Insights into the phylogenetic, structural and functional evolution of LHC superfamily in photosynthetic organisms

Photosynthesis is the fundamental process for the survival of photosynthetic organisms. The light-harvesting complexes (LHCs) play a crucial role in light energy capture and transfer. Despite their conserved role in energy transfer, the evolutionary basis for functional diversification of LHCs across photosynthetic lineages remains largely unclear. In this study, we performed phylogenetic analyses based on 65 genomes covering all major linages of photosynthetic organisms and identified 1,922 LHC proteins, which were classified into four groups: LHCA, LHCB, LHC-like, and FCP. The LHC gene family has undergone dynamic diversification through lineage-specific mechanisms in which green algae primarily utilized dispersed duplications, while land plants increasingly relied on whole-genome duplications (WGDs). Structural analyses revealed key adaptive modifications: PSI-LHCI transitioned from a double-layer crescent antenna in green algae to a simplified single-layer configuration in land plants, while PSII-LHCII in angiosperms replaced the N-LHCII trimer with CP24 to optimize light harvesting. Expression profiling revealed the functional diversification of different LHC members, with LHCA/LHCB members showing constitutive expression in photosynthetic tissues and strong induction of abiotic stresses, while LHC-like exhibited specialized responses to specific environmental challenges. Our study enhances better understanding of the evolutionary scenario of LHC superfamily during the evolution of photosynthetic organisms, and provides a foundation for future research on the molecular mechanisms underlying the adaptation of LHCs to extreme environments. • Identification and phylogenetic analysis of 1,922 LHC proteins across 65 photosynthetic species reveals four conserved subgroups: LHCA, LHCB, LHC-like and FCP. • Green algae and land plants separately employe dispersed duplications and whole-genome duplications to expand their LHC members. • The light-harvesting antennae experienced structural simplification during plant terrestrialization: LHCI layers reduced from two to one, and LHCII replaced the N-LHCII trimer with CP24 monomer, reflecting an adaptation to high-light condition on land. • LHCA/B members are constitutively expressed in photosynthetic tissues, while LHC-like members show stress-specific induction.