Biochimica et Biophysica Acta 1819 (2012) 149–153

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Biochimica et Biophysica Acta

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / b b a g r m

RNA regulation in plant abiotic stress responses☆

Kentaro Nakaminami a, Akihiro Matsui a, Kazuo Shinozaki b, Motoaki Seki a, c,⁎
a
Plant Genomic Network Research Team, RIKEN Plant Science Center, Japan
b
Gene Discovery Research Group, RIKEN Plant Science Center, Japan
c
Kihara Institute for Biological Research, Yokohama City University, Japan

a r t i c l e i n f o a b s t r a c t

Article history: RNA regulatory processes such as transcription, degradation and stabilization control are the major
Received 15 June 2011 mechanisms that determine the levels of mRNAs in plants. Transcriptional and post-transcriptional regulations
Received in revised form 27 July 2011 of RNAs are drastically altered during plant stress responses. As a result of these molecular processes, plants are
Accepted 29 July 2011
capable of adjusting to changing environmental conditions. Understanding the role of these mechanisms in
Available online 5 August 2011
plant stress responses is important and necessary for the engineering of stress-tolerant plants. Recent studies
Keywords:
in the area of RNA regulation have increased our understanding of how plants respond to environmental
RNA regulation stresses. This review highlights recent progress in RNA regulatory processes that are involved in plant stress
Abiotic stress response responses, such as small RNAs, alternative splicing, RNA granules and RNA-binding proteins. This article is part
Non-coding RNA of a Special Issue entitled: Plant gene regulation in response to abiotic stress.
Alternative splicing © 2011 Elsevier B.V. All rights reserved.
Post-transcriptional regulation
RNA-binding proteins

1. Introduction 2. Non-coding RNAs

Environmental stresses such as drought, heat, salinity and low
temperature are major limiting factors for plant geographical
distribution and productivity. These stresses are expected to increase
in the future due to drastic changes in climate, much of which are
driven by global warming. Agriculture will be affected greatly by these
changes. Plants can acquire tolerance to these environmental stresses
through advanced molecular breeding techniques and genetic
engineering, therefore it is important to understand the molecular
mechanisms of these responses.
In natural conditions, plants are exposed to a variety of
environmental stresses. In order to understand the molecular
mechanisms of tolerance and adaptation, many stress-inducible
genes have been identified and characterized. Recently, various
types of RNA regulatory factors and processes such as small RNAs,
antisense RNAs, alternative splicing, RNA decay, RNA stability control
and RNA-binding proteins have emerged as new research areas
involved in plant stress responses (Fig. 1). In this review, we
summarize the recent findings on RNA regulation of plant stress
responses.
Recently, transcriptome analyses using high-density microarrays
and high throughput sequencing technologies have revealed a vast
number of non-coding RNAs (ncRNAs) that are expressed from
unannotated genomic regions. These ncRNAs include small RNAs,
such as micro RNAs (miRNAs) and small interfering RNAs (siRNAs), as
well as long non-coding RNAs such as natural antisense RNAs. These
ncRNAs are expected to be involved in transcriptional and post-
transcriptional regulation of gene expression and modulation of RNA
stability and translation.
2.1. Small RNAs
Small RNAs, such as miRNAs and siRNAs, are short 20 to 24-
nucleotide single-stranded RNAs. Small RNAs regulate the expression
of their complementary genes by affecting mRNA levels, chromatin
remodeling and DNA methylation. Several stress-responsive small
RNAs have been identified in plants [1,2] and their roles in the
detoxification of reactive oxygen species (ROS) have been demon-
strated [3]. Functional roles of the small RNAs in stress signaling
networks are summarized in recent reviews [4–6].

