Free Radical Biology and Medicine 122 (2018) 181–192

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Free Radical Biology and Medicine

journal homepage: www.elsevier.com/locate/freeradbiomed

Post-transcriptional regulation of the oxidative stress response in plants T

a,b a,b,⁎ a,b,1
Valerie Van Ruyskensvelde , Frank Van Breusegem , Katrien Van Der Kelen
a
Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium
b
Center for Plant Systems Biology, VIB, 9052 Ghent, Belgium

A R T I C LE I N FO A B S T R A C T

Keywords: Due to their sessile lifestyle, plants can be exposed to several kinds of stresses that will increase the production of
Post-transcriptional gene regulation reactive oxygen species (ROS), such as hydrogen peroxide, singlet oxygen, and hydroxyl radicals, in the plant
RNA-binding proteins cells and activate several signaling pathways that cause alterations in the cellular metabolism. Nevertheless,
Oxidative stress when ROS production outreaches a certain level, oxidative damage to nucleic acids, lipids, metabolites, and
Redox regulation
proteins will occur, finally leading to cell death. Until now, the most comprehensive and detailed readout of
oxidative stress responses is undoubtedly obtained at the transcriptome level. However, transcript levels often do
not correlate with the corresponding protein levels. Indeed, together with transcriptional regulations, post-
transcriptional, translational, and/or post-translational regulations will shape the active proteome. Here, we
review the current knowledge on the post-transcriptional gene regulation during the oxidative stress responses in
planta.

1. Introduction
Increased reactive oxygen species (ROS) levels caused by pertur-
bations in production and scavenging homeostasis have an important
impact on the cellular environment. Hydrogen peroxide (H2O2), su-
peroxide (O2•−), singlet oxygen (1O2), and hydroxyl radicals (OH•) can
indiscriminatively interact with almost all cellular building blocks.
However, ROS can also initiate specific interactions with nucleic acids,
proteins, lipids, and metabolites. Whereas in extreme stress situations
such excessive interactions lead to overall cellular damage, targeted
interactions can trigger specific signaling events resulting in an al-
teration of the cellular metabolism toward a protective status to
counteract the imposed environmental assault [1]. The most compre-
hensive and detailed readout of the oxidative stress responses in various
organisms and cell types is certainly obtained at the transcriptome
level. Thanks to the initial advent of hybridization-based microarray
technologies and nowadays sequencing-based transcriptome methods,
our insights into the nature and dynamics of variations in transcript
levels provoked by increased ROS levels have probably reached a sa-
turation level in the most widely used model organisms [2–4]. Although
some groups of transcripts respond faithfully to multiple and generic
oxidative stress conditions, comparative studies that assessed the
relative contributions of specific ROS types, such as H2O2 or 1O2, and
their accumulation in particular organelles to changes in transcript le-
vels [5,6], demonstrated that various ROS transcriptional footprints can
be discerned during developmental processes and under biotic and
abiotic stress conditions [4,7]. Similar meta-analyses have been helpful
in indicating the ROS involvement in organellar and retrograde sig-
naling events [8–10].
In Arabidopsis thaliana plants, various ROS-generating treatments
(e.g. methyl viologen [MV], antimycin A, high light stress, and H2O2)
and/or perturbations in ROS-scavenging enzymes (such as in the cata-
lase cat2-2 mutants) trigger dramatic transcriptional changes (Fig. 1)
[4,7]. Most probably, these modifications are mainly regulated at the
gene expression level through combinations of promoter-embedded cis-
regulatory elements, transcription factors, and transcriptional reg-
ulators and are driven by upstream regulators, such as receptor-like
kinases, kinases, and phosphatases.
The largest number of differentially expressed transcripts can be
identified in plants shifted from low to high light. Exposure of dark-
grown fluorescent (flu) mutants to light for a few hours also leads to
massive transcriptional changes shortly after the transfer. In contrast,
transcriptome modifications will be less pronounced in wild-type plants
transferred to MV-containing medium. MV is a chemical that causes

Abbreviations: 8-oxo-G, 8-hydroxyguanosine; ABA, abscisic acid; APX, ascorbate peroxidase; AS, alternative splicing; CEF, circled electron flux; CSD, CuZn-superoxide dismutase; DST,
DownSTream; MV, methyl viologen; NDH, NADH-dehydrogenase; NMD, nonsense-mediated decay; NPC, nuclear pore complex; PB, processing body; Poly(A), polyadenylated; PPR,
pentatricopeptide repeat; PTC, premature termination codon; RBD, RNA-binding domain; RBP, RNA-binding protein; RNP, ribonucleoprotein particle; ROS, reactive oxygen species; SG,
stress granule; SR, serine/arginine; UTR, untranslated region
⁎
Corresponding author at: VIB-UGent Center for Plant Systems Biology, Technologiepark 927, 9052 Ghent, Belgium.
E-mail address: frank.vanbreusegem@psb.ugent.be (F. Van Breusegem).
1
Current address: Wetenschappelijk Instituut Volksgezondheid-Institut Scientifique de Santé Publique, 1050 Brussels, Belgium.

