A new type of structural compensation between the lengths of two perpendicularly oriented RNA double helices was found in the archaeal selenocysteine tRNA from Methanococcus jannascii. This tRNA contains only four base-pairs in the T-stem, one base-pair less than in all other cytosolic tRNAs. Our analysis shows that such a T-stem in an otherwise normal tRNA cannot guarantee the formation of the normal interactions between the D and T-loops. The absence of these interactions would affect the juxtaposition of the two tRNA helical domains, potentially damaging the tRNA function. Ln addition to the short T-stem, this tRNA possesses another unprecedented feature, a very long D-stem consisting of seven base-pairs. Taken as such, a seven base-pair D-stem will also disrupt the normal interaction between the D and T-loops. On the other hand, the presence of the universal nucleotides in both the D and T-loops suggests that these loops probably interact with each other in the same way as in other tRNAs. Here, we demonstrate that the short T-stem and the long D-stem can naturally compensate each other, thus providing the normal D/T interactions. Molecular modeling has helped suggest a detailed scheme of mutual compensation between these two unique structural aspects of the archaeal selenocysteine tRNA. In the light of this analysis, other structural and functional characteristics of the selenocysteine tRNAs are discussed. (C) 1999 Academic Press.