The Rapid Evolution of De Novo Proteins in Structure and Complex

Abstract

Recent studies in the rice genome-wide have established that de novo genes, evolving from non-coding sequences, enhance protein diversity through a stepwise process. However, the pattern and rate of their evolution in protein structure over time remain unclear. Here, we addressed these issues within a surprisingly short evolutionary timescale (<1 million years for 97% of Oryza de novo genes) with comparative approaches to gene duplicates. We found that de novo genes evolve faster than gene duplicates in the intrinsic disordered regions (IDRs, such as random coils), secondary structure elements (such as α-helix and β-strand), hydrophobicity, and molecular recognition features (MoRFs). In de novo proteins, specifically, we observed an 8-14% decay in random coils and IDR lengths and a 2.3-6.5% increase in structured elements, hydrophobicity, and MoRFs, per million years on average. These patterns of structural evolution align with changes in amino acid composition over time as well. We also revealed higher positive charges but smaller molecular weights for de novo proteins than duplicates. Tertiary structure predictions showed that most de novo proteins, though not typically well-folded on their own, readily form low-energy and compact complexes with other proteins facilitated by extensive residue contacts and conformational flexibility, suggesting a faster-binding scenario in de novo proteins to promote interaction. These analyses illuminate a rapid evolution of protein structure in de novo genes in rice genomes, originating from non-coding sequences, highlighting their quick transformation into active, protein complex-forming components within a remarkably short evolutionary timeframe.