Repeat-Induced Point Mutations Drive Divergence between Fusarium circinatum and Its Close Relatives

Abstract

The Repeat-Induced Point (RIP) mutation pathway is a fungal-specific genome defense mechanism that counteracts the deleterious effects of transposable elements. This pathway permanently mutates its target sequences by introducing cytosine to thymine transitions. We investigated the genome-wide occurrence of RIP in the pitch canker pathogen, Fusarium circinatum, and its close relatives in the Fusarium fujikuroi species complex (FFSC). Our results showed that the examined fungi all exhibited hallmarks of RIP, but that they differed in terms of the extent to which their genomes were affected by this pathway. RIP mutations constituted a large proportion of all the FFSC genomes, including both core and dispensable chromosomes, although the latter were generally more extensively affected by RIP. Large RIP-affected genomic regions were also much more gene sparse than the rest of the genome. Our data further showed that RIP-directed sequence diversification increased the variability between homologous regions of related species, and that RIP-affected regions can interfere with homologous recombination during meiosis, thereby contributing to post-mating segregation distortion. Taken together, these findings suggest that RIP can drive the independent divergence of chromosomes, alter chromosome architecture, and contribute to the divergence among F. circinatum and other members of this economically important group of fungi.

Genome-Wide Analyses of Repeat-Induced Point Mutations in the Ascomycota

“…The study of RIP has allowed important conclusions to be drawn regarding the role of this process in fungal evolution. Apart from maintaining genome integrity, RIP can bring about a range of functionally consequential genetic changes ( Rouxel et al, 2011 ; Meerupati et al, 2013 ; King et al, 2015 ; Testa et al, 2016 ; van Wyk et al, 2019a ). This is because RIP activity can lead to the formation of long stretches of AT-rich sequences, causing such genomic regions to be generally gene sparse ( Rouxel et al, 2011 ; van Wyk et al, 2019a ).…”

“…Apart from maintaining genome integrity, RIP can bring about a range of functionally consequential genetic changes ( Rouxel et al, 2011 ; Meerupati et al, 2013 ; King et al, 2015 ; Testa et al, 2016 ; van Wyk et al, 2019a ). This is because RIP activity can lead to the formation of long stretches of AT-rich sequences, causing such genomic regions to be generally gene sparse ( Rouxel et al, 2011 ; van Wyk et al, 2019a ). Also, large-scale accumulation of RIP products promotes the loss of sequence similarity between homologous DNA sequences ( Ellison et al, 2011 ; van Wyk et al, 2019a ), while RIP-associated methylation brings about suppressed recombination ( Ellison et al, 2011 ).…”

“…This is because RIP activity can lead to the formation of long stretches of AT-rich sequences, causing such genomic regions to be generally gene sparse ( Rouxel et al, 2011 ; van Wyk et al, 2019a ). Also, large-scale accumulation of RIP products promotes the loss of sequence similarity between homologous DNA sequences ( Ellison et al, 2011 ; van Wyk et al, 2019a ), while RIP-associated methylation brings about suppressed recombination ( Ellison et al, 2011 ). The combined effects of these processes contribute to lineage divergence and lineage-specific evolution, as have been observed in fungi such as Neurospora tetrasperma ( Ellison et al, 2011 ; Sun et al, 2017 ) and species in the Fusarium fujikuroi complex ( van Wyk et al, 2019a ).…”

“…Although sliding window-based approaches have been previously established, these have not been adopted widely due to the extensive occurrence of false positive results associated with the use of overly lenient parameters ( Hane and Oliver, 2008 ; van Wyk et al, 2019b ). To exacerbate the matter further, most analyses of RIP are performed within the bounds of gene-level duplications or TE repeats ( Hane and Oliver, 2008 ) and do not take into account the fact that RIP may “leak” beyond the bounds of genetic targets, thereby affecting adjacent genomic regions ( Irelan et al, 1994 ; Rouxel et al, 2011 ; Van de Wouw et al, 2018 ; van Wyk et al, 2019a ). The consequence of all these complexities and limitations is that our understanding of the extent of RIP on a genome-wide scale remains unclear, because such information cannot be readily extrapolated from TE and gene-level RIP analyses.…”

Unique Patterns of Mating Pheromone Presence and Absence could Result in the Ambiguous Sexual Behaviours of Colletotrichum Species

“…Interestingly, certain Colletotrichum species, particularly those belonging to the orbiculare species complex, have surprisingly high RIP values; up to 56% in C. trifolii. This is signi cantly higher that other reports of genome-wide RIP content, including those for N. crassa (15%) and various Fusarium species (up to 6.4%) (48). The signi cance of these high RIP levels needs to be further investigated as it may have noteworthy implications for the evolutionary history and future of this genus.…”