Lewis John D, Saperas Núria, Song Yue, Zamora Maria Jose, Chiva Manel, Ausió Juan
Department of Biochemistry and Microbiology, University of Victoria, P.O. Box 3055, Petch Building, Victoria, British Columbia, Canada V8W 3P6.
Proc Natl Acad Sci U S A. 2004 Mar 23;101(12):4148-52. doi: 10.1073/pnas.0308721101. Epub 2004 Mar 15.
We present evidence that chordate protamines have evolved from histone H1. During the final stages of spermatogenesis, the compaction of DNA in many organisms is accomplished by the replacement of histones with a class of arginine-rich proteins called protamines. In other organisms, however, condensation of sperm DNA can occur with comparable efficiency in the presence of somatic-type histones or, alternatively, an intermediate class of proteins called protamine-like proteins. The idea that the highly specialized sperm chromosomal proteins (protamines) and somatic chromosomal proteins (histones) could be related dates back almost to the discovery of these proteins. Although this notion has frequently been revisited since that time, there has been a complete lack of supporting experimental evidence. Here we show that the emergence of protamines in chordates occurred very quickly, as a result of the conversion of a lysine-rich histone H1 to an arginine-rich protamine. We have characterized the sperm nuclear basic proteins of the tunicate Styela montereyensis, which we show consists of both a protamine and a sperm-specific histone H1 with a protamine tail. Comparison of the genes encoding these proteins to that of a sister protochordate, Ciona intestinalis, has indicated this rapid and dramatic change is most likely the result of frameshift mutations in the tail of the sperm-specific histone H1. By establishing an evolutionary link between the chromatin-condensing histone H1s of somatic tissues and the chromatin-condensing proteins of the sperm, these results provide unequivocal support to the notion that vertebrate protamines evolved from histones.
我们提供的证据表明，脊索动物的鱼精蛋白是由组蛋白H1进化而来的。在精子发生的最后阶段，许多生物体中DNA的压缩是通过用一类富含精氨酸的蛋白质（即鱼精蛋白）取代组蛋白来实现的。然而，在其他生物体中，精子DNA的浓缩在体细胞型组蛋白存在的情况下，或者在一类称为类鱼精蛋白的中间蛋白质存在的情况下，也能以相当的效率发生。高度特化的精子染色体蛋白（鱼精蛋白）和体细胞染色体蛋白（组蛋白）可能相关的观点几乎可以追溯到这些蛋白质的发现之时。尽管从那时起这个概念经常被重新审视，但一直完全缺乏支持性的实验证据。在这里，我们表明，脊索动物中鱼精蛋白的出现非常迅速，这是由于富含赖氨酸的组蛋白H1转化为富含精氨酸的鱼精蛋白的结果。我们已经对海鞘Styela montereyensis的精子核碱性蛋白进行了表征，我们发现它由一种鱼精蛋白和一种带有鱼精蛋白尾巴的精子特异性组蛋白H1组成。将编码这些蛋白质的基因与姐妹原索动物Ciona intestinalis的基因进行比较，表明这种快速而显著的变化很可能是精子特异性组蛋白H1尾巴中移码突变的结果。通过在体细胞组织的染色质浓缩组蛋白H1和精子的染色质浓缩蛋白之间建立进化联系，这些结果为脊椎动物鱼精蛋白由组蛋白进化而来的观点提供了明确的支持。
