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Abiotic Stress Responses are Governed by Reactive Oxygen Species and Age

Authors:
  • Center of Plant Systems Biology and Biotechnology, Plovdiv, Bulgaria

Abstract

Plants grown under abiotic stress conditions such as salinity, drought, cold, or heat display a variety of molecular, biochemical, and physiological changes including excessive generation of reactive oxygen species (ROS). The over‐production of ROS causes DNA damage and protein cross‐linking, which can lead to poor molecular transport, reduced enzyme activity, and loss of cell functions. The accumulation of ROS in response to stress also activates several signalling pathways which, in coordination with hormones such as ethylene and abscisic acid (ABA), allow for an adaptive response to stress, resulting in adjustments in plant growth and development in an attempt to maximise survival. Thus, the increase in ROS level by environmental stress results in both damage and an adaptive response; the outcome of the stress, i.e. survival or death then depends on the severity of the stress in combination with the stress response. In this article, we review elements of abiotic stress responses, in particular how ROS work together with the hormones ethylene and ABA to induce distinct stress responses in tissues of different age.
Annual Plant Reviews (2018) 1, 1–32 http://onlinelibrary.wiley.com
doi: 10.1002/9781119312994.apr0611
ABIOTIC STRESS RESPONSES
ARE GOVERNED BY REACTIVE
OXYGEN SPECIES AND AGE
Aakansha Kanojia and Paul P. Dijkwel
Institute of Fundamental Sciences, Massey University, Palmerston North, New Zealand
Abstract: Plants grown under abiotic stress conditions such as salinity, drought,
cold, or heat display a variety of molecular, biochemical, and physiological
changes including excessive generation of reactive oxygen species (ROS). The
over-production of ROS causes DNA damage and protein cross-linking, which
can lead to poor molecular transport, reduced enzyme activity, and loss of cell
functions. The accumulation of ROS in response to stress also activates several
signalling pathways which, in coordination with hormones such as ethylene
and abscisic acid (ABA), allow for an adaptive response to stress, resulting in
adjustments in plant growth and development in an attempt to maximise survival.
Thus, the increase in ROS level by environmental stress results in both damage
and an adaptive response; the outcome of the stress, i.e. survival or death then
depends on the severity of the stress in combination with the stress response.
In this article, we review elements of abiotic stress responses, in particular how
ROS work together with the hormones ethylene and ABA to induce distinct stress
responses in tissues of different age.
Keywords: abiotic stress, abscisic acid, age-related changes, ageing, ethylene,
reactive oxygen species, stress response
1 Introduction
The earth’s environment is constantly changing, and this has accelerated
in the past century as a result of the industrial era (Abram et al., 2016).
Current global warming is believed to increase the frequency of extreme
weather events (Cai et al., 2014b) and globally impacts ecosystems and crop
production (Chapin et al., 2000; Lesk et al., 2016). Since plants cannot move
Annual Plant Reviews Online, Volume 1. Edited by Jeremy Roberts.
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A Kanojia & PP Dijkwel
away to escape from stressful environmental conditions, they have evolved
sophisticated mechanisms to adapt to stress. Plants respond differently to
multiple environmental stress such as drought, cold, salt stress, and ozone,
but, early ageing and onset of senescence is a common stress-induced
response (Munné-Bosch and Alegre, 2004). Early ageing due to stress is also
accompanied with over-production of ROS (reactive oxygen species). ROS
are a group of free radicals derived from oxygen and are continuously gener-
ated as by-products of basic metabolic processes such as photosynthesis and
respiration (Arora et al., 2002; Gill and Tuteja, 2010). ROS in moderate levels
are actively involved in plant growth and development, such as trichome
development, leaf shape, root hair elongation, reproductive growth, and
senescence (Gapper and Dolan, 2006). However, excessive generation of
ROS occurs when plants are exposed to biotic or abiotic stress (Bhattacharjee,
2012). High ROS levels may add to the already present burden of growing
in unfavourable conditions, but they also function as stress-signalling
molecules (Suzuki et al., 2012) and therefore ultimately allow plants to adapt
and survive the imposed stress. ROS are also regulated by and regulate the
stress-related phytohormones, abscisic acid (ABA) and ethylene (Wilkinson
and William, 2010; Steffens, 2014; Mou et al., 2016; Zhang et al., 2016b). ABA,
together with ROS, can provide stress resistance by adjusting the stomatal
aperture (Sah et al., 2016). Ethylene plays a role in the induction of leaf
senescence and as such helps decrease leaf surface area and evaporation,
while valuable nutrients present in the senescing leaves can be remobilised
(Müller and Munné-Bosch, 2015; Valluru et al., 2016). Thus, ROS, together
with the hormones ethylene and ABA, play essential roles in the plant stress
response, and in the following section we summarise a selection of research
in this area and present ideas on how plants may optimise survival.
2 Reactive Oxygen Species
ROS radicals contain unpaired electrons which attack stable molecules to nd
another electron (Tripathy and Oelmüller, 2012). When the attacked molecule
loses its electron, it becomes a free radical itself. Once the process has started,
the chain reaction can continue for thousands of events, resulting in the pro-
duction of different ROS radicals (Hekimi et al., 2011). Typical characteristics
of ROS are that they are short-lived, unstable, and react with other molecules
to achieve stability (Halliwell, 2006). ROS radicals include singlet oxygen
(1O2), superoxide (O2•−), hydrogen peroxide (H2O2), and hydroxyl radical
(OH) (Miller et al., 2010; You and Chan, 2015). Plants continuously produce
ROS as normal by-products of metabolism that are generated in all cellular
compartments, but a wide range of stressful conditions such as UV radiation,
salinity, chilling, heat, and drought can lead to the over-production of ROS
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
(Tripathy and Oelmüller, 2012). Different types of ROS and their production
sites are described below.
The chloroplast is one of the major sites that act as a source for ROS
generation during photosynthesis (Foyer and Noctor, 2009). Photosynthesis
involves major electron transport complexes (ETCs), namely, photosystem
I (PS I), photosystem II (PS II), and the cytochrome b6f complex (Nelson,
2011). Under regular conditions, the electron ows from excited PS centres to
NADP, which is further reduced to NADPH and then enters the Calvin cycle
to reduce the nal electron acceptor CO2. Stress conditions such as salinity
lead to the excessive uptake of Na+and Clions, which results in limited
CO2xation due to overcrowding of ETCs (Elstner and Osswald, 1994;
Hasegawa et al., 2000; Abogadallah, 2010). The impaired photosynthetic
electron transport chain induces the formation of 1O2at PSII and O2•−
radicals at PSI and PSII as waste products (Elstner and Osswald, 1994).
The 1O2radicals are very toxic as they can react with biological molecules
and directly oxidise unsaturated fatty acids, proteins, and DNA (Halliwell,
2006). The O2•− radicals are short-lived and moderately reactive radicals
(Apel and Hirt, 2004). When plants are treated with herbicides such as
oxadiazon, oxyuorfen, and bentazon, 1O2and O2•− radicals are most likely
over-produced in the chloroplast, which may damage the whole photosyn-
thetic machinery (Halliwell, 1991; Krieger-Liszkay, 2005; Balasaraswathi
et al., 2017).
Similar to chloroplasts, mitochondria also have ETCs through which ATP
is formed from ADP and Pi. The well-known sites of ROS generation in mito-
chondria ETC are complexes I and III (Sharma et al., 2012). A number of
enzymes existing in the mitochondrial matrix are known to generate ROS
(Taylor et al., 2002; Taylor, 2005). The enzyme 1-galactono-γ-lactone dehy-
drogenase produces O2•− indirectly by feeding electrons to the ETC, while
enzymes such as aconitase produce O2•− directly (Rasmusson et al., 2008).
Although mitochondrial ROS generation takes place under regular respira-
tory conditions, ROS levels increase in response to changes in the environ-
ment (Kaushik and Roychoudhury, 2014). Paraquat, cold, and drought stress
lead to the production of O2•− radicals in mitochondria, which causes severe
damage to proteins (Murphy, 2009). UV-B stress induces a H2O2burst, which
further produces OH radicals by reacting with Fe2+and Cu+within the
mitochondria (Huang et al., 2016; Niu and Liao, 2016). Amongst all radicals,
OH are one of the most reactive in the family of ROS and can possibly react
with all biomolecules including lipids, proteins, and DNA (Apel and Hirt,
2004; Dikalov, 2011).
Peroxisomes can also efciently produce ROS under stressed conditions
including drought, salinity, ozone, or cadmium (Del Río and López-Huertas,
2016) and are major sites of H2O2generation (Del Río et al., 2006). H2O2
radicals are very stable but moderately reactive, as compared to other ROS
species, and these radicals can also travel easily across cell membranes (Rani
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A Kanojia & PP Dijkwel
et al., 2015). H2O2functions as a messenger and can induce stress responses,
including the initiation of programmed cell death (PCD) (Gechev et al., 2006).
