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Unconventional Recombination in the Mating Type Locus of Heterothallic Apple

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Unconventional Recombination in the Mating Type Locus of Heterothallic Apple G3: Genes|Genomes|Genetics Early Online, published on February 21, 2017 as doi:10.1534/g3.116.037853 1 Unconventional recombination in the mating type locus of heterothallic apple 2 canker pathogen Valsa mali 3 Zhiyuan Yin, Xiwang Ke, Zhengpeng Li, Jiliang Chen, Xiaoning Gao, Lili Huang* 4 5 State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant 6 Protection, Northwest A&F University, Yangling 712100, Shaanxi, China 7 8 9 Reference numbers for publicly available data: 10 The raw Illumina reads of isolate SXLC146: SRP075864 11 The nucleotide sequence of MAT1-2 idiomorph: KX349090 12 13 1 © The Author(s) 2013. Published by the Genetics Society of America. 14 Running title: Mating type locus of Valsa mali 15 Keywords: Cytospora sp., sexual reproduction, MAT, unequal recombination 16 *Correspondence 17 Lili Huang 18 State Key Laboratory of Crop Stress Biology for Arid Areas, College of Plant 19 Protection 20 Northwest A&F University, Yangling, Shaanxi 712100, China 21 Tel: 0086-29-8709-1312, e-mail: [email protected] 22 23 24 2 25 Abstract 26 Sexual reproduction in filamentous ascomycetes is controlled by mating type (MAT) 27 locus, including two idiomorphs MAT1-1 and MAT1-2. Understanding the MAT locus 28 can provide clues for unveiling the sexual development and virulence factors for 29 fungal pathogens. The genus Valsa (Sordariomycetes, Diaporthales) contains many 30 tree pathogens responsible for destructive canker diseases. Sexual stage of these 31 ascomycetes is occasionally observed in nature and no MAT locus has been reported 32 up till now. Thus, we identified the MAT locus of apple canker pathogen V. m a l i , 33 which causes extensive damage and even death to trees. V. m a l i is heterothallic that 34 each isolate carry either MAT1-1 or MAT1-2 idiomorph. However, the MAT structure 35 is distinct from that of many other heterothallic fungi in Sordariomycetes. Two 36 flanking genes COX13 and APN2 were cooperated into the MAT locus, possibly by 37 intra-chromosomal rearrangement. After the acquisition of foreign genes, unequal 38 recombination occurred between MAT1-1/2 idiomorphs, resulting in a reverse 39 insertion in MAT1-2 idiomorph. Evolutionary analysis showed that these three 40 complete MAT1-1-2, COX13 and APN2 genes in this region diverged independently 41 due to different selection pressure. Null hypothesis tests of 1:1 MAT ratio of 86 V. 42 mali isolates from four different provinces showed a relatively balanced distribution 43 of the two idiomorphs in the fields. These results provide insights into the evolution 44 of the mating systems in Sordariomycetes. 45 46 3 47 Introduction 48 Sexual reproduction is important in pathogenic ascomycetes because new 49 combinations of virulence alleles are created through outcrossing (McDonald and 50 Linde 2002). Mating in filamentous ascomycetes is typically controlled by a single 51 locus termed mating-type (MAT) locus, including two alleles called MAT1-1 and 52 MAT1-2. These alleles have been termed ‘idiomorphs’ due to their high sequence 53 divergence (Metzenberg and Glass 1990). Filamentous ascomycetes generally exhibit 54 self-incompatible (heterothallic) or self-compatible (homothallic) lifestyles. In 55 heterothallic ascomycete fungi, the MAT locus carries either MAT1-1 or MAT 1-2 56 idiomorph, which contains at least a MAT1-1-1 α-domain gene or a MAT1-2-1 57 high-mobility-group (HMG) domain gene, respectively. In addition, several additional 58 genes are also found in various ascomycetes, although the functions of these genes 59 remain obscure (Dyer et al. 2016). These mating-type genes function in not only 60 controlling sexual development, but also regulating fungal secondary metabolites and 61 hyphal morphology (Kuck and Bohm 2013). Thus, understanding the MAT locus can 62 provide insights into the sexual development and virulence factors in filamentous 63 ascomycetes. 64 65 The genus Valsa (Sordariomycetes, Diaporthales) contains more than 500 species, 66 including many aggressive tree pathogens responsible for canker diseases. Valsa 67 cankers affect more than 70 species of trees worldwide, and often cause extensive 68 damage to trees (Agrios 2005). V. m a l i Miyabe et Yamada [anamorph Cytospora 4 69 sacculus (Schwein.) Gvrit.], causing destructive canker on apple and resulting in 70 severe yield losses in eastern Asia (Lee et al. 2006; Li et al. 2013), mainly infects 71 apple by conidia while ascospores are not common (Wang et al. 2014; Liu et al. 2016) 72 (Figure 1). Of the 150 infected apple bark samples from different regions in China, 73 only eight form dead trunks have ascostromata with ascospores (Wang 2007). In 74 addition, the sexual reproduction of Valsa spp. cannot be induced in the laboratory up 75 till now, and no MAT locus in Va lsa has been reported. Thus, in this study, we 76 identified and delineated the structure of MAT locus of V. m a l i using comparative 77 genomic approaches, and investigated the evolution of MAT genes and loci in V. m a l i 78 and closely related species. 