https://doi.org/10.1016/j.freeradbiomed.2018.02.032
Received 7 December 2017; Received in revised form 22 February 2018; Accepted 23 February 2018
Available online 02 March 2018
0891-5849/ © 2018 Elsevier Inc. All rights reserved.
V. Van Ruyskensvelde et al.
Fig. 1. Amount of differentially expressed genes after various ROS-gen-
erating treatments. Black and grey bars represent the amount of up- and
downregulated genes, respectively. Abbreviations: DEGs, differentially ex-
pressed genes; D-L, dark to light shift; tAPX, thylakoidal ascorbate peroxidase;
AA, antimycin A; HL, high light; O3, ozone; RGCL, restricted gas and continuous
light; DMTU, dimethylthiourea; GSH, reduced glutathione. Data obtained from
Willems et al. [4].
accumulation of superoxide radicals in the chloroplasts. Similarly,
spraying plants with H2O2 will result in less pronounced transcriptional
changes (Fig. 1) [4,7].
With the involvement of redox-based signals in many, if not all,
biotic and abiotic stress responses in plants, an overall indication re-
mains prominent for their role in the adaptation in plant growth and
performance in response to changing environments [11]. However, the
insights into these sensing and regulatory events leading to transcrip-
tional changes are still at their early stages. For example, binding of
Rap2.4a, an AP2-type transcription factor, to the promoter of the 2-Cys
peroxiredoxin A gene (2CPA) and regulating its expression level has
been shown to be redox regulated. Strongly reducing and oxidizing
conditions diminish the Rap2.4a-binding activity by promoting
monomer and oligomer formations, respectively, whereas under control
conditions or upon slightly increased ROS levels, Rap2.4a dimerizes
and activates 2CPA expression [12]. In addition, protein-protein in-
teractions with RADICAL-INDUCED CELL DEATH 1 (RCD1) support the
expression of 2CPA and other genes that encode chloroplast antioxidant
enzymes, such as thylakoid-bound and stromal ascorbate peroxidase
(tAPX and sAPX) and CuZn-superoxide dismutase 2 (CSD2) [12–14].
Another example is OXIDATIVE SIGNAL-INDUCIBLE 1 (OXI1), a
serine/threonine mitogen-activated protein kinase kinase kinase
(MAPKKK), of which the expression and kinase activity are induced by
several H2O2-generating stimuli [15]. Kinase activity assays have
proven that OXI1 is essential to fully stimulate the MAPKs MPK3 and
MPK6 that are known to be vital players in signal transduction path-
ways in response to H2O2 and to regulate the balance between growth
and defense [16].
In addition to the rather detailed knowledge on the oxidative re-
sponses at the transcriptional level, insights are emerging on the impact
of ROS and its subsequent effects at the post-transcriptional, proteome,
and post-translational levels [17–19]. However, a systems-wide view on
the impact and consequences of oxidative stress on these different levels
is still lacking.
Besides quantitative differences, oxidative stress and ROS signaling
events will also steer qualitative changes in the transcriptome, such as
alternative splicing, editing, and polyadenylation. These events will
finally affect translation rates and, hence, help in shaping the resulting
proteome. Globally, transcriptome and proteome are poorly correlated,
implying the importance of post-transcriptional regulation. Under am-
bient growth conditions, 27–46%, 40%, and 40–70% of the proteomes
from Arabidopsis, rice (Oryza sativa), and maize (Zea mays) are de-
termined via transcriptional regulation, respectively [20–22]. The re-
maining difference can be explained by regulation at the post-
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Free Radical Biology and Medicine 122 (2018) 181–192
transcriptional, translational, and post-translational levels generating
the final proteome. Not unimportantly, part of this variability can be
attributed to measurement noise and technological bias [20]. Recently,
investigation of the protein-to-mRNA ratios, both in and across different
human tissues, revealed that mean-level protein variability can indeed
result from transcriptional regulation, because most of the highly
abundant proteins have high mRNA levels [23]. Nevertheless, when
proteomes of different tissues are compared, protein variability gets
poorly explained by mRNA levels, indicating the importance of post-
transcriptional regulation to shape tissue-specific proteomes [22–25].
Here, we review the current understanding on the impact of in-
creased ROS and ROS/redox-based signaling events on quantitative and
qualitative aspects of RNA homeostasis and diversity in plants. Post-
transcriptional regulation events act as an underexplored upfront reg-
ulatory switch as part of the defense response of plants during en-
vironmental stresses.
2. Post-transcriptional regulation and the role of RNA-binding
proteins during oxidative stress responses
Before their translation into proteins, mRNAs are subjected to a
number of processing and maturation steps, such as capping, (alter-
native) splicing [(A)S], (alternative) polyadenylation, stabilization,
export, and translation initiation. To this end, mRNAs are bound by a
plethora of RNA-binding proteins (RBPs). RBPs are a large and het-
erogeneous group of proteins that can bind single-stranded (ss)RNA
and/or double-stranded (ds)RNA molecules via one or more RNA-
binding domains (RBDs), including the RNA-recognition motif (RRM),
the K-homology (KH) domain (binding both ssRNA and ssDNA), the
dsRBD (binding dsRNA in a sequence-independent manner), RNA-
binding zinc finger (ZnF) domains, the cold shock domain, the
PIWI-ARGONAUTE-ZWILLE domain, pentatricopeptide repeats (PPRs),
the DEAD/DEAH Box domain, and Pumilio repeats [26–29]. In addi-
tion, some RBPs contain one or more auxiliary domains, such as gly-
cine-rich, arginine-rich, arginine-glycine, serine-arginine (SR), and ar-
ginine-aspartate repeats, and Tudor-SN [26–30] that are involved in
protein-protein interactions and dictate the RNA-binding specificity,
hence providing a regulation mechanism for the RBP function [31,32].
Based on the presence of RBDs, approximately 1600 genes in
Arabidopsis are estimated to encode RBPs (own unpublished data),
comparable with the 1542 RBPs annotated in the human genome [33].
Several plant RBPs are specific, such as the flowering time control
protein FCA (AT4G16280) and FPA (AT2G43410), both involved in the
flowering pathway, as well as some PPR proteins that function in RNA
metabolism in chloroplasts and mitochondria, thus probably per-
forming plant-specific functions [34–36]. Moreover, the sessile nature
of plants might enhance the need for an increased number of RBPs with
more versatile functions to be able to cope with highly variable en-
vironmental conditions. Based on genome analysis of RRM- and KH-
containing RBPs in Arabidopsis, these RBPs were found to feature
combinations of protein domains that differ from those of metazoan
RBPs [28].
Although the number of functionally studied RBPs in plants is still
limited, some progress has been made. RBPs have been demonstrated to
play a crucial role during normal plant growth and development [37],
but research on RBPs with a regulatory role during oxidative stress
responses in planta is still in its infancy. Here, we will highlight some
examples of the role of RBPs in the post-transcriptional stress responses,
more specifically during capping, (A)S, (alternative) polyadenylation,
RNA stability, and in translational control (Fig. 2 and Table 1).
2.1. mRNA capping and polyadenylation in response to oxidative stress
The first step in pre-mRNA maturation is the addition of a 7-me-
thylguanosine (m7G) cap at the 5′ end of the pre-mRNA that will in-
crease transcript stability and translational efficiency. The
V. Van Ruyskensvelde et al. Free Radical Biology and Medicine 122 (2018) 181–192

Fig. 2. Graphical overview of all post-transcriptional processes regulated by the oxidative stress response. RNA processes are indicated in italics, whereas
proteins affected by oxidative stress and discussed in this review are indicated in green, next to the RNA processes in which they are involved. UTR, introns, and
exons are depicted as grey, white, and black rectangles, respectively. NPC, nuclear pore complex.

C-TERMINAL DOMAIN PHOSPHATASE-LIKE 1 (CPL1/SHINY4 [SHI4]/
FIERY2 [FRY2]) and the KH domain-containing nuclear localized pu-
tative RBP SHINY1 (SHI1/CPL2/RCF3) can modulate cold and abscisic
acid (ABA) stress responses by interacting with each other via the
dsRNA-binding motif 1 (dsRBM1) of SHI1 [38,39]. As KH domain-
containing proteins can bind both ssDNA and ssRNA, SHI1 could direct
CPL1 to the promoter of a target gene and/or the nascent mRNA, in
which CPL1 may dephosphorylate Ser-5 on the C-terminal domain
(CTD) of polymerase II, thereby inhibiting transcription by preventing
mRNA capping and blocking the transition from transcription initiation
to elongation of stress-responsive genes [38,39]. Nevertheless, whether
ROS play a role in mRNA capping is unknown.
Intriguingly, mRNA capping is not limited to the nucleus, but
appears to take place in the cytoplasm as well, giving the cells the
opportunity to ‘recap’ decapped mRNA and to make them available
again for translation. The cytosolic murine capping enzyme enhances
the recovery of sodium arsenite-induced oxidative stress in murine er-
ythroleukemia cells [69], showing the importance of ‘recapping’
mRNAs after stress treatment. In addition to mammalian cells [70],
cytoplasmic capping is also observed in Trypanosomes [71], but, to our
knowledge, cytoplasmic capping has still not been detected in plants.
Another level of post-transcriptional regulation is polyadenylation.
CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR 30
(CPSF30), a polyadenylation factor subunit homolog, is implicated in
oxidative stress tolerance [40,41]. Due to alternative polyadenylation,
this gene gives rise to two different polypeptides: the smaller one

Table 1
Proteins and sRNAs involved in post-transcriptional processes under several stress conditions. Proteins and sRNA discussed in this review are listed.
Abbreviations: 3-AT, 3-amino-1,2,4-triazole; BSO, buthionine S,R sulfoximine; MV, methyl viologen.
Protein/sRNA Plant RNA metabolism Stress Refs.

