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Evolution of the Mating Types and Mating Strategies in Prominent Genera in the Botryosphaeriaceae

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Evolution of the Mating Types and Mating Strategies in Prominent Genera in the Botryosphaeriaceae Fungal Genetics and Biology 114 (2018) 24–33 Contents lists available at ScienceDirect Fungal Genetics and Biology journal homepage: www.elsevier.com/locate/yfgbi Regular Articles Evolution of the mating types and mating strategies in prominent genera in T the Botryosphaeriaceae ⁎ Jan H. Nagel, Michael J. Wingfield, Bernard Slippers Department of Biochemistry, Genetics and Microbiology, Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria 0001, South Africa ARTICLE INFO ABSTRACT Keywords: Little is known regarding mating strategies in the Botryosphaeriaceae. To understand sexual reproduction in this Idiomorph fungal family, the mating type genes of Botryosphaeria dothidea and Macrophomina phaseolina, as well as several Heterothallic species of Diplodia, Lasiodiplodia and Neofusicoccum were characterized from whole genome assemblies. Homothallic Comparisons between the mating type loci of these fungi showed that the mating type genes are highly variable, Ancestral state reconstruction but in most cases the organization of these genes is conserved. Of the species considered, nine were homothallic Dothideomycetes and seven were heterothallic. Mating type gene fragments were discovered flanking the mating type regions, which indicates both ongoing and ancestral recombination occurring within the mating type region. Ancestral reconstruction analysis further indicated that heterothallism is the ancestral state in the Botryosphaeriaceae and this is supported by the presence of mating type gene fragments in homothallic species. The results also show that at least five transitions from heterothallism to homothallism have taken place in the Botryosphaeriaceae. The study provides a foundation for comparison of mating type evolution between Botryosphaeriaceae and other fungi and also provides valuable markers for population biology studies in this family. 1. Introduction domain (Turgeon and Yoder, 2000). The gene organization at the MAT1 locus, as well as the position of Two modes of sexual reproduction exist in fungi, heterothallism and the locus in the genome is moderately conserved in the Ascomycota. homothallism. In heterothallic fungi, two individuals of opposite The MAT1 locus may contain either the MAT1-1-1 or MAT1-2-1, alone mating compatibility types must be present in order for sexual re- or with one or more ancillary mating type genes. The naming of mating production to take place (Ni et al., 2011). Homothallism is character- type genes follows the system described by Turgeon and Yoder (2000) ized by indiscrimate mating, i.e. one fungal individual can mate with and has recently been revised in order to correct inconsistent/incorrect any other individual of its species, including itself. Both thallism states application of the mating type gene nomenclature (Wilken et al., 2017). have advantages. Homothallism allows unrestricted sexual compat- In many ascomycetes, the MAT1 locus is flanked by the SLA2 and ibility that is beneficial when the probability of encountering a mating APN2/DNA lyase genes (Debuchy and Turgeon, 2006). partner is low and the benefits of occasional outcrossing outweigh the Homothallism can occur in various forms, i.e. primary homo- cost of more frequent haploid selfing. Conversely, heterothallism is thallism, pseudohomothallism and mating type switching (Wilson et al., better suited to situations where mating partners are encountered fre- 2015). Primary homothalism occurs when both mating type idiomorphs quently, but the fitness cost for selfing is high (Billiard et al., 2012). are present in one genome, either at the same locus (Pöggeler et al., Ascomycetes have a bipolar mating system that is usually de- 1997; Yun et al., 1999, 2000) or at unlinked loci (Galagan et al., 2005; termined by a single locus (Butler, 2010). The ascomycete mating type Lopes et al., 2017). Additionally the MAT1-1-1 and MAT1-2-1 genes can genes occur at the MAT1 locus. In heterothallic fungi the genes are be fused in a single functional gene that contains both the alpha-box idiomorphic between the two mating types; that is the genes at the and HMG domains (Yun et al., 1999). MAT1 locus are not homologous between the two mating types The Botryosphaeriaceae is a family of fungi that commonly occur in (Idnurm, 2011). The MAT1-1 idiomorph is defined as containing the woody plants as endophytes and many species are also important op- MAT1-1-1 gene that possesses an alpha box protein domain (Turgeon portunisitic tree pathogens (Slippers and Wingfield, 2007). Sexual and Yoder, 2000). Likewise the MAT1-2 idiomorph contains the MAT1- structures in these fungi are rarely observed in nature or under la- 2-1 gene that produces a protein with the high mobility group (HMG) boratory conditions (Phillips et al., 2013; Slippers et al., 2017). This, ⁎ Corresponding author. E-mail address: [email