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The origin of the genetic code theories and their relationships, a review.

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BioSystems 80 (2005) 175–184
The origin of the genetic code: theories and their
relationships, a review
Massimo Di Giulio∗
Institute of Genetics and Biophysics ‘Adriano Buzzati-Traverso’, CNR,
Via G. Marconi 10, 80125 Naples, Italy
Received 3 August 2004; received in revised form 12 November 2004; accepted 18 November 2004
Abstract
A review of the main theories proposed to explain the origin of the genetic code is presented. I analyze arguments and data
in favour of different theories proposed to explain the origin of the organization of the genetic code. It is possible to suggest
a mechanism that makes compatible the different theories of the origin of the code, even if these are based on a historical or
physicochemical determinism and thus appear incompatible by definition. Finally, I discuss the question of why a given number
of synonymous codons was attributed to the amino acids in the genetic code.
© 2004 Elsevier Ireland Ltd. All rights reserved.
Keywords: Genetic code theories; Coevolution; Stereochemistry; Error-minimization hypothesis; Codon plurality; Molecular weight of amino
acids
1. Introduction
The theories suggested to explain the origin of the
genetic code are of two kinds. One of them is based
on a historical determinism (Wong, 1975), the others
on a physicochemical determinism (Sonneborn, 1965;
Woese et al., 1966; Woese, 1967). There is the weak
possibility that an early origin of the genetic code indicates that it was based on physicochemical (stereochemical) forces (Di Giulio, 1998). Alternatively, a late
origin of the code in the development of life might indi∗
Tel.: +39 081 7257313; fax: +39 081 5936123.
E-mail address: [email protected]
cate that this origin was not based on these forces since
‘the system’ might have already abandoned the strictly
physicochemical determinism. It seems natural to think
that a late phase of the origin of life witnessed the origin
of the genetic code as several dozen macromolecules
are required to achieve the code, but we cannot be sure
that this was the case (Di Giulio, 1998, in press).
In this review, I analyze arguments and data in favour
of different theories proposed to explain the origin of
the organization of the genetic code. Furthermore, I
try to answer the question of why there exists a given
number of synonymous codons attributed to the amino
acids in the genetic code. This question is not often
considered in papers on the origin of the code.
0303-2647/$ – see front matter © 2004 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.biosystems.2004.11.005
176
M. Di Giulio / BioSystems 80 (2005) 175–184
2. The stereochemical theory and evidence in
favour
The stereochemical theory claims the origin of the
genetic code must lie in the stereochemical interactions between anticodons or codons and amino acids
(Crick, 1968). The theory suggests, for example, asparagine must have been codified by the codons AAU
or AAC as asparagine is somehow stereochemically
correlated with these codons. Several models have been
proposed which indeed seem to define a stereochemical
relationship between anticodons or codons and amino
acids (Gamow, 1954; Pelc and Welton, 1966; Welton
and Pelc, 1966; Dunnill, 1966; Woese, 1967; Black,
1973, 1995; Melcher, 1974; Nelsestuen, 1978;
Balasubramanian et al., 1980; Marlborough, 1980;
Hendry et al., 1981; Shimizu, 1982; Yarus, 1991;
Szathmary, 1993).
