Download Role of L-Ascorbic Acid in Rice Plants

Reviews and Opinions
1
Role of L-Ascorbic Acid in Rice Plants
Ching Huei Kao *
Department of Agronomy, National Taiwan University, Taipei 10617, Taiwan ROC
ABSTRACT
INTRODUCTION
The role of ascorbic acid (AsA) in rice plants
is reviewed. It is now well established that AsA in
rice plants is biosynthesized through D-mannose/
L-galactose pathway. Monodehydroascorbate
(MDHA) and dehydroascorbate (DHA) can be
recycled to AsA by MDHA reductase and DHA
reductase, respectively. AsA content in rice plants
can be altered through manipulation of AsA
biosynthetic or recycling pathways. Evidence is
provided to show that AsA plays a critical role in
regulating tiller formation, as well as in resistance
to environmental stress.
Key words: Ascorbic acid, Rice, Stress, Tiller.
L-Ascorbic acid (AsA; vitamin C) or simply
ascorbate, a naturally occurring compound, plays
a multifunctional role in both plants and animals.
AsA has a key role in keeping human health. In
contrast to the most animals, humans are unable
to synthesize AsA due to a mutation to the gene
encoding L-gulono-1,4-lactone oxidase, the last
enzyme in the AsA biosynthesis in animals (Gallie
2013a). Thus, plants provide the major source of
AsA in human diet. AsA has many functions in
plants, including preventing plants from reactive
oxygen species (ROS) damage, cofactor of many
enzymes, regulating cell division, cell expansion,
cell wall metabolism, shoot apical meristem
formation, root development, photosynthesis, leaf
senescence, hormones (ethylene and gibberellins)
biosynthesis, abiotic and biotic stress, and
flowering time (Anjum et al. 2015, Gallie 2013a,
Zhang 2013). Additionally, AsA can function as a
precursor for the biosynthesis of oxalic and
L-tartaric acid in certain plants (DeBolt et al. 2007).
Compared with Arabidoposis, the role of AsA
in rice plants is less well known. For the purpose
of increasing our understanding the role of AsA
in rice plants, several strategies have been used to
alter endogenous AsA levels. In this review, an
attempt has been made to show the role of AsA in
growth, development, and stress tolerance in rice
plants.
抗壞血酸與水稻生理
高景輝*
國立臺灣大學農藝系
摘要
本 文 旨 在 綜 合 討 論 抗 壞 血 酸 (ascorbic
acid; AsA)在水稻所扮演之角色。目前已知水
稻抗壞血酸係經由 D-mannose/L-galactose
途徑合成。單脫氫抗壞血酸與脫氫抗壞血酸，
可經由單脫氫抗壞血酸還原及脫氫抗壞血酸
還原酵素作用轉變為抗壞血酸。水稻抗壞血
酸之含量可透過合成與回復(recycling)之途
徑而改變。證據顯示，抗壞血酸可調控水稻
分糱之形成及增加水稻對逆境之抗性。
關鍵詞︰抗壞血酸、水稻、逆境、分蘗。
* 通信作者, [email protected]
投 稿 日 期： 2014 年 10 月 23 日
接 受 日 期： 2014 年 12 月 16 日
作 物 、 環境 與生 物 資 訊 12:1-7 (2015)
Crop, Environment & Bioinformatics 12:1-7 (2015)
189 Chung-Cheng Rd., Wufeng District, Taichung City
41362, Taiwan ROC
BIOSYNTHESIS, TRANSPORT,
OXIDATION, AND REYCLING OF
ASCORBIC ACID
AsA biosynthesis occurs in almost all plant
tissues. A complex network for producing AsA
through L-galactose (Gal), D-galacturonate, and
myoinositol has been proposed (Smirnoff
2011,Venkatesh and Park 2014). It is now widely
accepted that Gal pathway is the major plant
pathway for AsA biosynthesis (Anjum et al. 2015,
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Crop, Environment & Bioinformatics, Vol. 12, March 2015
Ishikwa et al. 2006, Smirnoff 2011, Venkatesh and
Park 2014). Gal pathway is also named as
Smirnoff-Wheeler pathway or D-mannose
(Man)/Gal pathway. Man/Gal pathway of AsA
biosynthesis consists of the formation of AsA
from
guanosine
diphosphate
mannose
(GDP-Man), GDP-L-galactose (GDP-Gal), Gal,
and L-galactono-1,4-lactone (GalL) (Fig. 1). All the
genes involved in this pathway are well
characterized.
