Segmental Duplications Drive the Evolution of Accessory Regions in a Major Crop Pathogen

Abstract

Many pathogens evolved compartmentalized genomes with conserved core and variable accessory regions which carry effector genes mediating virulence. The fungal plant pathogen Fusarium oxysporum has such accessory regions, often spanning entire chromosomes, yet understanding of their evolution in strains that infect the same host remains limited. Here, we define the pan-genome of 69 diverse Fusarium strains that cause Fusarium wilt of banana, a significant constraint to global banana production, and demonstrate that segmental duplications drive the evolution of accessory regions. Accessory regions are highly variable and encode distinct gene repertories, with evolutionarily less constrained, younger genes and in planta-induced effectors, which differ between strains infecting the same banana cultivars. We show that recent segmental duplications and aneuploidy of accessory chromosomes cause the expansion of accessory regions in some Fusarium species. Taken together we conclude that extensive recent duplications drive the evolution of accessory regions in Fusarium, which contribute to the evolution of virulence.

A deep genetic analysis of banana Fusarium wilt pathogens of Cuba in a Latin American and Caribbean diversity landscape

“…Taken together, our analyses provide a high-resolution and genome-wide dataset to describe genetic diversity in FWB - causing Fusarium spp. in an unparalleled manner that matches recent genome-wide analyses (van Westerhoven et al ., 2023: Maryani et al ., 2023).…”

“…To determine the relationship of the sequenced Cuban isolates with other banana-infecting Fusarium spp., we included whole-genome sequencing data of 58 previously sampled FWB pathogen isolates from different species and geographical locations (Table S4). To identify sequence variation, the sequencing reads were aligned against the chromosome-level genome assembly of the F. odoratissimum II5 (NRRL 54006) reference strain (van Westerhoven et al ., 2023) using BWA-mem (v. 0.7.17) (Li, 2013). The SNPs of the 80 isolates compared with the reference genome assembly were called based on the GATK best practices (Auwera et al ., 2013), using GATK4 (v. 4.2.0.0).…”

“…To account for the presence/absence variation between the genomes, we excluded SNPs located on the highly variable genomic regions (chromosome 1, pos. 0-1.2 Mb, and chromosome 12) (van Westerhoven et al ., 2023) as well as SNPs with any missing values. The maximum likelihood phylogenetics tree of the concatenated SNPs was inferred using RAxML (v. 8.2.12, - m GTRCAT).…”

“…The entire collection was deposited in the microbial culture collection of the Instituto de Investigaciones de Sanidad Vegetal (INISAV, Cuba) with a copy at the Laboratory of Phytopathology of Wageningen University & Research (WUR; Table S1). The total data set that was analyzed in this study comprised the Cuban panel of 170 isolates, complemented by a collection of 210 isolates from the Americas and a set of 33 isolates representing a global panel that was analyzed earlier (Ordóñez et al, 2023).…”

“…To further corroborate the DArT-based taxonomic classification, we compared wholegenome short-read sequences of 22 Cuban isolates together with 58 Fusarium isolates from a global panel of fully sequenced isolates(van Westerhoven et al, 2023; Table S5); the 22 Cuban isolates represent the range of diversity in terms of race, lineage, host, and geographic origin across the country. With this collection of isolates, we identified nearly 1,4 million high-quality SNPs and subsequently constructed a maximum-likelihood based phylogenetic tree.…”