The first stereochemical model was suggested in
1954 by Gamow, before the discovery of the genetic
code. Gamow (1954) proposed a ‘key and lock’ relation between amino acids and the rhomb-shaped ‘holes’
formed by various nucleotides in the DNA. This model
has the elegant property of being able to encode only 20
amino acids. Later, Melcher (1974) built models defining a stereochemical correlation between anticodon nucleotides and their amino acids. The feature of these
models (Melcher, 1974) was the intercalation of the
amino acid and the binding of the aliphatic amino acids
hydrogen atoms through hydrogen bonds to the ␲electrons of the bases. Balasubramanian et al. (1980)
constructed models based on oligoribonucleotides of
five residues having a purine at the 3 -end and an U at
the 5 -end, and any combination of three bases in the
middle. These pentaribonucleotides, which the authors
(Balasubramanian et al., 1980) consider to be a prototRNA, are shown to have a conformation capable of
receiving the relating amino acid. Hendry et al. (1981)
constructed models by eliminating the second base of
a codon in B-DNA in order to analyze the proprieties
of the ‘cavities’ thus formed. The authors (Hendry et
al., 1981) observed that the l-amino acids adapt well
to these cavities if the conventional physicochemical
principles of hydrogen bonding and sterical constraints
are used. Shimizu (1982) proposed a model based on
a complex of four bases on the tRNAs. These complexes are formed of the anticodon nucleotides and the
discriminator base at the fourth position of the 3 -end
of tRNAs. These complexes are able to possess a lock
and key relationship with the corresponding amino acid
(Shimizu, 1982).
The heterogeneity of stereochemical models seems
to suggest that there were interactions between amino
acids and anticodons or codons or, more generally,
with RNA or DNA. Whether or not these interactions
were specific and led to the organization of the genetic code has yet to be proven. The model offered
by Shimizu (1982), seems to be based on a variety of
experimental evidence (see Szathmary, 1993). Furthermore, numerous hairpin structures housing anticodons
have been constructed (Shimizu, 1995) so as to make
these structures similar to the stereochemical model
(Shimizu, 1982). These hairpin structures were specifically aminoacylated with their cognate amino acids
in the presence of aminoacyl-adenylate and a dipeptide, valyl-aspartic (Shimizu, 1995). The author claims
that his results are compatible with a stereochemical
origin of the genetic code (Shimizu, 1995). (However,
the validity of this analysis (Shimizu, 1995) has been
questioned (Larkin et al., 2001).)
Moreover, the stereochemical theory has received
new strength thanks to the findings of Yarus’ group
(Yarus, 1988, 1991, 1993, 1998, 2000; Yarus and
Christian, 1989; Lozupone et al., 2003). Recent evidence on the stereochemical hypothesis suggests that
a record of the genetic code’s origin is available today,
in the structures of RNA binding sites for amino acids
(Yarus, 2002). This data begin with the RNA structure
of the Tetrahymena guanosine site for the self-splicing
G cofactor (Yarus and Christian, 1989). When this
site was located, it contained arginine codons and also
bound arginine, which acted as a competitive inhibitor
of self-splicing (Yarus, 1988). This finding could be
generalized to the notion that amino acid binding sites
made of ribonucleotides would generally contain an excess of the codons and anticodons, a hypothesis testable
by selection of new aptamers. A recent review of selections for RNA affinity for six amino acids (arginine,
glutamine, isoleucine leucine, phenylalanine and tyrosine) found codons and anticodons in excess in 26
known binding sites with probability of the order or
smaller than 10−11 (assuming placement of triplets at
random) (Yarus, 2002). This concentration of triplets
is striking despite the fact that only one half of amino
acids (three of six: arginine, tyrosine and isoleucine)
showed coding triplets in excess. For isoleucine, the
M. Di Giulio / BioSystems 80 (2005) 175–184
argument can be carried a step further because the simplest binding site (having the fewest nucleotides) and
therefore the most prevalent isoleucine-binding RNA
under a variety of conditions, contains codons and anticodons within the binding site (Lozupone et al., 2003).
These data can be combined to argue that a substantial
fraction of the genetic code (for half of the amino acids,
judging from this evidence) was derived by extracting
parts of primordial amino acid binding structures, and
that these essentially physicochemical coding assignments survived to the modern code (Yarus, 2002).
3. The physicochemical and ambiguity
reduction theories: evidence in favour
The physicochemical theory claims that the force
defining the origin of the genetic code structure was
the one that tended to reduce the deleterious effects of
physicochemical distances between amino acids codified by codons differing in one base (Sonneborn, 1965;
Woese et al., 1966). In particular, Sonneborn (1965)
identified the selective pressure reducing the deleterious effects of mutations as the force defining the amino
acid allocations in the genetic code table (Ardell and
Sella, 2001; Sella and Ardell, 2002). Whereas, Woese
et al. (1966) maintained that the driving force defining genetic code organization must lie in a selective
pressure tending to reduce the translation errors of the
ancestral genetic message.