protected] (B. Slippers). https://doi.org/10.1016/j.fgb.2018.03.003 Received 5 December 2017; Received in revised form 1 March 2018; Accepted 7 March 2018 Available online 09 March 2018 1087-1845/ © 2018 Elsevier Inc. All rights reserved. J.H. Nagel et al. Fungal Genetics and Biology 114 (2018) 24–33 however, does not necessarily imply that species of Botryosphaeriaceae 2.2. Characterization of mating type and surrounding genes fail to undergo sexual reproduction. For example, physical evidence of sexual reproduction has never been observed for Diplodia sapinea, but The presence of mating type genes from the genome sequences was most likely takes place when considering population genetics data determined by performing a local tBLASTx (Camacho et al., 2009) (Bihon et al., 2012a, 2012b). Consistent with this view, the mating type search using the MAT and adjacent genes from D. sapinea (KF551229 genes in D. sapinea were subsequently characterized and these showed and KF551228) (Bihon et al., 2014). The relevant contigs were ex- that the fungus is heterothallic (Bihon et al., 2014). The MAT1-1 idio- tracted from genome sequences and annotated using WebAugustus morph of D. sapinea contains the MAT1-1-1 gene, as well as the MAT1- (http://bioinf.uni-greifswald.de/augustus/). The identities of the an- 1-8 gene, whereas the MAT1-2 idiomorph contains the MAT1-2-1 genes, notated genes were determined by BLASTp against the NCBI nr-data- as well as a novel MAT1-2-5 gene. Bihon et al. (2014) further showed base. The annotations were further manually refined by comparison that all but one of the populations considered did not deviate sig- with existing homologs on NCBI. The resultant annotated loci of se- nificantly deviate from the 1:1 ratio between the two mating type quence data generated in this study were deposited in GenBank idiomorphs, further supporting sexual reproduction in this species. (Table 1). The mating type gene annotations from publically available The mating type genes in several other Botryosphaeriales have re- genome data are provided in Supplementary File 1. Mating type genes cently been characterized (Amorim et al., 2017; Lopes et al., 2017; were assessed for functional domains by performing a search against Marsberg et al., 2016; Wang et al., 2016). A genome assembly for NCBI’s conserved domain database (CDD BLAST) (Marchler-Bauer Neofusicoccum parvum was used to identify the mating type genes of this et al., 2014). species and revealed both MAT1-1 and MAT1-2 idiomorphs in the genome, indicating primary homothallism (Lopes et al., 2017). Primer sets that allowed amplification of the MAT1-1-1 and MAT1-2-1 genes 2.3. Comparison of mating type locus organization from other species in this genus were also developed (Lopes et al., 2017). Similarly, a genome assembly was used to characterize the In order to compare the organization of the mating type genes and mating type genes of Botryosphaeria dothidea, which was shown to be flanking genes between species, BLASTn was used to assess the simi- homothallic (Marsberg et al., 2016). The mating type locus in Phyllos- larity between sequences. EasyFig version 2.2.2 (Sullivan et al., 2011) ticta citricarpa (Phyllostictaceae) (Amorim et al., 2017; Wang et al., was used to perform synteny analysis based on pairwise BLASTn simi- 2016) and P. capitalensis (Wang et al., 2016) has also been characterized larity between taxa using a maximum E-value cut-off of 0.0001. This using a similar genomics based approach, showing that P. citricarpa is approach was also used to assess the presence of partial MAT gene heterothallic and P. capitalensis is homothallic. fragments at the mating type locus. Intergenic regions on either side of Recent studies on the mating type genes in species of the mating type genes were investigated for the presence of sequences Botryosphaeriales have highlighted various knowledge gaps regarding with homology to the MAT1-1-1, MAT1-1-8, MAT1-2-1 or MAT1-2-5 sexual reproduction in these fungi. For example, questions arise re- genes. Where only a single mating type was available for a species (i.e. garding the conservation of mating types, i.e. the conservation of nu- D. corticola, D. scrobiculata and L. pseudotheobromea), the genes of the cleotide and amino acid sequence of the mating type genes, the con- opposite mating type from the closest available species was used to servation of the genes occurring at the mating type locus and the determine the presence of mating type gene fragments in the intergenic conservation of the genomic location of the mating type locus. It is also regions flanking the mating type genes. not known how thallism has evolved in this family; whether the most recent common ancestor of the Botryosphaeriaceae was homothallic or heterothallic or how frequently changes to the ancestral mating strategy 2.4. Phylogenetic comparisons and ancestral state reconstruction have evolved. Furthermore, a scarcity of mating type markers capable of amplifying a broad range of species, other than those for Phylogenetic analyses of the MAT1-1-1 and MAT1-2-1 genes were Neofusicoccum spp. developed by Lopes et al.
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