CPL1/SHI4/FRY2 Arabidopsis thaliana mRNA capping; polyadenylation Cold [38,39]

SHI1/CPL2/RCF3 Arabidopsis thaliana mRNA capping; polyadenylation Salt, ABA, cold, heat [38,39]
CPSF30 Arabidopsis thaliana Polyadenylation 3-AT, BSO, MV [40,41]
PAPS1 Arabidopsis thaliana Polyadenylation MV, biotrophs [42,43]
GRP7 Arabidopsis thaliana (Alternative) splicing; RNA export H2O2, ABA, drought, cold, freezing, salt, mannitol [44–47]
LOS4 Arabidopsis thaliana RNA export Cold [48]
NUP160/SAR1 Arabidopsis thaliana RNA export Cold [49]
ESD4, SIZ1, sumoylation Arabidopsis thaliana RNA export H2O2, MV, heat [50,51]
SLG1, SLO1, SLO2, AHG11 Arabidopsis thaliana RNA editing ABA [52–54]
OCP3 Arabidopsis thaliana RNA editing Pathogen [55]
PrfB3 Arabidopsis thaliana RNA stability MV, high light [56]
CAF1 Arabidopsis thaliana RNA degradation MV, salt [57]
miR528 Oryza sativa, Zea mays RNA degradation H2O2, drought [58,59]
miR398 Arabidopsis thaliana RNA degradation High light, heavy metal, salt, MV, ozone, heat [60–63]
SRO5-P5CDH nat-siRNA Arabidopsis thaliana RNA degradation H2O2, salt [64]
1
MBS Arabidopsis thaliana Translation O2, high light [65]
RceIF5A Arabidopsis thaliana Translation Heat, mannitol, H2O2 [66]
RBCL Chlamydomonas reinhardtii RNA oxidation H2O2 [67]
TRM4B Arabidopsis thaliana RNA methylation H2O2, MV [68]