A similar theory is the ambiguity reduction hypothesis. This theory claims that group codons differing in one base were assigned to groups of physicochemical similar amino acids, and the genetic code
reached its current organization through the lowering of the ambiguity in the coding within and between groups of amino acids (Woese, 1965; Fitch and
Upper, 1987). Only one study conducted on 300 tRNAs
sequences specific for 8 amino acids (Fitch and Upper,
1987) is in favour of the ambiguity reduction theory (Woese, 1965; Fitch and Upper, 1987). Other and
equivalent analyses are in favour of the coevolution
theory (Di Giulio, 1992a, 1994a, 1995; Chaley et al.,
1999; Bermudez et al., 1999).
A point of view that is different in some aspects
from this hypotheses regards whether there was physicochemical affinity between amino acids and the doublets/triplets coding for them, which might have or-
177
ganized the genetic code. Some studies suggest that
this might have been the case (Weber and Lacey, 1978;
Jungck, 1978; Lacey et al., 1992).
On the other hand, the physicochemical hypothesis
(Sonneborn, 1965; Woese et al., 1966) is based on
a lot of evidence suggesting a relationship between
the physicochemical properties of amino acids and
the structure of the genetic code (Pelc, 1965; Woese
et al., 1966; Epstein, 1966; Goldberg and Wittes, 1966;
Volkenstein, 1966; Alff-Steinberger, 1969; Nagyvary
and Fendler, 1974; Nelsestuen, 1978; Weber and Lacey,
1978; Jungck, 1978; Wetzel, 1978; Wolfenden et al.,
1979; Jurka et al., 1982; Lacey and Mullins, 1983;
Swanson, 1984; Sjostrom and Wold, 1985; Taylor
and Coates, 1989; Di Giulio, 1989a,b, 1991, 1992a,
1994a; Haig and Hurst, 1991; Lacey et al., 1992, 1993;
Siemion and Stefanowicz, 1992; Szathmary, 1993;
Goldman, 1993; Baumann and Oro, 1993; Di Giulio
et al., 1994; Hartman, 1995; Di Giulio and Medugno,
1998, 1999, 2001; Freeland and Hurst, 1998a,b; Knight
et al., 1999; Freeland et al., 2000a,b; Ardell and Sella,
2001, 2002; Sella and Ardell, 2002; Freeland et al.,
2003; Zhu et al., 2003; Archetti, 2004). Therefore, at
some stages in the origin of the genetic code, the properties of amino acids must have sustained a remarkable
role in structuring its organization. In particular,
Freeland and Hurst (1998a) investigated: (1) the
effect of weighting transition errors differently from
transversion errors and (2) the effect of weighting each
base differently, depending on reported mistranslation
biases. They concluded that not only the genetic code is
extremely efficient at minimizing the effects of errors,
but also that its structure reflects biases in these errors
(Freeland and Hurst, 1998a,b). Whereas, Freeland
and Hurst (1998b) compared the error-minimizing
ability of the genetic code with that of alternative
codes which, rather than being a random selection, are
restricted such that amino acids from the same biosynthetic pathway all share the same first base. They
concluded that although on average the restricted set
of codes show a slightly higher efficiency than random
ones, the real genetic code remains extremely efficient
relative to this subset (P = 0.0003) (Freeland and Hurst,
1998b). This indicates that for the most part, historical
factor do not explain the load-minimization property
of the genetic code (Freeland and Hurst, 1998b). Furthermore, the importance of selection is supported by
the finding that the genetic code’s efficiency improves
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M. Di Giulio / BioSystems 80 (2005) 175–184
relative to that of historical related codes after
allowance is made for realistic mutational and mistranslational biases (Freeland and Hurst, 1998b). Once
mistranslational biases have been considered, fewer
than 4 per 100,000 alternative codes are better than the
current genetic code (Freeland and Hurst, 1998b). Also,
Freeland et al. (2000b) have shown that if theoretically
possible genetic code structures are reflecting plausible
biological constraints, and amino acids dissimilarity is
quantified using data of substitution frequencies, then
the code is at or very close to a global optimum for error
minimization. (However, the validity of this analysis
(Freeland et al., 2000b) has been questioned (Di Giulio,
2001).) More recently, Freeland et al. (2003) have
further reinforced the error-minimizing hypothesis.
