Oxidative Damage to Plants || Plant Signaling under Environmental Stress

Chapter 18

Plant Signaling underEnvironmental Stress

Mohammad Miransari

18.1 INTRODUCTION

Plants experience different environmental stresses and may be able to induce

tolerance by utilizing morphological and physiological mechanisms. Various

other mechanisms are also able to mitigate environmental stress in plants.

For example, to increase their water efficiency under drought stress, plants

decrease their leaf surface by rolling it or changing the angle, control the

behavior of their stomata, and hence keep their water (Ford et al., 2011).

The physiological changes under stress include the production of different

products, such as osmolytes and enzymes; activation of different signaling

pathways; etc. Controlling plant growth under stress by the activation of sig-

naling pathways, which is in fact a plant response to handle the stress, is of

great importance. There are a set of signaling pathways activated under stress

including mitogen-activated protein kinase signaling, reactive oxygen species

and redox signaling, as well as hormonal signaling (Asai et al., 2002;

Hirayama and Shinozaki, 2010; Munne-Bosch et al., 2013). The role of

microRNAs under stress is also of significant importance, as they also enable

the plant to respond to stress. Under stress, the methylation of DNA, remo-

deling of chromatin, histone methylation/acetylation, and processes related to

small RNAs alone or combined may modify gene expression, rearrange the

genome and hence influence plant tolerance to stress (Figs 18.1 and 18.2)

(Jones, 2006; Guo and Lu, 2010; Lelandais-Briere et al., 2011; Grativol

et al., 2012).

There are different techniques used to evaluate plant response under

stress; one of them is proteomics. Using the proteomic technique it is possi-

ble to investigate which genes and hence proteins are activated and produced

under stress (Evers et al., 2012; Swami et al., 2011). Accordingly, the pro-

duction of tolerant plants under stress may be possible. Depending on the

kind of stress, different genes and proteins are activated and produced.

541P. Ahmad (Ed): Oxidative Damage to Plants. DOI: http://dx.doi.org/10.1016/B978-0-12-799963-0.00018-6

© 2014 Elsevier Inc. All rights reserved.

http://dx.doi.org/10.1016/B978-0-12-799963-0.00018-6

18.2 STRESS AND MITOGEN-ACTIVATED PROTEINKINASE SIGNALING

Plant signaling pathways are among the most important plant responses to

stress, enabling the plant to survive under stress. There are different signaling

pathways activated under stress, including mitogen-activated protein kinase

Primary and translend activation

Antimicrobialpeptides & chemicais

ROS, PCD JA ET R-genesignaling

Resistance to bacteria, oomycetes & fungi

ROS NOPCD

Camalexinaocumulation

PAD3 PR1 PDF1,2

MPK3,6priming

ROS, PCD

Transient KK K K

Micrbial signalsand receptors

Long-term activationLong-term constitutive activationtemperature/humidity-dependent

Sustained

BAK 1BKK 1BIR 1

SOBIR

?

? ?

?

MEKK1 & MKKKsMEKK1 & MKKKs MEKK1 & MKKKs

MKK4,5,9MKK1,2,6 MKK4,5,9

MPK3,6MPK3,6MKK4,11

MEKK1 & MKKKs

MKK1,2

MPK4

TFsP

Potential TF targets

WKY, ERF, ZFP, MYB, NAC, bZIP

WKY, ERF, MYB, ZFP, NAC, AP2, RLK, PK, PP2C,PROPER, CYP, PUB, GST, PER, OXR, LOX, ACS

Gene regulation

ERF1SA

MKS 1JA, ET

PHOS32 VIP1 ERF104 ACS2,6

PP2Cs MKP1

NIA2

MKP1PTP1

WKY33

NOA1RBOHSNC1P

P P PP P P P

Gene regulation Gene regulation

FIGURE 18.1 The network of MAPK signaling pathways in response to different biological and

stress parameters, combined with other signaling pathways, including the reactive oxygen species

and hormonal signaling. (From Tena et al. (2011) with kind permission from Elsevier.)

FIGURE 18.2 The regulation of response genes under stress by cross talk between epigenetic

parameters including DNA methylation and histone modification resulting in plant tolerance under

stress. (From Grativol et al. (2012) with kind permission from Elsevier.)

542 Oxidative Damage to Plants

(MAPK) signaling. These are from the serine/threonine family, modifying

plant response under stress. They are phosphorylated and activated by MAPK

kinase in their cascade. MPAK kinase is also activated by MAPKK kinase.

Different MAPK kinases have been indicated in plants including tobacco,

alfalfa, chorispora bungeana and Arabidopsis (Fig. 18.3) (Zhang et al.,

2006a, b, c; Sinha et al., 2011; Ahmad et al., 2011; Miransari et al., 2013).

Different activities in plants are regulated by MAPK signaling pathways,

including: 1) modification of plant response to stress, 2) cellular cycles such

as mitosis and cytokinesis, 3) development of stomata, 4) hormonal signal-

ing, 5) plant immunity, and 6) plant tissue abscission (Wang et al., 2007b;

Cho et al., 2008). Under stress the cellular surface receptors are activated,

resulting in the production of intercellular signaling pathways, which are

able to modify the cellular environment and hence handle the stress (Asai

et al., 2002; Tor et al., 2009). Accordingly, the MAPK signaling pathway

results in the transduction of signals to the nucleus and hence appropriate

adjustment of cellular homeostasis (Sinha et al., 2011).

