Molecular Plant Advance Access published November 2, 2008
Molecular Plant
•
Pages 1–16, 2008
Protein-Repairing Methionine Sulfoxide
Reductases in Photosynthetic Organisms: Gene
Organization, Reduction Mechanisms, and
Physiological Roles
Lionel Tarrago, Edith Laugier and Pascal Rey1
ABSTRACT Methionine oxidation to methionine sulfoxide (MetSO) is reversed by two types of methionine sulfoxide reductases (MSRs), A and B, specific to the S- and R-diastereomers of MetSO, respectively. MSR genes are found in most organisms
from bacteria to human. In the current review, we first compare the organization of the MSR gene families in photosynthetic
organisms from cyanobacteria to higher plants. The analysis reveals that MSRs constitute complex families in higher plants,
bryophytes, and algae compared to cyanobacteria and all non-photosynthetic organisms. We also perform a classification,
based on gene number and structure, position of redox-active cysteines and predicted sub-cellular localization. The various
catalytic mechanisms and potential physiological electron donors involved in the regeneration of MSR activity are then described. Data available from higher plants reveal that MSRs fulfill an essential physiological function during environmental
constraints through a role in protein repair and in protection against oxidative damage. Taking into consideration the expression patterns of MSR genes in plants and the known roles of these genes in non-photosynthetic cells, other functions of
MSRs are discussed during specific developmental stages and ageing in photosynthetic organisms.
Key words:
Genome; methionine; methionine sulfoxide reductase; oxidation; photosynthetic organisms; protein repair.
INTRODUCTION
Oxidative modification to amino acids in their lateral chain
leads to changes in activity and conformation for many proteins (Davies, 2005). Sulfur-containing residues are the most
susceptible to oxidative damage due to their high reactivity
with reactive oxygen species (ROS). Cysteines can be engaged
in disulfide bridges or oxidized to sulfenic or sulfinic forms,
and methionine can be oxidized to methionine sulfoxide
(MetSO). However, most of these modifications are reversible
through the action of thiol reductases. While oxidized forms
of cysteine are reduced by thioredoxins, glutaredoxins, and
sulfiredoxin, methionine sulfoxide is reduced back to methionine by methionine sulfoxide reductases (MSRs) through
redox-active cysteines (Davies, 2005).
Most organisms possess two types of MSRs, A and B, that
display an absolute specificity towards the two S- and R-MetSO
diastereoisomers, respectively, but do not share any sequence
or structure similarity (Brot et al., 1981; Grimaud et al., 2001;
Lowther et al., 2002). Both types are required for maintaining
basal levels of MetSO, since oxidation of Met leads to a racemic
mixture of isomers. Most MSRAs and MSRBs possess two redox-
active cysteines and function generally using a similar threestep catalytic mechanism that involves the formation of a cysteine sulfenic acid intermediate, the subsequent formation of
a disulfide bond and, lastly, the regeneration of reduced MSR
by a reducing system, generally thioredoxin (Trx) (BoschiMuller et al., 2000; Lowther et al., 2000; Kumar et al., 2002;
Olry et al., 2002; Rouhier et al., 2007). Note some MSRB proteins, present in most organisms, lack the second resolving cysteine and are reduced through a different mechanism (Sagher
et al., 2006a, 2006b; Vieira Dos Santos et al., 2007; Kim and
Kim, 2008).
MSR proteins fulfill essential functions in stress tolerance
and during ageing in bacterial, yeast, and mammal cells. In
1
To whom correspondence should be addressed. E-mail [email protected],
fax 33 4 42 25 62 65, tel. 33 4 42 25 47 76.
ª The Author 2008. Published by the Molecular Plant Shanghai Editorial
Office in association with Oxford University Press on behalf of CSPP and
IPPE, SIBS, CAS.
doi: 10.1093/mp/ssn067
Received 23 July 2008; accepted 12 September 2008
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
CEA, DSV, IBEB, Laboratoire d’Ecophysiologie Moléculaire des Plantes, Bâtiment 161, SBVME, CEA-Cadarache, 13108 Saint-Paul-lez-Durance, Cedex, France
2
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Tarrago et al.
d
MSR Proteins in Photosynthetic Organisms
RESULTS
Organization of MSR Gene Families in Photosynthetic
Organisms and Comparison with Non-Photosynthetic
Organisms
We performed a systematic search of MSR genes in the sequenced genome data available, particularly those of photosynthetic organisms for which MSRs were not indexed: Vitis
vinifera, Physcomitrella patens, algae, and cyanobacteria.
Table 1 shows the number of MSR genes in various living
organisms. Compared to mammals, yeast, and E. coli, which
possess generally two to four MSR genes, eukaryotic photosynthetic organisms display more complex families. Thus, higher
plants, such as Arabidopsis and rice, and the moss Physcomitrella patens possess 14, 6, and 8 MSR genes, respectively,
and six to eight MSR genes are present in the genome of
the three algae, for which data are available. With regard
to the cyanobacterial kingdom, in which the genome of many
species has been sequenced, MSR families are much more simple, with generally three genes present in the 20 species that
we have analyzed (Table 1 and data not shown). One striking
observation arising from Table 1 is the absence of MSR with
a catalytic selenocysteine (Sec) instead of a Cys in all photosynthetic organisms, except for one MSRA type in algae. Note that
Sec MSRBs are present only in mammals (Table 1).
Regarding MSRAs, non-photosynthetic organisms possess
only one gene whereas all photosynthetic organisms have
at least two genes. The bacterial MSRA gene is present as
a whole transcription unit or in an operon fused to the MSRB
coding sequence. As shown in Neisseria meningitidis, MSRA
can be also included in a trimodular gene coding for Trx,
MSRA, and MSRB domains (Ezraty et al., 2005; Wu et al.,
Table 1. Number of MSRA and MSRB Genes in Various Photosynthetic and Non-Photosynthetic Organisms.
MSRA
Kingdom
Sec
Cys
Arabidopsis thaliana
–
Populus trichocarpa
–
Vitis vinifera
Photosynthetic
Oryza sativa
eukaryotes
Physcomitrella patens
Chlamydomonas reinhardtii
Ostreococcus lucimarinus
Photosynthetic prokaryotes
Non-photosynthetic eukaryotes
Non-photosynthetic prokaryote
Organism
MSRB
Sec
1-Cys
2-Cys
5*
–
1
8
5
–
1
3
–
3
–
1
2
–
4
–
1*
2
–
5
–
1
2
1
4
–
1
2
1
2
–
2
1
Ostreococcus tauri
1
3
–
2
1
Anabaena sp. PCC 7120
–
2
–
1
–
Synechocystis sp. PCC 6803
–
2
–
1
–
Synechococcus sp. CC9311
–
2
–
2
–
Homo sapiens
–
1*
1
2**
–
Drosophila melanogaster
–
1*
–
–
1*
Saccharomyces cerevisiae
–
1
–
–
1
Escherichia coli
–
1
–
–
1
Asterisk (*) indicates possible alternative splicing for one gene. Sec and Cys indicate genes encoding selenocysteine-containing and cysteinecontaining enzymes, respectively.
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
yeast, deletion and overexpression of MSRA gene result in reduced and increased viability, respectively (Koc et al., 2004).
Deletion of MSRB does not noticeably affect yeast life span,
but strains deficient for both MSRA and MSRB exhibit a greater
reduction in viability compared to MSRA-deficient strains,
demonstrating the essential role of the two MSR types. In
mammal cells, the abundance of MSRs decreases upon ageing
(Petropoulos et al., 2001; Picot et al., 2004) and diseases
(Gabbita et al., 1999). Modifying the expression of MSRA genes
revealed their participation in the responses to oxidative stress
(Moskovitz et al., 1998; Ruan et al., 2002). Very recently, overexpression of human mitochondrial MSRB2 has been reported
to protect lymphoblastic leukemia cells from protein damage
and to increase cell survival under oxidative stress (Cabreiro
et al., 2008). Altogether, these studies demonstrate that MSRs
are key components in the control of oxidative damage associated with the development of disorders and the process of
ageing.
