Evolutionary trajectories and subfunctionalization of 2 key methyltransferase regulator subfamilies in plants

Abstract DNA methylation, a conserved epigenetic mark in both plants and animals, plays a critical role in growth, development, and adaptability. This study explores the origin, evolution, and functional diversification of 2 key methyltransferase regulators, DNAJ-domain-containing protein 1/2/3 (DNAJ1/2/3) and SU(VAR)3-9 HOMOLOG 1/3 (SUVH1/3), in plants. By analyzing genomic data from 21 algae and 86 land plants, we discovered that DNAJ1/2/3 originated within Magnoliopsida, while SUVH1/3 emerged in ferns and evolved through retrotransposition. Both protein families have undergone multiple duplication events and positive selection throughout plant evolution, resulting in their expansion and functional divergence. In dicotyledons, DNAJ1/2/3 diverged into 3 subclades, whereas SUVH1/3 underwent a common duplication event in its ancestral lineage, resulting in 2 subgroups. Structural domain analysis revealed that the evolution of PHD fingers in DNAJ1/2/3 and AT domains in SUVH1/3, under selective pressure, enhanced their interaction capabilities and contributed to the formation of complexes involved in DNA methylation and demethylation regulation. Expression profile analysis across various plant taxa demonstrated tissue-specific expression patterns, with higher expression levels observed in meristematic tissues and active cell regions. These findings elucidate the evolutionary patterns of DNAJ1/2/3 and SUVH1/3 and offer insights into their functional diversification in plants.