Flavin oxidase is a basic enzymatic component of peroxisomes, which pro-
duces H2O2radicals (Van der Zand and Tabak, 2013). In peroxisomes, O2•−
radicals are produced at two sites: one site is positioned in the matrix, where
xanthine oxidase is involved in the generation of O2•−, and the second site
is located in the membrane, where O2•− generation is NAD(P)H dependent
(Del Rio et al., 2002).
NADPH oxidase is a membrane-bound enzyme complex that plays an
important role in ROS generation under stressed conditions (Laloi et al.,
2004). NADPH oxidase catalyses the transfer of electrons from cytoplasmic
NADPH to oxygen, to form O2•− radicals. Thus, NADPH facilitates the
formation of O2•− in the plasma membrane which is dismutated to H2O2
(Kwak et al., 2003; You and Chan, 2015). Due to over-production of ROS in
the plasma membrane, NADPH-dependent oxidase is found to be involved
in damaging proteins (Apel and Hirt, 2004; Qu et al., 2017).
A plant cell wall is a dynamic and an essential component of several
biological processes. During developmental processes and interactions with
the environment, the cell wall provides mechanical strength to withstand the
stress conditions (Tenhaken, 2015). Cell walls are considered as active sites
for ROS generation. Under stressed conditions such as drought or salinity,
cell-wall-localised lipoxygenases are actively involved in the generation
of ROS radicals such as H2O2,O
2•−,OH, and 1O2(Hou et al., 2015).
Cell-wall-localised peroxidases are also involved in the synthesis of ROS
radicals (Gupta et al., 2016). During stressed conditions such as drought or
potassium deciency, cell-wall-localised peroxidase promotes ROS gener-
ation which makes plants sensitive to stress if over-produced (Kim et al.,
2010; Maia et al., 2013). Interestingly, a number of cell wall proteins are also
known to be involved in the oxidative burst, namely, hydroxyproline-rich
glycoproteins, chitin-binding proline-rich glycoproteins, and proline-rich
proteins (O’Brien et al., 2012).
In summary, excess ROS production in response to abiotic stress can occur
at multiple sites within and outside the plant cells. Moreover, the long-lived
ROS H2O2can cross membranes, and for these reasons – despite being poten-
tially damaging – ROS are effective stress-signalling molecules as well.
2.1 ROS Scavenging Antioxidants
ROS have dual effects on plant metabolism: on the one hand they act as
damaging by-products of general metabolism, and on the other hand they
act as signalling molecules. This requires that plants have sophisticated
measures to keep ROS under tight control (Sharma et al., 2012). In plants,
ROS homeostasis is controlled by enzymatic and non-enzymatic antioxidant
systems. Non-enzymatic antioxidants include the chief cellular redox buffers
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
glutathione (GSH), ascorbic acid (AA), carotenoids, and tocopherols. Enzy-
matic antioxidants include superoxide dismutase (SOD), catalases (CAT),
ascorbate peroxidase (APX), monodehydroascorbate reductase (MDHAR),
dehydroascorbate reductase (DHAR), and glutathione reductase (GR)
(Mitton et al., 2017). They all contribute to ROS homeostasis (Kaushik and
Roychoudhury, 2014).
The non-enzymatic antioxidant GSH is an essential antioxidant located
in almost all cellular organelles such as ER, cytosol, mitochondria, vacuole,
chloroplasts, apoplast, and peroxisomes (Islam et al., 2017; Jiménez et al.,
1998). GSH is the potential scavenger of H2O2and the most toxic ROS like
OH radicals (Briviba et al., 1997; Gill et al., 2012; Yousuf et al., 2012). AA is
another important non-enzymatic antioxidant which is abundantly present
in most plant cell types, organelles, and the apoplast (Conklin and Barth,
2004; Podgórska et al., 2017). AA can directly detoxify O2•−,OH, 1O2,and
H2O2to H2O by the APX reaction (Noctor and Foyer, 1998; Zechmann, 2014).
The oxidation of AA further leads to the formation of enzymatic antioxidants
such as monodehydroascorbate (MDA) and dehydroascorbic acid (DHA)
(Park et al., 2016). DHA is then further reduced to AA by DHAR using GSH
as a reducing substrate (Yang et al., 2009). Thus, DHAR plays an impor-
tant role in maintaining AA in its reduced form (Hernández et al., 2001).
Amongst enzymatic antioxidants, SOD catalyses the dismutation of O2•− to
H2O2and constitutes the rst line of defence in nearly all cells exposed to
oxygen (Gupta et al., 1993; Perl et al., 1993; Scandalios, 2005; Sz˝
oll˝
osi, 2014;
Moustaka et al., 2015). The enzyme CAT was the rst enzymatic antioxidant
discovered and characterised (Kirkman and Gaetani, 1984). CAT catalyses
the breakdown of chemical H2O2to H2OandO
2(Sharma and Ahmad, 2014)
and has one of the highest turnover rates of all enzymes: in 1 min, one CTA
enzyme can convert approximately 6 million molecules of H2O2to O2and
H2O (Gill and Tuteja, 2010).
Plant cells are evidently equipped with outstanding enzymatic and
non-enzymatic antioxidant defence mechanisms to keep ROS under tight
control. A number of studies have shown that high levels of ROS scav-
engers induce resistance to different environmental stressed conditions in
plants. For example, it was found that the oxidative stress produced during
drought stress could be minimised by increasing the production of ROS
scavenging enzymes such as SOD, APX, and GSH, ultimately resulting in
resistance to water-decit conditions in Arabidopsis (Nakabayashi et al., 2014;
Ramanjulu and Bartels, 2002). In Arabidopsis, the over-expression of cytosolic
APX exhibited tolerance to salinity stress as compared to the control wild
type plants (Lu et al., 2007). Also, under high temperature stress, plants
induce expression of stress-related proteins, which increases the antioxidant
activity of SOD and CAT (Fahad et al., 2017). These antioxidants scavenge
the ROS and thereby reduce the oxidative damage otherwise caused by
ROS. The importance of SOD in response to cold stress was conrmed in
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A Kanojia & PP Dijkwel
SOD-over-expressing alfalfa lines, which showed increased tolerance to
chilling stress (Lee and Lee, 2000; Mckersie et al., 1993).
Consistent with expectations, a number of studies have also shown that cell
damage increases with reduced antioxidant activity and over-production of
ROS. For example, a decline in the activity of ROS scavenging enzymes CAT
and SOD promoted ROS levels and resulted in senescence-associated lipid
peroxidation (Bhattacharjee, 2005). Moreover, an antioxidant APX-decient
mutant in Arabidopsis displayed increased sensitivity to salinity stress
because of elevated H2O2, indicating that APX is a salt stress-induced ROS
scavenger (Chen et al., 2015; Huang et al., 2005). Another recent study in
rice showed that gene silencing of OsAPX4 caused ROS-mediated early
senescence (Ribeiro et al., 2017).
Thus, plants have efcient ROS scavenging systems, and scavenging effec-
tiveness plays a role in the outcome of the stress-induced ROS production, i.e.
damage and/or adaptive changes in plant growth and development, leading
to death or survival (Liebthal and Dietz, 2017; Podgórska et al., 2017; Suzuki
et al., 2012).
2.2 ROS and Ethylene
Ethylene is well known for its commercial use in the stimulation of ripening
of crops, fruits, and vegetables (Pech et al., 2012). Indeed, it is a key hormone
in regulating leaf senescence, ower senescence, abscission, and fruit ripen-
ing (Jibran et al., 2013; Zacarias and Reid, 1990). The relatively simple ethy-
lene biosynthesis pathway was elucidated by Yang and Hoffman in 1984 and
starts with the formation of the amino acid 1-aminocyclopropane-1-carboylic
acid (ACC) from S-adenosyl--methionine (SAM), catalysed by ACC syn-
thase (ACS). ACC oxidase (ACO) subsequently catalyses the conversion of
ACC to ethylene gas. The multi-gene family that encodes the enzymes ACS
and ACO is expressed differentially in response to a range of external and
internal cues (Müller and Munné-Bosch, 2015). Consistently, the production
of ethylene varies during plant growth, and increased ethylene biosynthesis
is observed during stress-induced senescence, age-induced senescence, or as
a result of damage (Koyama, 2014).