With regard to photosynthetic organisms, the first report
providing evidence for MSR activity was published in the eighties by Sanchez et al. (1983), who found that the activity was
mostly localized in chloroplast extracts from various higher
plants. The molecular identification and characterization of
MSR enzymes have been performed much later, revealing
the complexity of MSR gene families in higher plants compared to other organisms (Rouhier et al., 2006). In this review,
we analyze the MSR gene families in photosynthetic organisms
from cyanobacteria to higher plants by performing a comparison of the number of genes and of their sequence features.
Then, we focus on the characteristics and specificities of MSRs
in photosynthetic cells with regard to their regeneration
mechanisms and physiological functions.
Tarrago et al.
MSRA Gene Families in Photosynthetic Organisms
The model plant, Arabidopsis thaliana, possesses five MSRA
genes, with a putative alternative splicing for AtMSRA5
(Table 2). AtMSRA1 to AtMSRA3 are predicted to be located
in cytosol, AtMSRA4 is plastidial (Romero et al., 2004), and
AtMSRA5.1 and 5.2 could be routed to endoplasmic reticulum
or secretory pathway. In other higher plants, the organization of MSRA genes appears somewhat less complex, with
only three types represented based on the similarity with
Arabidopsis genes. Each type generally possesses a proper predicted sub-cellular localization: cytosol, plastid, or endoplasmic
reticulum. Populus trichocarpa possesses five MSRA genes, two
pairs of them being closely related: PtMSRA2.1 and PtMSRA2.2,
PtMSRA4.1 and PtMSRA4.2, and PtMSRA5. Analysis of Oryza
sativa genome reveals the presence of four genes, with one being possibly alternatively spliced (Table 2) and the search in the
first release of the Sorghum bicolor genome allowed also four
MSRA genes to be found (Supplemental Text File 3). Analyzing
the Vitis vinifera genome, we identified three genes, named
VvMSRA3, VvMSRA4, and VvMSRA5. The search in Physcomitrella patens genome indicates that the moss possesses five
MSRA genes, PpMSRA4.1 and PpMSRA4.2 producing cytosolic
proteins, PpMSRA3 and PpMSRA4.3 encoding plastidial
enzymes, and PpMSRA5 encoding a predicted mitochondrial
MSR Proteins in Photosynthetic Organisms
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3
product. Since identification of MSRA genes in Chlamydomonas reinhardtii has been previously performed by V. Gladyshev’s
team (Novoselov et al., 2002; Table 3) and due to the very peculiar characteristics displayed for some of them, we conserved
for green algae MSRA genes this nomenclature, which does not
correspond to that used above. Note that the identified MSRA
genes in Ostreococcus lucimarinus and Ostreococcus tauri
genomes were named in step with Chlamydomonas genes.
The three green algae possess one cytosolic selenocysteinecontaining MSRA protein, named CrMSRA1 (Novoselov
et al., 2002), OlMSRA1, and OtMSRA1. C. reinhardtii genome
contains four other MSRA genes: CrMSRA2, CrMSRA3, and
CrMSRA4 encoding proteins predicted to be mitochondrial,
and CrMSRA5, a protein likely plastidial. O. lucimarinus and
O. tauri genomes possess two and three other MSRA genes,
respectively (Table 3). Note that the predicted sub-cellular
localization of green algae’s genes should be considered
very carefully, the plastidial enzymes being often predicted
to be addressed to mitochondrion (Dr S. Lemaire, personal
communication).
All cyanobacteria possess two MSRA genes (Table 4 and data
not shown), except Thermosynechococcus elongatus BP-1,
which has only one gene, and Chlorobium tepidium TLS, for
which the unique MSRA enzyme is encoded as a part of a bimodular protein including also one MSRB domain (data not shown).
On the basis of sequence alignment (Supplemental Figure
1), we constructed an unrooted phylogenetic tree that allowed
separation of most MSRAs of photosynthetic organisms in six
groups (Figure 1). MSRAs from higher plants are distributed in
two distinct groups; the first contains cytosolic and plastidic
MSRA1 to MSRA4, sharing 53–93% similarity, and the second
includes MSRA5 isoforms, for which the overall similarity
ranges from 43 to 67%. Proteins of the two groups share only
15–36% similarity. Intron/exon structure is also highly conserved in the genes forming the two groups. Indeed, MSRA1
to MSRA4 genes possess two exons, and MSRA5 genes display
four exons, except PpMSRA5, which has no intron (Table 2).
PpMSRA4.2, which possess three exons, can be included neither in this group, nor in the closest group to that including
most higher plant MSRAs and containing also Chlamydomonas
MSRA3 and MSRA4 proteins. The other MSRA proteins of
green algae and cyanobacteria constitute three groups. In
the first, Ostreococcus MSRA3 and MSRA4 proteins are clustered with one isoform from the cyanobacteria Anabaena
sp. PCC 7120, Synechococcus sp. CC9311, and Synechocystis
sp. PCC 6803. Proteins of this group share 23–75% overall similarity. Except the second MSRA of Anabaena sp. PCC 7120,
other cyanobacteria MSRAs form one group with CrMSRA2,
CrMSRA5, and O. tauri and O. lucimarinus MSRA2s, in which
global similarity ranges from 21 to 41%. The last group of
MSRAs is constituted by selenocysteine-containing proteins,
which share 43–68% similarity, and are present only in green
algae. Evolutionary analyses suggest an independent loss of
selenoproteins in higher plants, cyanobacteria, yeast, and
some mammals (Novoselov et al., 2002). The sequence
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
2005). It is worth mentioning that, in several eukaryotic nonphotosynthetic organisms, the unique MSRA gene is expressed
as three distinct transcripts, allowing sub-cellular localization
in mitochondrion, nucleus, and cytosol (Kim and Gladyshev,
2006).
In the case of MSRBs, we propose to distinguish two types,
the 1-Cys type and the 2-Cys type, which display one or two
redox-active cysteines, respectively (Table 1). Similarly to
MSRA genes, non-photosynthetic organisms, but also cyanobacteria, possess a reduced number of MSRB genes compared
to photosynthetic eukaryotes. Indeed, most prokaryote
genomes contain only one MSRB gene (Delaye et al., 2007).
Saccharomyces cerevisiae and Drosophila melanogaster
possess also one MSRB gene, the fruit fly gene being alternatively spliced allowing addressing the protein to cytosol and
mitochondrion (Kim and Gladyshev, 2006). Mammals possess
three MSRB genes, one coding for a selenocysteine-containing
enzyme (MSRB1) and two for cysteine-containing MSRBs
(MSRB2 and MSRB3). N-terminal and C-terminal extensions
in MSRB3, resulting from alternative splicing, allow protein
repartition in most sub-cellular compartments (Kim and
Gladyshev, 2006).
Compared to non-photosynthetic eukaryotes, fewer MSR
genes could be processed through alternative splicing in photosynthetic eukaryotes. In these organisms, which display complex MSR gene families, the distribution of MSR isoforms in the
various sub-cellular compartments likely originates from products encoded by distinct genes. In animal cells, alternative
splicing would allow the production of distinct MSR isoforms
and their distribution among cell compartments.
d
4
Table 2. Description of MSRA Genes and Proteins in A. thaliana, O. sativa, P. trichocarpa, P. patens, and V. vinifera.
