From photoprotection to growth: shifts in high-light acclimation strategies associated with molecular evolutionary rates in duckweeds

Molecular evolutionary rates vary widely among organisms, yet the biological mechanisms underlying this variation and its evolutionary consequences remain poorly understood. In plants, the absence of an early-segregated germline raises the possibility that growth- and environment-dependent physiological processes could influence mutation accumulation and, ultimately, substitution rates. Here, we integrated phylogenomics, global distribution data, growth measurements, chlorophyll fluorescence, RNA-seq, and metabolomics to investigate the relationship between molecular evolutionary rate variation and ecophysiological strategies in duckweeds (Araceae, Lemnoideae), which show marked lineage-specific heterogeneity in molecular evolutionary rates. Phylogenomic analyses confirmed substantial branch-length differences among duckweed lineages. Nonsynonymous and synonymous divergence scaled proportionally across all lineages, indicating that this heterogeneity is not accompanied by differences in selective constraint. A broad survey of global distributions showed that lineages with and without prominent anthocyanin accumulation differed in their geographic ranges, suggesting ecological differentiation associated with light environments. Under experimental high-light conditions, lineages without prominent anthocyanin accumulation showed higher relative growth rates and maintained higher photosynthetic efficiency than anthocyanin-accumulating lineages. Further analyses revealed distinct high-light acclimation strategies: Spirodela polyrhiza, representing lineages with prominent anthocyanin accumulation, preferentially induced photoprotective pathways, including anthocyanin-related pathways and non-photochemical quenching, whereas Wolffia australiana, representing lineages without prominent anthocyanin accumulation, showed stronger induction of mitochondrial oxidative phosphorylation genes, co-enriched with the cytosolic ribosome and translational machinery, and broader changes in primary metabolism and energy/redox-related metabolites. These results suggest that duckweed lineages differ in how they balance photoprotection, photochemical energy use, and downstream metabolic capacity under high light, and that such ecophysiological divergence could be associated with lineage-specific variation in molecular evolutionary rates via growth-associated DNA replication and redox-dependent processes that influence mutation accumulation.