Ethylene and H2O2are important cell-signalling molecules, also known
to work in concert to modulate stomatal aperture, cell elongation, and
a variety of stress responses (Desikan et al., 2006; Mittler et al., 2004; Wi
et al., 2010). Studies have shown that ethylene along with H2O2acts as
a positive regulator of PCD during stress, through the activation of ACS
and ACO (Dennis et al., 2000; Wang et al., 2002). In cotton, exogenous
ethylene enhanced the production of H2O2within 6 h, whereas exogenous
H2O2stimulated the biosynthesis of ethylene only after 1 day of application
(Qin et al., 2008). In plants, aerenchyma tissue forms air channels, which
provide gaseous exchange between the shoots and the roots (Dennis et al.,
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
2000). It has been found in Arabidopsis that hypocotyls and roots can induce
the formation of lysigenous aerenchyma in response to hypoxia, and this
process involves H2O2and ethylene signalling (Muhlenbock et al., 2007;
Feifei et al., 2017). A connection between ROS and ethylene is also conrmed
by various studies on mutants that are defective in ethylene signalling
or biosynthesis. For example, the ethylene-over-production mutants eto1
and eto2 displayed sensitivity to oxidative stress and promoted cell death,
while the ethylene-insensitive mutants ein3 and etr1 exhibited resistance to
oxidative stress (Jung et al., 2009; Overmyer et al., 2000; Tuominen et al.,
2004). All these studies support an intricate relationship between ethylene
and ROS in the regulation of various plant responses.
Despite being a positive regulator of senescence in plants, the action of
ethylene also induces tolerance to several abiotic stresses. Ethylene plays an
important role in mediating the response to low potassium conditions by
increasing ROS accumulation and changing root morphology (Jung et al.,
2009). Additionally, ethylene, accompanied by ROS accumulation, induced
root hair elongation in Arabidopsis seedlings adapting to low ammonium
levels (Zhu et al., 2016). In Arabidopsis, members of ethylene-responsive
element-binding factors (ERFs) were identied that are involved in normal
plant growth and development, and also function in response to stress by
modulating the ROS regulatory pathway (Ecker, 1995; Nakano, 2006). For
instance, the increase in expression of ERF1 in plants displayed resistance
to drought, low temperature, and salinity, suggesting its positive role in
abiotic stress tolerance (Cela et al., 2011; Cheng et al., 2013; Xu et al., 2007).
Moreover, enhanced expression of ERF protein-JERF3 in tobacco plants
also induced resistance to drought, freezing, and salinity, coinciding with
reduced ROS accumulation (Wu et al., 2008). Also, in tobacco plants the
function of ERF transcription factor TERF1 was investigated conrming its
role in ROS scavenging and providing tolerance to oxidative stress (Zhang
et al., 2016a). Recently, EMS-induced ethylene-insensitive tobacco mutants
were isolated and found to exhibit drought tolerance as well when grown on
mannitol-containing medium. The mutants showed a higher survival rate
along with increased antioxidant activity, suggesting a role for ethylene in
water-decit conditions (Wang et al., 2016b). In Arabidopsis, over-expression
of ERF74 displayed enhanced resistance to water decit, heat, high light,
and aluminium stress coinciding with a ROS burst in the early stages of
the imposed stress, while transgenic lines with reduced erf74 expression
showed increased stress sensitivity along with a negligible ROS burst
(Yao et al., 2017). This study furthermore provided evidence that ERF74 is
involved in controlling stress tolerance by managing ROS homeostasis in an
RbohD-dependent way. It was also found that ethylene delays ABA-induced
stomatal closure, suggesting a role for ethylene in increasing the rate of tran-
spiration. However, it could also be that the function of ethylene-dependent
inhibition of stomatal closure under drought stress is to avoid an overburden
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A Kanojia & PP Dijkwel
of O2molecules as waste by-products of photosynthesis, and this could
explain the twofold role of ethylene during osmotic stress tolerance (Tanaka
et al., 2005).
All these studies together suggest that despite the positive regulators of
senescence and potential toxicity, ethylene and ROS have a dual role either in
cell survival or cell death under abiotic stress conditions. The intricate role of
ethylene in ripening and senescence furthermore suggests that the dual effect
of ethylene and ROS signalling on plant responses probably not only depends
on the type and severity of the stress but also on the age of the stressed plant
tissue.
2.3 ROS and ABA Hormone Regulation
The plant hormone ABA is involved in the regulation of various plant devel-
opmental processes including cell division, elongation, seed development,
seed dormancy, vegetative growth, and oral induction (Finkelstein, 2013;
Raghavendra et al., 2010). In addition to ethylene, ABA levels also increase
in response to various abiotic stresses, and therefore, both hormones are sug-
gested to have roles during abiotic stress responses (Lee and Luan, 2012; Leng
et al., 2014).
Abiotic stresses such as cold, temperature, salinity, and drought increase
both ABA and ROS in stressed tissues (Mehrotra et al., 2014). It was also
shown that drought and salinity promote the biosynthesis of ABA, coincid-
ing with massive change in expression of stress-responsive genes (Boursiac
et al., 2013; Shinozaki and Yamaguchi-Shinozaki, 2007). It was also found
that exogenous application of ABA delays drought-induced wilting and
provides resistance to water-decit conditions (Mehrotra et al., 2014). An
increase in ABA levels by abiotic stress leads to stomatal closure through
the increase of NADPH oxidase activity and a resulting increase in H2O2
production. This causes reduced transpiration and results in drought-stress
tolerance (Assmann, 2003; Desikan et al., 2004; Li et al., 2011; Liu et al., 2010;
Melotto et al., 2006; Neill et al., 2002; Sinclair et al., 1984; Xu et al., 2016;
Ye et al., 2011). Li et al. (2017) showed that over-expression of the OsASR5
gene caused a rise in ABA and H2O2-induced stomatal closure as well as
prevented inactivation of drought-stress-related proteins and provided
enhanced drought tolerance to transgenic rice plants. In Arabidopsis,the
combined effect of heat and salinity stress on ABA signalling mutant abi1
resulted in increased susceptibility to the stress as compared to the wild
type plants (Suzuki et al., 2016). Later, it was found that the increased
sensitivity to salt stress of the abi1 mutant plants resulted from the defective
stomatal closure and elevated H2O2in leaves (Zandalinas et al., 2016).
Additionally, the silencing of the ABA-activated kinase SAPK2 in Arabidopsis
resulted in highly drought-susceptible plants, presumably caused by the
higher transpiration rate as a consequence of the increased ROS level,
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
decreased antioxidant machinery, and fully open stomata (Lou et al., 2017).
While these studies show how stress-induced increases in ABA and H2O2
levels cause stomatal closure and drought resistance in stomatal cells, other
studies highlight the antagonistic effect of ABA in decreasing the ROS
levels and increasing stress tolerance. For instance, the ABP9 gene, which
encodes a bZIP transcription factor, plays an important role in regulating
ABA responses (Wang, 2002). Transgenic Arabidopsis and cotton plants
over-expressing ABP9 had reduced stomatal aperture, ROS levels, and cell
death and greater tolerance to drought, salinity, cold, and oxidative stress
as compared to wild-type plants (Wang et al., 2017a; Zhang et al., 2011).
Likewise, in cadmium-stressed purple owering stalk, it was found that
exogenous application of ABA lowered the H2O2and O2•−; induced SOD,
APX, and GR antioxidant activity; and provided resistance to cadmium stress
(Shen et al., 2017). Moreover, pre-harvest sprouting (phs) rice mutants with
impaired carotenoid and ABA biosynthesis were isolated, and these mutants
displayed higher ROS abundance and pre-harvest sprouting, suggesting
that ABA plays an important role in inhibition of pre-harvest sprouting in
crops through limiting ROS accumulation (Fang et al., 2008). Treatment of
drought-stressed apple species with melatonin furthermore enhanced stress
tolerance by increasing the antioxidant activity and decreasing the ABA
and H2O2levels, and this resulted in the stomata to be more closed during
the imposed stress (Li et al., 2015). These studies indicate that in addition
to reducing the transpiration rate through ABA and ROS-induced stomatal
closure, plants comprise other adaptive mechanisms such as ABA-induced
reduction of ROS coupled with elevated antioxidant levels. Nevertheless,
the effect of ABA on ROS levels likely depends on stress levels and cell type,
especially in the case of the highly specialised stomatal cells.
2.4 ROS Signalling: Interplay Among MAPKS, Ethylene, and ABA
In Arabidopsis, 60 MAPKKKs, 10 MAPKKs, and 20 MAPKs have been clas-
sied (MAPK Group, 2002). A number of MAPK cascades were found to be
activated in response to abiotic stress (De Zelicourt et al., 2016), and Arabidop-
sis MPK3 and MPK6 were shown to play key roles in ROS signalling under
environmental stress conditions (Jalmi and Sinha, 2015). The expression of
the genes encoding these proteins is induced by ozone treatment, and plants
that lack MPK3 or MPK6 are hypersensitive to ozone (Miles et al., 2005), and
stress-induced MPK3 and MPK6 expression leads to ROS accumulation and
ethylene biosynthesis, which induces early leaf senescence (Li et al., 2012).