|
Cytosol (2)
C44 C194 C200
Q9LY15
218
Cytosol (3)
C60 C210 C216
Q9LY14
202
Cytosol (3)
C44 C194 C200
2
P54150
258
Plastide
C100 C250 C256
1555
4
Q9SL43
254
ER / SP (2)
C71 C228
1588
3
Q3E7T3
192
ER / SP (2)
C71
4
2056
2
NP_001053116
187
Cytosol (2)
C34 C179 C185
Os04g40620
4
833
2
Q7XUP6
190
Cytosol (1)
C37 C182
MSRA4.1
Os10g41400.1
10
2489
2
NP_001065403
263
Plastid (4)
C105 C255 C261
MSRA4.2
Os10g41400.2
10
1656
1
ABB47990
211
Plastid (4)
C105
2189
4
NP_001056737
254
ER / SP (2)
C71 C228
614
2
422117 (AAS46231)
190
Cytosol (1)
C31 C182 C188f
Chromosomea,b
Arabidopsis thaliana
MSRA1
At5g61640
5
1356
2
Q9FKF7
MSRA2
At5g07460
5
1380
2
MSRA3
At5g07470
5
1805
2
MSRA4
At4g25130
4
1474
MSRA5.1
At2g18030.1
2
MSRA5.2
At2g18030.2
2
MSRA2.1
Os04g40600
MSRA2.2
Oryza sativa
Populus trichocarpa
Vitis vinifera
Physcomitrella
patens ssp. patens
Gene (bp)
Number
of exons
Protein
accession number
Number of
amino acids
MSRA5
Os06g04650
6
MSRA2.1
gw1.XII.577.1
LG XII
MSRA2.2
gw1.XV.1862.1
LG XV
603
2
252426 (AAS46231)
190
Cytosol (2)
C31 C182 C188
MSRA4.1
estExt_fgenesh4_pg.C_LG_XV0857
LG XV
2279
2
824833 (AAS46232)
264
Plastid (1)
C104 C256 C260f
MSRA4.2
estExt_Genewise1_v1.C_2320013
Scaffold 232
2311
2
746976 (AAS46232)
262
Plastid (1)
C104 C256 C260
MSRA5
grail3.0019030401
LG VII
2641
4
ABK96610
252
ER / SP (1)
C59 C69 C226
MSRA3
GSVIVT00014205001
16
7855
2
CAO62325
254
Plastid (1)
C96 C246 C252
MSRA4
GSVIVT00015923001
17
1596
2
CAO64197
190
Cytosol (2)
C31 C182 C188
MSRA5
GSVIVT00036803001
4
12 939
4
CAO48234
252
ER / SP (5)
C69 C226
MSRA3
e_gw1.97.9.1
Scaffold 97
1301
3
ABK95276
267
Plastid (3)
C109 C259 C265
MSRA4.2
estExt_fgenesh1_pm.C_950004
Scaffold 95
1172
3
XP_001767588
168
Cytosol (ND)g
C11 C160 C166
MSRA4.1
estExt_fgenesh1_pg.C_3040009
Scaffold 304
2028
3
XP_001781486
205
Cytosol (3)
C47 C197 C203
MSRA4.3
estExt_fgenesh1_pm.C_4470004
Scaffold 447
2120
3
NP_001056737
272
Plastid (1)
C114 C264 C270
MSRA5
estExt_gwp_gw1.C_1740036
Scaffold 174
939
1
XP_001767815
208
Mitochondrion (4)
C23 C180
Gene accession numbers are from TAIR for A. thaliana, JGI for P. trichocarpa, and P. patens, TIGR for O. sativa, and Genoscope for V. vinifera.
a Chromosomes of P. trichocarpa are designed by Linkage Group (LG).
b P. patens MSRAs and P. trichocarpa MSR4.2 are localized in unclassified scaffolds. Protein accession numbers are from Swissprot/TrEMBL (http://expasy.org/sprot/) or NCBI Entrez
(www.ncbi.nlm.nih.gov/Entrez/), except for PtMSRA2.1 and PtMSRA2.2, which are from JGI. Accession number of closest homologues found in NCBI are in brackets.
c TargetP Reliability Class (RC) from 1 to 5, with 1 indicating the most reliable prediction, is in brackets. ER, endoplasmic reticulum; SP, secretory pathway.
d Catalytic Cys are in bold and numbers indicate positions in precursor proteins.
e Romero et al., 2004.
f Rouhier et al., 2007.
g PpMSRA4.2 is predicted to be addressed to ER, but the predicted peptide signal contains one potential catalytic cysteine. ND, non-determined value.
MSR Proteins in Photosynthetic Organisms
202
Gene accession
number
d
Potential
Redox Cysd
Name
Tarrago et al.
Sub-cellular
localization (RC)c
Organism
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C91 C180
Cytosol (3)
257
|
5
alignment data and the tree presented in Figure 1 show that
plastidic and cytosolic MSRAs from higher plants form a homogenous group rather distant from those of cyanobacteria,
likely indicating that MSRA genes encoding plastidial isoforms
do not have a cyanobacterial origin.
C47 C136
C135
Mitochondrion (4)
262
Chlamydomonas MSRA genes are localized in unclassified scaffolds. Protein accession numbers are from Swissprot/TrEMBL (http://expasy.org/sprot/).
TargetP Reliability Class (RC) from 1 to 5, with 1 indicating the most reliable prediction, is in brackets.
Catalytic Cys or Sec are in bold and numbers indicate positions in precursor proteins.
Kim et al., 2006b.
Gene accession numbers are from JGI.
a
b
c
d
Q00WE9
2
812
1400010063
MSRA4
14
estExt_gwp_GeneWisePlus.C_Chr_14.00010054
MSRA3
14
678
1
Q00WF0
U59
Mitochondrion (4)
308
gw1.12.00.324.1
MSRA2
12
927
1
Q00YB9
C103 C192
Mitochondrion (3)
Mitochondrion (5)
305
202
Q011V2
A4SAR1
2
1
609
1995
20
9
e_gw1.09.00.407.1
e_gwEuk.20.289.1
MSRA3
MSR Proteins in Photosynthetic Organisms
MSRB Gene Families in Photosynthetic Organisms
MSRA1
Ostreococcus tauri
Plastid (3)
295
1
888
gwEuk.12.468.1
MSRA2
12
U59
C132
Plastid (5)
202
A4S2H7
1
609
e_gwEuk.9.453.1
Ostreococcus lucimarinus
MSRA1
9
A4S5A8
C179 C358 C367
Plastid (5)
260
estExt_fgenesh2_pg.C_40343
MSRA5
Scaffold 4
2977
9
A8I1K5
C94 C239
C60
Mitochondrion (1)
389
estExt_fgenesh2_pg.C_10042
MSRA4
Scaffold 1
5264
13
A8HPB8
C163 C308
Mitochondrion (3)
Mitochondrion (1)
335
228
A8HXY3
A8IZ70
4
10
3392
1903
e_gwH.21.79.1
MSRA3
Scaffold 3
FER_estExt_fgenesh2_pg.C_30380
MSRA2
Scaffold 21
U20d
Cytosol (4)
160
Q8H6T1
6
2984
FER_Chlre2_kg.scaffold_2000166
MSRA1
Chlamydomonas reinhardtii
Scaffold 2
Protein
accession number
Number
of exons
Gene
(bp)
Chromosomea
Gene accession number
Name
Organism
Table 3. Description of MSRA Genes and Proteins in C. reinhardtii, O. lucimarinus, and O. tauri.
d
In a previous work, we described the nine genes forming the
MSRB family in A. thaliana (Vieira Dos Santos et al., 2005; Table
5). AtMSRB1 displays only one conserved redox active cysteine
and thus belongs to the 1-Cys type, whereas all others have
two catalytic cysteines and are related to the 2-Cys type.
AtMSRB1 and AtMSRB2 encode plastidial isoforms, AtMSRB3,
a product routed to endoplasmic reticulum (Kwon et al., 2007),
and AtMSRB4 to AtMSRB9, proteins predicted to be cytosolic.
