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Transposons Passively and Actively Contribute to Evolution of the Two-Speed Genome

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Transposons Passively and Actively Contribute to Evolution of the Two-Speed Genome Downloaded from genome.cshlp.org on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press 1 Transposons passively and actively contribute to evolution of the two-speed genome 2 of a fungal pathogen 3 4 Luigi Faino1#, Michael F Seidl1#, Xiaoqian Shi-Kunne1, Marc Pauper1, Grardy CM van den 5 Berg1, Alexander HJ Wittenberg2, and Bart PHJ Thomma1* 6 7 1Laboratory of Phytopathology, Wageningen University, Droevendaalsesteeg 1, 6708 PB 8 Wageningen, The Netherlands 9 2Keygene N.V., Agro Business Park 90, 6708 PW Wageningen, The Netherlands 10 11 #These authors contributed equally to this work 12 *Corresponding author: Prof. dr. Bart PHJ Thomma 13 Chair, Laboratory of Phytopathology 14 Wageningen University 15 Droevendaalsesteeg 1 16 6708 PB Wageningen 17 The Netherlands 18 Email: [email protected] 19 20 21 Running title: Genome evolution by transposable elements 22 Keywords: Genome evolution; transposable element; plant pathogen; Verticillium dahliae; 23 segmental genome duplication 1 Downloaded from genome.cshlp.org on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press 24 Abstract 25 Genomic plasticity enables adaptation to changing environments, which is especially relevant 26 for pathogens that engage in “arms races” with their hosts. In many pathogens, genes 27 mediating virulence cluster in highly variable, transposon-rich, physically distinct genomic 28 compartments. However, understanding of the evolution of these compartments, and the role 29 of transposons therein, remains limited. Here, we show that transposons are the major 30 driving force for adaptive genome evolution in the fungal plant pathogen Verticillium dahliae. 31 We show that highly variable lineage-specific (LS) regions evolved by genomic 32 rearrangements that are mediated by erroneous double-strand repair, often utilizing 33 transposons. We furthermore show that recent genetic duplications are enhanced in LS 34 regions, against an older episode of duplication events. Finally, LS regions are enriched in 35 active transposons, which contribute to local genome plasticity. Thus, we provide evidence 36 for genome shaping by transposons, both in an active and passive manner, which impacts 37 the evolution of pathogen virulence. 2 Downloaded from genome.cshlp.org on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press 38 Introduction 39 Genomic plasticity enables organisms to adapt to environmental changes and occupy novel 40 niches. While such adaptation occurs in any organism, this is particularly relevant for 41 pathogens that engage in co-evolutionary “arms races” with their hosts (Raffaele and 42 Kamoun 2012; Seidl and Thomma 2014; Dong et al. 2015). In these interactions, hosts utilize 43 their surveillance system to detect invaders and mount appropriate defenses, involving 44 detection of invasion patterns by immune receptors, while pathogens secrete so-called 45 effector molecules to support host colonization and counteract immune responses (Rovenich 46 et al. 2014; Cook et al. 2015). This tight interaction exerts strong selection pressure on both 47 partners and incites rapid genomic diversification (McDonald and Linde 2002). 48 Although sexual reproduction drives genotypic diversity, not all eukaryotes regularly 49 reproduce sexually, including many asexual fungal phyla (McDonald and Linde 2002; 50 Heitman et al. 2007; Flot et al. 2013). However, in such asexual organisms adaptive genome 51 evolution also occurs, mediated by various mechanisms ranging from single-nucleotide 52 polymorphisms to large-scale structural variations that can affect chromosomal shape, 53 organization and gene content (Seidl and Thomma 2014). Verticillium dahliae is a soil-borne 54 fungal pathogen that infects susceptible hosts through their roots and colonizes the water- 55 conducting xylem vessels, leading to vascular wilt disease (Fradin and Thomma 2006). 56 Despite its presumed asexual nature, V. dahliae is a highly successful pathogen that causes 57 disease on hundreds of plant hosts (Fradin and Thomma 2006; Klosterman et al. 2009; 58 Inderbitzin and Subbarao 2014). Using comparative genomics, we recently identified 59 genomic rearrangements in V. dahliae that lead to extensive chromosomal length 60 polymorphisms (de Jonge et al. 2013). Moreover, the genomes of V. dahliae strains were 61 found to contain highly dynamic, repeat-rich, lineage-specific (LS) regions (Klosterman et al. 62 2011; de Jonge et al. 2013). Intriguingly, these LS regions are enriched for in planta-induced 63 effector genes that contribute to fungal virulence (de Jonge et al. 2013). Similarly, many 64 filamentous pathogens are considered to have evolved so-called “two-speed” genomes with 65 gene-rich, repeat-poor genomic compartments that contain core genes that mediate general 3 Downloaded from genome.cshlp.org on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press 66 physiology and evolve slowly, whereas plastic, gene-poor and repeat-rich compartments are 67 enriched in effector genes that mediate virulence in interactions with host plants and evolve 68 relatively quickly (Raffaele and Kamoun 2012). 