3.1. Effect of Environmental Conditions
In agreement with the biochemical function of MSRs in the maintenance of Met redox status, the first microarray data gained in Arabidopsis revealed that environmental constraints leading to oxidative stress result in increased expression of most
MSR genes [
46]. In the last years, the expression patterns of these genes have been refined in various types of photosynthetic organisms in relation with abiotic, but also biotic constraints. The data gained in higher plants are summarized in
Table 1.
Consistently with the data reported in Arabidopsis, oxidative stress conditions generated by manganese deficiency or copper excess in
C. reinhardtii and
U. fasciata algae lead to up-regulation of
MSRA genes [
72,
73]. In
C. reinhardtii, the expression of three
MSRB genes (
1.1,
1.2 and
2.1) is induced in very high light conditions and upon treatment with H
2O
2 [
74]. Data that are more meaningful regarding the physiological factors regulating expression of
MSR genes were gained in relation with the activity of the photosynthetic chain. In
U. fasciata, the transcript levels of
MSRA and
MSRB genes peak following 1-h light exposure [
75]. Most interestingly, the use of various inhibitors of the photosynthetic electron chain revealed that the expression of these genes differentially depends on the redox status of components belonging to the cytochrome
b6f complex or downstream complexes. This strongly supports the hypothesis that the photosynthetic activity level, which modulates plastidial redox homeostasis, plays an essential role in pathways regulating the expression of
MSR genes. As these genes are nuclear-encoded, these pathways very likely involve retrograde signaling from plastid to nucleus.
Numerous studies report that oxidative stress conditions are associated with up-regulation of
MSR gene expression in higher plants (
Table 1). Thus, MV treatment leads to increased transcript or protein levels of tobacco MSRB3, tomato MSRA2, A4 and A5, rice MSRB1, rye MSRA, and Arabidopsis MSRA4, MSRB7, and MSRB8 [
51,
55,
58,
67,
76,
77]. More physiological constraints that impair the cell redox homeostasis enhance
MSR expression. For instance, copper excess leads to
MSRB5 up-regulation in rice [
70]. In Arabidopsis, exposure to cadmium triggers the antioxidant defense system, notably the expression of most
MSR genes, but also provokes a decrease in the abundance of plastidial MSRBs [
78,
79]. In
Brassica juncea, such a treatment results in a higher amount of cytosolic MSRA2 [
80]. In other respects, increased amounts of plastidial MSRs (A4, B1 and B2) were observed in Arabidopsis plants exposed to photooxidative stress conditions generated by high light and low temperature conditions [
50]. In rye, high light conditions induce the accumulation of a cytosolic MSRA protein [
67].
Regarding other environmental constraints, many studies reported increased
MSR expression in conditions leading to osmotic stress such as water shortage, high salt, and low temperature (
Table 1). This was first established from microarray data in the Arabidopsis plant model [
46,
47]. In maize, most
MSR genes are up-regulated in root, stem and leaf in the presence of polyethylene glycol (PEG) or NaCl with distinct kinetics depending on gene type and organ [
48]. Consistently, in rice,
MSRA4.1 and
MSRB1.1 expression is enhanced by mannitol, high salt and low temperature [
55]. In other respects, a higher MSRA protein abundance was observed in cold-hardened rye plants [
67] and in maize seedlings, low temperature induces the expression of
MSRA5 in mesocotyl [
81]. In soybean, Chu et al. [
69] reported differential expression of the five
MSRB genes in response to drought and high salt. Most importantly, they observed that three of them (
MSRB2,
B3 and
B5) show increased transcript levels in response to drought, but only in leaf and at distinct vegetative or reproductive stages. In tobacco,
MSRA4 expression is up-regulated by dehydration and cold, but not modified by high salt [
59], whereas that of
MSRB3 is enhanced by cold and salt [
58]. Finally, in tomato,
MSRA3 and
MSRA4 are substantially up-regulated by mannitol, high salt, and low temperature [
82]. Altogether, these data give strong credence for essential functions of MSRs in plant responses to osmotic constraints. Accordingly, in the
Atriplex halimus halophyte species, cultivation in the presence of 300 mM NaCl increased the abundance of plastidial MSRA concomitantly to a higher total MSR activity in a salt-tolerant genotype compared to a salt-sensitive one [
83]. However, in barley, an increased protein amount of one MSR isoform was noticed using a proteomic approach in a salt-susceptible genotype compared to a salt-tolerant one [
84], and no difference was noticed in the amount of plastidial MSRs in two cultivars exhibiting contrasted response to water deficit [
85]. In other respects, exposure to carbonate, which induces alkaline stress in addition to osmotic and ionic stresses, leads to the expression of most
MSRB genes in
Glycine soja whether in leaf or in root [
60].
In comparison, less is known regarding the expression of
MSR genes in response to biotic stress. The first evidence was provided in Arabidopsis plants that display a strongly increased
MSRA4 transcript level following infection by the cauliflower mosaic virus, but no change in response to a virulent
Pseudomonas syringae strain [
49]. In papaya, infection by the ringspot virus leads to up-regulation of
MSRB1 expression in the late stages [
54]. Most interestingly, some
MSR genes could be involved in plant immune responses. Thus, in poplar leaves, the abundance of a plastidial MSRB is unchanged during infection by an incompatible rust
M. larici-populina strain, whereas the protein level increases in the presence of a compatible strain. In contrast, the amount of another MSRB strongly decreases after infection either with compatible or incompatible fungi [
50]. In pepper, the level of a transcript coding for a plastidial MSRB isoform first strongly decreases following infection both with compatible and incompatible
Xanthomonas axonopodis strains, and then is restored to the initial level only in the case of the compatible reaction [
56]. In
A. thaliana, avirulent and virulent
P. syringae strains lead to very distinct expression patterns for
MSRB7 and
MSRB8, both being much more strongly up-regulated in the case of an incompatible reaction [
86]. Moreover, an increased
MSRA2 transcript level was noticed early following infection of Arabidopsis seedlings by the parasite plant
Orobanche ramosa [
87]. Altogether, these data indicate that MSRs likely participate in immunity mechanisms and active defense against most types of biotic constraints, to which plants are exposed.