So far, Arabidopsis is the plant displaying the highest number
of MSRB genes. Indeed, P. trichocarpa possesses four MSRB
genes, named PtMSRB1, PtMSRB3.1, PtMSRB3.2, and PtMSRB5
based on the similarity with Arabidopsis genes. O. sativa genome contains three MSRB genes, OsMSRB1, OsMSRB3, and
OsMSRB5, OsMSRB1 transcript being probably alternatively
spliced. Similarly, three MSRB genes have been identified in
the Sorghum bicolor genome, one related to the 1-Cys type
and the two others to the 2-Cys type (Supplemental Text File
3). We identified three MSRB genes in Vitis vinifera genome,
named VvMSRB1, VvMSRB3.1, and VvMSRB3.2. VvMSRB1 and
VvMSRB3.2 are likely routed to plastids whereas VvMSRB3.1
would be cytosolic. The search of homologs in P. patens
genome reveals the presence of three genes, PpMSRB1,
PpMSRB2.1, and PpMSRB2.2, encoding products related to
AtMSRB1 and AtMSRB2, respectively. PpMSRB1 and
PpMSRB2.2 are predicted to be localized in plastid whereas
PpMSRB2.1 could be cytosolic. In contrast to MSRA genes,
the description of MSRB families in green algae has not been
carried out previously. Consequently, we propose a nomenclature for C. reinhardtii, O. lucimarinus, and O. tauri, based on
the similarity with Arabidopsis MSRB genes and on the presence of one or two redox cysteines. The three green algae’s
genomes contain two genes homologous to AtMSRB1. O. lucimarinus and O. tauri possess one gene homologous to
AtMSRB2, whereas Chlamydomonas possesses two very similar
genes, CrMSRB2.1 and CrMSRB2.2.
All cyanobacteria, for which the genome sequence is
known, contain generally only one 1-Cys MSRB, and sometimes two, except Rhodopseudomonas palustris CGA009,
which possesses also one 2-Cys MSRB. Based on protein alignment (Supplemental Figure 2), we constructed a phylogenetic
tree (Figure 2) showing that MSRBs of photosynthetic organisms are divided into two main groups, with sequence similarity between the two groups ranging from 18 to 47%. The first
contains eukaryotic 2-Cys MSRBs, sharing overall similarity
from 36 to 95%, and could be subdivided in two subgroups,
containing higher plants 2-Cys MSRBs in the first and green algae 2-Cys MSRBs in the second. Overall similarity ranges from
52 to 95% for higher plants 2-Cys MSRBs and from 45 to 72%
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
Number of
amino acids
Sub-cellular
localization (RC)b
Potential Redox
Cys/Secc
Tarrago et al.
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Tarrago et al.
d
MSR Proteins in Photosynthetic Organisms
Table 4. Description of MSRA and MSRB Genes and Proteins in Cyanobacteria.
Organism
Anabaena sp. PCC 7120
Name
Gene accession
number
Protein
accession number
Number of
amino acids
Potential
Redox Cysa
all1062
Q8YXZ4
163
C21
alr1675
Q8YWD8
222
C56 C202 C211
MSRA1
sync_1640
Q0I9M7
240
C46 C193
MSRA2
sync_2210
QOI814
226
C49 (C200)
MSRA1
sll1394
P72622
222
C57 C203 C212
MSRA2
slr1795
P72800
214
C45
MSRA1
tll0885
Q8DKH4
224
C57 C203
Anabaena sp. PCC 7120
MSRB1
alr3901
Q8YQD2
164
C153
Synechococcus sp. CC9311
MSRB1.1
sync_0016
Q0IE67
170
C158
MSRB1.2
sync_2456
Q0I7C1
141
C127
Synechococcus elongatus PCC 6301
MSRB1.1
syc1907_c
Q5N0S3
140
C120
MSRB1.2
syc1161_d
Q5N2W9
202
C187
Synechococcus sp. WH 8102
MSRB1.1
SYNW0338
Q7U9C0
131
C120
MSRB1.2
SYNW0016
Q7UA81
168
C156
Synechocystis sp. PCC 6803
MSRB1
sll1680
P72779
176
C165
Thermosynechococcus elongatus BP-1
MSRB1
tlr1214
Q8DJK9
135
C119
Synechococcus sp. CC9311
Synechocystis sp. PCC 6803
Thermosynechococcus elongatus BP-1
Gene accession numbers are from CyanoBase and protein accession numbers from Swissprot/TrEMBL (http://expasy.org/sprot/).
a Catalytic Cys are in bold and numbers indicate positions in precursor proteins.
for green algae proteins. In the second main group including
all 1-Cys MSRBs, MSRB1s from higher plants, moss, and Synechococcus sp. CC9311 MSRB1.2 are clustered and share 47–98%
similarity. Three other subgroups could be defined: CrMSRB1,
Synechococcus sp. CC9311 MSRB1.2, and Ostreococcus
MSRB1.2s in the first, the two cyanobacterial Synechocystis
sp. PCC 6803 and Anabaena sp. PCC 7120 MSRB1s in the second, and the two atypical Ostreococcus MSRB1.1s sharing only
8–17% similarity with other MSRBs in the third. Their closest
homologue CrMSRB1.2 cannot be clearly attached to a subgroup. To the exclusion of Ostreococcus MSRB1.1s, overall similarity between 1-Cys MSRB1s ranges from 23 to 83%. Genes
coding for 2-Cys MSRBs and 1-Cys MSRBs in higher plants
are composed of three to four and four to five exons, respectively (Table 5). One extra exon is also found in genes encoding
1-Cys MSRBs of O. lucimarinus and O. tauri. The intron/exon
structure and the clear distribution into two groups suggest
a distinct origin for the two types of MSRB genes. Since all
1-Cys MSRB genes from higher plants are clustered with those
of cyanobacteria and code for plastidic proteins, we propose
that this type of MSRBs in photosynthetic eukaryotes arose
from a prokaryotic cyanobacterial ancestor, in consideration
of the endosymbiotic theory.
disulfide bond after nucleophilic attack of the ‘resolving’ cysteine; and (3) reduction of the disulfide bridge by a reductant
(Lowther et al., 2000; Boschi-Muller et al., 2008). In vitro,
dithiothreitol (DTT) is a ubiquitous reducing agent for most
MSR enzymes (Brot et al., 1981; Sagher et al., 2006b). Thioredoxin (Trx) appears to be the major physiological reductant for
all MSRA and many MSRB enzymes (Figure 4; Brot et al., 1981;
Kumar et al., 2002). Accordingly, MSRA and MSRB proteins
have been isolated as Trx targets in Chlamydomonas (Lemaire
et al., 2004) and in higher plants (Marchand et al., 2004; Rey
et al., 2005). Trxs are small and ubiquitous disulfide reductase
proteins, present in all organisms, with an active site CGPC.
They function as electron donors and play an essential role
in many processes in plants, such as regulation of protein activity or control of redox homeostasis, by supplying the reducing power needed to reduce disulfide bonds (Meyer et al.,
2005; Vieira Dos Santos and Rey, 2006). Compared to most
other living organisms, plants display a great variety of Trx
types. Meyer et al. (2005) reported the presence of no less than
40 Trxs or Trx-like genes in A. thaliana genome. This remarkable diversity could indicate a functional specialization or
a high level of redundancy.
MSRAs
Catalytic Mechanisms and Electron Donors to MSRs
Despite the absence of similarity between MSRAs and MSRBs,
both generally share a common reaction mechanism including
three steps (Figure 3A): (1) formation of a sulfenic acid intermediate on the ‘catalytic’ cysteine after reduction of one mole
of Met per mole of enzyme; (2) formation of an intramolecular
MSRA proteins possess one catalytic cysteine required for
S-MetSO reduction and one or two recycling cysteines involved
in the regeneration mechanism. As shown for E. coli and Bos
taurus proteins, two resolving cysteines are involved in the formation of two subsequent disulfide bonds, the first being
formed between the catalytic cysteine (CysA) and the first
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MSRA1
MSRA2
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MSR Proteins in Photosynthetic Organisms
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The nomenclature At, Cr, Os, Ol, Ot, Pt, Pp, and Vv was used for Arabidopsis thaliana, Chlamydomonas reinhardtii, Oryza sativa, Ostreococcus lucimarinus, Ostreococcus tauri, Populus trichocarpa, Physcomitrella patens ssp. patens, and Vitis vinifera, respectively. The groups
containing higher plants MSRA1s to MSRA4s and MSRA5s are in dark and light green, respectively. Algae and cyanobacteria MSRAs are
included in brown, light yellow, and yellow groups and selenocysteine-containing MSRAs in the orange group. The tree was built as described in Methods.
resolving (CysB), the second between the two resolving cysteines (CysB and CysC). Regarding photosynthetic kingdoms,
the biochemical characteristics of only poplar cytosolic and
plastidial MSRAs have been investigated by Rouhier et al.
