Evolutionary dynamics of mitochondrial genomes and intracellular transfers among diploid and allopolyploid cotton species.

Background: Plant mitochondrial genomes (mitogenomes) exhibit extensive structural variation yet extremely low nucleotide mutation rates, phenomena that remain only partially understood. The genus Gossypium, a globally important source of cotton, offers a wealth of long-read sequencing resources to explore mitogenome and plastome variation and dynamics accompanying the evolutionary divergence of its approximately 50 diploid and allopolyploid species.

Results: Here, we assembled 19 mitogenomes from Gossypium species, representing all genome groups (diploids A through G, K, and the allopolyploids AD) based on a uniformly applied strategy. A graph-based mitogenome assembly method revealed more alternative structural conformations than previously recognized, some of which confirmed the mitogenome structure reported in earlier studies on cotton. Using long-read data, we quantified alternative conformations mediated by recombination events between repeats, and phylogenetically informative structural variants were noted. Nucleotide substitution rate comparisons between coding and non-coding regions revealed low mutation rates across the entire mitogenome. Genome-wide mapping of nuclear organellar DNA transfers (NUOTs) in Gossypium revealed a nonrandom distribution of transfers in the nuclear genome. In cotton, the fate of NUOT events varied, with mitochondrion-to-nucleus transfer (NUMT) predominantly retained as short fragments in the nuclear genome, with more plastid sequences integrated into the nucleus. Phylogenetic relationships inferred using different data sets highlighted distinct evolutionary histories among these cellular compartments, providing ancillary evidence relevant to the evolutionary history of Gossypium.

Conclusions: A comprehensive analysis of organellar genome variation demonstrates complex structural variation and low mutation rates across the entire mitogenome and reveals the history of organellar genome transfer among the three genomes throughout the cotton genus. The findings enhance our general understanding of mitogenome evolution, comparative organellar and nuclear evolutionary rates, and the history of inter-compartment genomic integration.