Possible evolutionary steps in the genetic code

Vol. 107, No. 1, 1982 July 16, 1982

BIOCHEMICAL

AND BIOPHYSICAL

RESEARCH COMMUNICATIONS Pages 225-228

POSSIBLE EVOLUTIONARY STEPS IN THE GENETIC CODE Thomas H. Jukes Space Sciences Laboratory University of California, Berkeley Berkeley, CA 94720 Received

May

24,

1982

In mammalian mitochondrial codes, fourfold codons wobble-oair with UNN anticodons so that U wobbles with U, C, A and G. Twofold oyrimidine-terminated codons pair with GNN and twofold purine-terminated codons pair with UNN. lhese properties enable a prediction to be made for evolution of the universal genetic code. It was postulated (1) that an archetypal code of 16 quartets coded for 15 amino acids. If this code used UNN anticodons, then duplication of tRNA genes, followed by mutations in the anticodons and aminoacylation sites, would give rise to the present universal code.

Tqe genetic genetic

code

of codons

code in mitochondria (2,

with

in the

anticodon, having

with

U, such

wobble

of codons

proposal currently cases,

rules

findings

"lost"

in which

an anticodon

place

(2).

phenylalanine,

these

between

Also,

U

amino

UUY, pair and amino

acids

CAR, pair

with

anticodons

examples

follow

ciassical

acids that

other

two codons

a pathway

I suggested

an earlier

to a single

15 amino

to postulate

form.

pyrimidine-terminated the

takes

universa

("quartets")

such as phenylalanine,

Both

the

groups

codons

such as glutamine,

glutamine.

from

tKNA with

pairing

G, such as GAA for

possible

from

was the suggestion have

fourfold

by a singie

codons

codons,

universal

was assigned only

that

U, C, A and G in four

with

make it

have evolved

include

is

respects

(3).

present

code might

valine,

U, such as UUG for

pairing

code to its

would

starting

in certain

translated

two pyrimidine-terminated

with

These

are

with

two purine-terminated

starting

differences

as UAC for

wobbling

an anticodon

having

One of the

such as GUN, valine,

starting

acids

3).

differs

archetypal

amino rather the

(4)

that code

acid

(Table

than

the

doublets

of codons, in the

expansion universal

in which

20.

acids

of the genetic

each quartet

The archetypai

present amino

codon

the

i).

archetypal

(one

for

Embodied

were

and have,

those

code in the that

in eight

case of isoleucine)

in a

0006-291X/82/130225-04$01.00/0 225

Copyright 0 1982 by Academic Press, Inc. AN rights of reproduction in any form reserved.

Vol. 107, No. 1, 1982 quartet

to another

BIOCHEMICAL amino

histidine

was formerly

histidine

and the

If code

archetypal is

that

mutational

tRNA,

of this

in yeast

in its

nature

fairly

the present

three

anticodons

with

anticodon

UAC.

CCA without

Trp

the

amino

The archetypal to GUA, pairing an anticodon,

acid

tyrosine

with

for

code.

by which

the anticodon duplicate

evidently

with

has taken

use of CUN for

leucine

as in the

universal

1).

to produce,

for

respectively,

when the Trp

which

retained

originally

coded

anticodon

UAU and UAC.

did

anticodon

place

and the

fourth

retaining

mutated

to

include tRNAsVal,

from

UCA to

UCA was therefore

duplicate

lost,

so

when a duplication

tRNAs underwent

a mutation

UAU, was "recaptured"

by

by AUN. not

duplicate,

The two codons

and became chain-terminating

code (5).

four

tRNAMet was formed

and one of the

would

recently

example,

anticodon

tRNA and the anticodon The present

steps

A

while

of the code took

Subsequent

with

place

of leucine,

(Table

underwent

UUA and UUG.

instead

code

anticodon

became charged

Thus tRNA paired

expansion

postulatior

with

The second it

the

The first

tRNAphe,

so that

mitochondrial

threonine

was formed

The other,

the steps

UUU and UUC.

the

place,

the

In one of these,

site,

acid

trace

universal

tRNAs.

with

that

the archetypal

procedures,

codon.

now codes

use CUN for

of the

tRNA took

UAU to CAU.

isoleucine,

example,

GAC, CAC and IAC,

duplication

former

present

and mutations

UGA became a stop

of its from

tRNA

the

acceptance

the

that

Thus,

procedure to

in amino

universal

duplications

possible

UAA.

simple

additional

is

the anticodon

has retained

By these

of codons

the pairing

aminoacylation

These

function.

glutamine.

two identical

mitochondria.