2.2. Antisense RNAs

☆ This article is part of a Special Issue entitled: Plant gene regulation in response to
abiotic stress. Whole transcriptome studies under abiotic stresses using Arabidopsis
⁎ Corresponding author at: Plant Genomic Network Research Team, RIKEN Plant
Science Center (PSC), RIKEN Yokohama Institute, 1-7-22 Suehiro-cho, Tsurumi-ku,
tiling arrays have revealed that about 7000 novel transcriptional units,
Yokohama 230-0045, Japan. Tel.: + 81 45 503 9587; fax: + 81 45 503 9584. including those that are stress-responsive map to antisense strands of
E-mail address: mseki@psc.riken.jp (M. Seki). protein-coding genes [7]. Most of these transcripts are longer than 500 nt

1874-9399/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.bbagrm.2011.07.015
150 K. Nakaminami et al. / Biochimica et Biophysica Acta 1819 (2012) 149–153
Non-coding RNAs
miRNAs
siRNAs
Antisense RNAs
Degradation
(Processing bodies)
Fig. 1. Various types of RNA regulations function in plant stress responses. Non-coding RNAs are involved in the regulation of transcription, alterative splicing and mRNA degradation.
mRNAs are degraded in processing bodies and stored in stress granules. RNA-binding proteins (RBPs) are involved in all aspects of RNA regulations.
and do not have sequence similarity with protein-coding genes,
suggesting the existence of long non-protein coding antisense RNAs.
Most of them belong to pairs of the fully overlapping sense–antisense
transcripts (fSATs). Interestingly, a significant linear correlation between
the expression ratios (treated/untreated) of the sense transcripts and the
ratios of the antisense RNAs was observed in the fSATs. The sequences of
RD29A and CYP707A1 antisense RNAs that are drought- and ABA-
inducible, were complementary to that of the sense mRNAs, indicating
that expression of the antisense RNAs depends on that of the sense mRNAs
[7]. Deep sequencing analysis has revealed that mutations of ABH1 and
EIN5 (XRN4), which are involved in mRNA processing and mRNA
degradation, respectively, affect the level of small RNAs mapped on the
antisense strand of endogenous protein-coding genes [8]. As the siRNAs
are generated from double-stranded RNAs, these results also indicate that
a certain type of antisense RNA is synthesized from mRNA templates. On
the other hand, expression of the FLOWERING LOCUS C (FLC) antisense
RNA, COOLAIR (cold induced long antisense intergenic RNA), was
controlled by a cold-inducible promoter which exists downstream of
the FLC gene [9]. A tiling array analysis of circadian regulation showed that
the majority of the rhythmic antisense transcripts overlapped with
circadian-regulated sense transcripts with a similar phase of expression
and that the distribution of the antisense RNAs was enriched toward
morning [10]. These data indicate that antisense RNAs are synthesized
through various mechanisms.
Biological functions of the antisense RNAs remain unclear in most
cases. Abiotic stress can induce expression of sense and antisense
transcripts from several transposons, retrotransposons and pseudo-
genes, which are a source of siRNAs [11,12]. Sense and antisense
transcript pairs have the potential to produce endogenous siRNAs. After
heat stress, a copia-type retorotransposon named ONSEN became
transcriptionally active and synthesized extrachromosomal DNA copies.
Heat-induced expression and transgenerational retrotransposition of
ONSEN were suppressed by siRNA-mediated silencing [13]. The cold-
induced FLC antisense transcript, COOLAIR, has a role in the epigenetic
silencing of FLC, that acts transiently in response to cold stress [9,14].
Two long intronic non-coding RNAs, COLDAIR (cold assisted intronic
non-coding RNA), that exists in the sense direction relative to FLC
mRNA, and COOLAIR, are required for establishing tri-methylated
histone H3 Lys27 at the FLC locus through the interaction of COLDAIR
with the polycomb repressive complex 2 (PRC2) [15]. COOLAIR and
STRESS
Genome
Transcription
Alternative splicing
mRNAs
Stabilization
(mRNPs)
(Stress granules)
Translation
Proteins
COLDAIR have specific mechanisms of chromatin modification mediated
gene silencing other than RdDM (RNA-dependent DNA methylation).
Previous studies have also shown that antisense RNAs participate in a
broad range of regulation such as gene silencing, RNA stability, RNA
editing and translational inhibition [16–19].
3. Alternative splicing
Alternative splicing significantly increases protein diversity in
higher eukaryotes [20]. In plants, it is known that alternative splicing
is frequently associated with environmental conditions, such as
abiotic stress [21,22]. Genome-wide studies by RNA-seq using an
Illumina high throughput sequencer indicated that alternative
splicing events occur in at least 42% of genes in Arabidopsis. It was
also found that the relative abundance of unproductive isoforms with
premature termination codons (PTC) of some essential regulatory
genes can be regulated by the nonsense mediated mRNA decay
(NMD) surveillance machinery under abiotic stress [22].
Several splicing and splicing-related factors function in the abiotic
stress response. SR proteins are a family of RNA-binding proteins
which contain a serine/arginine-rich region in their C-termini and
function as essential factors for alternative splicing [23]. Alternative
splicing of pre-mRNAs encoding several Arabidopsis SR proteins are
controlled by heat and cold stress. [24]. In response to heat stress, a
splicing factor, IRE1b (inositol-requiring transmembrane receptor
protein kinase/endoribonuclease-1b), that functions in endoplasmic
reticulum (ER) stress responses, splices the mRNA-encoding bZIP60, a
basic leucine-zipper domain transcription factor, that is required for
the up-regulation of binding protein 3 (BIP3) [25]. The floral initiator
Shk1 kinase binding protein (SKB)1/protein arginine methyltransferase
(PRMT)5, which is a type II arginine methyltransferase, mediates the salt
stress response by regulating transcription and pre-mRNA splicing. This
is accomplished through alterations of the methylation status of
histone4 arginine3 (H4R3) symmetric dimethylation (H4R3sme2) and
LSM4, a small nuclear ribonucleoprotein Sm-like4 [26]. Two subunits of
the nuclear cap-binding complex (CBP), CBP20 and CBP80 also affect
alternative splicing of stress-related genes [27].
Arabidopsis homologs of polypyrimidine tract-binding proteins
(PTBs), which are key splicing factors, are localized in processing
 K. Nakaminami et al. / Biochimica et Biophysica Acta 1819 (2012) 149–153 151

