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Research Whole Genome Comparisons of Ergot Fungi bioRxiv preprint doi: https://doi.org/10.1101/2020.04.13.039230; this version posted May 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Article type: Research 2 3 Whole genome comparisons of ergot fungi reveals the divergence and evolution of species 4 within the genus Claviceps are the result of varying mechanisms driving genome evolution 5 and host range expansion 6 7 Stephen A. Wyka1, Stephen J. Mondo1,2, Miao Liu3, Jeremy Dettman3, Vamsi Nalam1, Kirk D. 8 Broders4* 9 10 1 Department of Agricultural Biology, Colorado State University, Fort Collins, CO 80523, USA. 11 2 U.S. Department of Energy Joint Genome Institute, Berkeley, CA 94720, USA. 12 3 Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa K1A 13 0C6, Canada. 14 4 Smithsonian Tropical Research Institute, Apartado 0843-03092 Panamá, República de Panamá. 15 * Corresponding authors: Kirk D. Broders, email: [email protected] pg. 1 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.13.039230; this version posted May 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 16 Abstract: 17 The genus Claviceps has been known for centuries as an economically important fungal 18 genera for pharmacology and agricultural research. Only recently have researchers begun to 19 unravel the evolutionary history of the genus, with origins in South America and classification of 20 four distinct sections through ecological, morphological, and metabolic features (Claviceps sects. 21 Citrinae, Paspalorum, Pusillae, and Claviceps). The first three sections are additionally 22 characterized by narrow host range, while sect. Claviceps is considered evolutionarily more 23 successful and adaptable as it has the largest host range and biogeographical distribution. 24 However, the reasons for this success and adaptability remain unclear. Our study elucidates 25 factors influencing adaptability by sequencing and annotating 50 Claviceps genomes, 26 representing 21 species, for a comprehensive comparison of genome architecture and plasticity 27 in relation to host range potential. Our results show the trajectory from specialized one-speed 28 genomes (sects. Citrinae and Paspalorum) towards adaptive two-speed genomes (sects. Pusillae 29 and Claviceps) through co-localization of transposable elements around predicted effectors and a 30 putative loss of repeat-induced point mutation resulting in unconstrained tandem gene 31 duplication coinciding with increased host range potential and speciation. Alterations of genomic 32 architecture and plasticity can substantially influence and shape the evolutionary trajectory of 33 fungal pathogens and their adaptability. Furthermore, our study provides a large increase in 34 available genomic resources to propel future studies of Claviceps in pharmacology and 35 agricultural research, as well as, research into deeper understanding of the evolution of adaptable 36 plant pathogens. 37 pg. 2 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.13.039230; this version posted May 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 38 Keywords: adaptive evolution, gene family expansion, two-speed genomes, fungal plant 39 pathogens, RIP, ergot 40 41 Introduction: 42 Fungi, particularly phytopathogenic species, are increasingly being utilized to gain 43 insight into the evolution of eukaryotic organisms, due to their adaptive nature and unique 44 genome structures (Gladieux et al. 2014; Dong et al. 2015). Adaptation and diversification of 45 fungal species can be mediated by changes in genome architecture and plasticity such as genome 46 size, transposable element (TE) content, localization of TEs to specific genes, genome 47 compartmentalization, gene duplication rates, recombination rates, and presence/absence 48 polymorphism of virulence factors (Dong et al. 2015; Möller & Stukenbrock 2017). The 49 presence or absence of repeat-induced point (RIP) mutation is also an important mechanism for 50 fungal genome evolution, as RIP works on a genome-wide scale to silence transposable elements 51 and duplicated genes, which can also “leak” onto neighboring genes (Galagan et al. 2003, 2004; 52 Raffaele & Kamoun 2012; Urguhart et al. 2018; Möller & Stukenbrock 2019). It is becoming 53 increasingly evident that variations in these factors can be used to classify genomes as a one- 54 speed (one-compartment), such as the powdery mildew fungi Blumeria graminis f.sp. hordei and 55 f.sp tritici, two-speed (two-compartment), such as the late blight pathogen Phytophthora 56 infestans, or multi-speed (multi-compartment) such as the multi-host