183
V. Van Ruyskensvelde et al.
encodes a protein similar to the yeast and mammalian polyadenylation
factor subunits YTH1P and the 30-kD subunit of CPSF30 [40] and the
longer one contains the CPSF30-related domain and a second domain
connected to the mammalian splicing-related factor YT521-B [72]. A
knockout in the short version of the encoded polypeptides is sufficient
to trigger tolerance to oxidative stress by selective alteration of the
poly(A) site for a subset of transcripts and not by general gene ex-
pression reprogramming [41,73]. Similarly, knocking out CPSF30 in
lesion-simulating disease1 (lsd1), mitogen-activated protein kinase 4
(mapk4), constitutive expressor of pathogenesis-related genes 5 (cpr5), and
cat2 mutants will suppress their cell death phenotype [74]. Addition of
poly(A) tails protects the mRNA from unregulated degradation during
export to the cytoplasm and the recruitment of the translational ma-
chinery. Hence, alternative polyadenylation can influence these pro-
cesses and modify the protein functionality as well. Approximately 70%
of the Arabidopsis genes entail more than one poly(A) site [75]. CPSF30
activity is regulated in two different manners. First, because it loses its
RNA-binding activity when bound to calmodulin via its calmodulin-
binding domain, it can be regulated calcium dependently [40].
Nevertheless, complementation of the cpsf30 mutant with a mutant
CPSF30 protein incapable of binding calmodulin is still sufficient to
restore oxidative stress sensitivity, implying a calmodulin-independent
effect on oxidative stress tolerance [73]. Second, two cysteine residues
in one of the CCCH Zn finger motifs in CPSF30 form a disulfide bond, of
which the reduction impairs its endonuclease activity. Hence, the
CPSF30 activity in Arabidopsis is regulated in a redox-regulated manner
[76,77].
Another example is PAPS1, one of the four canonical nuclear
poly(A) polymerases identified in Arabidopsis. Similar to cpsf30 mu-
tants, mutants lacking a functional PAPS1 gene are more tolerant to
oxidative stress than wild-type plants [42]. Transcripts with an altered
poly(A) pattern in paps1 mutants include those coding for ribosomal
proteins and proteins involved in plastidial redox homeostasis. Genes
with modified transcript abundancies in the cpsf30 mutants have a re-
duced poly(A) tail length in paps1 mutants, suggesting a functional
linkage between CPSF30 and PAPS1. Interestingly, paps1 cpsf30 double
mutants are not viable, indicating that both genes target at least some
overlapping transcripts. However, a yeast two-hybrid experiment un-
covered that both proteins do not directly interact with each other.
Fluorescence emission measurements revealed that in the paps1 mu-
tants the chloroplasts are in a more oxidized state than those in the wild
type [42]. In addition, paps1 mutants experience a constitutive immune
response independent from salicylic acid, but via the EDS1/PAD4
pathway [43]. Through the constitutive occurrence of low oxidative
stress levels, these plants are primed toward more harsh oxidative stress
treatments, explaining the increased tolerance of paps1 mutants to MV
and the biotrophic oomycete Hyaloperonospora arabidopsidis [42,43].
Recently, an increase in noncanonical alternative polyadenylation
has been reported upon hypoxia treatment in Arabidopsis [78]. These
noncanonical polyadenylated mRNA isoforms mapped to the 5′-un-
translated region (UTR), introns, and protein-coding regions. Surpris-
ingly, isoforms with poly(A) tails mapping to the 5′-UTR were as stable
as canonical poly(A) mRNA and seemed to be highly associated with
polysomes. In contrast, poly(A) isoforms mapping to introns and pro-
tein-coding regions were less stable and underrepresented in the poly-
somes, indicative of a negative regulation of the corresponding gene
expression levels [78].
2.2. Oxidative stress affects (alternative) splicing
During splicing, intronic sequences are removed from the pre-mRNA
by the spliceosome, which consists of five small nuclear ribonucleo-
protein particles together with many splicing factors [79]. Multiple
splice sites in genes offer the option to process transcripts in multiple
ways, producing numerous mRNA isoforms, thus expanding the pro-
teome complexity. In Arabidopsis, AS is a widespread phenomenon,
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Free Radical Biology and Medicine 122 (2018) 181–192
because approximately 60% of the intron-containing genes undergo AS
[80,81]. Intron retention is most prevalent in Arabidopsis [25,81] and
can result in the degradation of the transcript due to the presence of
premature stop codons that activate the nonsense-mediated decay
(NMD) pathway [82,83]. Alternatively, the transcripts can be retained
in the nucleus, where they can be stored temporally as a consequence
[84]. Other AS events include exon skipping, alternative 5′ and 3′ splice
sites, and a combination thereof. Exon skipping can exclude or re-
arrange discrete protein domains, possibly resulting in a different
functionality and altered subcellular targeting of the protein [85].
When plants are exposed to salt stress, 5% of all intron-containing genes
are differentially spliced. The alternative splice site selection occurs
most frequently four nucleotides up- or downstream of the dominant
sites and exon skipping tends to link with alternative splice site selec-
tion. Gene ontology enrichment analysis revealed that these genes
function in response to stresses and RNA splicing [86].
AS is controlled by a plethora of factors, such as SR proteins [87,88]
and heterogeneous (hn)RNPs [89,90] that can bind to regulatory se-
quence motifs in the transcripts. In addition, transcripts of genes in-
volved in AS regulation are alternatively spliced upon one or more
stress treatments, such as cold and heat stresses [91–93]. However,
treatment of seedlings with H2O2 or methyl jasmonate did not affect the
expression or splicing patterns of SR genes [92]. The importance of AS
to modify the stress response has recently been summarized [80,94],
but instances of the direct involvement of ROS or redox-dependent
mechanisms in (A)S are limited.
The impact of ROS on the splicing of a specific gene is illustrated by
the GUARD CELL OUTWARD RECTIFYING K+ (GORK) channel that is
involved in NaCl-induced programmed cell death in a ROS-dependent
manner [95,96]. Transcript levels of these GORK channels increase
upon cold, drought, ozone, and salt stresses [97]. Reverse transcription-
polymerase chain reaction analysis revealed the presence of two GORK
mRNA isoforms after exposure to ozone stress: a functional small in-
tron-free mRNA and a larger mRNA still containing introns 10 and 11
[96]. Surprisingly, the correctly spliced intron-free isoform is only
present when subjected to ozone, whereas under all other conditions
only the not completely spliced isoform is detectable, suggesting that
ozone-activated splicing proteins are needed to fully splice the pre-
mRNA of GORK. Although the effect on cell cultures treated with MV
was the same, it was abolished by treatment with the O2•− scavenger
Tiron or H2O2, strongly hinting at a specific role for O2•− in the reg-
ulation of GORK splicing to establish K+ effluxes during ozone-induced
programmed cell death [96].
A more indirect example on how oxidative stress can alter splicing
patterns is provided by the GLYCINE-RICH RNA-BINDING PROTEIN 7
in Arabidopsis (AtGRP7), of which the protein levels are strongly up-
regulated upon H2O2 treatment [46]. AtGRP7 has been shown to affect
ABA, drought, cold, freezing, and osmotic (salt and mannitol) stress
tolerances [44,45,47]. In addition, it influences AS via a direct inter-
action with transcripts including its own transcripts, but also those from
other stress-related genes, such as the SQUAMOSA PROMO-
TER-BINDING PROTEIN-LIKE 2 (SPL2) and the GLUTATHIONE S-