bodies (PBs) [28], suggesting that subsequent mRNA decay is has been reported that cold shock domain proteins (CSDs) are also
connected with alternative splicing. important for stress responses and plant development [42,43].

5.1. RRM containing proteins

4. Degradation and stability control of RNAs
AtGRP7 (Arabidopsis Glycine Rich Protein 7) confers high freezing
mRNA levels are not only regulated by transcription but also by
tolerance when overexpressed in plants [44]. The AtGRP7 protein
degradation and stabilization. RNA regulation particles such as
exhibited chaperone activity in vivo and the N-terminal RRM domain
processing bodies (PBs), which are involved in mRNA degradation,
was required for this activity [45]. To identify the targets of AtGRP7, a
and stress granules (SGs), which are involved in mRNA stabilization,
transcriptome analysis in AtGRP7-overexpressing plants was per-
are new areas of study that are progressing rapidly [29,30].
formed and revealed that expression of several abiotic and biotic
In eukaryotic cells, mRNA degradation generally begins with
stress-related genes such as PR proteins, RD29A, COR15A and PDF
deadenylation. Subsequently, mRNAs are decapped and degraded in
were altered [46]. AtRZ-1a is cold-inducible RNA-binding protein
the 5′ to 3′ direction, or degraded in the 3′ to 5′ direction by
containing RRM, GR and ZnF domains. AtRZ-1a overexpressing plants
exoribonucleases [31]. mRNA decay such as decapping, deadenylation
exhibited high freezing tolerance [47]. AtRZ-1b and 1c complemented
and degradation by exoribonucleases occur within PBs. Recent studies
the cold sensitivity of E. coli BX04, which is a quadruple deletion
have shown that several factors, which are involved in the
mutant of cold shock domain proteins in E. coli [48]. Studies have also
degradation of mRNA, affect plant stress tolerance. AtCAF1 is a CCR4
shown that GRP proteins play important roles in stress responses in
associated factor and the CCR4-CAF1 mRNA deadenylation complex is
other plants. It has been demonstrated that rice GRPs such as OsGRP1,
a major site of mRNA degradation. AtCAF1 is wound inducible and
4 and 6 can complement the cold-sensitive BX04 E. coli mutant [49].
Atcaf1 mutants exhibit salt tolerance [32], indicating that the CCR4-
RNAi transgenic plants of OsDEG10 (Oryza sativa Differentially
CAF1 mRNA deadenylation complex is involved in biotic and abiotic
Expressed Genes 10), were sensitive to high light and cold stress
stress responses. XRN4, which is an exoribonuclease involved in a
[50]. Expression of a Nicotiana tabacum glycine-rich RNA-binding
major mRNA degradation pathway in the cytoplasm, is also involved
protein (NtGRP), which exhibited RNA-binding activity, was induced
in abiotic stress responses (Nakaminami, Matsui et al. unpublished
by flooding stress [51].
data). DCP1, DCP2, DCP5 and VARICOSE are components of PBs that
AtTZF1 is an Arabidopsis tandem zinc finger protein that has been
are involved in decapping activity with DCP5 being essential for PB
localized to PBs and SGs and has been proposed to be involved in RNA
formation [33,34]. However their functions in the stress responses are
regulation [52]. OsRZ2, an Oryza sativa (CCHC)-type zinc finger-
not well understood.
containing glycine-rich RNA-binding protein, exhibited chaperone
Stress granules (SGs) are also important for the regulation of
activity and complemented the cold sensitivity of E. coli BX04 and the
mRNA levels [29]. Unlike PBs, SGs contain translation initiation
Arabidopsis mutant atgrp7 [53]. GhZFP1, which is a novel CCCH-type
factors, the 40S ribosomal subunit, the poly(A)-binding protein and
zinc finger protein from Gossypium hirsutum, enhances salt stress
some RNA-binding proteins that store mRNAs. Tudor-SN, (TSN),
tolerance and fungal disease resistance [54].
which is an RNA-binding protein, functions in RNA stability control
