Adjustments, extinction, and remains of selenocysteine incorporation machinery in the nematode lineage

RNA. 2014 Jul;20(7):1023-34. doi: 10.1261/rna.043877.113. Epub 2014 May 9.

Abstract

Selenocysteine (Sec) is encoded by an UGA codon with the help of a SECIS element present in selenoprotein mRNAs. SECIS-binding protein (SBP2/SCBP-2) mediates Sec insertion, but the roles of its domains and the impact of its deficiency on Sec insertion are not fully understood. We used Caenorhabditis elegans to examine SBP2 function since it possesses a single selenoprotein, thioredoxin reductase-1 (TRXR-1). All SBP2 described so far have an RNA-binding domain (RBD) and a Sec-incorporation domain (SID). Surprisingly, C. elegans SBP2 lacks SID and consists only of an RBD. An sbp2 deletion mutant strain ablated Sec incorporation demonstrating SBP2 essentiality for Sec incorporation. Further in silico analyses of nematode genomes revealed conservation of SBP2 lacking SID and maintenance of Sec incorporation linked to TRXR-1. Remarkably, parasitic plant nematodes lost the ability to incorporate Sec, but retained SecP43, a gene associated with Sec incorporation. Interestingly, both selenophosphate synthetase (SPS) genes are absent in plant parasitic nematodes, while only Cys-containing SPS2 is present in Sec-incorporating nematodes. Our results indicate that C. elegans and the nematode lineage provide key insights into Sec incorporation and the evolution of Sec utilization trait, selenoproteomes, selenoproteins, and Sec residues. Finally, our study provides evidence of noncanonical translation initiation in C. elegans, not previously known for this well-established animal model.

Keywords: Caenorhabditis elegans; SBP2; SECIS-binding protein; selenocysteine; selenoprotein; translation initiation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Biological / genetics*
  • Amino Acid Sequence
  • Animals
  • Base Pairing
  • Base Sequence
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism*
  • Codon, Terminator
  • Evolution, Molecular*
  • Gene Silencing*
  • Metabolic Networks and Pathways / genetics*
  • Molecular Sequence Data
  • Phylogeny
  • RNA, Transfer / genetics
  • RNA, Transfer / metabolism
  • Selenocysteine / genetics
  • Selenocysteine / metabolism*
  • Selenoproteins / genetics

Substances

  • Codon, Terminator
  • Selenoproteins
  • Selenocysteine
  • RNA, Transfer