ( B ) Cavendish banana plant in Mozambique showing external FWB symptoms, caused by TR4 [ 27 ].…”

“…In 2013, the first incursion outside South East Asia was reported in Jordan [ 20 ] ( Fig 1 ). Since then, 12 incursions followed in the Middle East [ 21 ], the Indian subcontinent [ 22 ], Africa [ 23 , 24 ], and most recently in Latin America [ 25 – 27 ] ( Fig 1 ).…”

“…Upon the first report of TR4 in the Guajira department in 2019 [ 25 ], Colombia declared a state of emergence entailing sanitary control measures as well as aerial and on-the-ground inspections as part of the containment strategy [ 32 ]. Nevertheless, in 2021, TR4 also appeared in the neighboring Magdalena department [ 27 ], demonstrating the spread of TR4 irrespective of the implemented containment strategies. A recent incursion in Peru [ 26 ] illustrates ongoing local and global spread but is considered to be independent of the presence of TR4 in Colombia [ 27 ].…”

“…Nevertheless, in 2021, TR4 also appeared in the neighboring Magdalena department [ 27 ], demonstrating the spread of TR4 irrespective of the implemented containment strategies. A recent incursion in Peru [ 26 ] illustrates ongoing local and global spread but is considered to be independent of the presence of TR4 in Colombia [ 27 ]. However, this can only be concluded after sufficient sampling in Colombia.…”