Intron Position as an Evolutionary Marker of Thioredoxins and
Thioredoxin Domains
Mariam Sahrawy,
1
Vale ´rie Hecht,
2
Javier Lopez-Jaramillo,
1
Ana Chueca,
1
Yvette Chartier,
2
Yves Meyer
2
1
Department of Plant Biochemistry, Estacion Experimental del Zaidin, Consejo Superior de Investigaciones, Cientificas, Professor Alberada 1,
18008-Granada, Spain
2
Laboratoire de Physiologie et Biologie Mole ´culaire des Plantes, Universite ´/Centre National de la Recherche Scientifique URA, 565 Avenue
de Villeneuve, 66860 Perpignan, Cedex, France
Received: 14 September 1995 / Accepted: 4 November 1995
Abstract. In contrast to prokaryotes, which typically
possess one thioredoxin gene per genome, three different
thioredoxin types have been described in higher plants.
All are encoded by nuclear genes, but thioredoxins m and
f are chloroplastic while thioredoxins h have no transit
peptide and are probably cytoplasmic. We have cloned
and sequenced Arabidopsis thaliana genomic fragments
encoding the five previously described thioredoxins h, as
well as a sixth gene encoding a new thioredoxin h. In
spite of the high divergence of the sequences, five of
them possess two introns at positions identical to the
previously sequenced tobacco thioredoxin h gene, while
a single one has only the first intron. The recently pub-
lished sequence of Chlamydomonas thioredoxin h shows
three introns, two at the same positions as in higher
plants. This strongly suggests a common origin for all
cytoplasmic thioredoxins of plants and green algae. In
addition, we have cloned and sequenced pea DNA ge-
nomic fragments encoding thioredoxins m and f. The
thioredoxin m sequence shows only one intron between
the regions encoding the transit peptide and the mature
protein, supporting the prokaryotic origin of this se-
quence and suggesting that its association with the transit
peptide has been facilitated by exon shuffling. In con-
trast, the thioredoxin f sequence shows two introns, one
at the same position as an intron in various plant and
animal thioredoxins and the second at the same position
as an intron in thioredoxin domains of disulfide isomer-
ases. This strongly supports the hypothesis of a eukary-
otic origin for chloroplastic thioredoxin f.
Key words: Thioredoxins — Introns — Phylogeny
Introduction
Thioredoxins are proteins (approximately 100–120
amino acids) implicated in various oxidoreductive reac-
tions. They contain an active site with the conserved
dicysteine sequence of WCxxC able to form a disulfide
bridge in the oxidized state (Holmgren 1985). Thiore-
doxins have been characterized in all pro- and eukary-
otes. It is generally assumed that thioredoxins are disul-
fide reductases able to break disulfide bridges of target
proteins, but they may function to a lesser extent in the
opposite way, promoting disulfide bridge formation, at
least in vitro. Prokaryotes and vertebrates typically pos-
sess only one thioredoxin gene per genome, while fungi
contain multiple but closely related thioredoxins. The
situation is far more complex in higher plants where
three different thioredoxin types have been character-
ized. Thioredoxins h have no transit peptide (Marty and
Meyer 1991) and are consequently assumed to be cyto-
plasmic; nevertheless a rice thioredoxin h has been de-
tected as a major phloem sap protein (Ishiwatari et al.
1995). We have recently shown that Arabidopsis
thaliana encodes at least five different thioredoxins of Correspondence to: Y. Meyer
J Mol Evol (1996) 42:422–431
© Springer-Verlag New York Inc. 1996