Mitochondrial genomes in the iconic reindeer lichens: Architecture, variation, and synteny across multiple evolutionary scales

ABSTRACT

Variation in mitochondrial genome composition across intraspecific, interspecific, and higher taxonomic scales has been little studied in lichen obligate symbioses. Cladonia is one of the most diverse and ecologically important lichen genera, with over 500 species representing an array of unique morphologies and chemical profiles. Here, we assess mitochondrial genome diversity and variation in this flagship genus, with focused sampling of two clades of the “true” reindeer lichens, Cladonia subgenus Cladina, and additional genomes from nine outgroup taxa. We describe composition and architecture at the gene and the genome scale, examining patterns in organellar genome size in larger taxonomic groups in Ascomycota. Mitochondrial genomes of Cladonia, Pilophorus, and Stereocaulon were consistently larger than those of Lepraria and contained more introns, suggesting a selective pressure in asexual morphology in Lepraria driving it toward genomic simplification. Collectively, lichen mitochondrial genomes were larger than most other fungal life strategies, reaffirming the notion that coevolutionary streamlining does not correlate to genome size reductions. Genomes from Cladonia ravenelii and Stereocaulon pileatum exhibited ATP9 duplication, bearing paralogs that may still be functional. Homing endonuclease genes (HEGs), though scarce in Lepraria, were diverse and abundant in Cladonia, exhibiting variable evolutionary histories that were sometimes independent of the mitochondrial evolutionary history. Intraspecific HEG diversity was also high, with C. rangiferina especially bearing a range of HEGs with one unique to the species. This study reveals a rich history of events that have transformed mitochondrial genomes of Cladonia and related genera, allowing future study alongside a wealth of assembled genomes.

KEYWORDS:

• Ascomycetes
• Cladoniaceae
• fungi
• North America
• organelle
• transposable elements

ACKNOWLEDGMENTS

This research was conducted as part of the doctoral dissertation of J.R.H. Christopher Blair, Elizabeth Alter, Jessica Allen, and Yoshihito Ohmura were influential advisors on this research and as such deserve a great thanks. Some collections and sequence data were provided by the Kane and Tripp laboratories at the University of Colorado Boulder. Collections from Japan were acquired with the assistance of Evgeny Davydov, Irina Galanina, and Alexander Paukov, as well as the Ohmura laboratory at the Tokyo Museum of Nature and Science. Additional thanks are extended to Troy McMullin, John Franklin, Jim Battaglia, and Carly Anderson for their assistance in collections and sequence data generation. Finally, we thank Jennifer Dorey, Robin Sleith, Carlos Rodrigues-Vaz, Simon Verlynde, Lydia Paradiso, Charlie and Katie Zimmerman, and Sarah Hardy for supporting the authors throughout this project.

DATA ACCESSIBILITY STATEMENT

Raw sequence reads are deposited in the SRA (BioProjects PRJNA731936 and PRJNA770763). Individual assembled mitochondrial genomes are deposited in GenBank under accession numbers OL989692–OL989772 (TABLE 1).

DISCLOSURE STATEMENT

No potential conflict of interest was reported by the authors.

SUPPLEMENTARY MATERIAL

Supplemental data for this article can be accessed online at https://doi.org/10.1080/00275514.2022.2157665.

Additional information

Funding

This work was supported by the National Science Foundation [#1432629]; National Science Foundation [1542639]. This research was funded by multiple sources, including the National Science Foundation (NSF) dimensions project grants 1432629 (to James Lendemer) and 1542639 (to collaborators at the University of Colorado, Boulder) and the Japan Society for the Promotion of Science (JSPS) short-term fellowship.