during plant stress responses. In Arabidopsis, TSN is important for
5.2. Cold shock domain proteins
salinity stress tolerance as shown by its ability to stabilize the levels of
stress-responsive mRNAs that encode secreted proteins [35]. It has
WCSP1, a wheat cold shock domain protein, is specifically induced
been reported that TSN interacts with the Ras-GTPase-activating
by cold stress [55]. WCSP1 has RNA-binding and nucleic acid melting
protein (GAP) SH3-binding protein, G3BP, which is a component of
activities in vivo and in vitro [56,57]. Knock out mutants of Arabidopsis
SGs [36]. Branco-Price et al. [37] demonstrated that hypoxia stress
cold shock domain protein 3, AtCSP3, showed freezing-sensitivity and
significantly reduced translation without the reduction of transcrip-
overexpression of AtCSP3 in plants showed enhanced freezing tolerance
tion of mRNAs. This indicated that the inhibition of translation
[58]. Overexpression of Arabidopsis cold shock domain protein 1
initiation and transient mRNA sequestration occurred under hypoxia
(AtCSP1/CSDP1) delayed seed germination under dehydration and
stress conditions [37] and that selective mRNA translation is an
salinity stress, while overexpression of AtCSP2/CSDP2 promoted seed
important mechanism for this stress response. Translatome analysis
germination under salinity stress [59]. AtCSP2 complemented the cold
using ribosome-associated mRNA immunoprecipitation is a powerful
sensitivity of the E. coli BX04 mutant and exhibited nucleic acid melting
technique that has been used to determine the translational profiling
activity [60]. Oryza sativa cold shock domain protein 1 and 2 (OsCSP1
of selective mRNAs and translational control [38].
and 2) exhibited nucleic acid-binding activity and complemented the
PBs and SGs are sometimes co-localized in the cytoplasm,
cold sensitivity of the E. coli BX04 mutant [61].
suggesting that they interact with each other and play important
AtCSP1 and 3 are cold inducible, however AtCSP2 and 4 are
roles in the mRNA life cycle [39]. It has been reported that HSP90
involved not only in stress responses, but also in plant development
chaperone activity is important for the formation of PBs and SGs [40].
such as floral transition and embryo development [62]. AtCSP2 is also
Several recent studies have shown that RNA degradation and stability
expressed in meristematic regions suggesting that AtCSP2 is involved
control are necessary for plant stress responses. These data implies
in plant development [60,63]. Arabidopsis cold shock domain protein
that PBs are cooperated with SGs in the RNA regulatory processes.
4, AtCSP4/AtGRP2b, is important for late embryonic development.
AtCSP4/AtGRP2b affects expression of several embryonic related
5. RNA-binding proteins genes [64]. OsCSP1, 2 are also expressed in meristematic reproductive
tissues suggesting that the OsCSPs are involved in not only stress
RNA-binding proteins act directly or indirectly in the post- responses but also plant development [61]. Collectively, these data
transcriptional regulation of other regulatory factors. There are many indicate an essential role of RNA chaperones in cold adaptation and
kinds of RNA-binding proteins and they are categorized based on their development in higher plants.
structure and binding specificity. The most conserved domain/motif is
the RNA recognition motif (RRM) and it is conserved from bacteria to 6. Conclusions and perspectives
animals. RRM-containing proteins also have other domains such as
glycine-rich (GR), SR dipeptides and zinc finger (ZnF) domains, RNA regulation studies in the abiotic stress responses have progressed
indicating that these proteins have various functions [41]. Recently it remarkably in recent years. The mechanisms of transcriptional and
152 K. Nakaminami et al. / Biochimica et Biophysica Acta 1819 (2012) 149–153