TRANS-FERASE Ζ-1 (GSTZ1) under optimal growth conditions [98].
SPL2 is downregulated after heat shock and plays a role in heat stress
memory [99], whereas GSTZ1 is upregulated after sorbitol treatment
[100]. However, no changes in transcript levels of these genes are ob-
served in plants overexpressing GRP7 grown in the absence of any stress
[101], suggesting that GRP7 plays a role in modifying the functionality
and localization of the corresponding protein instead of in altering the
expression levels via AS under normal growth conditions. Nevertheless,
identification of RNA targets of GRP7 and their expression levels in
plants subjected to oxidative stress will be indispensable to determine
its role in the oxidative stress responses.
Similarly, the suborganellar targeting of the plastidic H2O2-
scavenging ascorbate peroxidase (APX) is regulated by AS. Both in
spinach (Spinacia oleracea) and tomato (Solanum lycopersicum), at least
V. Van Ruyskensvelde et al.
four alternatively spliced plastid APX isoforms (tAPX-I, sAPX-I, sAPX-II,
and sAPX-III) occur via AS events at the 3′-terminal region. Retention of
the ultimate exon in the tAPX isoform ensures the presence of the hy-
drophobic C-terminal part needed for targeting to the thylakoid mem-
branes. Signals triggering these tissue-specific AS events remain un-
known [102].
The respiratory burst oxidase homolog B (RbohB) gene from maize
provides another example of the importance of AS events during stress
responses. Two isoforms are formed via AS, RbohB-α and RbohB-β, with
tissue- and development-specific expression profiles, of which RbohB-α
is the most prevalent [103]. RbohB-β retains intron 11 that includes a
premature termination codon; hence, it will probably be degraded via
NMD. When maize plants are subjected to abiotic stresses, such as cold,
heat, UV, or salinity, RbohB-α mRNA levels increase. In addition, the
RbohB-β/RbohB-α ratio is lower after these stress treatments than that of
nonstressed plants, hinting at a stress-specific production of a specia-
lized mRNA isoform [103].
Although our knowledge on how ROS can alter AS is still limited, AS
is undoubtedly a relevant post-transcriptional regulation step that acts
during the plant response upon environmental stresses.
2.3. Has oxidative stress an impact on the mRNA export?
Once matured, mRNAs need to be exported to the cytoplasm before
translation into proteins. These mRNA molecules are part of large
messenger (m)RNP complexes in which they are associated with a
heterogeneous mix of proteins [104]. These complexes are actively
transported to the cytoplasm via nuclear pore complexes (NPCs). Ob-
viously, altered mRNA nuclear export rates of specific mRNAs affect the
downstream protein production and, thus, influence physiological
processes, including the stress responses. In situ hybridizations of Ara-
bidopsis and yellow lupin (Lupinus luteus) seedlings revealed that during
hypoxia poly(A) RNAs not needed for the stress responses are retained
in the nucleus [105], whereas re-aeration of the seedlings restored the
mRNA export to the cytoplasm. These data are coherent with the strong
reduction of the translation initiation by hypoxia and the reversal of
this repression upon reoxygenation [106]. The highest accumulation of
poly(A) mRNA in the nucleus during hypoxia occurs in the Cajal bodies
and mutants completely lacking Cajal bodies have an enhanced sensi-
tivity to hypoxia and a strong poly(A) RNA reduction in the nucleus,
indicating that Cajal bodies are not only involved in poly(A) RNA sto-
rage, but also improve the stability of these RNA molecules [105].
Nevertheless, not all mRNAs are retained in the nucleus or transla-
tionally inhibited. For example, ALCOHOL DEHYDROGENASE 1
(ADH1), a core oxygen-deprived gene, is transcriptionally upregulated
under hypoxia and exported to the cytoplasm [105,107]. In addition,
ribosome footprinting and RNA-sequencing (RNA-seq) on polysomal
RNA revealed that ADH1 mRNA is occupied by ribosomes and, thus,
probably translated into proteins [106,107]. These data hint at a se-
lective mRNA export of genes involved in survival to hypoxia stress.
Several Arabidopsis mutants defective in mRNA export that influence
the cold stress tolerance have been identified: GRP7 [45], LOW EXPR-
ESSION OF OSMOTICALLY RESPONSIVE GENES4 (LOS4) [48], and
NUCLEOPORIN160 (AtNUP160/SAR1) [49]. Although their transcript
levels are not affected by abiotic stress treatments, mutants in these
genes have an increased sensitivity to cold stress.
Moreover, mutations in the small ubiquitin-like modifier (SUMO)
protease ESD4 and the SUMO E3 ligase SIZ1 display an enhanced nu-
clear poly(A) retention [51], involving sumoylation in nuclear export.
Furthermore, several abiotic stresses, such as oxidative stress and heat
stress, increase the levels of SUMO-conjugated proteins [50]. In mam-
mals, oxidative stress inactivates SUMO isopeptidases [108,109]. Su-
moylation seemingly acts upstream of the mRNA export in plants, be-
cause any disparity in SUMO homeostasis leads to nuclear mRNA
retention, most probably through sumoylation of proteins involved in
mRNA export [51].
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Free Radical Biology and Medicine 122 (2018) 181–192
2.4. Oxidative stress and RNA editing
Many of the mitochondrially and chloroplastically encoded tran-
scripts are edited before their translation into proteins. These editing
factors encode PPR proteins and are involved in other organellar RNA
maturation steps as well, such as splicing and cleavage [110]. RNA
editing comprises C-to-U and, to a lesser extent, U-to-C conversions in
the mRNA-coding region [111,112]. Furthermore, A-to-I conversions
have been observed in tRNAArg that appeared to be essential for effi-
cient chloroplast translation [113]. RNA editing is a site-specific pro-
cess that can create new start/stop codons, affect (A)S, micro (mi)RNA
maturation, and amino acid changes, thereby possibly altering the
protein activity and interactions with other proteins and/or nucleic
acids [114]. Mutants in mitochondrial RNA-editing factors, such as
SLOW GROWTH1 (SLG1 [AT5G08490] and SLO1 [AT2G22410]), SLO2
(AT2G13600), and ABA HYPERSENSITIVE GERMINATION11 (AHG11),
lead to defective RNA-editing of transcripts encoding proteins involved
in the electron transport chain, i.e. nad3, nad4, and nad9 [52–54].
Mutations in these RNA-editing factors cause ABA hypersentivity and
trigger increased levels of ROS-responsive genes [52–54]. Nevertheless,
the specific role of ROS in RNA editing is still not unraveled. In the
chloroplasts, the nucleus-encoded homeodomain-containing protein
OVEREXPRESSOR OF CATIONIC PEROXIDASE3 (OCP3) edits the mRNA
of the NADH-dehydrogenase (ndhB), a subunit from the NDH complex
involved in the circled electron flux (CEF) around photosystem I (PSI)
[55]. Upon fungal attack, the OCP3 expression levels are down-
regulated, thereby disturbing the editing process of ndhB and creating
an altered NDH complex, with a defective CEF as a consequence. Such a
defective CEF has been hypothesized to generate local ROS molecules
[55], because a functional chloroplastic NDH complex is thought to
reduce the ROS formation, thereby generating disease resistance
[115,116].
2.5. Oxidative stress influences RNA stability
Cellular transcript abundancies are determined by mRNA synthesis
and degradation rates. Thus, increased steady-state levels measured by
microarray or RNA-seq experiments can be a combination of increased
mRNA synthesis via enhanced promoter activity, degradation inhibi-
tion, and/or improved transcript stability. Several characteristics of the
transcript mRNA govern its stability: transcripts derived from intron-
containing genes are significantly more stable than those from intron-
less genes. Also the presence of one or more sequence elements in the
UTRs affect the transcript stability [117]. Similarly, the 5′-UTR, 3′-UTR,