(2007). The recycling mechanism of PtMSRA2.1 is slightly different from that of the bacterial and mammal enzymes, with
the first disulfide bond formed between the most C-terminal
cysteine (CysC) and the catalytic one (CysA). All higher plant
MSRAs possess the three cysteines equivalent to those of
PtMSRA2.1 (Table 2 and Supplemental Figure 1), indicating
that they likely follow a similar regeneration mechanism. Note
that most enzymes from higher plants related to the MSRA5
type do not display any conserved cysteine, raising the ques-
tion of their ability to reduce MetSO. With regard to green algae and cyanobacteria, all MSRAs possess a conserved catalytic
cysteine, except MSRA1s, which display a selenocysteine at the
corresponding position (Tables 3 and 4). Kim et al. (2006)
showed that this isoform does not require a resolving cysteine
for MetSO reduction and proposed that the selenenic acid intermediate could be directly reduced by thioredoxin (Figure
3B). Chlamydomonas MSRA3, which is the sole green algae isoform possessing the three cysteines conserved in higher plants,
likely reduces MetSO via a mechanism similar to that of the
poplar enzyme. Interestingly, several MSRAs from green algae
and cyanobacteria, such as CrMSRA5 and sll1394, possess resolving cysteines equivalent to those of the Bos taurus enzyme,
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
Figure 1. Phylogenetic Tree of MSRAs from Photosynthetic Organisms.
8
Table 5. Description of MSRB Genes and Proteins in Viridiplantae.
|
Name
Gene accession
number
Chromosomea,b
Arabidopsis thaliana
MSRB1
At1g53670
1
MSRB2
Vitis vinifera
Physcomitrella patens ssp. Patens
Chlamydomonas reinhardtii
Ostreococcus lucimarinus
Ostreococcus tauri
1579
5
1564
3
Protein
accession number
Number of
amino acids
Q9C8M2
Q9C5C8
Sub-cellular
localization (RC)c
Potential
Redox Cysd
202
Plastide
C186f
202
e
Plastid
C134 C187f
g
MSRB3
At4g04800
4
1656
3
Q9M0Z6
176
ER
C108 C161
MSRB4
At4g04810
4
1156
3
Q9M0Z5
139
Cytosol (2)
C69 C122
MSRB5
At4g04830
4
1226
3
Q9ZS91
139
Cytosol (3)
C69 C122
MSRB6
At4g04840
4
2030
4
Q8GWF4
153
Cytosol (2)
C85 C138
MSRB7
At4g21830
4
1074
3
Q8VY86
144
Cytosol (4)
C76 C129
MSRB8
At4g21840
4
1193
3
O49707
143
Cytosol (4)
C75 C128
MSRB9
At4g21850
4
1123
3
Q84JT6
143
Cytosol (5)
C76 C129
MSRB1.1
LOC_Os06g27760.1
6
2850
4
Q69XS8
214
Plastid (4)
C202
MSRB1.2
LOC_Os06g27760.2
6
1746
5
Q69XS8
207
Plastid (4)
C202
MSRB3
LOC_Os05g33510
5
2552
3
Q6AUK5
229
Plastid (3)
C159 C212
MSRB5
LOC_Os03g24600.1
3
3300
3
Q84PA1
136
Cytosol (2)
C71 C124
MSRB1
eugene3.00110858
LG XI
3841
5
A9PF53
198
Plastid (3)
C187
MSRB3.1
estExt_Genewise1_v1.C_LG_I4275
LG I
2686
4
707507
214
Plastid (1)
C146 C199
MSRB3.2
fgenesh1_pg.C_LG_IX000814
LG I
2414
3
767763
217
Plastid (3)
C149 C202
MSRB5
eugene3.00081881
LG VIII
1293
3
565286
133
Cytosol (2)
C68 C121
MSRB1
GSVIVT00027935001
19
3221
4
A7P298
190
Plastid (2)
C187
MSRB3.1
GSVIVT00019868001
5
2092
3
A7NWC5
138
Cytosol (2)
C68 C121
MSRB3.2
GSVIVT00005758001
3
7398
3
A5BF60
197
Plastid (3)
C127 C180
MSRB1
estExt_Genewise1.C_3170021
Scaffold 317
2403
5
225394
208
Plastid (5)
C191
MSRB2.1
estExt_Genewise1.C_1440019
Scaffold 144
2131
3
A9SZZ7
139
Cytosol (3)
C72 C125
MSRB2.2
fgenesh1_pm.scaffold_280000001
Scaffold 280
1575
3
A9TPF2
204
Plastid (2)
C137 C190
MSRB1.1
e_gwW.1.716.1
Scaffold 1
2771
6
A8HMM4
188
Mitochondrion (1)
C174
MSRB1.2
e_gwW.19.243.1
Scaffold 19
2371
7
A8IWQ7
242
Mitochondrion (2)
C211
MSRB2.1
e_gwH.43.72.1
Scaffold 43
1886
5
A8JAQ8
170
Mitochondrion (3)
C103 C158
MSRB2.2
estExt_fgenesh2_pg.C_430081
Scaffold 43
1933
6
A8JAR0
140
Cytosol (2)
C71 C128
MSRB1.1
0500010056
5
764
1
A4RX03
213
Mitochondrion (2)
C199
MSRB1.2
fgenesh1_pg.C_Chr_13000110
13
988
2
A4S6G6
130
Cytosol (2)
C117
MSRB2
gwEuk.1.778.1
1
504
1
A4RRT7
168
Plastid (5)
C103 C157
MSRB1.1
0500010053
5
640
2
Q019W7
200
Mitochondrion (3)
C186
MSRB1.2
e_gw1.13.00.311.1
13
420
1
Q00X40
229
Plastid (3)
C215
MSRB2
gw1.01.00.541.1
1
507
1
6189
179
Plastid (2)
C103 C157
Gene accession numbers are from TAIR for A. thaliana, JGI for P. trichocarpa, and P. patens, TIGR for O. sativa, and Genoscope for V. vinifera.
a Chromosomes of P. trichocarpa are designed by Linkage Group (LG).
b C. reinhardtii and P. patens. MSRBs are localized in unclassified scaffolds. Protein accession numbers are from Swissprot/TrEMBL (http://expasy.org/sprot/) or NCBI Entrez
(www.ncbi.nlm.nih.gov/Entrez/), except for OtMSRB2, PtMSRB3.1, PtMSRB3.2, PtMSRB5, and PpMSRB1 (JGI).
c TargetP Reliability Class (RC) from 1 to 5, with 1 indicating the most reliable prediction, is in brackets.
d Catalytic Cys are in bold and numbers indicate positions in precursor proteins.
e Vieira Dos Santos et al., 2005;
f Tarrago et al. (unpublished data);
g Kwon et al., 2007.
MSR Proteins in Photosynthetic Organisms
Populus trichocarpa
4
Number
of exons
d
Oryza sativa
At4g21860
Gene
(bp)
Tarrago et al.
Organism
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The nomenclature At, Cr, Os, Ol, Ot, Pt, Pp, and Vv was used for Arabidopsis thaliana, Chlamydomonas reinhardtii, Oryza sativa, Ostreococcus lucimarinus, Ostreococcus tauri, Populus trichocarpa, Physcomitrella patens ssp. patens, and Vitis vinifera, respectively. 1-Cys MSRB
group and 2-Cys MSRB group are on dark and light gray backgrounds, respectively. Subgroups containing 1-Cys MSRBs or 2-Cys MSRBs from
higher plants are in light and dark green, respectively. 1-Cys MSRBs and 2-Cys MSRBs from algae and cyanobacteria are positioned in
orange, light yellow and yellow subgroups, except atypical Ostreococcus MSRB1.1s, which are in brown. The tree was built as described
in Methods.
with the GYC signature for CysB, indicating that these enzymes
could use a potential reduction mechanism similar to mammal
MSRAs (Tables 3 and 4 and Supplemental Figure 1). At the present time, no investigation has been carried out to analyze the
specificity of the various Trx types as electron suppliers to
MSRAs in photosynthetic organisms.
