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AR TICLE Mitochondrial Introgression And doi:10.5598/imafungus.2018.09.01.04 IMA FUNGUS · 9(1): 37–48 (2018) Mitochondrial introgression and interspecies recombination in the ARTICLE Fusarium fujikuroi species complex Gerda Fourie, Nicolaas A. Van der Merwe, Brenda D. Wingfield, Mesfin Bogale, Michael J. Wingfield, and Emma T. Steenkamp Department of Genetics, Biochemistry and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, South Africa; corresponding author e-mail: [email protected] Abstract: The Fusarium fujikuroi species complex (FFSC) is an economically Key words: important monophyletic lineage in the genus Fusarium. Incongruence observed evolutionary history among mitochondrial gene trees, as well as the multiple non-orthologous copies FFSC of the internal transcribed spacer region of the ribosomal RNA genes, suggests heteroplasmy-associated mitochondrial recombination that the origin and history of this complex likely involved interspecies gene hybridization flow. Based on this hypothesis, the mitochondrial genomes of non-conspecific introgression species should harbour signatures of introgression or introgressive hybridization. species concepts The aim of this study was therefore to search for recombination between the mitochondrial genomes of different species in the FFSC. Using methods based on mt genome sequence similarity, five significant recombinant regions in both gene and intergenic regions were detected. Using coalescent-based methods and the sequences for individual mt genes, various ancestral recombination events between different lineages of the FFSC were also detected. These findings suggest that interspecies gene flow and introgression are likely to have played key roles in the evolution of the FFSC at both ancient and more recent time scales. Article info: Submitted: 12 January 2018; Accepted: 18 February 2018; Published: 27 February 2018. INTRODUCTION material into the genome of that parental species. The process of introgressing new genetic material into the gene The Fusarium fujikuroi species complex (FFSC, previously pool of a species is referred to as “introgressive hybridization” referred to as the Gibberella fujikuroi species complex) is (Anderson & Hubricht 1938). In nature, interspecies gene one of several monophyletic assemblages in the genus flow is generally thought to be limited by species isolation Fusarium (phylum Ascomycota, order Hypocreales) (Geiser mechanisms, such as vegetative incompatibility, pheromone- et al. 2013). This complex is well-known for the many well- receptor recognition, intersterility and post-zygotic nuclear- documented plant pathogens and mycotoxin producers it cytoplasmic incompatibility systems that restrict or prevent includes (Kvas et al. 2009). Previous work suggests that the exchange of genetic material between species (Giraud the FFSC likely emerged during the middle-to-late Miocene et al 2008). In many Fusarium species, including those in (O’Donnell et al. 2013) and that its evolutionary history could the FFSC, laboratory-based mating studies have shown that have involved interspecies gene flow (O’Donnell & Cigelnik the level of reproductive isolation is not complete and that 1997). Such interspecies interactions have also been various species are capable of interbreeding (Desjardins et described from other Fusarium species (e.g. F. oxysporum al. 2000, Leslie et al. 2004b). and F. graminearum species complexes) (Ma et al. 2010, The mitochondrial (mt) genome is potentially a valuable O’Donnell et al. 2000a) and, in the FFSC, was suggested to tool for studying hybridization and introgression in fungi. explain the existence of multiple non-orthologous copies of Fungal mitochondria are mostly inherited from the maternal the internal transcribed spacer region of the ribosomal RNA parent (Taylor 1986), but cross-species interactions would genes (O’Donnell & Cigelnik 1997). often lead to a short-lived heteroplasmic state in which Interspecies gene flow is typically associated with the hybrid individual would harbour mt haplotypes from hybridization and introgression (Stuckenbrock 2016). both parents (Ballard & Whitlock 2004, Barr et al. 2005). Hybridization is the production of viable and recombinant Recombination between the different haplotypes would offspring by non-conspecific individuals. Introgression occurs cause the introduction and/or replacement of new genes/ when short-lived hybrids backcross with individuals from regions on one or both mt genomes. Such signatures of the the parental species, allowing incorporation of new genetic ancestral cross-species interactions thus would be retained © 2018 International Mycological Association You are free to share - to copy, distribute and transmit the work, under the following conditions: