Abstract
Plant pathogens continuously evolve to evade host immune responses. During host colonization, many fungal pathogens secrete effectors to perturb such responses, but these in turn may become recognized by host immune receptors. To facilitate the evolution of effector repertoires, such as the elimination of recognized effectors, effector genes often reside in genomic regions that display increased plasticity, a phenomenon that is captured in the two‐speed genome hypothesis. The genome of the vascular wilt fungus Verticillium dahliae displays regions with extensive presence/absence polymorphisms, so‐called lineage‐specific regions, that are enriched in in planta‐induced putative effector genes. As expected, comparative genomics reveals differential degrees of sequence divergence between lineage‐specific regions and the core genome. Unanticipated, lineage‐specific regions display markedly higher sequence conservation in coding as well as noncoding regions than the core genome. We provide evidence that disqualifies horizontal transfer to explain the observed sequence conservation and conclude that sequence divergence occurs at a slower pace in lineage‐specific regions of the V. dahliae genome. We hypothesize that differences in chromatin organisation may explain lower nucleotide substitution rates in the plastic, lineage‐specific regions of V. dahliae.
Highlights
We provide evidence that disqualifies horizontal transfer to explain the observed se‐ quence conservation and conclude that sequence divergence occurs at a slower pace in lineage‐specific regions of the V. dahliae genome
No significant differences between LS and core genome regions were found in alignments with V. tricorpus, V. klebahnii and V. zaregamsianum
If the increased sequence conservation would be caused by horizontal transfers, V. dahliae and V. tricorpus each should have been involved in at least five such transfers during their evolution to explain the difference in median sequence identity between LS and core genome regions (Figure 4, Table 1)
Summary
Genomes of Verticillium albo‐atrum PD747, Verticillium alfal‐ fae PD683, V. dahliae JR2 and VdLs17, Verticillium isaacii PD618, Verticillium klebahnii PD401, Verticillium nubilum PD621, Verticillium tricorpus PD593 and MUCL9792, Verticillium zaregamsianum PD739 were previously assembled (Faino et al, 2015; Klosterman et al, 2011; Seidl et al, 2015; Shi‐Kunne, Faino, Berg, Thomma, & Seidl, 2018) and sequence reads of Verticillium nonalfalfae isolates TAB2 and Rec are publicly available (Bioproject PRJNA283258; Jelen, Jonge, Peer, Javornik, & Jakse, 2016). To investigate whether other Verticillium species carry LS re‐ gions that display high interspecific sequence identity, we performed alignments using V. tricorpus strain PD593 as a reference because of its high degree of completeness with seven of the nine scaffolds probably representing complete chromosomes (Table S2; Shi‐Kunne et al, 2018) This species belongs to the Flavexudans clade, in contrast to V. dahliae that belongs to Flavnonexudans. To explain the high sequence identity through the occurrence of interspecific horizontal DNA transfers, a minimum of five such transfers must have occurred that involve V. dahliae to ex‐ plain the differences in median sequence identities of LS and core genome regions with the other Verticillium species (Figure 4, Table 1). In congru‐ ence with this hypothesis, sequence comparisons of coding and intergenic regions between V. dahliae and V. nonalfalfae revealed that increased sequence conservation occurs in coding regions as well as intergenic sequences (Figure 7b), suggesting that the increased sequence conservation is driven by a mechanism that affects whole LS regions, rather than by selection
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