Biosynthesis of the stress-hormone ethylene is also regulated by MPK3 and
MPK6: synthesis of the hormone requires ACS, and both ACS2 and ACS6,
which belong to type 1 ASC isoforms, are substrates of MPK3 and MPK6
(Liu and Zhang, 2004; Wang et al., 2002). As a consequence of unfavourable
environmental conditions, MPK3 and MPK6 phosphorylate ACS2 and ACS6,
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A Kanojia & PP Dijkwel
which leads to an increase in ACS activity and concomitant ethylene biosyn-
thesis (Han et al., 2010). Thus, abiotic stress conditions link MPK3 and MPK6
functions with ethylene signalling and ROS over-production.
Various studies have increased the understanding of ABA signalling in the
activation of MAPKs to mediate stress responses through stomatal closure
and balancing ROS and antioxidant activity (de Zelicourt et al., 2016). Sev-
eral genes encoding MAPKs were reported in Arabidopsis to be activated via
ABA signalling such as MPK1, MPK2, MPK9, MPK7, MPK12, and MPK14
(Danquah et al., 2015; Jammes et al., 2009; Ortiz-Masia et al., 2007). MAPK
cascades involving MKK4, MKK5, MPK3, and MPK6 were also found to be
involved in both stomatal development and aperture, and this was medi-
ated in an ABA-dependent manner (Gudesblat et al., 2007). MKKK18 is an
ABA-activated kinase involved in stomatal development, plant growth reg-
ulation, and senescence (Mitula et al., 2015; Matsuoka et al., 2015), and the
recent knockout and over-expression of MAPKKK18 in Arabidopsis conrmed
a role for this gene in suppression of drought-stress resistance mediated by
the ABA signalling pathway (Li et al., 2015). Moreover, in cotton plants, the
over-expression of GhMKK3 displayed enhanced tolerance to drought stress
via ABA-induced stomatal closure (Wang et al., 2016a). Similarly, in Arabidop-
sis, over-expression of ZmMKK1 showed enhanced antioxidant activity and
high expression of ABA-responsive genes, resulting in increased tolerance to
water-decit and salt stress (Cai et al., 2014a). In addition, over-expression
of the Raf-like MAPKKK gene, GhRaf19 in cotton plants, displayed higher
ROS abundance and reduced resistance to drought and salinity in transgenic
plants, suggesting a function for this gene in osmotic stress responses by
modulating cellular ROS levels (Jia et al., 2016). All these studies have uncov-
ered a crucial role for MAPKs and ABA signalling in regulating abiotic stress
responses.
The hormones ethylene and ABA, ROS messengers, and MAPK cascades
all play central roles in plant development and abiotic stress responses. ROS
and MAPKs are activated in response to hormone actions, but also feedback,
or regulate hormone responses. Therefore, all these stress signallers are
intricately connected and likely play diverse roles during different types of
stress, in different tissues or a tissue of a different age. Nevertheless, ROS
over-production seems to be key to many stress responses, although the
effect of these can differ. For example, as a result of many abiotic stresses,
ROS-mediated closing of stomata takes place through various signalling
pathways, and this limits the gaseous exchange in the cell (Hetherington
and Woodward, 2003). During drought stress this may be lifesaving, but
it also increases the production of ROS within the leaf (Singh et al., 2017).
This may further induce a stress response which may cause leaf death, a
potentially harmful response. Indeed, a variety of transgenic studies, as
mentioned before, show that limiting ROS levels can cause increased stress
resistance. Moreover, activation of MPK3/MPK6 during stress induces ROS
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
production and ethylene biosynthesis that ultimately results in early ageing
or cell death in plants (Li et al., 2012; Ye et al., 2015). However, stress-induced
expression of MPK3 and MPK6 also contributes to the survival of plants by
controlling ROS over-production (Pitzschke and Hirt, 2008). It may depend
on the amount of ROS over-production whether the MAPK signalling
pathway induces ethylene biosynthesis leading to cell death or promotes
ABA-mediated stress tolerance via stomatal closure or an enhanced antioxi-
dant mechanism. Thus, while the past decades have seen rapid progress in
the understanding of ROS signalling, the many gaps in our knowledge may
make it difcult to predict what happens under eld conditions to plants
that efciently limit ROS production (Liu and He, 2017).
3 Adaptive Mechanism in Plants to Cope with Abiotic Stress
Plants are sessile in nature and cannot move away from adverse environ-
mental conditions. Therefore, plants need to respond in other ways to protect
themselves from environmental stress. In nature, different stresses such as
cold, drought, or heat may demand diverse responses, leading to distinct
adaptations in plants (Mittler, 2002). The visible adaptive response depends
on the severity of stress and can include leaf growth arrest, lesion formation,
onset of leaf senescence, and delayed or early owering. In addition, plants
can gauge mildly stressful conditions and respond by preparing for survival
against future stressful conditions of the same kind in a process called
hardening or priming (Tuteja and Singh Gill, 2013; Ha et al., 2012; Hancock
et al., 2001; Jajic et al., 2015; Sahoo et al., 2017). Exogenous application of
osmoprotectants or priming agents prior to an expected stress can success-
fully be used to induce enhanced resistance to multiple abiotic stresses in
plants, and this strategy is being successfully used in agriculture to improve
stress resistance of crop plants (Savvides et al., 2016). For example, natural or
chemical compounds including putrescine, spermine, vitamins, hormones,
and oligosaccharides can be exogenously applied prior to the expected
stress event (Aranega-Bou et al., 2014; Ebeed et al., 2017). Hence, plants
have evolved effective mechanisms to cope with a variety of stresses and
stress severities, and these mechanisms can be manipulated to increase crop
productivity.
3.1 Priming-Induced Abiotic Stress Tolerance in Plants
Priming is an emerging eld in the management of crops and produce
against damaging effects of environmental stress (Savvides et al., 2016).
The commercial storage of fruits at low temperature increases shelf life,
but storage between 0 and 5 C can cause chilling injuries or cold stress,
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A Kanojia & PP Dijkwel
especially in eshy fruits. Recently, a study has shown that priming of
peach fruits right after harvest by controlled, delayed cooling for 48 h at
20 C resulted in reduced chilling injuries as compared to fruits directly
exposed to cold temperature (Tanou et al., 2017). In the eld, soil salinity is
a major agricultural problem because of decreased irrigation water quality
and mineral weathering causing a slow increase in soil salinity (Flowers,
2004). Recent studies have shown that priming of Triticum aestivum plants
with 1 mmol ABA caused higher antioxidant activity and resistance to
salinity stress by protecting the photosynthetic electron transport chain
(Wang et al., 2017a,b). Also, pre-treatment of tomato plants with the proton
pump inhibitor omeprazole increased ROS levels and resulted in improved
shoot and root mass and plant nutritional status during salinity stress
(Van Oosten et al., 2017). Moreover, drought is a common abiotic stress to
plants, and priming has been conrmed by various studies to enhance the
tolerance to water-decit conditions: the priming of Medicago sativa plants
with the antioxidant melatonin enhanced the osmoprotection and antiox-
idant activity and conferred enhanced tolerance to a prolonged drought
period (Antoniou et al., 2017). In addition, seed priming with salicylic acid,
jasmonic acid, or paclobutrazol signicantly increased drought resistance
in rice plants (Samota et al., 2017). Increased stress resistance as a result
of priming resulted in marked improvements in shoot biomass compared
to the non-primed plants. For example, maize seeds which were primed
with silicon produced plants with signicantly increased leaf size and
fresh weight after being exposed to alkaline stress as compared to plants
developed from non-primed seeds (Abdel et al., 2016). Moreover, Arabidopsis
plants pre-treated with 50 mM NaCl displayed enhanced tolerance to desic-
cation, resulting in plants with greener leaves and a larger rosette size than
non-primed control plants (Sani et al., 2013). Thus, priming has proven to be
an effective approach in the improvement of crops under stressed conditions
because it improves not only survival but also yield.
Priming is believed to increase stress tolerance because the priming induces
an endogenous stress responses that allows the plants to handle future stress
with greater tolerance (Gamir et al., 2014). It is suggested that in primed
plants the protective effect is caused by increased ROS signalling which acti-
vates several signalling cascades, hormones, small peptides, and antioxidants
(Borges et al., 2014; Colcombet and Hirt, 2008; Mittler et al., 2011). Indeed,
exogenous application of H2O2increased drought and salinity stress resis-
tance in plants by modulating multiple processes including photosynthetic
activity, ROS scavenging, and turgor (Hossain et al., 2015). An effect of the
priming-induced increased ROS levels may be enhanced antioxidant activity,
resulting in restricted over-production of ROS as a result of subsequent stress
(Afzal et al., 2011; Hussain et al., 2016; Rejeb et al., 2014). Therefore, prim-
ing induces increased stress resistance, without apparent negative effects on
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
plant growth, primarily by controlling ROS over-production in response to
various subsequent stresses (Conrath, 2011).