4. The coevolution theory and evidence in
favour
The coevolution hypothesis of the origin of the genetic code (Wong, 1975) suggests that the origin of
the genetic code should be sought in the biosynthetic
relationships between amino acids. In particular, this
hypothesis maintains that early on in the genetic code
few amino acids (perhaps five) were codified: the precursors (Wong, 1975). As the other amino acids arose
biosynthetically from these precursors, part or all of the
codon domain of the precursor amino acid was passed
to the product amino acids (Wong, 1975).
The mechanism through which the precursor amino
acids passed part or all their codon domain to the
precursor amino acids is postulated by the coevolution theory as occurring on tRNA-like molecule on
which this theory suggests the biosynthetic transformation between amino acids took place (Wong, 1975).
If the biosynthetic pathways linking up the amino acids
took place on tRNA-like molecules, then a tRNAlike molecule bearing a product amino acid evolving
from the biosynthetic transformation of a given precursor amino acid must clearly have recognized some
of codons belonging to the precursor. Therefore, this
molecule was able to evolve naturally towards a tRNA
specific for that particular product amino acid and its
reassigned codons.
There are a number of observations and suggestions pointing out that the biosynthetic pathways of
amino acids played a fundamental role in structuring
the organization of the genetic code table (Nirenberg
et al., 1963; Pelc, 1965; Jukes, 1966; Dillon, 1973;
Wong, 1975, 1976, 1980, 1981; Brack and Orgel, 1975;
McClendon, 1986, 1987; Jurka and Smith, 1987a,b;
Wachtershauser, 1988; de Duve, 1991; Miseta, 1989;
Taylor and Coates, 1989; Danchin, 1989; Szathmary
and Zintzaras, 1992; Morowitz, 1992; Szathmary,
1993; Di Giulio, 1992a,b, 1993, 1994, 1995, 1996,
1997a–c, 1999, 2000a,b, 2001, 2002, 2003; Di Giulio
and Medugno, 1998, 1999, 2000, 2001; Di Giulio et al.,
1994; Edwards, 1996; Chaley et al., 1999; Bermudez
et al., 1999; Ardell and Sella, 2002; Zhu et al., 2003;
Archetti, 2004; Klipcan and Safro, 2004), thus corroborating the coevolution theory.
In particular, since the genetic code makes possible
the transformation of mRNA into proteins, a conjecture claims that some fundamental themes of protein
structure must be reflected in the genetic code table, as
these themes might have been the main selective pressure promoting the organization of the genetic code.
Di Giulio (1996) has tried to clarify how the physicochemical properties of amino acids are shared among
the pairs of amino acids that are in precursor–product
relationship and those that are not but which are nevertheless defined in the genetic code. He found (Di Giulio,
1996) that the pairs in precursor–product relationships
reflect the ␤-sheets of proteins through the ‘size’ of
amino acids (Di Giulio, 1996). This study (Di Giulio,
1996) would seem to have identified the main adaptive
theme promoting the organization of the genetic code
in the ␤-sheets. Furthermore, as the ␤-sheets of proteins are linked to the precursor–product relationships
and, it would also seem to provide strong evidence in
favour of the coevolution hypothesis.
Moreover, I believe some molecular fossils that
strongly corroborate the coevolution theory are the
main evidence in favour of it. Table 1 shows the biosynthetic pathways taking place on tRNAs, which in actual organisms transform one amino acid into another.
