Trends in Genetics
Volume 23, Issue 4, April 2007, Pages 158-161
Journal home page for Trends in Genetics

Update
Genome Analysis
Evolutionary history of 7SL RNA-derived SINEs in Supraprimates

https://doi.org/10.1016/j.tig.2007.02.002Get rights and content

The evolutionary relationships of 7SL RNA-derived SINEs such as the primate Alu or the rodent B1 elements have hitherto been obscure. We established an unambiguous phylogenetic tree for Supraprimates, and derived intraordinal relationships of the 7SL RNA-derived SINEs. As well as new elements in Tupaia and primates, we also found that the purported ancestral fossil Alu monomer was restricted to Primates, and provide here the first description of a potential chimeric promoter box region in SINEs.

Introduction

Short interspersed elements (SINEs) are known to occur throughout the genomes of eukaryotes. They originate from retroposition of small RNAs such as 7SL RNA, tRNA or their derivatives featuring internal RNA polymerase III promoters [1]. Active SINEs can cause hereditary diseases [2], enable genomic rearrangements [3] and be exapted into functional proteins 4, 5, 6. SINEs originally derived from 7SL RNA 7, 8, a component of the cytoplasmic signal recognition particle [9], have been found in primates [10], scandentians (tree shrews) [11] and rodents [12], all members of the placental mammalian clade Supraprimates 13, 14 (Euarchontoglires [15]), which also includes dermopterans (flying lemurs) and lagomorphs (rabbits). Assuming that 7SL RNA-derived SINEs arose in a common ancestor of these orders [16], they should also be present in the other two Supraprimate orders, but this has yet to be demonstrated [17].

The fossil Alu monomer (FAM) [16] was thought to be the oldest common ancestor of all 7SL RNA-derived SINEs [18]. Compared with human 7SL RNA, FAMs have a large central deletion (Figure 1) [16] and are believed to have given rise to subsequent monomeric sequences, namely the primate-specific free right Alu monomer (FRAM) [16], and to the free left Alu monomer (FLAM) of the A-subtype (FLAM-A, or FLA) [19]. In primates FLAM-C is a descendant of FLAM-A, and its fusion to FRAM gave rise to the predominating dimeric Alu family of 7SL RNA-derived SINEs [20].

The rodent proto-B1 element (PB1) is nearly identical to FLAM-A [18]. Rodent B1 elements are monomeric SINEs, but contain a diagnostic internal 29-bp duplication (Figure 1: B1 R). They descended from FLAM-A (or PB1) through PB1D with a characteristic deletion [17] that is lacking in the primate 7SL RNA-derived SINEs of the Alu family.

In Scandentia, the tree shrew-specific chimeric Tu type II SINEs (composed of tRNA and 7SL RNA parts) share with the rodents this diagnostic deletion in the left 7SL RNA-derived part [11]. Nishihara et al. used this shared deletion to suggest a possible evolutionary scenario with a more recent common ancestry of Tu type II and rodent B1 SINEs and, as a potential consequence, a sister group relationship of the orders Rodentia and Scandentia [11].

Because 7SL RNA-derived SINEs are specific for Supraprimates, their evolutionary histories are also of particular interest. However, because the current evidence for ordinal relationships within Supraprimates is partially contradictory, the distribution patterns, and the evolutionary history, of 7SL RNA-derived SINEs might differ from proposed scenarios. Some large-scale sequence data support the Euarchonta theory combining Primates, Dermoptera and Scandentia in one group 13, 15, whereas other studies indicate the placement of tree shrews with lagomorphs 21, 22, 23. Furthermore, similarities in lineage-specific 7SL RNA-derived SINEs [11] support a clustering of Rodentia and Scandentia, further confusing the issue. The phylogenetic position of lagomorphs within the placental tree is also equivocal, with some data supporting the monophyletic group Glires, comprising rodents and lagomorphs 15, 24, 25, and others placing lagomorphs as a sister group to a clade Cetferungulata+Xenarthra+Afrotheria [22]. Thus, to analyze the evolutionary history of Supraprimate-specific 7SL RNA-derived SINE retroposons, we chose first to resolve current controversies concerning the interordinal relationships within the Supraprimate clade and establish a robust evolutionary tree of this superorder.

Section snippets

Resolving the evolutionary tree of Supraprimates

We searched genomic sequences of mouse, rat, guinea pig, rabbit, tree shrew, chimpanzee, human and rhesus monkey with the local version of RepeatMasker (http://www.repeatmaster.org/) for phylogenetically informative retroposon presence–absence data conclusively to accept or reject current hypotheses of Supraprimate evolution (see Online Supplementary Material). We found 14 informative genomic loci that unambiguously define two main branches within Supraprimates (Figure 2, and Online

Elucidating the evolutionary history of 7SL RNA-derived SINEs

Placing the tree shrew in the Euarchonta clade, however, apparently contradicts one current hypothesis of 7SL RNA-derived SINE evolution [11] that makes use of a common diagnostic deletion (positions 64–73) in Rodent B1 and scandentian Tu type II SINEs to suggest a sister group relationship of Rodentia and Scandentia 11, 17. By contrast, our support for the separate Euarchonta and Glires clades, coupled with the common deletion in Rodentia and Scandentia, suggest that there is a common ancestry

Concluding remarks

Using a combination of genomic and trace sequence information we have established a clear phylogenetic framework of the Supraprimates that unambiguously confirms the clades Euarchonta and Glires. This enables us to elucidate and redefine the evolutionary history of 7SL RNA-derived SINE elements, the birth of which was traced to the common ancestor of Supraprimates. Instead of the previously proposed FAM element ancestor, which probably gave rise to only primate-specific SINEs, we propose a new

Acknowledgements

We thank Marsha Bundman for editorial assistance. This work was supported by the Deutsche Forschungsgemeinschaft (SCHM 1469 to J.S. and J.B.).

References (25)

  • P. Walter et al.

    Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum

    Nature

    (1982)
  • H. Nishihara

    Characterization of novel Alu- and tRNA-related SINEs from the tree shrew and evolutionary implications of their origins

    Mol. Biol. Evol.

    (2002)
  • Cited by (0)

    *

    These authors contributed equally to this work.

    View full text