3.2 Abiotic Stress-Induced Programmed Cell Death as an
Adaptive Response in Plants
Under certain stress conditions such as UV or ozone, cells that are no longer
needed commit suicide, which is mediated by a highly coordinated process
known as PCD (Tuzhikov et al., 2008). During this process only specic cells
are destroyed so that the neighbouring cells can survive the adverse effect
of the environmental stress (Wang and Bayles, 2013). The over-production of
ROS mediates PCD in many cell types (Petrov et al., 2015). In plants, differ-
ent stress factors such as heat shock, water decit, and salinity can cause the
initiation of PCD (Gaussand et al., 2011; Zuppini et al., 2010). UV-B radia-
tion that reaches the earth’s surface can also cause the activation of PCD, and
this is visible by the appearance of lesions or chlorotic areas (Nawkar et al.,
2013). UV-B exposure results in reduced photosynthetic capacity and cessa-
tion of leaf growth because of delayed cell division and cell expansion (Hec-
tors et al., 2010; Lo et al., 2005; Milchunas et al., 2004). Leaf growth resumes
once the leaf’s injury is repaired, but in the case of severe stress, it can lead to
premature leaf senescence (Suchar and Robberecht, 2015). Ozone is a major
photochemical oxidant and can also cause lesion formation in leaves. For
example, ozone caused leaf lesions in ozone-sensitive Arabidopsis accession
Wassilewskija, while ozone-tolerant accession Columbia was not affected by
the same stress levels (Tamaoki et al., 2003), indicating that ozone-stress resis-
tance is a genetically controlled trait.
Mild abiotic stress such as drought, salinity, or heat rapidly reduces plant
growth and development. The primary cause of stunted plant growth is stom-
atal closure which is useful in terms of reducing the transpiration rate, but
the closed stomata also lead to the reduction in photosynthesis (Kaya et al.,
2006; Manickavelu et al., 2006). The reduced energy production, leading to
delayed cell elongation and cell expansion, restricts the plant growth (Munns
and Termaat, 1986). Tolerance to mild osmotic stress can be achieved by accu-
mulation of osmoprotectants such as proline which helps in adjusting the
osmotic pressure as well as scavenging of various ROS radicals, and this may
cause only minor effects on plant growth (Nanjo et al., 1999; Saradhi et al.,
1995). Nevertheless, more pronounced osmotic stress can adversely affect
plant growth (Maggio et al., 2001; Fahad et al., 2017).
One of the most conspicuous consequences of abiotic stress is the onset
of senescence in adult leaves (Munns et al., 1995; Petronia et al., 2011). Leaf
senescence is a natural process that is a result of ageing or initiation of repro-
duction. It is the nal stage of leaf development which is usually marked by
the yellowing and withering of leaves and ultimately leads to the death of a
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A Kanojia & PP Dijkwel
leaf (Buchanan-Wollaston, 1997; Diaz et al., 2006; Guo and Gan, 2014). Senes-
cence is an essential process that allows the remobilisation of the nutrients
within the old senescent leaf so these can be used to support young growing
tissues (Himelblau and Amasino, 2001). However, senescence as a result of
abiotic stress can be considered unwanted as it may result in decreased plant
growth and yield (Sharabi-Schwager et al., 2009). However, as stress may
result in the shutdown of photosynthesis and growth, nutrients made avail-
able through the senescence of the older leaves may allow the plant to survive
and reproduce. The apparent positive effect of abiotic stress-induced senes-
cence of the older leaves on the survival of the whole plant can also be seen
in a number of transgenic plant lines in which stress resistance was affected
by the transgene. For example, in Arabidopsis, the autophagy-related mutants
atg5,atg7,andnbr1 are more sensitive to heat and drought stress as compared
to wild-type plants (Zhou et al., 2013). However, careful observation of plant
phenotypes shows that the old leaves have undergone senescence, and the
young leaves remained green and viable. Similarly, drought stress on ascor-
bate and GSH-decient mutants (vtc-2 and pad-2) also displayed advanced
yellowing in old leaves, but young leaves remained green (Kofer et al., 2014).
The biosynthesis of ABA is upregulated during environmental stress
and as part of the senescence programme (Khan et al., 2013). Pyrabactin
resistance1-like (PYL) belongs to the family of ABA receptors that function
in ABA and drought-stress signalling. Arabidopsis lines over-expressing
PYL9 displayed a greater tolerance to drought stress and ABA-induced leaf
senescence of old leaves in an ethylene-independent manner (Zhao et al.,
2016). This example clearly indicates that ABA-induced senescence of the
old leaves during water decit is important for the survival of young tissues.
Thus, premature leaf senescence as a result of stress affects productivity, but
it is also an important strategy adopted by plants to assure the survival of
young leaves. Therefore, the stress response depends on leaf age, and we
propose that ROS is a factor linking the two. Consistent with this, ARA-
BIDOPSIS A-FIFTEEN (AAF) modulates redox homeostasis in Arabidopsis,
and transgenic lines over-expressing AAF (oxAAF) displayed early senes-
cence and stress sensitivity in an age-dependent manner (Chen et al., 2012).
The physiological parameters used to monitor the progression of senescence
in the third rosette leaves after 49 days of germination displayed accelerated
senescence as compared to 28-days-old leaves. Moreover, accelerated senes-
cence was found during ozone exposure due to over-production of ROS
in Arabidopsis (Miller et al., 1999). In addition to this, research has shown
that expression of ROS-responsive genes is upregulated in fully expanded
Arabidopsis rosette leaves, prior to the initiation of senescence (Breeze et al.,
2011). This indicates that once leaves reach maturity, an increase in ROS
production leads to the progressive onset of senescence, and this is consistent
with ROS playing a central role in the initiation of senescence in old leaves
(Sedigheh et al., 2011; Schippers et al., 2008).
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
As described earlier, ROS, ABA, and ethylene also function in plant sur-
vival during environmental stress. Here, we propose that (i) the dual role of
ROS, ABA, and ethylene in either leaf death or survival is ultimately deter-
mined by leaf age and (ii) that stress-induced leaf senescence of old leaves
benets the survival of the whole plant. One purpose of early senescence in
stressed plants is to complete the life cycle quickly, allowing early initiation of
ower development and seed production (Buchanan-Wollaston, 1997; Lamb,
2012; Kazan and Lyons, 2016). However, whether plants can survive and com-
plete reproduction depends on the severity of stress (Xu et al., 2010). Under
severe stress, suppression of various biochemical and physiological processes
eventually leads to the death of the whole plant (Munns et al., 1995; Pandey
et al., 2017).
Altogether, plants’ response to stress can have at least three different out-
comes: mild stress may have limited impact on plant growth and develop-
ment, but it can result in a priming effect, hardening the plant for future
stress of a similar kind. Secondly, more severe stress will induce leaf senes-
cence in the older leaves, allowing those leaves to continue to function as
a nutrient and energy source and allowing the growing parts of the plant
to survive. Finally, unmanageable stress will lead to the death of the plant.
These responses are illustrated in Figure 1, where Arabidopsis plants were
treated with increasing periods of continues darkness, followed by a recovery
period. Two days of dark treatment had limited effect on plant growth, while
4 days of darkness allowed the survival of the young leaves, at the expense of
the older leaves. Here, the young leaves showed a strong survival response,
while the older leaves died. Six days of darkness did not allow the survival of
the plant even though Figure 1 shows that the older leaves were completely
wilted, while the younger leaves still appeared pale green. Therefore, these
2 days dark stress 4 days dark stress 6 days dark stress
(a) (b) (c)
Mild stress Prolonged stress Severe stress
Figure 1 Distinct response to stress in Arabidopsis plants. Eighteen-days-old
Arabidopsis plants, grown under long-day conditions in a growth chamber, were treated
with 2 (a), 4 (b), or 6 (c) days of total darkness and were then allowed to recover for
3 days under long-day conditions. Representative plants were photographed. The bar
represents 10 mm.
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15
A Kanojia & PP Dijkwel
three responses are more likely part of a continuum where initially a survival
response is set in motion, but that depending on leaf age, continued stress
will result in senescence of older leaves, allowing survival of young leaves
for as long as possible.