79 80 Materials and Methods 81 Strains and culture conditions 82 All strains used in this study were deposited at the Laboratory of Integrated 83 Management of Plant Diseases in College of Plant Protection, Northwest A&F 84 University, Yangling, PR China (available upon request). Cultures were grown on 85 potato dextrose agar (PDA) medium with a layer of cellophane at 25°C. 86 87 Identification of the V. mali MAT locus 88 Mating type locus of V. m a l i strain 03-8 was identified by BLASTP searches against V. 89 mali proteome (> 1E–5) using protein sequences of MAT1-1-1 and MAT1-2-1 from 90 closely related species Cryphonectria parasitica as query sequences, which suggests 5 91 that V. mal i is heterothallic and strain 03-8 carries the MAT1-1 idiomorph. MAT1-2 92 candidate isolates were then identified by PCR using a VmMAT1-1-1 specific primer 93 pair. To identify the MAT1-2 idiomorph, the genome of isolate SXLC146 was 94 sequenced using Illumina HiSeq technology. Filtered paired-end reads were 95 assembled by ABySS v1.9.0 (Simpson et al. 2009) and gene models were predicted 96 using MAKER v2.31.8 (Holt and Yandell 2011). The raw Illumina reads of isolate 97 SXLC146 have been deposited at the Sequence Read Archive (SRA) database of 98 NCBI (SRP075864). The nucleotide sequence of MAT1-2 idiomorph has been 99 deposited at the GenBank database (KX349090). Primer pairs of VmMAT1-1-1 (F: 100 5'-GAAAGGTCGGAAAGGCAAAG-3' and R: 5'-AGAGTCGGGTCGGGCAAT-3') 101 and VmMAT1-2-1 (F: 5'-CAACATTGGCATTCAACTCA-3' and R: 102 5'-CTTGCTTCGTCGCTTCAC-3') were used for PCR detection of isolates from 103 different geographic regions. 104 105 Evolutionary analyses of MAT locus 106 Synteny of the MAT locus between MAT1-1 and MAT1-2 idiomorphs was analyzed 107 using GATA (Nix and Eisen 2005). Protein sequences of mating type genes were 108 aligned using MAFFT v7.245 (Katoh and Standley 2013), and poorly aligned regions 109 were removed by trimAl v1.4 (Capella-Gutiérrez et al. 2009). Maximum likelihood 110 trees were constructed by IQtree v1.3.11 (Nguyen et al. 2014) using the build-in best 111 evolutionary model selection function. Branch supports were assessed with ultrafast 112 bootstrap method (Minh et al. 2013) and SH-aLRT test (1000 replicates). Selection 6 113 pressure on mating type genes were tested at the codon level using the ete evol tool in 114 ETE package v3.0 (Huerta-Cepas et al. 2016). The coding sequence alignments of 115 these genes were constructed by ETE package using several build-in alignment tools, 116 and CodeML and Slr analyses were then performed by the ete-evol program. Sites 117 under selection were identified using the M2 and SLR models. Null hypothesis of 1:1 118 MAT ratio of V. mali was tested using chi-square goodness-of-fittest by the online tool 119 VassarStats (http://vassarstats.net/). 120 121 Transmission electron microscopy 122 Perithecium, ascus and ascospore of V. m a l i in the fields were investigated by 123 transmission electron microscopy (TEM). Ascostromata samples from the canker for 124 TEM were processed followed as Ke et al. (2013) described. For TEM, ultrathin 125 sections of specimens cut with a diamond knife were collected on copper grids. After 126 contrasting with uranyl acetate and lead citrae, the grids were examined with a TEM 127 1230 (JEOL) at 80 KV. 128 129 Results and discussion 130 Identification of MAT1-1 idiomorph 131 To identify the mating type locus in V. m a l i , protein sequences of core mating type 132 genes MAT1-1-1 (GenBank: AAK83346) and MAT1-2-1 (AAK83343) of closely 133 related species Cryphonectria parasitica were used to search against the genome of V. 134 mali strain 03-8 (GCA_000818155.1) (Yin et al. 2015). By performing BLASTP 7 135 searches, only MAT1-1-1 was found in strain 03-8. The absence of MAT1-2-1 136 HMG-box gene in the MAT locus of strain 03-8 suggests that V. m a l i is likely 137 heterothallic. VmMAT1-1-1 (VM1G_08160) contains the typical α-domain and 138 adjacent genes includes SLA2 (VM1G_08159), MAT1-1-2 (VM1G_08161), COX13 139 (VM1G_08162), APN2 (VM1G_08163) and MAT1-1-3 (VM1G_08164) (Figure 2). 140 Intriguingly, COX13 and APN2 locate in the MAT locus, while the location of SLA2 141 and APN2 is fairly conserved and often flanks the idiomorph among other mating type 142 genes in many other filamentous ascomycetes (Dyer et al. 2016), such as C.
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