Pan-Mitogenome Construction, Intraspecific Variation, and Adaptive Evolution of the Plant Pathogenic Fungus Claviceps purpurea

TL;DR

This study analyzes the mitochondrial genomes of 15 Claviceps purpurea strains to understand their genetic variation and evolutionary patterns.

Contribution

The study reveals the pan-mitogenome structure and adaptive gene loss in Claviceps purpurea, offering new insights into its evolution.

Findings

Accessory regions contribute significantly to mitogenome variation in C. purpurea.

The atp9 gene is absent in all strains, indicating potential adaptive gene loss.

Chinese and non-Chinese isolates form distinct phylogenetic lineages.

Abstract

Fungi of the genus Claviceps produce ergot alkaloids, a group of compounds with both 23 toxic and medicinal properties. Despite its significance in agriculture and medicine, little 24 is known about its mitochondrial genome. This study assembled, annotated, and analyzed 25 the mitochondrial genomes of 15 different strains from diverse host plants and regions. 26 Analysis of the C. purpurea pan-mitogenome demonstrated that the accessory regions, 27 with an average proportion of 48.23%, are the main contributor to mitogenome variation. 28 Analysis of the 14 protein-coding genes revealed Ka/Ks ratios below 1, indicating strong 29 purifying selection. Notably, the atp9 gene was absent in all strains, suggesting a potential 30 adaptive gene loss. Structural variations were predominantly located in the intergenic region 31 between rns and rnl. Phylogenetic analysis based on concatenated mitochondrial 32 genes placed Claviceps as most closely related to the genus Epichloë. The 15 C. purpurea 33 strains grouped into five well-supported subclades, with Chinese and non-Chinese isolates 34 forming distinct lineages. Among these, the Chinese strains ACCC 37001 and 35 KUNCC 11030 represented the earliest diverging lineages. This research helps us better 36 understand how this pathogen evolves and adapts to different environments, which may 37 aid in future efforts to control crop diseases and utilize its beneficial properties.

Claviceps purpurea is a specialized phytopathogenic fungus that infects grasses and produces pharmacologically active compounds, attracting considerable interest in genomic research. In this study, we assembled and annotated the complete mitogenomes of 15 C. purpurea strains isolated from different host plants, including seven newly sequenced isolates from China. Analysis of the C. purpurea pan-mitogenome demonstrated that the accessory regions, with an average proportion of 48.23%, are the main contributor to mitogenome variation. Analysis of the 14 protein-coding genes revealed Ka/Ks ratios below 1, indicating strong purifying selection. Notably, the atp9 gene was absent in all strains, suggesting a potential adaptive gene loss. Structural variations were predominantly located in the intergenic region between rns and rnl. Phylogenetic analysis based on concatenated mitochondrial genes placed Claviceps as most closely related to the genus Epichloë. The 15 C. purpurea strains grouped into five well-supported subclades, with Chinese and non-Chinese isolates forming distinct lineages. Among these, the Chinese strains ACCC 37001 and KUNCC 11030 represented the earliest diverging lineages. This study elucidates the intraspecific variation and evolutionary patterns of the mitogenome in C. purpurea and highlights the value of mitogenome in resolving phylogenetic relationships.

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