For example, in the pathway Asp-tRNAAsn → AsntRNAAsn an aspartic acid molecule is loaded onto a
tRNA specific for asparagine and an second enzyme
transforms aspartic acid into asparagine. The tRNA
loaded with asparagine in this way is accepted by ribosome and takes part in protein synthesis. There have
been several interpretations of these pathways (Ardell,
1998; Poole et al., 1998; Cavalier-Smith, 2001); it is
more than likely that they are fossils of a metabolic state
M. Di Giulio / BioSystems 80 (2005) 175–184
Table 1
The pathways currently transforming one amino acid into another while charged on a tRNA, together with their phylogenetic
distribution
Pathways
Phylogenetic
distribution
Glu-tRNAGln → Gln-tRNAGln
Asp-tRNAAsn → Asn-tRNAAsn
Bacteria and archaea
Bacteria (present in
minority) and archaea
Bacteria, archaea, and
eucarya
Bacteria and
organelles
Some archaea and
bacteria
Ser-tRNASec → Sec-tRNASec
Met-tRNAfMet → fMet-tRNAfMet
Lys-tRNAPyl → Pyl-tRNAPyl
For the original literature, see Bock et al. (1991), Ibba et al. (1997),
Tumbula et al. (2000) and Ibba and Soll (2002).
(Wong, 1976, 1988; Wachtershauser, 1988; de Duve,
1988, 1991; Benner et al., 1989; Danchin, 1989; Di
Giulio, 1992a,b, 1993, 1997a–c, 1999, 2000a–d, 2002;
Edwards, 1996). Di Giulio (2002) performed an evolutionary analysis, which seems to establish that these
pathways (Table 1) are ancient, possible molecular fossils of the mechanism that gave rise to the evolutionary organization of the genetic code. It seems to me
that the correspondence between the mechanism hypothesized by the coevolution theory (and based on
the transformation of the precursor amino acid into
the product, while they were loaded on a tRNA-like
molecule (Wong, 1975)), and the presence in actual organisms of these pathways (Table 1) is surprising and
therefore makes up an extremely strong corroboration
of this hypothesis. This is because, as molecular fossils these pathways (Table 1) would provide evidence
of significant value since they would have a high content of the history of early phases of life on earth, and
they might, therefore, remember the primordial stages
of the origin of the genetic code (Di Giulio, 2002).
5. Relationships between genetic code theories
While the relationships between the stereochemical and the physicochemical theories are sufficiently
clear, for example, the observations linking the physicochemical properties of amino acids to the properties
of dinucleoside monophosphates (Weber and Lacey,
179
1978; Jungck, 1978; Lacey et al., 1992) may be expressions of stereochemical interactions, the relationship
between the coevolution theory and the stereochemical or physicochemical theories seems to be much less
clear (Di Giulio, 1997b).
The coevolution theory seems to be compatible
with some aspects of the physicochemical and ambiguity reduction theories. Indeed, if there was a selective pressure tending to organize the code in columns
(Nelsestuen, 1978; Wolfenden et al., 1979; Sjostrom
and Wold, 1985; Di Giulio, 1989a; Taylor and Coates,
1989) then as the precursor amino acids gradually conceded part of their codon domain to the product amino
acids (Wong, 1975, 1988), these latter were attributed
with codons in the genetic code in such a way that
physicochemically similar amino acids were assigned
to the same code column. However, if we assume that
the observations regarding a relationship between the
physicochemical properties of amino acids and those
of anticodons are true (Weber and Lacey, 1978; Jungck,
1978), then we introduce constraints that generate difficulties, which require explanations (Di Giulio, 1997b).
If the allocations of amino acids in the genetic code
stem primarily from the biosynthetic relationships between amino acids as predicted by the coevolution theory (Wong, 1975), then the initial attribution of codon
domains to the precursor amino acids implies that the
assignment of codons to product amino acids was entirely defined prior to their biosynthetic appearance.
