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The structural requirements for assembly of functional
class II transfer RNA core regions have been examined by
sequence analysis and tested by reconstruction of alternative
folds into the tertiary domain of Escherichia coli
tRNA2Gln. At least four distinct designs
have been identified that permit stable folding and efficient
synthetase recognition, as assessed by thermal melting
profiles and glutaminylation kinetics. Although most large
variable-arm tRNAs found in nature possess an enlarged
D-loop, lack of this feature can be compensated for by
insertion of nucleotides either 3′ to the variable
loop or within the short acceptor/D-stem connector region.
Rare pyrimidines at nt 9 in the core region can be accommodated
in the class II framework, but only if specific nucleotides
are present either in the D-loop or 3′ to the variable
arm. Glutaminyl-tRNA synthetase requires one or two unpaired
uridines 3′ to the variable arm to efficiently aminoacylate
several of the class II frameworks. Because there are no
specific enzyme contacts in the tRNAGln core
region, these data suggest that tRNA discrimination by
GlnRS depends in part on indirect readout of RNA sequence
Structure-based engineering of the tertiary fold
of Escherichia coli tRNA2Gln
has enabled conversion of this transfer RNA to a class II
structure while retaining recognition properties of a
class I glutamine tRNA. The new tRNA possesses the
20-nt variable stem-loop of Thermus thermophilus
tRNASer. Enlargement of the D-loop appears essential
to maintaining a stable tertiary structure in this species,
while rearrangement of a base triple in the augmented D-stem
is critical for efficient glutaminylation. These data provide
new insight into structural determinants distinguishing
the class I and class II tRNA folds, and demonstrate a
marked sensitivity of glutaminyl-tRNA synthetase to alteration
of tRNA tertiary structure.
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