The Agaricus bisporus cox1 Gene: The Longest Mitochondrial Gene and the Largest Reservoir of Mitochondrial Group I Introns

Summary

This research revealed that the common button mushroom (Agaricus bisporus) contains the longest mitochondrial gene ever discovered, packed with genetic elements called introns. These findings help us understand how genes evolve and how genetic material can move between species. This impacts everyday life in several ways: • Helps scientists better understand mushroom biology which can improve cultivation techniques • Provides insights into how organisms evolve and adapt over time • Advances our knowledge of gene structure which can benefit biotechnology applications • Could lead to improved breeding methods for commercial mushroom production • Contributes to our understanding of how genetic information is organized and maintained in living things

Background

In eukaryotes, introns are found in nuclear and organelle genes across several kingdoms. Large introns (up to 5 kbp) are common in mitochondrial genomes of plants and fungi but rare in Metazoa, despite fungi and Metazoa being grouped together as Opisthokonts. Mitochondrial introns are classified into two groups (I and II) based on their RNA secondary structure involved in self-splicing. Most mitochondrial group I introns contain a ‘Homing Endonuclease Gene’ (heg) that enables intron transfer and site-specific integration (‘homing’) between species.

Objective

To determine and analyze the sequence and molecular organization of the cox1 gene in Agaricus bisporus, the most widely cultivated mushroom globally, to understand the evolution and dynamics of mitochondrial introns in fungi.

Results

The A. bisporus cox1 gene was found to be 29,902 nucleotides long, containing 19 introns (18 group I and 1 group II). This makes it both the longest mitochondrial gene and largest group I intron reservoir reported to date. The introns represent 94.7% of the gene sequence. Fifteen of the 18 group I introns harbor intact ORFs encoding putative functional homing endonucleases. Analysis revealed 240 group I introns across 53 fungal cox1 genes, sorted into 35 position classes, showing a wide and patchy distribution suggesting multiple events of loss and gain through evolution.

Conclusion

The evolution of eukaryotic mitochondrial genomes appears to be trending toward group I intron loss. However, in some fungal species, particularly in Dikarya, complete elimination seems counterbalanced by lateral transfer of these mobile genetic elements. The A. bisporus cox1 gene represents the largest group I intron reservoir described, possessing representatives of more than half of all position classes, with most containing intact and potentially functional homing endonuclease genes.
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