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Evolutionary significance of RNA-containing enzymes

Will Fischer wfischer at bio.indiana.edu
Tue Oct 11 11:24:30 EST 1994


Dale R. Worley (drw at taylor.mit.edu) wrote:
: According to the dogma du jour, the progenote (last common ancestor of
: all surviving living things) used DNA as its genetic material and
: proteins for most of its catalytic agents.  That suggests that all
: surviving RNA-containing catalytic agents have pre-progenote origins.
: In particular, the intron splicing systems seem to all involve
: ribozymes, thus suggesting that introns were present in the progenote.

: On the other hand, both the eubacteria and the archaebacteria lack
: introns, whereas the eukaryotes have introns, which would suggest that
: introns arose only in the early ancestors of the eukaryotes.

: Does anybody have a fix on the current thinking in these areas?

BIAS ALERT:  I work in Jeff Palmer's lab, and think introns are recent.
	I think most "current thinking" (and certainly most current
	evidence) is on our side.

First things first:  you have to distinguish between group I & II
self-splicing introns (which are present in some bacteria, archaes, and
phage) and eukaryotic spliceosomal introns.  The former are clearly
pretty old (~ 3.5 BY), but the antiquity of the latter is hotly debated.  
In the following, I'm talking about spliceosomal introns.

The introns-early hypothesis essentially means exons-early:  the idea is
that primordial genes were assembled from shuffled exons, and that
introns developed from the stuff that was in-between exons.  This is the
view in the textbooks (e.g. Watson et al. Mol. Biol. of the Gene).
Some eukaryotic genes have clearly been assembled by exon shuffling, but
there's little evidence for this happening very early (i.e. at the
progenote stage).  A recent attempt to test the exon theory of genes
(Stoltzfus et al. 1994) found no significant correspondence between
protein domains and intron position in several paradigm cases.

Cavalier-Smith suggested in 1991 that spliceosomal introns are derived
from self-splicing introns that came into the cell in the genome of the
proto-mitochondrion.  This neatly explains the absence of spliceosomal
introns in primitively amitochondrial eukaryotes and
{archae,eu}bacteria.  Palmer and Logsdon (1991) used this phylogenetic
distribution to argue the same case, that introns "were inserted late
in eukaryotic evolution into pre-formed genes".  Following
Cavalier-Smith's proposal, some work has been done on mapping the RNA
components of the spliceosome onto the conserved domains of group II
self-splicing introns.

Note that "late" in this context means about a billion years ago
The controversy continues (see Hurst's News&Views in the Sept_29
Nature), but parsimony is on the side of the introns-late advocates.

-- WF

Recent References:

Introns-late:

T. Cavalier-Smith (1991) Intron phylogeny:  a new hypothesis.  
	Trends in Genetics 7,145-148.

W.F. Doolittle and A. Stoltzfus (1993)  Genes-in-pieces revisited.
	Nature 361, 403.  (News&Views re: Tittiger et al. 1993)

J.D. Palmer & J.M. Logsdon, Jr. (1991)  The recent origins of introns.
	Current Opinion in Genetics and Development 1, 470-477.

A. Stoltzfus, D.F. Spencer, M. Zuker, J.M. Logsdon,Jr. and W.F. Doolittle
	(1994)  Testing the exon theory of genes:  The evidence from
	protein structure.  Science 265, 202-207 (8 July 1994).

Introns-early:

R. Kersanach et al. (1994) Nature 367, 387-389.  (But see the related
	correspondence in Nature 369, 526-528 (16 June 1994).)

C. Tittiger, S. Whyard and V.K. Walker (1993)  A novel intron site in
the triosephosphate isomerase gene from the mosquito Culex tarsalis.
Nature 361, 470-472.

Undecided-but-leaning-towards-introns-early:

L.D. Hurst (1994) The uncertain origin of introns.  Nature 371, 381-382.
	(29 September 1994; News & Views review of the August CIAR meeting
	in Halifax)

____________________________________________________________
Will Fischer				wfischer at indiana.edu

Department of Biology                   Voice:  812-855-2549
Jordan Hall                             Voice2: 812-333-2433
Indiana University                      FAX:    812-333-7922
Bloomington, Indiana 47405 USA          FAX2:   812-855-6705



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