Thus, we have to explain how the physicochemical correlations between the product amino acids and their anticodons (or codons) (Weber and Lacey, 1978; Jungck,
1978; Di Giulio, 1992, 1996, 1997) with the observation that these latter were assigned before the biosynthetic appearance of product amino acids (Di Giulio,
1997). It is clear that the mechanism of codon
concession from the precursors to the products
creates difficulties because the evolving product
amino acids took pre-assigned codons, and moreover physicochemical correlations between product
amino acids and anticodons (or codons) must be
true.
To solve this difficulty, the hypothesis of the coevolution between the origin of anticodons (and/or codons)
and the evolution of amino acids was suggested (Di
Giulio, 1998). If the organization of the genetic code
was defined by: (1) the biosynthetic relationships between amino acids and (2) the anticodon–amino acid
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M. Di Giulio / BioSystems 80 (2005) 175–184
interactions, then it is reasonable to assume that there
might have been a coevolution between the origin of
anticodons and the biosynthetic pathways of amino
acids in such a way that the anticodons came into
contact with the amino acids on RNA hairpin structures (Hopfield, 1978; Di Giulio, 1992, 1994, 1995,
1996; Shimizu, 1995). (In a model of the origin of the
tRNA molecule the anticodons/codons are in the stems
of hairpin structures near the amino acid attachment
site (Di Giulio, 1992, 1995)). The coevolution theory
claims that the codon domains of the precursor amino
acids must have been pre-assigned so as to ensure the
contiguity of the amino acids in precursor–product relationships (Wong, 1975). Thus, it becomes easier to
explain why the physicochemical properties of amino
acids are reflected in the genetic code together with the
observation that the biosynthetic relationships of amino
acids are also reflected, and that these two forces did
not act independently (Di Giulio, 1992, 1996, 1997b).
In fact, we need to simply postulate that the evolving
anticodons still belonging to the precursor amino acids
played an active role in selecting the emergent product
amino acids. For instance, in the biosynthetic transformation Glu → Pro, only when an amino acid (Pro)
capable of physicochemical interaction with the anticodons NGG developed, did the process of exploring
the products of Glu terminate as far as these anticodons
are concerned. Therefore, this model (Di Giulio, 1998)
considers that the product amino acids were not at
all specified in the early phase of genetic code origin
(Wong, 1975) and whereas their selection did indeed
depend on anticodons, it was also determined by the
history of the biosynthetic relationships between amino
acids.
This model (Di Giulio, 1998) which thus sees the
evolving anticodons playing an active role in the selection of the product amino acid as it affects and addresses
the biosynthetic transformations of the precursor amino
acid, makes compatible the coevolution theory (Wong,
1975) with the stereochemical theory (Woese, 1967)
and part of the physicochemical theory (Weber and
Lacey, 1978; Jungck, 1978; Lacey and Mullins, 1983;
Lacey et al., 1992).
Finally, although this model (Di Giulio, 1998)
makes compatible the theories of the origin of the genetic code, nevertheless I believe that the coevolution
theory and the stereochemical theory are incompatible since these are based on a different determinism:
historical the former, physicochemical the later.
6. Why was a given number of synonymous
codons attributed to the amino acids in the
genetic code?
In the genetic code table, we have to explain why
various amino acids are codified by a different number
of synonymous codons.
A negative correlation it has been repeatedly observed between the number of codons specifying for
Fig. 1. Relation between the number of codons attributed to amino acids in the genetic code and the molecular weight of amino acids (Hasegawa
and Miyata, 1980; Di Giulio, 1989a; Taylor and Coates, 1989; Dufton, 1997).
M. Di Giulio / BioSystems 80 (2005) 175–184
amino acids in the genetic code and the ‘size’ of amino
acids (Hasegawa and Miyata, 1980; Di Giulio, 1989a;
Taylor and Coates, 1989; Dufton, 1997). For instance,
there is a negative correlation between the number of
codons and the molecular weight of amino acids (Fig. 1;
Hasegawa and Miyata, 1980; Di Giulio, 1989a; Taylor
and Coates, 1989).