Attribution: You must attribute the work in the manner specified by the author or licensor (but not in any way that suggests that they endorse you or your use of the work). Non-commercial: You may not use this work for commercial purposes. No derivative works: You may not alter, transform, or build upon this work. For any reuse or distribution, you must make clear to others the license terms of this work, which can be found at http://creativecommons.org/licenses/by-nc-nd/3.0/legalcode. Any of the above conditions can be waived if you get permission from the copyright holder. Nothing in this license impairs or restricts the author’s moral rights. VOLUME 9 · NO. 1 37 Fourie et al. in the species’ mt genomes, despite the fact that one of the Mt genome sequencing and assembly mt haplotypes would typically be purged from subsequent To determine the mt genome sequence for F. temperatum populations (Rand 2001). In fish, for example, Wilson & isolate CMWF 389 and F. mangiferae isolate CMWF 1214 Bernatchez (1998) described an ancient introgession in (Table 1), total genomic DNA was extracted as described Salvelinus namaycush (trout) due to the presence of a previously (Groenewald et al. 2006) and subjected to ARTICLE single mt haplotype belonging to S. alpines (arctic char) in pyrosequencing at Inqaba Biotechnologies (Pretoria, South the S. namaycush population. In plants, Jaramillo-Correa Africa) on a single lane using the GS-FLX platform (Roche & Bousquet (2005) described mitochondrial recombination 454 system, Life Sciences, CT). After exclusion of low quality between Picea mariana (black spruce) and P. rebens (red reads, those encoding mt sequences were identified using spruce) as a result of introgressive hybridization in the zone BLAST comparison to the available FFSC mt genomes (Al- of contact between these conifers in north-eastern North Reedy et al. 2012, Fourie et al. 2013). The mt reads for the America. Examples from fungi are still limited, but Fourie two species were subsequently assembled de novo with the et al. (2013) hypothesized that the incongruence observed CLC Genomics Workbench software version 6.0 (CLC bio, among gene trees inferred from mitochondrial genes could Århus, Denmark). The order and orientation of contigs were have resulted from recombination between the mt genomes determined using F. circinatum, F. verticillioides, and F. fujikuroi of non-conspecific species. as reference genomes. Gaps between contigs were filled In this study we considered the hypothesis that introgres- manually by Sanger sequencing. Protein coding and tRNA sion or introgressive hybridization occurred in the history of mt genes were identified with MFANNOT and RNAweasel the FFSC. Our first aim was to identify and characterize re- (http://megasun.bch.umontreal.ca) (Lang et al. 2007), as well gions in the mt genomes of extant FFSC species that po- as tRNAscan-SE (Lowe & Eddy 1997). Gene identities were tentially originate from such interspecies gene flow events. confirmed with BLASTp comparisons against NCBI. For this purpose, the mt genomes for two FFSC species (i.e. F. mangiferae and F. sterilihyphosum) were determined and Mt genome-based recombination analysis used to complement those (F. circinatum, F. verticillioides (RDP, Bootscan, Geneconv and Maximum χ²) and F. fujikuroi) already in the public domain (Al-Reedy et al. The Recombination Detection Program (RDP) package version 2012, Fourie et al. 2013). These genomes were then subject- 3.44 (Martin et al. 2010) was used to screen for possible ed to the recombination detection method (Martin & Rybicki recombination events in the five FFSC mt genomes and the 2000), Bootscan (Martin et al. 2005), Geneconv (Padidam et individual gene datasets using RDP (Martin & Rybicki 2000), al. 1999) and Maximum χ² (Smith 1992) analyses that were Bootscan (Martin et al. 2005), Geneconv (Padidam et al. 1999) designed for detecting interspecific recombination (Martin et and Maximum χ² (Smith 1992). Since these tools differ with al. 2010). The second aim of this study was to utilize a co- regards to their power to detect recombination (Wiuf et al. 2001, alescent-based approach for detecting ancestral recombina- Posada 2002), results from all four recombination detection tion in the mt genes of extant FFSC species (Price & Carbone methods were compared and only recombination identified 2005). We purposefully did not employ phylogenetic methods by all four methods were considered. For these analyses (see given the low sequence diversity observed in the mt genes of below), the five mt genomes and the individual gene datasets the FFSC and other fungi (e.g. Seifert et al. 2007, Huang et were aligned using the CLC Genomics Workbench software. al. 2008, Fourie et al. 2013). For
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