Protamines from liverwort are produced by post-translational cleavage and C-terminal di-aminopropanelation of several male germ-specific H1 histones

• Published in: The Journal of biological chemistry Vol. 294; no. 44; pp. 16364 - 16373
• Main Authors: D’Ippolito, Robert Anthony, Minamino, Naoki, Rivera-Casas, Ciro, Cheema, Manjinder S., Bai, Dina L., Kasinsky, Harold E., Shabanowitz, Jeffrey, Eirin-Lopez, Jose M., Ueda, Takashi, Hunt, Donald F., Ausió, Juan
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01-11-2019; American Society for Biochemistry and Molecular Biology
• Subjects: 14-3-3 protein; Amino Acid Sequence - genetics; Animals; Chromatin - metabolism; chromatography; di-aminopropanelation; electron microscopy (EM); Hepatophyta - metabolism; histone; histone H1; Histones - metabolism; Male; Marchantia; Marchantia - metabolism; mass spectrometry; mass spectrometry (MS); Mass Spectrometry - methods; Plant Biology; protamines; Protamines - genetics; Protamines - metabolism; Protein Processing, Post-Translational - physiology; Spermatids - metabolism; Spermatogenesis - physiology; Spermatozoa - metabolism; protamines; 14-3-3 protein; histone H1; di-aminopropanelation; chromatography; mass spectrometry; Marchantia; histone; mass spectrometry (MS); electron microscopy (EM)
• ISSN: 0021-9258; 1083-351X
• DOI: 10.1074/jbc.RA119.010316

Protamines are small, highly-specialized, arginine-rich, and intrinsically-disordered chromosomal proteins that replace histones during spermiogenesis in many organisms. Previous evidence supports the notion that, in the animal kingdom, these proteins have evolved from a primitive replication-independent histone H1 involved in terminal cell differentiation. Nevertheless, a direct connection between the two families of chromatin proteins is missing. Here, we primarily used electron transfer dissociation MS-based analyses, revealing that the protamines in the sperm of the liverwort Marchantia polymorpha result from post-translational cleavage of three precursor H1 histones. Moreover, we show that the mature protamines are further post-translationally modified by di-aminopropanelation, and previous studies have reported that they condense spermatid chromatin through a process consisting of liquid-phase assembly likely involving spinodal decomposition. Taken together, our results reveal that the interesting evolutionary ancestry of protamines begins with histone H1 in both the animal and plant kingdoms.