MSRBs
The catalytic mechanisms and the regeneration by reductant
of 1-Cys and 2-Cys MSRBs implicate one or two cysteines, respectively. Nearly 60% of MSRBs from various organisms possess the two redox-active cysteines and thus belong to the
2-Cys MSRB type (Neiers et al., 2004). The resolving cysteine,
corresponding to Cys-63 in E. coli MSRB, is part of the conserved motif GCGWP and is involved in the regeneration of
Cys-117, the catalytic cysteine included in the active site
RXCXN, through the formation of an intramolecular disulfide
bridge followed by Trx reduction (Figure 3A) (Olry et al., 2004;
Kim and Gladyshev, 2005; Boschi-Muller et al., 2008). The
remaining 40% MSRBs, including two mammalian MSRBs, lack
the resolving cysteine, which is generally replaced by a threonine or a serine, and correspond to the 1-Cys MSRB type. Contrasting data have been published concerning the function of
Trx in the reduction of this MSRB type. Kim and Gladyshev
(2005) and Sagher et al. (2006b) reported that two mammal
MSRBs, MSRB2 and MSRB3, are poorly reduced by Trx. However, very recently, Kim and Kim (2008) reported that a specific
type of Trx, located in mitochondria like MSRB2 and MSRB3,
could efficiently serve as a reductant for the latter. Besides
demonstrating the ability of Trxs to reduce all MSRB types, this
study points out that MSRs possess specific electron donors
even in animal cells where the number of Trxs is much lower
than in plant cells. Moreover, Kim and Kim (2008) provided
biochemical evidence that Trx could physically interact via
an intermolecular disulfide bond with the sulfenic acid form
of MSRBs. In other respects, Sagher et al. (2006a, 2006b)
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Figure 2. Phylogenetic Tree of MSRBs from Photosynthetic Organisms.
10
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Tarrago et al.
d
MSR Proteins in Photosynthetic Organisms
The catalytic mechanisms of MSRs implicate one to three cysteines. The reduction of MetSO consists of the attack of the catalytic cysteine
onto the sulfur of MetSO, leading to the release of methionine and formation of sulfenic acid.
(A) In the case of MSRAs or of 2-Cys MSRBs, possessing a resolving cysteine, a disulfide bond is formed, which is then reduced by Trxs. For
MSRAs possessing a third redox cysteine, a second disulfide bridge is formed between the two resolving cysteines, which is then reduced by
a reductant.
(B) In the case of MSRs possessing only one redox cysteine, mostly 1-Cys MSRBs, the sulfenic acid is very likely directly reduced by Trxs or Grx
thanks to two redox cysteines or with the help of glutathione for Grxs after formation of an intermolecular disulfide (pathway 1). Another
mechanism could involve the reduction of glutathionylated MSR by Grx after reduction of sulfenic acid by GSH (pathway 2).
Figure 4. Pathways of Reduction of
Protein-Bound MetSO in Plants.
MetSO in proteins is reduced back to Met
through the action of MSRs. MSRAs and 2Cys MSRBs are reduced by Trxs. In cytosol,
NADPH-dependent thioredoxin reductase
(NTR) uses NADPH to reduce Trxs,
whereas, in plastid, ferredoxin is the initial electron donor to ferredoxin-dependent thioredoxin reductase (FTR), which
reduces Trxs. In the case of 1-Cys MSRBs,
the peculiar Trx CDSP32 is able to transfer
electrons likely provided by FTR and Grxs
reduce MSRBs thanks to GSH, which is
recycled by glutathione reductase (GR) using NADPH as an initial source of
electrons.
reported that thionein, the reduced Cys-rich apoprotein of
metallothionein, and selenocompounds such as selenocystamine and selenocystine could reduce mammal 1-Cys type
MSRBs. Additional work is needed to determine whether these
compounds function in vivo as physiological reductants.
The catalytic mechanisms of plant MSRBs have been recently
investigated. Sequence analysis shows that all possess the catalytic Cys. 2-Cys MSRB isoforms have one resolving cysteine (Table
5 and Supplemental Figure 2). Except OtMSRB1.1, all 1-Cys
MSRBs of photosynthetic organisms have a threonine in place
of the resolving cysteine. In other respects, four non redoxactive cysteines, disposed in two CXXC motifs, are conserved
in MSRBs from higher plants, moss, green algae, and cyanobac-
teria, with the exception of CrMSRB1.2, OlMSRB1.1, and
OtMSRB1.1. The two motifs are implicated in the fixation of
one zinc atom and are critical for the folding and activity of
MSRBs (Kumar et al., 2002). Note also that AtMSRB2, AtMSRB6,
and two cyanobacterial 2-Cys MSRBs contain an extra-cysteine
just before the first CXXC motif, whereas several 1-Cys
MSRBs have an extra-cysteine included in this motif. No other
cysteine, that could constitute an alternative potential resolving
cysteine as shown for Xanthomonas campestris protein (Neiers
et al., 2004), is present in 1-Cys MSRBs from photosynthetic
organisms.
The plastidic 2-Cys MSRB from Arabidopsis, AtMSRB2, was
first shown to be reduced by poplar Trx h1, whereas the activity
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Figure 3. Catalytic Mechanisms of MSRA and MSRB Proteins.
Tarrago et al.
MSR Proteins in Photosynthetic Organisms
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11
The recycling mechanism of 1-Cys MSRBs likely implicates
the direct reduction by Trxs and Grxs of the sulfenic acid generated upon catalysis and the formation of a transient intermolecular disulfide (Kim and Gladyshev, 2005; Kim and Kim,
2008) that might be reduced via the participation of one resolving cysteine in the electron donor or via glutathione (Figure 3B). However, in the case of Grxs displaying only one redox
active cysteine (Vieira Dos Santos et al., 2007), a GSH adduct
could be formed on the MSRB catalytic cysteine and subsequently reduced by Grx as proposed for some types of peroxiredoxins (Gama et al., 2008). Further work is needed to
elucidate the pathway through which the activity of 1-Cys
MSRBs is regenerated and to determine whether Trxs and Grxs
share common catalytic mechanisms in this process.
Expression and Functional Analysis of MSR Genes in
Photosynthetic Organisms
At the present time, the knowledge about the expression pattern and the function of MSR genes is very scarce in photosynthetic organisms other than higher plants, not to say completely
non-existent in the case of cyanobacteria and mosses. In the
model alga Chlamydomonas reinhardtii, no functional analysis
of MSRs based on a genetic approach has been still reported.
CrMSRA2 gene expression is triggered in Chlamydomonas when
subjected to manganese deficiency (Allen et al., 2007). Note
that this deficiency leads also to increased expression of genes
encoding for glutathione and ascorbate peroxidases, and is associated with susceptibility to organic peroxides. The authors
proposed that CrMSRA2 participates with other antioxidant
genes in response to the oxidative stress resulting from manganese deficiency. As mentioned above, algae are the only photosynthetic organisms possessing selenocysteine-containing
MSRA proteins (Novoselov et al., 2002). The presence of a catalytic selenocysteine instead of a cysteine in CrMSRA1 confers
a much higher efficiency for reducing MetSO (Kim et al.,
2006) and selenium has been found to be required for optimal
growth of algae (Novoselov et al., 2002). Chlamydomonas possesses other antioxidant enzymes (glutathione peroxidase and
thioredoxin-reductase) with the catalytic cysteine replaced by
a selenocysteine. However, no difference in sensitivity to MetSO
and H2O2 was observed in algae cultures grown either in the
presence or in the absence of selenium. In Chlamydomonas,
Lemaire et al. (2004) identified one MSRA (CrMSRA4) among
proteins targeted by thioredoxin, which is known to fulfill a major role in the response to oxidative stress in most organisms
(Arner and Holmgren, 2000; Vieira Dos Santos and Rey,
2006). This last finding and the few reports about the expression
of MSR genes in algae give credence for the involvement of
these genes in the tolerance of unicellular algae to oxidative
stress conditions. But, thorough investigations particularly using genetic approaches have to be performed to firmly assess
this function.
