Whole genome comparisons of ergot fungi reveals the divergence and evolution of species within the genus Claviceps are the result of varying mechanisms driving genome evolution and host range expansion

Abstract

1 2 Genus-wide comparison reveals divergence and evolution of the four sections within the 3 genus Claviceps are the result of varying mechanisms driving genome evolution and host 4 range 5 6 Abstract: 16 Background: 17 The genus Claviceps has been known for centuries as an economically important fungal 18 genera for pharmacology and agricultural research. Despite this little is known about its 19 evolution. Only recently have researchers begun to unravel the evolutionary history of the genus, 20 with origins in South America and classification of four distinct sections through ecological, 21 morphological, and metabolic features (Claviceps sects. Citrinae, Paspalorum, Pusillae, and 22 Claviceps). The first three sections are additionally characterized by narrow host range, while 23 sect. Claviceps is considered evolutionarily more successful and adaptable as it has the largest 24 host range and biogeographical distribution. However, the reasons for this success and 25 adaptability remain unclear.26Results: 27 Our study elucidates these factors by sequencing and annotating 50 Claviceps genomes, 28 representing 21 species, for a comprehensive comparison of genome architecture and plasticity 29 in relation to host range potential. Our results show the trajectory from specialized one-speed 30 genomes (C. sects. Citrinae and Paspalorum) to adaptive two-speed genomes (C. sects. Pusillae 31 and Claviceps) through co-localization of TEs around predicted effectors and loss of RIP 32 resulting in unconstrained tandem gene duplication coinciding with increased host range 33 potential and speciation.34 Conclusions: 35 Alterations of genomic architecture and plasticity can substantially influence and shape 36 the evolutionary trajectory of fungal pathogens and their adaptability. Furthermore, our study 37 provides a large increase in available genomic resources to propel future studies of Claviceps in 38 pg. 3 pharmacology and agricultural research, as well as, research into deeper understanding of the 39 evolution of adaptable plant pathogens. 40 41

Sympatric divergence of the ergot fungus, Claviceps purpurea, populations infecting agricultural and nonagricultural grasses in North America

“…The genomes of the members in three GCs may also be evolving and adapting to other environmental pressures, resulting in subpopulations remaining separated. A recent comparative genomic analysis of the genus Claviceps found that species in the section Claviceps , such as C. purpurea , have adaptive genomes through colocalization of transposable elements around predicted effectors and a putative loss of repeat‐induced point mutation (Wyka, Mondo, Liu, Dettman, et al., 2020). This has resulted in unconstrained tandem gene duplication coinciding with increased host range potential and speciation (Wyka, Mondo, Liu, Dettman, et al., 2020).…”

“…A recent comparative genomic analysis of the genus Claviceps found that species in the section Claviceps , such as C. purpurea , have adaptive genomes through colocalization of transposable elements around predicted effectors and a putative loss of repeat‐induced point mutation (Wyka, Mondo, Liu, Dettman, et al., 2020). This has resulted in unconstrained tandem gene duplication coinciding with increased host range potential and speciation (Wyka, Mondo, Liu, Dettman, et al., 2020). These alterations in genomic architecture and plasticity can influence and shape the evolutionary trajectory of fungal pathogens and their adaptability.…”

“…This purifying or stabilizing selection may be purging deleterious genetic polymorphisms that arise from random mutations and transposon‐mediated gene duplication. However, Wyka, Mondo, Liu, Dettman, et al., 2020 did observed evidence of strong positive selection pressure on secondary metabolite genes and that the lpsA1 and lpsA2 (genes in the ergotamine synthesis pathway) were the results of a recombination event. It is possible that the combination of positive selection on secondary metabolite genes with purifying selection across the rest of the genome has resulted in a more specific, as yet undetected, niche adaptation followed by population stabilization that has resulted in the observed patterns in geographic and host overlap of the three GCs found in North America.…”

“…Overall, it appears that RPB 2 is under moderate selection pressure in all populations, while TEF1 ‐α and easE are under strong selection only in GC3, which might be associated with the divergence of GC3. Understandably, easE is experiencing positive selection (as inferred by a negative value of Tajima'D) because it is common that genes involving secondary metabolite production are under selective pressure (Wyka, Mondo, Liu, Dettman, et al., 2020). The observed high level of genetic variation (polymorphisms, nucleotide, and haplotype diversity) is consistent with the scenario of positive selection.…”

Transposable elements contribute to genome dynamics and gene expression variation in the fungal plant pathogenVerticillium dahliae

“…In many filamentous pathogens, effector genes are enriched in TE-rich and gene-sparse compartments, while they are typically underrepresented in TE-poor and gene-dense genomic regions that typically harbor housekeeping genes (Seidl and Thomma 2014;Dong, et al 2015;Frantzeskakis, et al 2020). TE-rich compartments are often characterized by increased substitution rates and increased occurrence of SVs and presence/absence polymorphisms (Raffaele, et al 2010;Croll and McDonald 2012;de Jonge, et al 2012;de Jonge, et al 2013;Dutheil, et al 2016;Fokkens, et al 2018;Gan, et al 2020;Wyka, et al 2020). Notably, a similar association of TEs with genes involved in immune responses has also been observed in plant hosts (Leister 2004;Kawakatsu, et al 2016;Mascher, et al 2017;Seidl and Thomma 2017).…”