Ruiz et al. 2017). Based on these results it was proposed that the NTRC-dependent
redox balance of 2-Cys PRX modulates the redox state of the pool of plastid TRX
and, consequently, the redox regulation of the TRX targets. These results provide an
explanation for the indirect participation of NTRC in the redox regulation of the
TRX-dependent processes of the chloroplast.
3 The Extraplastidial Thioredoxin Systems
While functions of chloroplastic TRX have been extensively studied, extraplastidial
TRX systems are much less characterized in plants. Among the around 40 TRX
found in Arabidopsis, at least 20 of them are extraplastidial isoforms, based on the
absence of a putative plastidial targeting sequence (Meyer et al. 2005, 2012).
However, for some of them, the respective localization is still unexplored. It is
now clearly established that functional TRX systems are present in most cellular
compartments, including mitochondria, cytosol, nucleus, and endomembrane systems (see Fig. 4). In contrast to the large number of extraplastidial TRX, only two
NTR genes (NTRA and NTRB in Arabidopsis) are found in the genome of most
higher plants, suggesting multiple subcellular localizations of these isoforms. Consistently, NTR isoforms were found dual or even triple targeted in cytosol, mitochondria, and nucleus in Arabidopsis and pea (Laloi et al. 2001; Serrato and Cejudo
2003; Reichheld et al. 2005; Marchal et al. 2014).
3.1 Cytosolic Thioredoxin System
Cytosolic TRX are composed of h-type (h for heterotrophic) and other type TRX.
TRXh isoforms have been mostly characterized in Arabidopsis but orthologues are
found in other plants including rice and poplar (Meyer et al. 2006). All TRXh
isoforms consist of a single TRX domain harboring a WCG(P)C active site and,
according to their respective clustering on phylogenetic trees, have been divided into
three different subtypes (I, II, III). TRX from type I (TRXh1, h3, h4, h5) are mainly
cytosolic and typically reduced by NTR (Rivera-Madrid et al. 1995). Type II (h2, h7,
h8) and type III (h9, h10, atypical CxxS1 and 2) TRXh are less characterized
isoforms. While predominantly located in the cytosol, TRXh2, h8, and h9 are also
located in the endomembrane system, presumably through the fact that they harbor
myristoylated/palmitoylated residues in their N-terminal extensions (see below)
(Traverso et al. 2013). Remarkably, while generally reduced by NTR, some TRXh
isoforms are also reduced by the alternative thiol reduction systems glutathione
(GSH)/glutaredoxin (GRX) (Gelhaye et al. 2003; Reichheld et al. 2007; Koh et al.
2008; Meng et al. 2010). For example, in Arabidopsis and poplar, TRXh9 is reduced
through a disulfide cascade mechanism involving the transient glutathionylation of a
Cys located in the N-terminal extension of TRXh9 (Koh et al. 2008).
On the Elaborate Network of Thioredoxins in Higher Plants
239
redox balance of 2-Cys PRX modulates the redox state of the pool of plastid TRX
and, consequently, the redox regulation of the TRX targets. These results provide an
explanation for the indirect participation of NTRC in the redox regulation of the
TRX-dependent processes of the chloroplast.
3 The Extraplastidial Thioredoxin Systems
While functions of chloroplastic TRX have been extensively studied, extraplastidial
TRX systems are much less characterized in plants. Among the around 40 TRX
found in Arabidopsis, at least 20 of them are extraplastidial isoforms, based on the
absence of a putative plastidial targeting sequence (Meyer et al. 2005, 2012).
However, for some of them, the respective localization is still unexplored. It is
now clearly established that functional TRX systems are present in most cellular
compartments, including mitochondria, cytosol, nucleus, and endomembrane systems (see Fig. 4). In contrast to the large number of extraplastidial TRX, only two
NTR genes (NTRA and NTRB in Arabidopsis) are found in the genome of most
higher plants, suggesting multiple subcellular localizations of these isoforms. Consistently, NTR isoforms were found dual or even triple targeted in cytosol, mitochondria, and nucleus in Arabidopsis and pea (Laloi et al. 2001; Serrato and Cejudo
2003; Reichheld et al. 2005; Marchal et al. 2014).
3.1 Cytosolic Thioredoxin System
Cytosolic TRX are composed of h-type (h for heterotrophic) and other type TRX.
TRXh isoforms have been mostly characterized in Arabidopsis but orthologues are
found in other plants including rice and poplar (Meyer et al. 2006). All TRXh
isoforms consist of a single TRX domain harboring a WCG(P)C active site and,
according to their respective clustering on phylogenetic trees, have been divided into
three different subtypes (I, II, III). TRX from type I (TRXh1, h3, h4, h5) are mainly
cytosolic and typically reduced by NTR (Rivera-Madrid et al. 1995). Type II (h2, h7,
h8) and type III (h9, h10, atypical CxxS1 and 2) TRXh are less characterized
isoforms. While predominantly located in the cytosol, TRXh2, h8, and h9 are also
located in the endomembrane system, presumably through the fact that they harbor
myristoylated/palmitoylated residues in their N-terminal extensions (see below)
(Traverso et al. 2013). Remarkably, while generally reduced by NTR, some TRXh
isoforms are also reduced by the alternative thiol reduction systems glutathione
(GSH)/glutaredoxin (GRX) (Gelhaye et al. 2003; Reichheld et al. 2007; Koh et al.
2008; Meng et al. 2010). For example, in Arabidopsis and poplar, TRXh9 is reduced
through a disulfide cascade mechanism involving the transient glutathionylation of a
Cys located in the N-terminal extension of TRXh9 (Koh et al. 2008).
On the Elaborate Network of Thioredoxins in Higher Plants
239