pathogen Fusarium 57 oxysporum (Dong et al. 2015; Frantzeskakis et al. 2019). These different “speeds” are 58 characterized by their potential adaptability such that one-speed genomes are often considered 59 less-adaptable, while two-speed and multi-speed genomes are often considered more-adaptable 60 (Dong et al. 2015; Frantzeskakis et al. 2019; Möller & Stukenbrock 2019). pg. 3 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.13.039230; this version posted May 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 61 The ergot fungi of the genus Claviceps (Ascomycota, Hypocreales) are biotrophic species 62 that share a specialized ovarian-specific non-systemic parasitic lifestyle with their grass hosts 63 (Píchová et al. 2018). Infections are fully restricted to individual unpollinated ovaries (Tudzynski 64 and Scheffer 2004), and the fungus actively manages to maintain host cell viability to obtain 65 nutrients from living tissue through a complex cross-talk of genes related to pathogenesis, such 66 as secreted effectors, secondary metabolites, or cytokinin production (Hinsch et al. 2015, 2016; 67 Oeser et al. 2017; Kind et al. 2018a, 2018b). Species of Claviceps are most notably known for 68 their production of toxic alkaloids and secondary metabolites but are also known for their 69 expansive host range and negative impact on global cereal crop production and livestock 70 farming. These negative effects on human and livestock health are the primary reason Claviceps 71 species are referred to as plant pathogens. However, under the light of co-evolution with their 72 grass hosts some Claviceps species are considered conditional defensive mutualists with their 73 hosts as they prevent herbivory and can improve host fitness (Raybould et al. 1998; Fisher et al. 74 2007; Wäli et al. 2013). 75 The genus Claviceps contains 59 species divided into four sections; sects. Claviceps, 76 Pusillae, Citrinae, and Paspalorum (Píchová et al. 2018). It was postulated that sects. Citrinae 77 and Paspalorum originated in South America, while sect. Pusillae experienced speciation 78 throughout the Eocene, Oligocene, and Miocene as these species encountered newly emergent 79 PACMAD warm-season grasses (subfamilies Panicoideae, Aristidoideae, Chloridoideae, 80 Micrairoideae, Arundinoideae, Danthonioideae) when an ancestral strain was transferred from 81 South America to Africa (Píchová et al. 2018). In contrast, the crown node of sect. Claviceps is 82 estimated at 20.4 Mya and was followed by a radiation of the section corresponding to a host 83 jump from ancestral sedges (Cyperaceae) to the BOP clade (cool-season grasses; subfamilies pg. 4 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.13.039230; this version posted May 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 84 Bambusoideae, Oryzoideae (syn: Ehrhartoideae) (Soreng et al. 2015), Pooideae) in North 85 America (Bouchenak-Khelladi et al. 2010; Píchová et al. 2018). Section Claviceps has the 86 largest host range with C. purpurea sensu stricto (s.s.) having been reported on up to 400 87 different species in clade BOP (Alderman et al. 2004, Píchová et al. 2018) across six tribes, and 88 retains the ability to infect sedges (Cyperaceae) (Jungehülsing and Tudzynski 1997). In contrast, 89 sect. Pusillae is specialized to the tribes Paniceae and Andropogoneae, and sects. Citrinae and 90 Paspalorum only infect members of tribe Paspaleae and tribe Cynodonteae, respectively 91 (Píchová et al. 2018). The shared specialized infection life cycle of the Claviceps genus, the 92 drastic differences in host range potential of different species, and geographic distribution 93 represent a unique system to study the evolution and host adaptation of eukaryotic organisms. 94 Despite their ecological and agriculture importance, little is known about the evolution 95 and genomic architecture of these important fungal species in comparison to other cereal 96 pathogens such as species in the genera Puccinia (Cantu et al. 2013; Kiran et al. 2016, 2017), 97 Zymoseptoria (Grandaubert et al. 2015, 2019; Estep et al. 2015; Poppe et al. 2015; Testa et al. 98 2015; Wu et al. 2017; Stukenbrock & Dutheil 2018), or Fusarium (Kvas et al. 2009; Ma et al. 99 2010; Rep & Kistler 2010; Watanabe et al. 2011; Sperschneider et al. 2015). Unfortunately, the 100 lack of genome data for the Claviceps genus has hampered our ability to complete comparative 101 analyses to identify factors that are influencing the adaptation of Claviceps species across the 102 four sections in the genus, and the mechanisms by which species of sect.
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