If arginine, which seems subject to particular selective constraints in mesophiles (Jukes, 1978), is eliminated from this correlation (Fig. 1) we obtain an increase in the significance (Di Giulio, 1989a). Therefore, for arginine this correlation is not true but, in fact,
it is true the inverse. It is likely that arginine has a
large number of synonymous in the genetic code as
this amino acid has the highest thermophily rank (Di
Giulio, 2000a–d), and under the hypothesis of a hot origin of life there was a selective advantage to attribute
six codons to arginine (Di Giulio, 2000a–d). Furthermore, Di Giulio (in press) have observed that there is
a statistically significant positive correlation between
the number of codons attributed to amino acids in the
genetic code and the values of the hydrostatic pressure
asymmetry index (PAI) of amino acids (i.e. a measurement of barophilicity of amino acids) (Di Giulio, in
press). In other words, the more barophilic amino acids
have, on average, a larger number of codons compared
to amino acids less used in barophiles (Di Giulio, in
press). Therefore, the significant and negative correlation between the number of codons and the molecular weight of amino acids (Fig. 1) seems to be nothing other than a expression of barophily by means of
the negative correlation between the pressure asymmetry index (PAI) of amino acids with the molecular
weight of amino acids (Di Giulio, in press). This is
because these two latter correlations would imply the
observed positive correlation between the number of
codons and the PAI values (Di Giulio, in press). The
high hydrostatic pressure was probably the main selective strength making the genetic code attribute a
given number of codons to amino acids (Di Giulio,
in press), and in particular, making it attribute, on average, more codons to the ‘smaller’ amino acids, i.e.
the more barophilic ones (Di Giulio, in press). While,
the molecular weight, i.e. the ‘size’ of amino acids
was probably the property on which natural selection acted to favour the construction of proteins that
were simply more stable at high hydrostatic pressure
(Di Giulio, in press).
181
7. Synthesis: the coevolution theory and the
ancestral metabolism
The coevolution theory of the origin of the genetic code identifies a tRNA-like molecule as a device through which precursor amino acids ceded part
or all of their codons to the product amino acids derived
from the former (Wong, 1975; Wachtershauser, 1988;
de Duve, 1991; Danchin, 1989; Di Giulio, 1994b).
This perhaps suggests that the ancestral metabolism
of amino acids took place on tRNA-like molecules.
However, there is no a priori reason why this should
have been limited only to amino acid metabolism. Evidently, the coevolution theory would seem to imply
that whole primitive metabolism took place on tRNAlike molecule (Di Giulio, 1994b). In actual fact, this
generalization of the coevolution theory (Di Giulio,
1994b) has also been suggested following completely
different arguments (Tyagi, 1981; Crothers, 1982;
Cedergren and Grosjean, 1987; Edwards, 1989;
Gibson and Lamond, 1990; Lamond and Gibson, 1990;
Szathmary, 1999). Therefore, the mechanism on which
the coevolution theory is based might be a manifestation of a much more general bond between ancestral
metabolism and tRNA-like molecules (Danchin, 1989).
Moreover, this link is assumed to have remained visible
in the correspondence between the biosynthetic pathways of amino acids and the structure of the genetic
code. And this makes sense as it is expected, more generally, that there should be a close link between the origin of metabolism itself and RNAs, that is, replication.
Acknowledgements
This work was carried out at the MCD Biology department of the University of Colorado at Boulder and
was supported by the NIH and NASA under Grant nos.
GM48080 and NCC21052, respectively, given to Dr.
M. Yarus. I thanks M. Buvoli for his ‘tautological advices’, I. de Zwart, M. Illangasekare, T. Janas, T. Janas,
M. Legiewicz, I. Majerfeld, and M. Yarus for useful
discussions and help.
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