and open reading frame (ORF) length as well as the presence of sec-
ondary structures, introns, small (s)RNA-binding sequences, and pseu-
doknots define the degradation vulnerability [117,118]. Genome-wide
profiling of uncapped mRNA molecules, with a monophosphate at their
5′ end and a 3' poly(A) tail, revealed that the decapping process is
tightly regulated [118]. Protein-encoding transcripts involved in es-
sential biological processes are weakly uncapped, whereas transcripts
of pseudogenes, transposon-related genes, or regulatory genes have
increased decapping rates [118]. How and where cytoplasmic RNA can
be processed, i.e. translated, sequestered, and degraded in polysomes,
stress granules (SGs), and processing bodies (PBs), respectively, and the
role of these processes during plant development and stress conditions
has already been reviewed [119]. Hence, we will focus on how oxida-
tive stress determines the mRNA fate in the cytoplasm.
The fact that oxidative stress can affect the mRNA stability is well
illustrated by SALT OVERLY SENSITIVE (SOS1), a plasma membrane
Na+/H+ antiporter [120]. Whereas SOS1 mRNA is unstable under
normal growth conditions, its stability increases under salt and H2O2
stresses in a concentration-dependent manner without affecting the
promoter activity. Treatment with the ROS antagonists di-
methylthiourea or deferoxamine reduced the SOS1 mRNA stability,
confirming the role of ROS in this process. The 3′ end of the SOS1
V. Van Ruyskensvelde et al.
mRNA that encodes the cytosolic part is responsible for this transcript
stability [120]. In addition, sos1 loss-of-function mutants show an en-
hanced tolerance to MV treatments and are hypersensitive to salt stress.
Yet, NADPH oxidase inhibition with diphenyleneiodonium has a similar
impact, implying that this tolerance depends on the NADPH oxidase
activity. In general, the following working model has been proposed:
when plants are subjected to salt stress, SOS1 is activated, directs the
Na+ export, and decreases the pH in the cytoplasm and, in turn, acti-
vation of NADPH oxidases produces apoplastic ROS that stabilize the
SOS1 mRNA [120].
Also in the chloroplasts, the mRNA molecules are stabilized by
oxidative stress. For example, the ribosomal peptide chain release
factor B3 (PrfB3) is part of a complex binding the mRNA of the PetB
gene encoding cytochrome b6, which forms the cytochrome b6f complex
in the thylakoid chloroplast membrane together with cytochrome f
[56]. This complex oxidizes the reduced plastoquinone, which in turn
can be reduced again by PSII during photosynthesis [121]. MV and high
light treatments decrease PrfB3 levels by 50% compared to the wild-
type levels. Moreover, PrfB3 mutants lack 3′-processed PetB transcripts
and are defective in the cytochrome b6f accumulation in the chlor-
oplasts. PrfB3 proteins are involved in the stabilization of 3′-processed
PetB transcripts by inhibiting the 3′-to-5′ exonucleotic degradation
[56]. Finally, increased levels of glutathione improve the mRNA sta-
bility of the ethylene-biosynthesizing enzyme 1-aminocyclopropane-1-
carboxylate oxidase [122].
2.6. Oxidative stress and its role in RNA degradation and decay
The initial and rate-limiting step in mRNA degradation is shortening
(deadenylation) of the poly(A) tail, whereafter the mRNA can be de-
graded from 3′ to 5′ or from 5′ to 3′, although the latter requires first
decapping of the mRNA [123]. In eukaryotes, deadenylation is mainly
mediated by the conserved CARBON CATABOLITE REPRESSOR4
(CCR4)-NEGATIVE ON TATA (NOT) complex, composed of two
de-adenylase subunits with 3′-to-5′ exonuclease activity, i.e. CCR4 and
the CCR4-ASSOCIATED FACTOR1 (CAF1) protein, and multiple NOT
enzymes [124]. In Arabidopsis, several CAF proteins are involved in
abiotic stress tolerance [57]. Mutants of AtCAF1a and AtCAF1b have
increased susceptibility to MV treatment. On top of this, AtCAF1a
mutants are more tolerant to salt stress, indicating that some of their
RNA targets are shared, whereas others are unique [57]. Identification
of the RNA targets of these proteins during optimal and suboptimal
growth conditions would reveal their mode-of-action under these
conditions.
Transcripts with premature termination codons (PTCs) can be pro-
duced by AS, transcription errors, or mutations. These aberrant tran-
scripts will be recognized by the NMD RNA surveillance system for
degradation. NMD is conserved in eukaryotes and is coupled with the
first round of translation in which potential PTCs will be detected
[125]. Moreover, NMD can also influence the abundance of normal
transcripts [126]. Mutants in the NMD surveillance revealed that nu-
merous transcripts targeted by NMD are linked with immune responses
and that degradation inhibition of these transcripts confer pathogen
resistance in plants [126].
Also binding-site sequences of small (s)RNA, e.g. miRNA and small
interfering (si)RNA, in the mRNA molecule can regulate the degrada-
tion rate [117,118]. miRNAs are generated from RNA polymerase II
transcripts containing stem loop structures that are cut in 18–24-nu-
cleotide-long miRNAs. Binding to their target RNAs will lead to RNA
cleavage or translation inhibition, whereby the latter occurs more fre-
quently in planta [127]. In rice, seven miRNAs responsive to H2O2
treatment have been identified with target genes involved in tran-
scriptional regulation, nutrient transport, auxin homeostasis, cell pro-
liferation, and programmed cell death [58]. For example, miR528 is
downregulated upon H2O2 and drought stress in rice and maize, re-
spectively [58,59]. In rice, INDOLE ACETIC ACID (IAA)-ALANINE
186
Free Radical Biology and Medicine 122 (2018) 181–192
RESISTANT 1 (IAR1) mRNA has been identified as a target of miR528
[58]. IAR1 enhances hydrolysis of IAA-amino acid conjugates and,
because free IAA is prone to oxidation and will be degraded under
oxidative stress conditions, increased IAR mRNA levels might com-
pensate the IAA loss in the cell under these conditions [58].
Also the expression of miR398 is altered during different types of
stresses. Upon various oxidative stress-favoring conditions, such as high
light, heavy metal, salinity, MV, and ozone stresses, a decrease in its
expression occurs [60–63]. Surprisingly, heat stress enhances miR398
expression, thereby improving thermotolerance [128]. miR398 is
regulated via direct binding by GRP7 and targets the transcripts of
CSD1 and CSD2 [62,129,130].
mRNA decay can also be triggered via natural (nat)-siRNAs derived
from natural antisense transcripts [64] as illustrated by SIMILAR TO
RCD ONE5 (SRO5) and Δ1-PYRROLINE-5-CARBOXYLATE DEHYDROG-
ENASE (P5CDH). The locus of P5CDH partially overlaps with the anti-
sense SRO5 locus, hence sharing sequence similarity at their 3′ end.
SRO5 expression is induced upon salt and H2O2 treatment, thereby
enabling the formation of SRO5-P5CDH dsRNA duplexes. These du-
plexes are processed by DICER-LIKE2 (DCL2) into the 24-nucleotide
SRO5-P5CDH nat-siRNA that targets the P5CDH mRNA for initial
cleavage. Further processing by DCL1 produces 21-nucleotide P5CDH
nat-siRNAs that promote P5CDH mRNA degradation [64]. P5CDH
converts proline into glutamate by oxidizing Δ1-pyrroline-5-carboxylate
(P5C) [131]. Decrease of its expression level results in accumulation of
proline needed for salt tolerance, but also generates ROS. However,
because sro5 plants are more sensitive to H2O2 than p5cdh and wild-
type plants, SRO5 has been proposed to reduce ROS accumulation by
inhibiting its production or enhancing its detoxification [64].
Besides RNA target sequences, other cis-elements can influence the
mRNA decay. One example is the DownSTream (DST) motif that ori-
ginally has been identified in the 3′-UTR of the unstable
AUXIN-INDUCIBLE SMALL AUXIN-UP RNA 1 (SAUR1) mRNA in soy-
bean (Glycine max) [132]. Genome-wide analysis revealed that this