In higher plants, the expression patterns and roles of MSR
proteins are comparatively more documented, although much
remains to be done, particularly to analyze the physiological
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
of AtMSRB1, the other plastidic MSRB belonging to the 1-Cys
type, could not be regenerated by this cytosolic Trx (Vieira Dos
Santos et al., 2005). Much more relevant information about
the identity of electron donors to these MSRBs from a physiological point of view has been gained in the work by Vieira Dos
Santos et al. (2007). Simple-module plastidic Trxs f, m, and y are
efficient reductants towards AtMSRB2, whereas another chloroplastic Trx, the type x, cannot reduce this MSRB. As AtMSRB2
possesses two redox-active cysteines, these data indicate that
the enzyme activity is very likely regenerated through a threestep catalytic mechanism implicating a disulfide exchange with
a Trx (Figure 3A), as reported for 2-Cys MSRBs from other
organisms (Kumar et al., 2002; Olry et al., 2004). The data
obtained on AtMSRB2, revealing a specificity among plastidic
Trxs as electron suppliers towards MSRBs, lead us to propose
that 2-Cys MSRBs located in other cell compartments also possess specific electron donors among Trxs, which display a tremendous variety in eukaryotic photosynthetic cells. For
instance, cytosolic MSRBs might be reduced by specific Trxs
h, such as h8 and h5, which are strongly induced by biotic
and abiotic stress conditions, leading to an increase in ROS levels (Reichheld et al., 2002; Laloi et al., 2004).
In contrast to AtMSRB2, all simple module Trx types were
found to be inefficient to provide electrons to AtMSRB1,
the 1-Cys type plastidic enzyme. This enzyme could only be reduced by the peculiar Trx CDSP32 (Chloroplastic Droughtinduced Stress Protein of 32 kDa) (Figure 4; Vieira Dos Santos
et al., 2007). This strong electron donor specificity was further
illustrated using NtMSRB1, the tobacco 1-Cys protein (Ding
et al., 2007). Note that MSRB1 was first isolated in potato (Solanum tuberosum) as a target of CDSP32 on an affinity column
(Rey et al., 2005), arguing for the physiological relevance of
the in-vitro activity results. CDSP32 is composed of two typical
thioredoxin modules, with only one active redox disulfide center in the C-terminal domain (Rey et al., 1998; Broin et al.,
2002). This protein is induced under severe environmental
stress conditions and is involved in the protection of the photosynthetic apparatus against oxidative damage (Broin et al.,
2000, 2002; Broin and Rey, 2003). Interestingly, although there
is no known mammalian homolog of CDSP32, this doublemodule Trx can serve as an electron donor to mammal MSRBs
lacking the resolving cysteine (Ding et al., 2007). In other
respects, glutaredoxins (Grx) have been identified as possible
physiological electron donors to the 1-Cys type MSRB (Figure 4;
Vieira Dos Santos et al., 2007), in agreement with the fact that
many proteins targeted by Trxs also interact with Grxs (Rouhier
et al., 2005). Grxs are small and ubiquitous oxidoreductases
similar to Trxs, with a typical glutathione-reducible dithiol
CXXC or monothiol CXXS active site. Similarly to Trxs, multigenic families encode plant Grxs with no fewer than 31 genes
in A. thaliana, but the physiological role remains unknown for
most of them. Interestingly, the di- and monothiol Grxs are
able to regenerate 1-Cys MSRB activity with comparable catalytic efficiency through mechanisms that remain to be clearly
delineated (Vieira Dos Santos et al., 2007).
d
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MSR Proteins in Photosynthetic Organisms
AtMSRA2 (Bechtold et al., 2004), or underexpressing AtMSRA4
(Romero et al., 2004). Conversely, the MSR activity measured in
chloroplast extracts strongly increased in plants overexpressing
AtMSRA4 (Romero et al., 2004). In agreement with activity data,
a higher MetSO content has been observed in plants with reduced expression levels of AtMSRB9, AtMSRB3, or AtMSRA4
genes, particularly under environmental constraints, and the
MetSO content was lower in plants overexpressing AtMSRA4
(Rodrigo et al., 2002; Bechtold et al., 2004; Romero et al., 2004).
Physiological functions have been attributed to some MSR
genes in higher plants on the basis of genetic approaches.
Bechtold et al. (2004) reported that Arabidopsis mutants deficient for AtMSRA2 display reduced growth and slow development under short-day conditions, but not under long-day
conditions. They proposed that cytosolic AtMSRA2 repairs oxidized proteins under long night periods to limit the loss of
energy resulting from an increased rate of protein turnover.
As abiotic constraints result in substantial changes in the expression of MSR genes, investigations have been performed
to characterize the phenotype and the tolerance of plants under- or overexpressing MSR genes under such conditions. Compared to wild-type, plants overexpressing AtMSRA4 display
a greater tolerance to severe photooxidative treatments generating damage within photosynthetic membranes such as
high light and methyl viologen treatment (Romero et al.,
2004). Conversely, Arabidopsis plants underexpressing
AtMSRA4 are more sensitive to these treatments. From these
data, plastidic MSRA has been proposed to play an essential
function in the tolerance and protection of photosynthetic
structures (Romero et al., 2004). The enzyme likely prevents oxidative damage to proteins due to the increased level of reactive oxygen species in chloroplast, a major site of production of
these deleterious species in plant cells during environmental
constraints (Foyer and Noctor, 2003). Very recently, Kwon
et al. (2007) reported that the AtMSRB3 gene, encoding a protein localized in the endoplasmic reticulum, is cold responsive.
They showed that plants lacking AtMSRB3 are more sensitive
to a methyl viologen treatment and lose their ability to tolerate freezing temperatures following a pre-treatment to cold
conditions. This report reveals a critical role of MSRs in the process of cold acclimation in plants. Taken together, the studies
on Arabidopsis mutants demonstrate that plant MSRs constitute key actors in the responses of plants to various environmental constraints, very likely through a role in the repair
of oxidatively damaged proteins.
DISCUSSION
Over the past few years, substantial information about the
characteristics and roles of MSRs has been gained in higher
plants, more particularly during environmental constraints.
However, we are far from having a full understanding of
the function of each isoform in these eukaryotic organisms
upon abiotic and biotic stress conditions. Further, MSRs very
likely play other key roles, such as in plant development.
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
functions of each isoform. In a previous review, we reported
the detailed expression patterns of MSRA and MSRB genes
in the plant model Arabidopsis thaliana (Rouhier et al.,
2006). We present here only a sum-up of the main expression
features of these genes. Most Arabidopsis MSR genes display
differential expression patterns, depending on organ type.
Thus, on the basis of transcript levels, AtMSRA4, AtMSRB1,
AtMSRB2, and AtMSRB6 genes are preferentially expressed
in leaves and in other green organs, whereas AtMSRA2,
AtMSRB5, AtMSRB7, AtMSRB8, and AtMSRB9 are more specifically expressed in roots. Many data also demonstrate that environmental and biotic stress conditions substantially modify
the expression of MSR genes in higher plants. In Arabidopsis,
AtMSRA4 expression is enhanced by oxidative treatments,
high light and salt treatment (Romero et al., 2004; Oh et al.,
2005; Vieira Dos Santos et al., 2005). In poplar, the abundance
of plastidic PtMSRA is higher in the case of an incompatible
reaction with the rust fungus Melanpsora larici-populina
(Vieira Dos Santos et al., 2005), and, in rye, the abundance
of a cytosolic MSRA protein increases during acclimation to
low temperature (In et al., 2005). With regard to MSRB genes,
AtMSRB3 is induced at the transcriptional level by low temperature in Arabidopsis (Kwon et al., 2007) and Arabidopsis plants
subjected to photooxidative stress conditions generated by
high light and low temperature exhibit noticeably higher levels of plastidic AtMSRB1 and AtMSRB2 proteins (Vieira Dos
Santos et al., 2005).