4 The Occurrence of Age-Related Changes Determines
the Outcome of the Stress Response
A huge amount of research has been done to understand how plants adapt in
response to environmental stress, with the aim to produce better-performing
crops under uctuation and, as a result of climate change, more unpredictable
environmental conditions. However, while relatively little is known about
how leaves of a different age respond to stress, a wide range of studies on
abiotic stress responses and leaf senescence allows us to propose a model
correlating ageing and stress response of individual leaves.
As part of the developmental ageing process of leaves, age-related
changes (ARCs) will take place (Figure 2). Such ARCs include cell division,
cell expansion, cell elongation, degradation of cellular components, devel-
opmental changes in hormone and ROS levels, and many more. Finally,
when leaves reach the nal stage of development, this occurrence of ARCs
leads to the decline in function of cells and onset of senescence (Caswell and
Salguero-Gomez, 2013). In addition, stress can induce early senescence in
mature, but not in young leaves, as discussed before. This has been clearly
shown by ethylene treatment of Arabidopsis plants, where only the older
leaves were able to respond to the senescence treatment with the onset of
senescence (Grbic and Bleecker, 1995; Jing et al., 2002, 2005). Even prolonged
ethylene treatment did not induce senescence in young leaves, and the
constitutive ethylene signalling mutant ctr1 did not show early senescence
(Grbic and Bleecker, 1995). This suggests that certain ARCs are required for
a leaf to become competent to senesce (Jibran et al., 2013). Moreover, the
phenotype of the ctr1 mutant suggests that a stress treatment in young leaves
can induce a strong survival response to that stress, resulting in old leaves
that do not respond to the ethylene signalling with senescence. Thus, we
propose that young leaves are unable to respond to stress with the onset of
senescence, while certain ARCs allow a mature leaf to senescence in response
to abiotic stress (Jibran et al., 2013). Finally, the occurrence of further ARCs
in old leaves causes senescence, even in the absence of environmental stress
(Jibran et al., 2013). The above-described idea is supported by research dating
more than three decades ago when a study showed that Beta vulgaris leaves
undergoing cell division were not affected by salinity stress, while extending
and fully extended leaves were found to be sensitive to salt treatment (Papp
et al., 1983). Also, an experiment conducted on Albizia leaves described the
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
effect of stress and age on the rhythmic frequency of opening and closure of
leaves. The study showed that mature leaves closed slowly and incompletely
as compared to young leaves when exposed to darkness, water stress, or
ethylene (Lee and Satter, 1983).
While the nature of the ARCs that allow a mature leaf to senesce in
response to stress is unclear, some recent reports point to ARCs that coincide
with decreased stress resistance of old leaves. In Arabidopsis leaves, DNA
repair efciency was highest in young leaves and lower in adult leaves
(Golubov et al., 2010), suggesting that an age-related reduced ability to
maintain genomic integrity may cause an old leaf to be more susceptible
to stress and ROS-related DNA damage. In addition to this, the production
of secondary metabolites is one of the strategies for protection against
environmental stress, and research conducted on Cistus ladanifer showed
that the amount of avonoids and terpenes in young leaves was greater
than in mature leaves (Valares Masa et al., 2016). The greater amount of
these compounds present in young leaves may allow for a higher resistance
to stressful conditions than the mature leaves by keeping the antioxidant
machinery active and by keeping ROS generation at acceptable levels (Fini
et al., 2011; Loreto et al., 2004). Therefore, there is evidence to suggest that
as a result of ARCs, leaves are programmed to become less tolerant to stress
over time (Figure 2).
Figure 2a describes a model that explains how ARCs determine whether
abiotic stress results in the survival or death of a leaf. The model is adapted
from the senescence window concept model proposed by Jing et al. (2002).
As described earlier, ARCs take place over the course of leaf development,
and some of these may decrease stress resistance over time. In addition, or as
a result of these ARCs, the chance for a leaf to senesce increases over time.
This leads to three distinct phases: the rst where a leaf is highly resistant to
stress, i.e. a leaf at this stage has not yet obtained the competence to senesce.
Then, as time progresses, increased ROS, ABA, and ethylene levels, together
with a decline in cytokinins, DNA repair and antioxidant activity may be
essential senescence-inducing ARCs. These ARCs result in the leaf to acquire
the competence to senesce, but leaves only do so in the presence of stress.
Finally, the leaf will die regardless of the presence of stress as a result of the
occurrence of sufcient senescence-inducing ARCs.
The consequence of this model explains the whole plant response to stress
(Figure 2b) where plants have leaves of a different age. The older, bottom
leaves are more likely to senesce in response to stress than the younger leaves,
while the reduced stress resistance of the middle leaves allow senescence to
occur as a result of severe stress levels, but not in case of mild stress. The
nutrients remobilised as a result of the senescence will then allow the highly
stress-resistant young leaves to survive as long as possible.
The model has important shortcomings, including a lack of evidence that
a decrease in stress resistance of individual leaves is actually programmed
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A Kanojia & PP Dijkwel
Environmental stress
Young
Young leaves
Adult leaves
Old leaves
Stress tolerance
Senescence-inducing ARCs
Stress-tolerant
phase
Adult
Stress-adaptive
senescence phase
Old
Stress-independent
senescence phase
Stress tolerance Senescence-inducing ARCs
Age-related changes
(a)
(b)
Figure 2 A tentative model showing stress response in different age of
leaves. (a) Leaves undergo age-related changes (ARCs) throughout their development.
These ARCs may include a gradual reduction in stress tolerance or the acquisition of
senescence-inducing ARCs. Young leaves therefore are highly tolerant to stress, while
mature leaves can respond to severe abiotic stress with the induction of leaf senescence.
Old leaves will senesce because of senescence-inducing ARCs. (b) Individual leaves of
plants exposed to environmental stress show a distinct response depending on their age.
Young leaves are in the stress-tolerant phase because of negligible senescence-inducing
ARCs, adult leaves are in the stress-adaptive phase because of gradually occurred
senescence-inducing ARCs, while old leaves senesce by default as a result of low stress
tolerance and increase of senescence-inducing ARCs.
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Abiotic Stress Responses Are Governed by Reactive Oxygen Species and Age
into the leaf developmental programme. In addition, it is not clear if
senescence-inducing ARCs actually exist, or whether the chance to senesce
is purely a result of reduced stress resistance. Moreover, what is the nature
of the ARCs, and how are they regulated? Nevertheless, we believe that it
is a working model that explains certain aspects of the plant stress response
and highlights the importance of age in that response. We expect that further
research will allow extension or modication of the model described here.
5 Final Remarks
As sessile organisms, plants have evolved exceptional resistance mecha-
nisms to cope with many abiotic stresses, and most plants can survive a
wide range of temperatures, water availabilities, and light intensities. It is
clear that ROS and phytohormones play important roles as stress sensors
and signalling molecules in many abiotic stress responses. However, they
play equally important roles in development and biotic stress responses,
and the question remains how these messengers can regulate so many
seemingly different processes. Recent omics approaches have helped reveal
the complexity of the regulation of stress responses, yet we are still far away
from fully understanding those. Nevertheless, it is clear that plants’ ability
to regulate the age-dependent life and death of individual organs is an
important strategy to survive adverse environmental conditions. We hope
that this article will stimulate future research to include the age factor as a
hard-wired regulatory checkpoint for the life–death decision of plant organs
in response to abiotic stress.
Related Articles
Reactive Oxygen Signaling in Plants
Oxidative Stress and Leaf Senescence
Ethylene and Senescence Processes
Ethylene Biosynthesis and Signaling: A Puzzle Yet to be Completed
The Role of Abscisic Acid in Stress Tolerance
Mitogen-Activated Protein Kinase Cascades in Plant Signaling
Abiotic Stress and Metabolomics
Environmental Regulation of Leaf Senescence
Nutrient Remobilization during Leaf Senescence
Molecular Regulation of Leaf Senescence
Genetic Manipulation of Leaf Senescence
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19
A Kanojia & PP Dijkwel
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... However, stress only induces senescence after individual leaves have reached a certain age. This suggests that the ability to senesce depends on the occurrence of certain age-related changes (ARCs) throughout plant development (Sade et al. 2018;Kanojia and Dijkwel 2018;Kim et al. 2017;Leng et al. 2017;Jibran et al. 2013;Woo et al. 2013;Lim et al. 2007a;Jing et al. 2005). ARCs are defined as any irreversible changes that are rigorously dependent on age and development. ...
... Early senescence is associated with increased ROS levels (Kan et al. 2021;Guo et al. 2017;Schippers et al. 2008;Jing et al. 2008;Kanojia and Dijkwel 2018). Since old101 plants show a delayed onset of senescence, we hypothesized that this may be a result of lower ROS levels. ...