These
genes
encode
GDP-D-mannose pyrophosphorylase (GMP),
GDP-D-mannose-3’5’-epimerase
(GME),
GDP-L-galactose
posphorylase
(GGP),
L-galactose-1-P
phosphatase
(GalPPase),
L-galactose
dehydrogenase
(GalDH),
and
L-galactono 1,4-lactone dehydrogenase (GalLDH).
Studies by Fukunaga et al. (2010) confirmed that
Man/Gal pathway is responsible for the synthesis
of AsA in rice shoots. They also found that the
AsA synthesis in rice shoots is regulated by light
and the promoter regions in genes encoding AsA
biosynthetic enzymes (GalPPase and GallDH)
contain light responsible cis-element.
All enzymes except GalLDH in the pathway
of AsA biosynthesis are located in the cytoplasm.
GalLDH is located within the mitochondrion
(DelBolt et al. 2007). Once the AsA is synthesized
on the inner mitochondrial membrane, it is
transported to different cellular compartments.
AsA transport is possibly mediated by facilitated
diffusion or active transport systems (Ishikawa et
al. 2006). The transport of AsA from the source to
sink tissues occurs via the phloem (Franceschi and
Tarlyn 2002). Manipulation of AsA transport in
the phloem may provide the useful approach to
increase the AsA content of fruits and tubers.
Ascorbate oxidase (AAO) and ascorbate
peroxidase (APX) are enzymes responsible for the
oxidation of AsA (Fig. 2). AAO is located in the
apoplast (Pignocchi et al. 2003). It catalyzes the
oxidation of AsA to monodehydroascorbate
(MDHA) using oxygen. The modulation of AAO
activity would result in the alteration of AsA
accumulation. APXs are members of the class I
family of heme peroxidases that catalyze the
reduction of hydrogen peroxide to water with
concomitant oxidation of AsA to MDHA (Terxeira
et al. 2004).
MDHA is reduced (or recycled) back to AsA
by monodehydroascorbate reductase (MDHAR)
using NADH/NADPH as electron donors (Fig. 2).
MDHA can also disproportionate to AsA and
dehydroascorbate (DHA) (Fig. 2). The rate of AsA
turnover is relatively fast (Conklin et al. 1997,
Pallanca and Smirnoff 2000), thus MDHA and
DHA should be efficiently recycled to maintain
the AsA pool size. AsA recycling by
dehydroascorbate reductase (DHAR) is another
means for a plant to recycle DHA into AsA (Fig.
2). If DHA is not recycled to AsA, it undergoes
irreversible hydrolysis to 2,3-diketogulonic acid
(Fig. 2). The importance of MDHAR- and
DHAR-mediated mechanisms of AsA recycling
has been excellently reviewed by Gallie (2003b).
Fig. 1. AsA biosynthetic pathway in plants.
Enzymes: 1,GMP; 2, GME, 3, GGP 4,
GalPPase; 5, GalDH, 6, GalLDH.
Fig. 2. Oxidation and recycling AsA in plants.
Enzymes: 1, AAO; 2, APX; 3, MDHAR;
4, DHAR.
Role of L-Ascorbic Acid in Rice Plants
All together, the AsA pool size is dependent
on the rate of AsA biosynthesis, ability of AsA
transport, and rate of AsA oxidation as well as
efficiency of AsA recycling.
ASCORBIC ACID IS INVOLVED
IN GROWTH AND TILLER
FORMATIION OF RICE PLANTS
GalLDH catalyzes the last step of the AsA
biosynthetic pathway in plants (Anjum et al. 2015,
Ishikwa et al. 2006, Smrnoff 2011, Venkatesh and
Park 2014), thus this enzyme is a good candidate
for controlling the variations in AsA contents of
plants. Using silencing and overexpressing
GalLDH techniques, Yu et al. (2010) have
generated transgenic rice plants with very
different levels of AsA. GalLDH-silencing and
-overexpression rice plants indeed have low and
high leaf AsA content, respectively, when
compared with wild type (Liu et al. 2011, Yu et al.
2010). GalLDH-silencing rice plants display a
reduced growth rate (plant height, root length,
and leaf weight) (Liu et al. 2011). It appears that a
lower leaf AsA content in rice plants suppressed
for GalLDH contribute to lower growth rate.