Few studies investigated the level of MSR activity during environmental stress conditions. Ferguson and Burke (1994) noticed up- and down-variations, depending on species (cotton,
pea, wheat, potato) in plants subjected to high temperature or
water deficit. In Arabidopsis, a severe decrease in the total cellular MSR activity occurs during cold and high salt treatments
(Oh et al., 2005). However, these authors noticed that
AtMSRA4 is induced by high salt, but not by low temperature.
In contrast, Romero et al. (2004) observed correlated increases
in the abundance of plastidic AtMSRA4 and in the total MSR
activity measured in leaf soluble fractions during environmental and oxidative stress conditions. Altogether, these data indicate that environmental stress exerts a strong control in the
regulation of the activity of MSR proteins, and that this control
is very likely achieved through distinct steps at the transcriptional and post-transcriptional levels. Further, each MSR gene
very likely displays its own and highly specific pattern of expression and activity. This hypothesis is supported by the findings of Bechtold et al. (2004), who observed two peaks in total
MSR activity in Arabidopsis plants grown under short-day conditions, one during the light period and the other in the dark.
The second peak of activity was partially attributed to
AtMSRA2, since it substantially diminished in a mutant lacking
this protein.
Insights about the functional roles of plant MSRs have been
gained in the past years using Arabidopsis mutants and transformants. Lower total MSR activities have been recorded in
Arabidopsis plants lacking AtMSRB9 (Rodrigo et al., 2002) or
Tarrago et al.
MSR Proteins in Photosynthetic Organisms
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13
(1) One group in which Met oxidation is used as a switch to
regulate signaling pathways. Thus, sulfoxidation of Met modulates in mammal cells the activities of calmodulin and of calmodulin-dependent protein kinase II, thus linking metabolic
activity to cell redox state (Gao et al., 1998; Bigelow and Squier,
2005; Erickson et al., 2008).
(2) The second group includes proteins termed scavenging
substrates, which do not exhibit a substantial decrease in their
activity when their methionines are oxidized. MSR proteins
constitute good candidates to play a direct antioxidant role,
since cyclic oxidation and reduction of Met could serve as
an efficient pathway to scavenge ROS in cells (Stadtman
et al., 2002; Weissbach et al., 2002).
(3) The last group corresponds to substrates damaged in their
function by Met oxidation, such as catalase that has been identified as a target of MSR in Helicobacter pylori (Alamuri and
Maier, 2006).
With regard to photosynthetic organisms, the small plastidic
heat shock protein, Hsp21, constitutes the unique characterized substrate of MSRs in higher plants (Gustavsson et al.,
2002). Hsp21 displays an N-terminal region very rich in methionine residues, and MSRA is required to maintain the chaperone-like activity of the protein via the reduction of oxidized
methionines in this domain (Sundby et al., 2005). The targeting
of MSR partners in algae or plant extracts using co-immunoprecipitation or affinity chromatography approaches, and
the identification of these partners by mass spectrometry
methods (Toda et al., 2003; Brock et al., 2005; Alamuri and
Maier, 2006) will help to gain substantial insight into the physiological roles of MSRs and their involvement in signaling
pathways or detoxification mechanisms during development
and stress conditions.
METHODS
Gene sequences were obtained from TAIR (www.arabidopsis.
org/) for Arabidopsis thaliana, JGI (http://genome.jgi-psf.org/
Poptr1_1/Poptr1_1.home.html) for Populus trichocarpa, TIGR
(www.tigr.org/tdb/e2k1/osa1/) for Oryza sativa, JGI (http://
genome.jgi-psf.org/Sorbi1/Sorbi1.home.html) for Sorghum bicolor, JGI (http://genome.jgi-psf.org/Phypa1_1/Phypa1_1.
home.html) for Physcomitrella patens ssp. patens, Genoscope
(www.genoscope.cns.fr/externe/GenomeBrowser/Vitis/)
for
Vitis vinifera, JGI (http://genome.jgi-psf.org/Chlre3/Chlre3.
home.html) for Chlamydomonas reinhardtii, JGI (http://
genome.jgi-psf.org/Ost9901_3/Ost9901_3.home.html)
for
Ostreococcus lucimarinus, JGI (http://genome.jgi-psf.org/
Ostta4/Ostta4.home.html) for Ostreococcus tauri, and CyanoBase (http://bacteria.kazusa.or.jp/cyanobase/) for cyanobacteria.
The predicted sub-cellular localization of eukaryote proteins
was the consensus obtained using TargetP (Emanuelsson
et al., 2000; www.cbs.dtu.dk/services/TargetP/) and Predotar
(Small et al., 2004; http://urgi.versailles.inra.fr/predotar/
predotar.html). Phylogenetic trees, based on protein
Downloaded from http://mplant.oxfordjournals.org/ at Pennsylvania State University on March 5, 2014
Indeed, some MSR genes are highly expressed during specific
developmental stages, such as AtMSRA3 in stamen and pollen
(Rouhier et al., 2006) or a MSRA1-related gene during maturation of strawberry fruit (Lopez et al., 2006). Regarding
other photosynthetic organisms, the knowledge at the present time is very poor, no report being available, for instance,
regarding the characterization of MSR genes in cyanobacteria. On the basis of the data reported in higher plants and
non-photosynthetic organisms, MSRs very likely participate
in the tolerance of unicellular photosynthetic organisms to
environmental constraints generating oxidative damage. In
other respects, the critical function of MSRs during ageing
and in the control of life span has been extensively documented in yeast, insect, and mammal cells, as mentioned in
the Introduction of this review. This is in agreement with
the accumulation of oxidative damage in proteins, like carbonyl groups or methionine sulfoxide, observed over time
in many organisms (Stadtman, 1992). In contrast, nothing is
known about the role of MSRs during the ageing process
in plants. In these organisms, leaf senescence is the ultimate
stage of leaf development and precedes plant death. An increase in the abundance of carbonylated proteins first occurs
during Arabidopsis leaf expansion, and then is followed by
a strong decrease prior to bolting and during flower development (Johansson et al., 2004). Further, in Arabidopsis, high
levels of carbonylated proteins are also observed during seed
maturation and germination (Job et al., 2005). Clearly, these
data show that the accumulation of carbonylated proteins in
plants is not a marker of the ageing process, but is associated
with specific stages of development. At the present time, no
report describing the level of MetSO in the various plant
organs and during the different developmental stages has
been published. We previously reported a higher abundance
of plastidial MSRs, particularly MSRBs, in young leaves compared to well expanded leaves during vegetative growth of
Arabidopsis (Vieira Dos Santos et al., 2005), suggesting a decrease in MSR activity with age in leaves of higher plants.
Thorough investigations have to be carried out to determine
whether the amount of MetSO in proteins is positively correlated with the level of carbonyl groups during specific developmental stages in plants and the precise roles of MSRs
during senescence in photosynthetic organisms.
The understanding of the physiological functions of MSRs in
photosynthetic organisms will undoubtedly progress via the
determination of the identity of their partners and substrates,
which remain largely unknown. Most MSRAs and MSRBs are
more efficient reducers for peptide-bound MetSO than for
free MetSO (Olry et al., 2002, 2004; Vieira Dos Santos et al.,
2005). Consequently, these reductases should be able to reduce all the proteins exhibiting methionine residues positioned on their surface, taking into consideration MetSO
accessibility to the active sites of both MSR types (BoschiMuller et al., 2008). Based on the consequences of Met oxidation in proteins, Oien and Moskowitz (2008) very recently
classified MSR substrates into three groups:
d
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Tarrago et al.
d
MSR Proteins in Photosynthetic Organisms
alignments made using ClustalW (Larkin et al., 2007), were
built thanks to MEGA4 (Tamura et al., 2007), using the neighbor-joining method (Saitou and Nei, 1987) and the Poisson
correction method (Zukerkandl and Pauling, 1965) to compute
evolutionary distances. Supplemental Text File 3 contains all
protein sequences indexed in this study including Sorghum
bicolor gene accession numbers.
SUPPLEMENTARY DATA
Supplementary Data are available at Molecular Plant Online.
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283, 16673–16681.
Davies, M.J. (2005). The oxidative environment and protein damage. Biochim. Biophys. Acta. 1703, 93–109.
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