motif is enriched in unstable transcripts in Arabidopsis [117]. Arabi-
dopsis FERRITIN1 (FER1) also contains the DST sequence in its 3′-UTR.
Treatment of cell suspensions with Fe or H2O2 triggered AtFER1 in-
stability [133]. In contrast, SAUR1 remains unchanged upon Fe treat-
ment, indicating that oxidative stress selectively targets mRNAs to the
DST-regulatory pathway by specific binding of one or multiple RBPs to
the DST element and/or the presence of additional elements in the
target mRNA molecules [133].
2.7. The effect of oxidative stress on translation
The final level in the post-transcriptional regulation is the transla-
tion control. Actively translated mRNAs are bound by ribosomes and
can be isolated by means of density centrifugation [134] or affinity
purification based on the expression of an epitope-tagged ribosomal
protein from the large ribosomal subunit [135,136]. These techniques
have been used to study differential translation in specific tissues or
under adverse conditions, such as cold [107], dehydratation [137], heat
and high salinity [138,139], hypoxia [24,106,140], ABA [141], ozone-
induced oxidative stress [142], high light [143], MV [144], and 1O2
[145]. In general, when plants have been subjected to oxidative stress
conditions, ribosomes halt at the translation initiation sites, before their
removal from the mRNA, leading to selective translational inhibition of
approximately half of the mRNAs present in the cell [106]. Whereas
synthesis of housekeeping proteins is inhibited under abiotic stress
conditions, a fraction of the transcripts is still translated, for instance
via the presence of Internal Ribosome Entry Sites (IRES) allowing cap-
independent translation initiation [146] or other existing sequence
and/or structural features (see below). In addition, as demonstrated
under oxygen deprivation conditions, global translation repression re-
sults in the needed energy preservation of ATP, because translation is
one of the most energy-consuming cellular processes [106,142,147].
V. Van Ruyskensvelde et al.
Furthermore, ribosome profiling or genome-wide mapping of mRNA
regions that are protected from nuclease digestion by ribosomes pro-
vide, besides the identification of actively translated messengers, also
information on the number of ribosomes per transcript, enabling
quantitative translation measurements [107,148,149]. Both polysomal
RNA sequencing and ribosomal profiling have revealed transcripts that
are translationally controlled under several abiotic stress conditions.
Protein synthesis is mostly regulated at the level of the translational
initiation, with the phosphorylation status of a number of translation
initiation factors possibly affecting the translation [150], thereby
linking directly post-transcriptional and post-translational regulation
events. In addition, plant-specific isoforms of the eukaryotic translation
initiation factors eIF4G/eIF4F (eIFiso4G/eIFiso4F) probably control the
translation of specific mRNA populations [151,152]. Moreover, eIF4A/
eIFiso4A might function as redox sensors of the translation initiation
through the formation of an intermolecular disulfide bond between two
eIF4E molecules, resulting in the loss of its cap-binding capacity and,
hence, translation inhibition [153]. The presence of upstream (u)ORFs
can block the translation from the main (m)ORF [137,154], thus pro-
viding a translational regulation mechanism during oxidative stress.
The enrichment of uORFs in the mRNA of regulatory proteins has been
suggested to modulate cell type-specific translation [144,155]. Several
other structural features can influence the translation efficiency during
oxidative stress: presence of one or more introns and/or motifs, low GC
levels in the 5′-UTR, short 5′-UTRs, and adenosine (A) residues in front
of the start codon of the mORF improve the general translation effi-
ciency [137,144,156]. Furthermore, cleavage of transfer (t)RNA and
ribosomal (r)RNA has been observed in plants subjected to H2O2
treatment. This process is conserved among all eukaryotes [157]. The
cleaved fragments are predicted to function in signaling processes and/
or tRNA fragments to inhibit translation by interacting with the trans-
lation machinery. Nevertheless, no changes are detected in the total
tRNA pool, indicating that cleavage of tRNA molecules plays no direct
role in translation inhibition [157]. Finally, mRNAs can be located to
subcellular particles, such as SGs and PBs. SGs form transiently under
adverse conditions and probably function in the temporary storage of
mRNAs, whereas mRNAs targeted to PBs can result in RNA degradation
[158]. In mammals, the physiology of oxidative stress-induced SGs
depend on the type of the oxidative stress inducer. For instance, SGs
formed after H2O2 treatment are smaller and more easily disassembled
than those formed by sodium arsenite [159]. SG formation by sodium
arsenite requires eIF2α phosphorylation that is not essential in H2O2-
induced SGs, potentially the reason for the different characteristics
between the two types of SGs [160,161]. In plants, SGs can be formed
upon arsenite and 1O2 stress, but the requirement of a phosphorylated
eIF2α in this process still needs to be elucidated [65,158]. Plants sub-
jected to H2O2, salt, and heat stress do not activate the eIF2α kinase
GENERAL CONTROL NONDEREPRESSIBLE 2 (GCN2) and do not re-
quire phosphorylated eIF2α to form SGs, whereas wounding, several
hormone treatments, UV, and cold stress can activate GCN2 [162]. The
Zn finger protein METHYLENE BLUE SENSITIVITY (MBS) functions as a
mediator in the 1O2 response and has been shown to associate with SGs
and PBs upon oxidative stress treatment [65]. In this manner, MBS
controls the translation and stability of specific mRNAs that are induced
in the 1O2 response. Overproduction of this protein increases the tol-
erance to high light in plants [65].
Similarly, overexpression of RceIF5A, a member of the eukaryotic
translation initiator factors from Rosa chinensis (Chinese rose), gen-
erates tolerance to heat, mannitol, and oxidative stress in Arabidopsis
[66] and increases the expression levels of CATALASE 3 (CAT3), GLU-
TATHIONE PEROXIDASE 3 (GPX3), and PYRROLE-5-CARBOXYLATE
SYNTHETASE (P5CS), whereas the opposite effect was observed in
plants with suppressed eIF5A expression [66]. The specific role of this
protein has still to be uncovered. In human cells, eIF5A has been shown
to be involved in polysome dissociation during translation inhibition
and SG formation upon oxidative stress and to require a hypusine
187
Free Radical Biology and Medicine 122 (2018) 181–192
modification for its function [163].
3. Oxidative stress leads to RNA modifications
ROS can also directly target RNA molecules. In accordance with
mammalian cells, RNA seems to be more vulnerable to oxidative stress
than DNA, more specifically to the formation of 8-hydroxyguanosine (8-
oxo-G) (or 8-hydroxydeoxyguanosine [8-oxo-dG] for DNA) [164–166].
Moreover, mRNA seems to be more sensitive to oxidation than other
RNA species and only specific cohorts are oxidized, indicating that RNA
oxidation is not a random process [167]. RNA oxidation can cause
translation errors by the formation of miscoded proteins, because 8-
oxo-G can pair with both C and A residues, or by ribosome stalling,
resulting in truncated proteins due to premature termination
[168,169]. Additionally, 8-oxo-G can misdirect miRNA to other target
sequences [170]. Currently, little is known on the control of oxidized
RNA via repair and/or degradation in plants. In HeLa cells, oxidized
RNA molecules localize to cytoplasmic foci that differ from SGs and
PBs, whereas in Chlamydomonas reinhardtii, it localizes to the pyrenoid
(a chloroplast microcompartment, in which CO2 is assimilated by the
Calvin cycle enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase
(Rubisco)), showing the importance of oxidized RNA compartmentali-
zation [67]. At the inner perimeter of the pyrenoid, chloroplastic SGs
(cpSGs) can be formed upon oxidative stress treatments and contain
chloroplast-encoded mRNAs and SG protein markers [171]. The for-
mation of these cpSGs upon oxidative stress first requires the dis-
assembly of the Rubisco holoenzyme, followed by the activation of the
RNA-binding activity of its large subunit (RBCL) to bind mRNA and the
degradation of the small subunit (RBCS) [171–173]. In addition, oxi-
dative stress promotes the aggregation potential of RBCL and in this
manner the assembly of cpSGs [171,172].
In Chlamydomonas lacking a functional RBCL, the oxidized RNA
levels are high. In contrast, RBCS mutants contain low amounts of
oxidized RNA and are more tolerant to oxidative stress [67]. These
results indicate that RBCL plays a role in controlling oxidized RNA le-
vels in the pyrenoid.
In Escherichia coli and HeLa cells, several RBPs have been identified
that specifically recognize oxidized RNA, among them the human het-
erogeneous ribonucleoprotein D0 (hHNRNPD0), hHNRNPC1/C2, and
the polynucleotide phosphorylase (PNPase) [174–176]. Suppression of
the expression of both hHNRNPD and hHNRNPC1/C2 increased the
sensitivity to H2O2 stress [174]. Similarly, downregulation of PNPase in
human and E. coli cells results in increased amounts of 8-oxo-G–con-
taining RNA and an enhanced sensitivity to H2O2 [176,177]. PNPase is
evolutionarily conserved and is also found in planta [178]. Never-
theless, the role of this PNPase in RNA oxidation is still unknown and,
currently, RBPs that bind 8-oxo-G RNA in planta have not been identi-
fied.
Besides the importance of post-transcriptional methylation of RNA
cytosine residues to 5-methylcytosine (m5C) in plant development, its
role in the oxidative stress response has recently been demonstrated
[68]. In plants, two classes of RNA methyltransferases have been de-
tected: DNA methyltransferase 2 (DNMT2) and tRNA-specific methyl-
transferase 4B (TRM4B), a homolog of the animal NSUN2. Tran-
scriptome-wide mapping of RNA m5C has revealed that TRM4B is
involved in the methylation of mRNA, long noncoding RNA, tRNA, and
other noncoding RNA with high frequencies at their 3′-UTR. Plants
deficient in TRM4B are highly sensitive to H2O2 and MV, but no phe-
notypical difference with wild-type plants is observed after exposure to
salt stress, hinting at a restricted role of this methyltransferase in the
oxidative stress responses. Trm4b-1 mutants have a reduced tRNA sta-
bility of specific tRNA molecules and constitutively activate genes in-
volved in the oxidative stress responses [68], again highlighting the
importance of the tRNA stability [157].
V. Van Ruyskensvelde et al.
4. Redox-regulated genes with RNA-binding properties
Multiple proteins are constitutively present in the cells and are ac-
tivated or deactivated by post-translational modifications (PTMs) trig-
gered by one or more cues. Phosphorylation, sumoylation, ubiquitiny-
lation, cysteine oxidation, glutathionylation, and methionine oxidation
of proteins is influenced by oxidative stress [17–19,179–183]. Nu-
merous proteins involved in cytosolic translation are redox regulated
[184], however redox regulation is not limited to proteins engaged in
protein translation, but also modifies proteins participating in other
post-transcriptional processes. As already mentioned, CPSF30, a poly-
adenylation factor subunit homolog, can be controlled in a redox-
regulated manner [76,77]. Another example is RNaseIII-like1 (RTL1), a
RNase III endonuclease, implicated in dsRNA cleavage of rRNA, small
nucleolar RNA, small nuclear RNA, and RNA decay, and of which the
expression levels are induced upon viral stress conditions [185]. This
protein has a conserved Cys230 that can be glutathionylated, thereby
negatively affecting the secondary structure of the protein and its RNA-
binding and/or RNA cleavage activity. The glutathionylation has been
suggested to protect Cys230 from irreversible ROS oxidation and to be
reverted by glutaredoxin [185]. In addition, RTL2, involved in the 3′
externally transcribed spacer (3′ ETS) cleavage of pre-rRNA, functions
as a dimer via disulfide bonds that only can be disrupted upon dithio-
threitol treatment, hinting at the redox-regulated activity of this protein
[186]. Similarly, ANGUSTIFOLIA, a negative regulator of salt and os-
motic stress responses that colocalizes to SGs in a stress-dependent
manner, is able to sense redox changes via its NAD(H) domain [187].
Besides sensing redox imbalances, RBPs can also modify ROS ac-
cumulation during stress responses. Upon heat stress, plants over-
expressing FCA have a higher antioxidant capacity than wild-type
plants, whereas fca mutants show the opposite effect, suggesting a role
for FCA in ROS detoxification [188]. In addition, FCA overexpressors
have an enhanced tolerance to MV and heat stress. FCA adjusts ROS
levels by interacting with the transcription factor ABA-INSENSITIVE5
(ABI5), thereby regulating the expression of several antioxidant-en-
coding genes, such as 1-CYSTEINE-PEROXIREDOXIN 1 (PER1), a pro-
tein responsible for the reduction of (alkyl) hydrogen peroxides [188].
Somehow surprisingly, several proteins with oxidoreductase activities
have been identified to possess RNA-binding properties. These redox-re-
lated proteins were present in the mRNA interactomes of Arabidopsis cell
cultures, mesophyll protoplasts, leaves, and etiolated seedlings grown
under optimal growth conditions [189–191]. Interestingly, CAT3 was
identified in all three mRNA interactome studies. RNA immunoprecipita-
tion and individual-nucleotide resolution CrossLinking and Im-
munoPrecipitation (iCLIP) experiments on plants grown under optimal
growth conditions revealed that CAT3 mRNA is one of the AtGRP7 targets,
among several other transcripts of genes involved in redox homeostasis
(e.g., CAT2, FER1, WRKY33, GPX1, and GOX1), strengthening the as-
sumption that GRP7 acts as a regulator of oxidative stress responses [130].
Lastly, proteins previously shown to participate in oxidative stress re-
sponses have been characterized as RBPs, such as ALDEHYDE DEHYDR-
OGENASE 7B4 that confers oxidative stress tolerance [189,192], FER1
(see above) [190,191], MONODEHYDRO-ASCORBATE REDUCTASE 6
(MDAR6) [189,190,193], and PROTOCHLOROPHYLLIDE OXIDOREDUC-
TASE B (PORB), hinting at a dual role for these proteins [190,191,194].
5. Conclusion and future perspectives
In this review, we summarized the involvement of post-transcrip-
tional gene regulation in the oxidative stress responses. Although sev-
eral RBPs are required for an appropriate reaction in planta, information
on their mode of action during these stress responses is still rather
limited. Identification of protein-protein interactors and their RNA
targets will broaden our understanding of their function under oxida-
tive stress conditions. In addition, a comprehensive inventory of the
mRNA-bound proteome during the oxidative stress responses will be
188
Free Radical Biology and Medicine 122 (2018) 181–192
one of the key requirements to further unravel the RBPs indispensable
in the oxidative stress signaling pathways.
Acknowledgments
We thank Zhicheng Zhang for his scientific input, Patrick Willems
for providing microarray data, and Martine De Cock for help in pre-
paring the manuscript. This work was supported by the Agency for
Innovation by Science and Technology (Industrial R&D project no.
100555), the Interuniversity Attraction Poles Program (IUAP P7/29
‘MARS’) initiated by the Belgian State, Science Policy Office, and the
Research Foundation-Flanders (Grant nos. G0D7914N and G055416N).
V.V.R. is indebted to the Agency for Innovation by Science and
Technology for a predoctoral fellowship (141029).
Conflict of interest/disclosures
None.
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