Smirnoff and Wheeler (2000) have proposed that
AsA could influence cell growth. Little is known
about the exact mechanisms by which AsA
regulates cell growth in plants. Further studies by
Liu (2013) demonstrated that GalLDH-silencing
rice plants have higher level of abscisic acid (ABA)
and jasmonic acid. Higher ABA contents have
also been reported in AsA defective Arabidopsis
mutant vtc1 (Pastori et al. 2003). It is possible that
AsA in rice leaves could regulate the growth
through interaction with plant hormones.
Tiller number is one of key factors that
determines rice grain yields (Wang and Li 2011).
It has been shown that seed priming by soaking
wheat seeds in AsA solution increases the number
of tillers, fertile tillers, biological and grain yield
(Jafar et al. 2012). Similar results were observed in
wheat leaves sprayed with AsA (Amin et al. 2008).
Rice tillers are specialized branches bearing
panicle. Recent work by Liu et al. (2013)
demonstrated that AsA-deficient rice plants
exhibit a significantly reduced tiller number. In
another report, they also showed that
GalLDH-suppressed rice plants display a reduced
3
seed sets and thousand-grain-weight (Liu et al.
2011). All these results strongly suggest that the
importance of AsA in determining rice yield.
Strigolactones are now considered as a new
class of plant hormone inhibiting shoot branching
(Gomez-Roldan et al. 2008, Umehara et al. 2008).
Recently, Cardoso et al. (2014) demonstrated that
Japonica
rice
Azucena
contains
high
strigolactone levels and is a low tillering cultivar,
whereas Indica rice Bala is a low-strigolactone
producer and is highly tillered. Strigolactones are
compounds derived from carotenoids. It is not
known whether the decline of carotenoids in
AsA-deficient rice plants plays a role in the
synthesizing strigolactones (Liu et al. 2013).
ASCORBIC ACID AND STRESS
TOLERANCE OF RICE
Oxygen is essential for the existence of
aerobic life, but toxic reactive oxygen species
(ROS) including the superoxide anion, hydroxyl
radical and hydrogen peroxide are generated in
all aerobic cells during metabolic processes
(Noctor and Foyer 1998). Injury caused by ROS,
known as oxidative stress, is one of the major
damaging factors in plants exposed to
environmental stresses. AsA is the most abundant
antioxidant in plants and plays a role in coping
with oxidative stress (Noctor and Foyer 1998).
The decrease in AsA content is prior to the
occurrence of toxicity in the leaves of rice
seedlings treated with Cd (Chao et al. 2010). AsA
and GalL, the precursor of AsA biosynthesis,
pretreatments significantly reduce Cd toxicity in
the leaves of rice seedlings (Chao and Kao 2010).
Similarly, heat shock-induced AsA accumulation
in leaves of rice seedlings results in an increase in
Cd tolerance (Chao and Kao 2010). AsA-deficient
Arabidopsis mutant vtc2-1 (60% less AsA than wild
type, Col-0) (Zechmann et al. 2011) showed high
sensitivity to Cd than wild type (Koffler et al.
2014). However, recent work demonstrated that
development of Cd toxic symptom is related to
low subcellular glutathione content rather than
AsA content (Koffler et al. 2014). It seems that low
glutathione content rather than low AsA content
in subcellular compartments is responsible for
high Cd sensitivity in this AsA-deficient
Arabidopsis.
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Crop, Environment & Bioinformatics, Vol. 12, March 2015
Surface ozone pollution may cause reduction
in rice yield (Sawada and Kohno 2009). Ozone
exposure results in ROS production. GME is an
important enzyme in AsA biosynthetic pathway.
Frei et al. (2012) screened rice mutants for
OsGME1 and identified a homozogous ‘TOS 17’
insertion mutant line (ND6172). This mutant,
20-30% lower AsA contents than wild type,
exhibits a higher visible leaf damage upon ozone
exposure. In an another report, Frei et al. (2010)
also exposed two chromosome segment
substitution lines (SL15 and SL41) of rice and their
parent ‘Nipponbare’ to ozone at 120 nl l-1. SL15
and ‘Nipponbare’ are more sensitive to ozone
damage than SL41.
Using gene expression
profiling by microarray hybridization, they
identified a potential ozone tolerance gene which
encodes AAO, an apoplastic enzyme responsible
for AsA degradation. The putative AAO gene
showed consistently lower expression in SL41
under ozone expression, which is linked to a
higher concentration of apoplastic AsA in LS41
exposed to ozone.
For maintenance of the AsA pool, AsA
recycling is required. MDHAR and DHAR are
two enzymes responsible for AsA recycling. Chen
et al. (2003) confirmed that overexpression of
DHAR in plants would increase AsA content
through improved recycling. A cDNA encoding
the rice DHAR was first cloned by Urano et al.
