Lineage-specific expansion and functional diversification of mTERF proteins sculpt organellar regulation in plants

The endosymbiotic origin of mitochondria and chloroplasts necessitated the transfer of thousands of genes to the host nucleus, yet the evolutionary paths leading to their functional specialization in organelles remain largely unexplored. Here, we investigate this fundamental question through a comprehensive analysis of the mitochondrial transcription termination factor (mTERF) family, nucleic acid-binding proteins critical for organellar gene regulation. We find that plant mTERFs underwent substantial lineage-specific expansion, diversifying into four major clades in angiosperms. Phylogenetic reconstruction reveals a complex evolutionary history: while chloroplast-targeted mTERFs and a subset of mitochondrial ones share a red algal origin, a novel clade of mitochondrial mTERFs emerged later in seed plants. This diversification underpins functional specialization in developmental transitions, such as the shift from vegetative to reproductive growth, and in environmental adaptation. Genetic analysis in Arabidopsis demonstrates that mTERF10, a positive regulator of salt tolerance, acts as a negative regulator of thermotolerance, illustrating how neofunctionalization facilitates adaptation to disparate stresses. Our study elucidates the evolutionary dynamics of nuclear-encoded organellar proteins and the regulatory networks they govern.