... However, early leaf senescence can be induced by adverse environmental conditions or by treatments with hormones that typically play a role in the plants' stress response, such as Jasmonic acid and ethylene (Hensel et al. 1993;Kim et al. 2015;Jing et al. 2005;Jibran et al. 2013). Crucially, however, these hormones were not able to induce leaf senescence in very young leaves (Hensel et al. 1993;Jing et al. 2002), suggesting that leaves need to acquire the competence to senesce before this destructive process can be induced (Jing et al. 2005;Kanojia and Dijkwel 2018). Thus, also stress-induced senescence appears to be dependent on the occurrence of ARCs, although these may include different ARCs than those required for the induction of developmental senescence. ...
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Article
Key message Our manuscript is the first to find a link between activity of SAL1/OLD101 against IP3 and plant leaf senescence regulation and ROS levels assigning a potential biological role for IP3. Abstract Leaf senescence is a genetically programmed process that limits the longevity of a leaf. We identified and analyzed the recessive Arabidopsis stay-green mutation onset of leaf death 101 (old101). Developmental leaf longevity is extended in old101 plants, which coincided with higher peroxidase activity and decreased H2O2 levels in young 10-day-old, but not 25-day-old plants. The old101 phenotype is caused by a point mutation in SAL1, which encodes a bifunctional enzyme with inositol polyphosphate-1-phosphatase and 3′ (2′), 5′-bisphosphate nucleotidase activity. SAL1 activity is highly specific for its substrates 3-polyadenosine 5-phosphate (PAP) and inositol 1, 4, 5-trisphosphate (IP3), where it removes the 1-phosphate group from the IP3 second messenger. The in vitro activity of recombinant old101 protein against its substrate IP3 was 2.5-fold lower than that of wild type SAL1 protein. However, the in vitro activity of recombinant old101 mutant protein against PAP remained the same as that of the wild type SAL1 protein. The results open the possibility that the activity of SAL1 against IP3 may affect the redox balance of young seedlings and that this delays the onset of leaf senescence.
... These hormones play a role in plant growth and development. In the case of biotic stress, they interact synergistically and antagonistically [108,112,113]. ...
... Even though the two types of stress do not seem to be related, the response to both is given by increased ROS and abscisic acid (ABA), the level of this hormone increases during abiotic stress, especially under drought conditions [112,113]. It increases in direct proportion to the stress of biotic and abiotic factors, to the point where it establishes equilibrium or to the point where the plant cannot keep up with the stressors and an imbalance occurs between stress and plant response, at which point PDC mechanisms arise to counteract abiotic stressors and stagnate development alongside other mechanisms to counteract abiotic factors [108]. ...
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Accelerating heavy metal pollution is a hot issue due to a continuous growth in consumerism and increased activities in various global industries. Soil contamination with heavy metals has resulted in their incorporation into the human food web via plant components. Accumulation and amplification of heavy metals in human tissues through the consumption of medicinal plants can have hazardous health outcomes. Therefore, in this critical review we aim to bring together published information on this subject, with a special highlight on the knowledge gaps related to heavy metal stress in medicinal plants, their responses, and human health related risks. In this respect, this review outlines the key contamination sources of heavy metals in plants, as well as the absorption, mobilization and translocation of metal ions in plant compartments, while considering their respective mechanisms of detoxification. In addition, this literature review attempts to highlight how stress and defensive strategies operate in plants, pointing out the main stressors, either biotic or abiotic (e.g., heavy metals), and the role of reactive oxygen species (ROS) in stress answers. Finally, in our research, we further aim to capture the risks caused by heavy metals in medicinal plants to human health through the assessment of both a hazard quotient (HQ) and hazard index (HI).
... Tolerance to biotic and abiotic stresses is determined by a complex integration of age-related factors and stress response pathways, which can be expressed through morphological plasticity, prevention of oxidative damage, and senescence control to ensure stress survival (Kanojia & Dijkwel 2018;Rankenberg et al., 2021). Age-dependent differential submergence tolerance has been previously observed (e.g., Nabben et al., 1999;Mauchamp et al., 2001;Groeneveld & Voesenek 2003;Sone & Sakagami, 2017;. ...
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Thesis
The term rheophyte describes a biological group of flood-tolerant plants confined to the beds of swift-running streams and rivers in nature and grow up to flood-level, but not beyond the reach of regularly occurring flash floods. Rheophytism occurs in non-vascular (liverworts, hornworts, and mosses) and vascular plants (ferns, lycophytes, gymnosperms, and angiosperms). The book Rheophytes of the world, together with its complement, published in 1981 and 1987, respectively, constitute the world references on rheophytism in plants. Although more than 35 years have passed since the publication of the first census of rheophytes, no researcher has attempted to update the number of taxa of this biological group in seed plants and/or have tried to compile data about these species from literature. Additionally, the published literature showed a lack of a morphological, biochemical, and molecular characterization in response to flooding in rheophytic species. In the first article of this thesis (Chapter II), we review the main topics associated with rheophytism, including morphological characteristics, genetic studies, geographic distribution, conservation, and evolutionary aspects. In addition, we updated the global rheophyte checklist, considering the two groups of seed plants (gymnosperms and angiosperms). Finally, we demonstrate the distribution of rheophytism in the angiosperms phylogeny and estimated the geographic distribution and richness of selected taxa on the world map for the first time. We compiled a dataset composed of 1,368 taxa (obligate, facultative, and unclassified rheophytes) distributed in 114 families and 508 genera in angiosperms and four taxa in gymnosperms (Podocarpaceae family). Of the 114 families plotted in the angiosperm phylogeny, at least 80 have obligate rheophytes. As expected, based on the first census of this biological group, the geographic distribution of rheophytes in flowering plants is mainly in the tropical and subtropical regions.The high richness of rheophytic taxa was primarily found in southern Mexico, southern China, Borneo, and northern and eastern Australia. In contrast, the geographic distribution of rheophytes in gymnosperms is restricted to New Caledonia and Tasmania. In the second article of this thesis (Chapter III), we characterize morphological, biochemical, and gene expression aspects of Dyckia brevifolia, an endangered rheophyte native to Brazil. Seedlings of this bromeliad were exposed to complete submergence and recovery in two-time frames: short-term submergence stress (10 days of complete submergence with five days of recovery) and long-term submergence stress (30 days of complete submergence with 15 days of recovery). Dyckia brevifolia has shown important adaptations to flooding tolerance, which include a quiescent strategy that consists of decreased shoot elongation underwater, conservation of chlorophyll, carotenoid and protein content during submergence, restriction of carbohydrate catabolism (mainly starch), and an efficient reactive oxygen species (ROS) detoxification system, mainly for hydrogen peroxide (H2O2) when completely submerged. During the recovery period after de-submergence, the species also displays key adaptive features, such as maintaining rosette turbidity, fast-growth resumption, total recovery of soluble sugars, increased chlorophyll and carotenoid content, and active capacity to mitigate ROS in the first fifteen days after reoxygenation. Taken together, these results demonstrate that the seedlings of this bromeliad show important adaptations to flooding stress and are well adapted to the rheophytic environment.
... Tolerance to biotic and abiotic stresses is determined by a complex integration of age-related factors and stress response pathways, which can be expressed through morphological plasticity, prevention of oxidative damage, and senescence control to ensure stress survival (Kanojia and Dijkwel, 2018;Rankenberg et al., 2021). Age-dependent differential submergence tolerance has been observed previously (e.g., Nabben et al., 1999;Mauchamp et al., 2001;Groeneveld and Voesenek, 2003;Sone and Sakagami, 2017;Bui et al., 2020). ...
Article
Complete submergence refers to the situation when floodwaters rise to levels where plants’ shoots and roots are entirely underwater. It can be viewed as a sequence of distinct stressors comprising submergence and de-submergence periods. A plant’s tolerance to this abiotic stress is determined by its ability to acclimate to both phases. Here we aimed to characterize the response of Dyckia brevifolia seedlings, a bromeliad native to Brazil, to submergence and de-submergence periods in short- and long-term stress time frames in terms of morphology, biochemistry, and gene expression. We demonstrated that D. brevifolia seedlings are tolerant to complete submergence, at least over the course of the time frame evaluated. All seedlings survived 30 d completely submerged, despite reduced dry weight and rosette area (as compared with control plants). This species adopts the low oxygen quiescence syndrome (LOQS) strategy, which comprises decreased shoot elongation underwater, downregulation of energy consumption processes, and carbohydrate catabolism (mainly starch) during the period of stress. In addition, chlorophyll and carotenoid contents were preserved, even after 1 month underwater. Furthermore, in D. brevifolia rosettes, the relative expression of hypoxia marker genes, such as alanine aminotransferase (AlaAT), pyruvate decarboxylase (PDC), and alcohol dehydrogenase (ADH), remained unchanged over the entire course of the short-term submergence stress (10 d). Mainly due to both ascorbate peroxidase (APX) and catalase (CAT) activities, this species also demonstrated an efficient reactive oxygen species (ROS)-detoxifying system, primarily for hydrogen peroxide (H2O2), when completely submerged. During the recovery period, in addition to maintaining rosette turgidity, D. brevifolia seedlings demonstrated fast-growth resumption, total soluble sugar recovery, accumulation of chlorophyll and carotenoid, and ROS scavenging. The combination of these responses contributes to the robust adaptation of D. brevifolia to the challenging recurrent fluctuations within its unique environment.