Table 1
RNA binding proteins involved in stress responses.

Functional category Gene Domain and motif Functional characteristic References

Splicing SR proteins RRM (RNA recognition motif) Involved in heat and cold tolerance [24]
SR (serine/arginine) dipeptides
CBP20, CBP80 RRM Affect alternative splicing of ABA related genes [27]
Degradation and AtCAF1 CRM (chloroplast RNA splicing Involved in wounding and salt tolerance [32]
stabilization control and ribosome maturation)
TSN Tudor, SN (staphylococcal nuclease) Involved in salt tolerance [35,36]
RNA chaperone AtGRP7 RRM, GR (glycine-rich), ZnF (zinc finger) Involved in stress response [45,46]
AtRZ-1a, b, c RRM, ZnF Involved in cold tolerance [47,48]
OsGRPs RRM, GR Involved in cold tolerance [49]
OsDEG10 RRM Involved in high light and cold tolerance [50]
NtGRPs RRM, GR Involved in flooding stress [51]
AtTZF1 ZnF, Ankyrin Repeat localized in PBs and involved in heat stress response [52]
OsRZ2 RRM, ZnF Involved in cold stress response [53]
GhZFP1 ZnF Involved in salt stress tolerance [54]
WCSP1 CSD (cold shock domain), GR, ZnF Involved in cold stress response [55,57]
AtCSP1/CSDP1 CSD, GR, ZnF Involved in dehydration or salinity stress [59]
AtCSP2/CSDP2/AtGRP2 CSD, GR, ZnF Involved in cold tolerance [60]
Involved in dehydration or salinity stress [59]
AtCSP3 CSD, GR, ZnF Involved in cold stress response [58]
OsCSP1 and 2 CSD, GR, ZnF Involved in cold stress response [61]

posttranscriptional regulation through ncRNAs like small RNAs and
antisense RNAs, have become better understood with recent advances in
whole transcriptome analyses. These include the use of high-density
microarrays and high throughput sequencing. Studies of PBs and SGs have
emerged as new and interesting areas of research in plant stress
responses. Localization and functional analysis of their components and
targets will provide more insight into how plants respond to stresses.
Notably, RNA-binding proteins are involved in all aspects of RNA
regulation such as transcription, splicing, and the control of decay and
stabilization (Table 1). It is essential to analyze the function of these RNA-
binding proteins in order to understand the mechanism of RNA regulation
in abiotic stress responses. Identification and analysis of factors that
interact with these RNA-binding proteins will help reveal the structure
and mechanism of RNA regulatory complexes.
Acknowledgements
This work was supported by a grant from RIKEN Plant Science
Center (to M. S.), Grants-in-Aid for Scientific Research on Kiban (C)
(no. 21570056) of the Ministry of Education Culture, Sports and
Technology of Japan (to M. S.) and the Special Postdoctoral
Researcher's Program from RIKEN to K. N.
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