Organelle genome evolution in the early-diverging brown algal lineage, Ishigeales

The order Ishigeales is an early-diverging lineage of brown algae that exhibits remarkable morphological diversity ranging from simple filamentous forms to robust terete and foliose thalli, which may reflect complex evolutionary histories in their organelle genomes. However, limited organellar genomic data for the Ishigeales, presently confined to Ishige okamurae, have hindered a comprehensive understanding of organelle genome dynamics in that order. To address this, we de novo assembled the complete plastomes and mitogenomes of the four Ishigeales species: Pilinia rimosa, Petroderma maculiforme, I. okamurae, and I. foliacea. Phylogenetic analyses based on plastome and mitogenome datasets using both concatenation and coalescent-based approaches supported the divergence order from the less complex filamentous morphology of Pi. rimosa to the more morphologically complex terete and foliose Ishige species, yet it also revealed a phylogenetic conflict at the branching point of Pe. maculiforme, suggesting an intricate evolutionary history in filamentous species. Both plastomes and mitogenomes exhibited extensive genomic rearrangement. Notably, mitochondrial genome expansion was observed in Pi. rimosa and Pe. maculiforme, and massive cox2 gene duplication was found in Pi. rimosa. These expansions were likely driven by the proliferation of tandem repeats, and most copies are likely under relaxed purifying selection. Analysis of synonymous substitution rate to the nonsynonymous substitution rate revealed the rapid divergence in several plastid genes between I. okamurae and I. foliacea. In particular, the DPOR gene family exhibited a signal of relaxed purifying selection, potentially linked to their distinct morphological changes in Ishige species. Overall, our findings reveal that Ishigeales underwent lineage-specific differentiation and dynamic evolutionary patterns in the organelle genomes along with morphological variation.