... Tolerance to biotic and abiotic stresses is determined by a complex integration of age-related factors and stress response pathways, which can be expressed through morphological plasticity, prevention of oxidative damage, and senescence control to ensure stress survival (Kanojia and Dijkwel, 2018;Rankenberg et al., 2021). Age-dependent differential submergence tolerance has been observed previously (e.g., Nabben et al., 1999;Mauchamp et al., 2001;Groeneveld and Voesenek, 2003;Sone and Sakagami, 2017;Bui et al., 2020). ...
... Globe's environment is continuously changing and one of the major factors responsible for this change is industrialization as it increases temperature by emitting large amounts of GHGs. The intensity of global warming is increasing gradually and has disturbed the global ecosystem (Kanojia & Dijkwel, 2018); however, the degree it will further disturb the global ecosystem is still dependent on human activities. Some impacts of climate change are shown in Fig. 1. ...
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Article
Climate change is among the most crucial concerns of the world. It is a serious threat to the global agriculture and its overall impact on global agriculture is yet not clear. A rise of 2.5-4.5◦C is expected in the global temperature until the end of 21st century. The amount of greenhouse gases particularly CO2 is increasing at an alarming rate and is enhancing the plant photosynthesis and productivity. However, this increase in productivity is counteract by the more negative effects of climate change on agriculture like increased evapotranspiration, drought, floods, changes in the amount and distribution of rainfall, higher pest infestations and more irrigation demand. Climate change also affects the nutrients availability and efficiency by influencing microbial activities and population in the soil. Therefore, adaptation of agriculture sector to the changing climate is indispensable because of its sensitivity and size. This review is aimed to document the possible impacts of climate change on agriculture, its causes and future projections. Some strategies are also advised to mitigate the emission of greenhouse gases, to reduce the negative impacts of climate change on agriculture and to make new policies keeping in view their broader consequences on agriculture.
... However, all the growth stages in plants are affected adversely by heat stress right from germination to growth and development, reproductive phase, seed yield (Hasanuzzaman et al., 2013;Ahmad et al., 2016), and seed quality in oilseed crops . The rise in global temperature will ultimately damage the ecosystem comprehensively (Kanojia and Dijkwel, 2018). Specifically, heat stress is a severe threat to oilseed crops as it impairs the production and quality of the yield; for example, the seed yield decreased up to 39% in camelina and 38% in canola under elevated temperature scenarios (Jumrani and Bhatia, 2018;Ahmad et al., 2021b). ...
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Abiotic stresses are considered to be the major factors causing a decrease in crop yield globally, these stresses include high and low temperature, salinity, drought, and light stress etc. To overcome the consistent food demand for the ever-growing population, various genes from micro-organisms and non-plant sources have been expressed in transgenic plants to improve their tolerance against abiotic stresses. Gene expression in transgenic plants through conventional methods are time-consuming and laborious that’s why advanced genetic engineering methods for example Agrobacterium-mediated transformation and biolistic methods are more accurate, useful, and less time-consuming. This review provides an insight into various bacterial genes for example mtID, codA, betA, ADH, IPT, DRNF1 and ggpPS, etc. that have been successfully expressed in transgenic plants against various abiotic stress for stress tolerance enhancement and crop yield improvement which exhibited good encouraging results. Genes from yeast (Saccharomyces cerevisiae) have been introduced in transgenic plants against drought and salinity stress. All these genes expressed from non-plant sources in plants can be very helpful to enhance crops for better yield productivity in the future to meet the demands of the consistently rising population of the world.
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Background As a fundamental metabolism, leaf photosynthesis not only provides necessary energy for plant survival and growth but also plays an important role in global carbon fixation. However, photosynthesis is highly susceptible to environmental stresses and can be significantly influenced by future climate change. Methods In this study, we examined the photosynthetic responses of Phragmites australis ( P . australis ) to three precipitation treatments (control, decreased 30%, and increased 30%) under two thermal regimes (ambient temperature and +4 °C) in environment-controlled chambers. Results Our results showed that the net CO 2 assimilation rate ( P n ), maximal rate of Rubisco ( V cmax ), maximal rate of ribulose-bisphosphate (RuBP) regeneration ( J max ) and chlorophyll (Chl) content were enhanced under increased precipitation condition, but were declined drastically under the condition of water deficit. The increased precipitation had no significant effect on malondialdehyde (MDA) content ( p > 0.05), but water deficit drastically enhanced the MDA content by 10.1%. Meanwhile, a high temperature inhibited the positive effects of increased precipitation, aggravated the adverse effects of drought. The combination of high temperature and water deficit had more detrimental effect on P . australis than a single factor. Moreover, non-stomatal limitation caused by precipitation change played a major role in determining carbon assimilation rate. Under ambient temperature, Chl content had close relationship with P n (R ² = 0.86, p < 0.01). Under high temperature, P n was ralated to MDA content (R ² = 0.81, p < 0.01). High temperature disrupted the balance between V cmax and J max (the ratio of J max to V cmax decreased from 1.88 to 1.12) which resulted in a negative effect on the photosynthesis of P . australis . Furthermore, by the analysis of Chl fluorescence, we found that the xanthophyll cycle-mediated thermal dissipation played a major role in PSII photoprotection, resulting in no significant change on actual PSII quantum yield ( Φ PSII ) under both changing precipitation and high temperature conditions. Conclusions Our results highlight the significant role of precipitation change in regulating the photosynthetic performance of P . australis under elevated temperature conditions, which may exacerbate the drought-induced primary productivity reduction of P . australis under future climate scenarios.
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Chemical, physical, and biotic factors continuously vary in the natural environment. Such parameters are considered as stressors if the magnitude of their change exceeds the current acclimation norm of the plant. Activation of genetic programs allows for conditional expansion of the acclimation norm and depends on specific sensing mechanisms, intracellular communication, and regulation. The redox and reactive oxygen species (ROS) network plays a fundamental role in directing the acclimation response. These highly reactive compounds like H2O2 are generated and scavenged under normal conditions and participate in realizing a basal acclimation level. Spatial and temporal changes in ROS levels and redox state provide valuable information for regulating epigenetic processes, transcription factors (TF), translation, protein turnover, metabolic pathways, and cross-feed, e.g., into hormone-, NO-, or Ca²⁺-dependent signaling pathways. At elevated ROS levels uncontrolled oxidation reactions compromise cell functions, impair fitness and yield, and in extreme cases may cause plant death.
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The aim of this research was to investigate how exogenous abscisic acid (ABA) alleviates cadmium (Cd) toxicity in purple flowering stalk (Brassica campestris L. ssp. chinensis) and evaluate whether it could be a potential choice for phytoremediation. Purple flowering stalk seedlings were cultivated in a hydroponic system with Cd at various concentrations (0–100 μmol L⁻¹) as controls and Cd plus ABA as the treatment in the growth media. The soluble proteins, chlorophyll contents and the activity of the antioxidant enzyme system were determined by previously established biochemical methods. The contents of soluble protein and chlorophyll, and the activities of superoxide dismutase (SOD, EC 1. 15.1.1), peroxidase (POD, EC 1.11.1.7), ascorbic peroxidase (APX, EC 1.11.1.11), glutathione reductase (GR, EC 1.8.1.7) and superoxide anion (O2·-) increased with the increase of external Cd concentrations, and then decreased in both Cd and Cd+ABA treatments, with higher activities of enzymes but lower level of O2·- in Cd+ABA than those in Cdonly treatments. It indicated that a stress adaptation mechanism was employed at lower Cd concentrations. The contents of malondialdehyde (MDA) and hydrogen peroxide (H2O2), increased with the increase of Cd concentrations in the growth medium, with the highest levels in the treatment of 100 μmol L⁻¹ Cd with lower levels in respective Cd+ABAtreatments than the Cd only treatmetns. Plants treated with 100 μmol L⁻¹ Cd plus ABA showed a 60% decrease in Cd content in the leaves but a 259% increase in Cd content in the roots. In summary, exogenous ABA might alleviate Cd toxicity in purple flowering stalk mainly by reducing the reactive oxygen species (ROS) though activing the antioxidant enzyme system and accumulating more Cd in roots.