Abstract

Many spliceosomal introns exist in the eukaryotic nuclear genome. Despite much research, the evolution of spliceosomal introns remains poorly understood. In this paper, we tried to gain insights into intron evolution from a novel perspective by comparing the gene structures of cytoplasmic ribosomal proteins (CRPs) and mitochondrial ribosomal proteins (MRPs), which are held to be of archaeal and bacterial origin, respectively. We analyzed 25 homologous pairs of CRP and MRP genes that together had a total of 527 intron positions. We found that all 12 of the intron positions shared by CRP and MRP genes resulted from parallel intron gains and none could be considered to be “conserved,” i.e., descendants of the same ancestor. This was supported further by the high frequency of proto-splice sites at these shared positions; proto-splice sites are proposed to be sites for intron insertion. Although we could not definitively disprove that spliceosomal introns were already present in the last universal common ancestor, our results lend more support to the idea that introns were gained late. At least, our results show that MRP genes were intronless at the time of endosymbiosis. The parallel intron gains between CRP and MRP genes accounted for 2.3% of total intron positions, which should provide a reliable estimate for future inferences of intron evolution.

Highlights

  • There are two opposing theories regarding when spliceosomal introns originated

  • In order to make the multiple alignments between cytoplasmic ribosomal protein (CRP) and mitochondrial ribosomal protein (MRP) genes more reliable, ribosomal protein (RP) genes of two bacterial species (Rickettsia prowazekii and Escherichia coli) were included in the analyses (Figure 1A, Figure S1, and Dataset S1)

  • We found 570 introns (265 intron positions) in the coding regions of the CRP genes and 423 introns (262 intron positions) in the coding regions of the MRP genes

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Summary

Introduction

There are two opposing theories regarding when spliceosomal introns originated. The introns-early theory proposes that primordial spliceosomal introns already existed at the beginning of life [1,2,3]. The earliest version of the intronsearly theory postulated that, during the course of evolution, introns were completely lost from prokaryotes while being partly retained in eukaryotes. The introns-late theory, on the other hand, holds that all spliceosomal introns were only recently inserted into eukaryotic genes [6,7]; the introns-late theory allows for some intron losses, it stresses that intron gains played the primary role in forming the modern pattern of introns. The debate between these two theories remains vigorous [4,8]

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