69 Plastic, fast-evolving genomic compartments in plant and animal pathogen genomes 70 concern particular regions that are either embedded within the core chromosomes or reside 71 on conditionally dispensable chromosomes (Thon et al. 2006; Fedorova et al. 2008; Haas et 72 al. 2009; Ma et al. 2010; Goodwin et al. 2011; Klosterman et al. 2011; Rouxel et al. 2011; de 73 Jonge et al. 2013). Irrespective of the type of organization of the “two-speed” genome, the 74 fast-evolving compartment is generally enriched for transposable elements (TEs) that are 75 thought to actively promote genomic changes by causing DNA breaks during excision, or by 76 acting as a substrate for rearrangement (Seidl and Thomma 2014). Nevertheless, the exact 77 role of TEs in the evolution of effector genes currently remains unknown (Dong et al. 2015). 78 We recently established gapless V. dahliae whole-genome assemblies using a combination 79 of long-read sequencing and optical mapping (Faino et al. 2015; Thomma et al. 2015). Here, 80 we exploit these novel assemblies for in-depth investigations into the molecular mechanisms 81 responsible for genomic variability, which is instrumental for adaptive genome evolution in V. 82 dahliae. 83 84 Results 85 Genomic rearrangements in Verticillium dahliae are associated with sequence similarity 86 Whole-genome alignments between strains V. dahliae strains JR2 and VdLs17 revealed 24 87 synteny disruptions (Fig.1A; Supplemental Fig. 1). To further increase their resolution, we 88 aligned long (average ~9 kb) sequencing reads derived from strain VdLs17 (Faino et al. 89 2015) to the strain JR2 assembly, and reads of which the two sides aligned to two distinct 90 genomic locations were used to determine breakpoints at high-resolution (Supplemental Fig. 91 2). After manual refinement, this procedure yielded 19 large-scale chromosomal 92 rearrangements; 13 inter-chromosomal translocations and six intra-chromosomal inversions 93 (Fig. 1; Table 1). While seven rearrangements were confined to regions smaller than 100 bp, 4 Downloaded from genome.cshlp.org on October 6, 2021 - Published by Cold Spring Harbor Laboratory Press 94 the remaining 12 concern larger genomic regions that could not be further refined due to the 95 presence of strain-specific or repeat-rich regions (Fig. 1A). 96 We subsequently assessed the occurrence of the 13 inter-chromosomal 97 rearrangements in nine other V. dahliae strains by querying paired-end reads derived from 98 these genomes for pairs of discordantly mapped reads (i.e. both reads fail to map at the 99 expected distance or location) when mapped onto the strain JR2 assembly, revealing distinct 100 rearrangement patterns (Supplemental Fig. 3). While some synteny breakpoints identified in 101 V. dahliae strain JR2 are either specific to V. dahliae strain VdLs17 (Chr1: 2,843,014- 102 2,843,020; Supplemental Fig. 4A) or common to all other V. dahliae strains (Chr1: 8,013,865- 103 8,013,868; Supplemental Fig. 4B), some are observed in only a subset of V. dahliae strains 104 (Chr3: 3,130,776-3,130,781; Supplemental Fig. 4C). 105 V. dahliae strains JR2 and VdLs17 are highly similar with only 8,622 SNPs difference 106 (0.024% nucleotide divergence). When focusing on the regions (10 kb) up- and downstream 107 of the nineteen identified synteny breakpoints, we observe ~200 SNPs (~0.05% divergence), 108 indicating a moderate increase in proximity of the breakpoints. Similarly, when considering all 109 V. dahliae strains, we observe a genome-wide average of 4.1 SNPs/kb, while around 110 breakpoints (10 kb up- and downstream) 6.3 SNPs/kb are found. 111 Genomic rearrangements are generally caused by double-strand DNA breakages 112 followed by unfaithful repair by mechanisms that utilize homologous sequences to repair 113 such breaks (Hedges and Deininger 2007; Krejci et al. 2012; Seidl and Thomma 2014). 114 Repetitive genomic elements, such as transposable elements (TEs), may give rise to 115 genomic rearrangements by providing an ectopic substrate that interferes with faithful repair 116 of the original break. Notably, out of 19 chromosomal rearrangements identified in V. dahliae 117 strain JR2, 15 co-localize with a repetitive element (Table 1; Supplemental Table 1). Of the 118 13 inter-chromosomal rearrangements, 12 could be reconstructed in detail (Fig. 1A; Table 1; 119 Supplemental Fig. 5&6). Eight of them occur over
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