(2000). The mRNA level of DHAR1, the protein
level of Dharlp, and the DHAR activity in rice
seedlings were elevated by high temperature,
indicating the protection role of DHAR at high
temperature. This cDNA was used in the
generation of transgenic Arabidopsis expressing
DHAR in the cytosol (Ushimar et al. 2006). The
overexpress of this enzyme enhances resistance to
salt stress (Ushimaru et al.2006). Martret et al.
(2011) also used this DHAR gene to generate
transgenic tobacco. They demonstrated that
DHAR enzyme can be successfully expressed in
the chloroplasts, leading to a significant
enhancement in the ability of the plant to
withstand cold and salt stress. Recently, Kim et al.
(2013) investigated whether DHAR affects rice
yield under normal environmental conditions.
Their
results
indicate
that
OsDHAR1
overexpression in rice plants increases AsA
content and enhances grain yield and biomass.
Compared with the work of DHAR
expression, few studies were conducted on the
expression of MDHAR in rice. Sultana et al. (2012)
demonstrated that overexpression of mangrove
MDHAR in rice exhibits an increase in AsA
content and enhanced tolerance to salt stress.
APX plays an important role in scavenging
ROS in plants. It is located in different cellular
compartments. In rice, APX genes have been
described: two cytosolic (OsAPX1 and OsAPX2),
two putative peroxisomal (OsAPX3 and OsAPX4),
and five chloroplastic isoforms (OsAPX5, OsAPX6,
OsAPX7, and OsAPX8) (Hong et al. 2007, Teixeira
et al. 2004, 2006). Recently, Lazzarotto et al. (2011)
identified a new class of rice heme perxoidases,
APX-R (APX-related), which is localized in both
chloroplasts and mitochondria and functionally
associated with APX. It has long been recognized
that prior exposure to heat shock temperatures
protect plants from the subsequent chilling stress
(Saltveit 1991). Rice seedlings pretreated with heat
shock temperature (42℃) for 24 h did not show
the subsequent chilling injury (4℃) (Sato et al.
2001). Heat shock induction of the APX1 gene has
been proved to be the cause of reduced chilling in
rice seedlings (Sato et al. 2001). Overexpression of
OsAPX1 in rice was later proved to be effective in
enhancing tolerance to chilling at booting stage
(Sato et al. 2011). Additionally, overexpression of
OsAPX2 in transgenic Medicago sativa or
Arabidopais improves salt tolerance compared
with wild plants (Guan et al. 2012, Lu et al. 2007,
Zhang et al. 2013). In contrast, down regulation of
OsAPX2 gene results in rice seedlings sensitive to
drought, salt, or cold stress, suggesting that rice
cytosolic APX2 plays a critical role in stress
tolerance (Zhang et al. 2013).
CONCLUSIONS AND PERSPECTIVES
AsA is now known to be biosynthesized
through Man/Gal pathway in rice plants. AsA
plays a critical role in scavenging stress-induced
ROS. Several key genes in the AsA biosynthetic
pathway have been introduced into rice plants
through genetic engineering to increase the AsA
content and consequently enhance tolerance to
stresses such as chilling, salinity and drought. Of
particular interest are the recent findings by Liu et
al. (2013) who emphasized the importance of AsA
in tiller formation of rice plants. Whether the
Role of L-Ascorbic Acid in Rice Plants
synthesis of strigolactones is related to the
synthesis of AsA in rice plants will be the subject
of further research. To maintain the AsA pool size,
MDHA and/or DHA should be recycled to AsA.
The studies of the role of MDHAR and/or DHAR
are essential to generation of AsA for
maintenance of ROS activity. To study whether
coover-expression of OsMDHAR and OsDHAR to
rice plants confers stress tolerance will be
rewarding. Biochemical methods are generally
used to analyze AsA content in stress-induced
rice plants. AsA content is rarely available in
individual cellular compartments. It would of
great interest to understand the importance of
subcellular AsA in enhancing stress tolerance.
Apoplastic AsA is associated with many
physiological functions such as cell division and
elongation, and its homeostasis in the apoplast is
easily disturbed. Studies of the changes in
apoplastic AsA to DHA ratio and AsA transport
across the plasmalemma in rice plants under
stress conditions are thus required.
ACKNOWLEDGEMENTS
Research in the author’s laboratory has been
supported by grants from the Ministry of Science
and Technology (formerly National Science
Council) of the Republic of China.
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