Neurospora

for

UAA to GAA, pairing

and retained

change

it

to form

to form

change

leucine,

that

codons,

code expanded

from

acid,

code embodied

an archetypal

mutated

by the quartet

amino

fourfold

UAA, duplicated

form

"new"

RESEARCH COMMUNICATIONS

or to a chain-terminating

coded

the archetypal

uses for

acid

AND BIOPHYSICAL

codons

but

mutated

UAA and UAG were because

they

from

left

UUA

without

had lost

cognate

tRNA. An analogous mitochondrial no tRNA pairing

event

seems recently

code in which with

them is

to have occurred

in the mammalian

AGA and AGG have become chain-terminating in the human, 226

bovine

or mouse mitochondrial

codons

and

genomes

Vol. 107, No. 1, 1982

BIOCHEMICAL Table

1.

AND BIOPHYSICAL

RESEARCH COMMUNICATIONS

Proposed Archetypal Genetic Code and Subsequent Evolution (From Ref. 1) Archetypal Assignments

Quartet ____-

Present Assignments

UUN

Phe

UUY-Phe UUR-Leu

CUN

Leu

No change

AUN

Ile

AUY-Ile AUA-Ile AUG-Met

GUN UCN CCN ACN GCN UAN

Val Ser Pro Thr Ala Tyr

No change No change No change No change No change UAY-Tyr UAR-CT

CAN

His

CAY-His CAR-Gln

AAN

Asn

AAY-Asn AAR-Lys

GAN

ASP

GAY-Asp GAR-Glu

UGN

CYS

UGY-Cys UGA-CT UGG-Tro

CGN AGN

Arg Ser

No change AGY-Ser AGR-Arg

GUY

No change

GGN

N = A, G, CT = chain

(6, It

7). is

These also

codons

noteworthy and

to

evolutionary

earlier

are

that

both

tryptophan

C or U; Y = U or termination

still

used

mitochondria

use

AUA and AUG for stages

in

for

C;

arginine both

methionine, the

R = A or

in

UGA and for

universal

G;

yeast UGG as

these

code

as

mitochondria

two

codes

for

examples

proposed

(5).

correspond

above.

ACKNOWLEDGEMENTS Support

from

NASA

Grant

NGR

05-003-460

and

the

assistance

of

Carol

Fegte

are

acknowledged.

REFERENCES _____ 1. Jukes, Press, 2.

Barrell,

T.H. (1968) in Molecules N.Y., p. 68.B.G.,

Anderson,

S.,

and Evolution Bankier,

A.T.,

227

de

(Second

printing),

Bruijn,

M.H.L.,

Columbia Chen,

E.,

Univ

BIOCHEMICAL

Vol. 107, No. 1, 1982

AND BIOPHYSICAL

Coulson, A.R., Drouin, J., Eperon, F ., Schreier, P.H., Smith, A.J.H., Natl. Acad. Sci. USA 77, 3164-3166. 3. Jukes,

T.H.

4. Crick,

F.H.C.

(1981) (1966)

J.

Mol. J. Mol.

Evol.

RESEARCH COMMUNICATIONS

I.C., Nierlich, D.P., Staden, R. and Young, 18,

Biol.

Roe, B.A., Sanger, I.G. (1980) Proc.

15-17.

19,

548-555.

5. Bonitz, S.B., Berlani, R., Coruzzi, G., Li, M., Macino, G., Nobrega, B.E. and Tzagoloff, A. (1980) Proc. F.B., Nobrega, M.P., Thalenfeld, Acad. Sci. USA 77, 3167-3170.

Natl.

6. Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H.L., Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger, F., Schreier, P.H., Smith, A.J.H., Staden, R. and Young, I.G. (1981) Nature 29J, 457-470. 7. Bibb, M.J., D.A. (1981)

Van Etten, R.A., Cell 26, 167-180.

Wright,

C.T.,

228

Walberg,

M.W. and Clayton,