MAPK signaling is able to regulate the activity of MAP, affecting the

dynamic of microtubules by phosphorylating the residues of serine and threo-

nine at the time of microtubules binding. MAPK signaling is perceived by

plant receptor protein kinases at the main plasma membrane (Beck et al.,

2011). This kind of network can control the activities of transcription factors,

hormones, enzymes, peptides, etc. in plants (Tena et al., 2011).

MAPK signaling is the plant response to different activities including the

alleviation of stresses. Hence, genetic modification of MAPK signaling may

MPKKK

Abioticstress

MPKK

MAPK AtMPK4ZmSIMK1

AtMPK7ZmMPK7

AtMPK3CbMPK3ZmMPK3 MMK3

MMK2

SIMK SAMKOsMPK3/4

NtWIPK/NtSIPK

NtMPK4

MKK4PsMPK2

SIPKKNtMEK2

OsMKK4

SIMKK

OMTK1NDPK2

AtMKK3AtMKK1

AtMKK2

AtMEKK1

Drought

Heavymetals

Cd2+ Cu

2+

As3+

AtMKK4/5

ANP1

OXI1

AtMPK6

? ? ?

?

?

?

? ? ?

? ?? ?

? ? ? ? ?

?

ColdSaltOxidative

stress Wound Ozone

FIGURE 18.3 The cross talk of different MAPK signaling components, shown for different

plants. Solid and dashed arrows indicate proven and postulated pathways, respectively. The ques-

tion mark is the component, which has yet to be indicated. (With kind permission from Sinha

et al., 2011.)

543Chapter | 18 Plant Signaling under Environmental Stress

be an effective method to increase plant resistance to stress. For example,

research has indicated that under drought stress the activation of MAPK sig-

naling results in the production of proline. The role of proline in plants under

stress has been reported by many workers (Katare et al., 2012; Koyro et al.,

2012; Rasool et al., 2013). The production of proline is controlled by differ-

ent protein kinases under drought, salinity and cold stress (Shou et al.,

2004a, b; Raghavendra et al., 2010; Krasensky and Jonak, 2012).

The role of MAPK signaling has been indicated in controlling the pro-

cesses of mitosis and cytokinesis by affecting microtubule transition.

Accordingly, Beck et al. (2011) used the mutant of Arabidopsis taliana to

show such an effect. As a result, the processes of mitosis and cytokinesis

were inhibited and bi- and multi-nucleate cells were formed, adversely

affecting the vegetative cellular growth.

Pan et al. (2012) isolated ZmMPK17, a maize (Zea mays L.) MAPK

gene, which is able to alleviate multiple stresses in plants. The gene tran-

scription is responsive to plant hormones such as ethylene, jasmonic acid,

abscisic acid, salicylic acid under suboptimal temperature, drought and salin-

ity stress. The related transcription elements are regulated by Ca21 and

hydrogen peroxide under stress. When ZmMPK17 was overexpressed, less

reactive oxygen species were produced in plants under stress by affecting the

process of antioxidant production. The transgenic plants were more tolerant

to the stress, resulting in enhanced germination rate and production of pro-

line and soluble sugars (Yang et al., 2013).

MAPK signaling pathways and reactive oxygen species are interactive;

the production of reactive oxygen species in plants can result in the activa-

tion of MAPK signaling pathways and the pathways are able to control the

production of such species. The exogenous use of hydrogen peroxide in

Arabidopsis thaliana can activate the MAPK signaling pathways and the

pathways are able to produce antioxidants (Pan et al., 2012).

Signaling by MAPK pathways may result in cellular activities including

cell division, differentiation and cellular responses to stress (Mishra et al.,

2006; Pan et al., 2012). Plants are able to form a network of MAPK signal-

ing pathways, which eventually results in efficient cellular responses by the

production of related stimuli (Mishra et al., 2006). Different molecules can

act as the substrate for MAPK signaling pathways such as protein kinases,

transcription factors and subsequent molecular cascade including MAPK2K

and MAPK3K as well as related receptors (Whitmarsh and Davis, 1998;

Cardinale et al., 2002).

There are 110 genes in Arabidopsis thaliana which are expressed during

the production of the MAPK signaling pathways: 10 MAPK molecules, 20

MAP2K molecules and 80 MAP3K molecules (Pitzschke et al., 2009). The

10 MAPK molecules are able to phosphorylate 570 proteins, with a high

number of transcription factors regulating plant growth and response to

stress. Phosphorylation can influence the activity of transcription factors by


affecting: the protein structure, their localization and activity and their inter-

action with other proteins (Fiil et al., 2009).

The Arabidopsis MKK1/MKK2-MPK4/MPK6 is able to regulate plant

response to stresses such as salt and cold (Gao et al., 2008; Qiu et al., 2008).

Arabidopsis MKK3 can affect plant immunity. MKK4/MKK5-MPK3/MPK6

are important signaling molecules in the regulation of plant development and

response to stress (Asai et al., 2002; Wang et al. 2011). The regulation of

cytokinesis and mitosis is by the activity of MKK6-MPK4/MPK11 (Beck

et al., 2010, 2011). Plant systemic resistance is activated by MKK7 (Zhang

et al., 2007). The MKK9-MPK3/MPK6 are important signaling molecules

affecting ethylene signaling and leaf senescence (Xu et al., 2008).

18.3 STRESS AND REACTIVE OXYGEN SPECIES ANDREDOX SIGNALING

Plants respond to stress by different morphological and physiological

mechanisms. Among different physiological mechanisms is the production of

different metabolites. For example, reactive oxygen species are produced

under stress, as a result of metabolic by-products, which can adversely affect

cellular structure and hence functioning. It is important for the plant cell to

maintain cellular homeostasis for redox processes (Van Aken et al., 2009;

Nick, 2013).

Under stress the production of reactive oxygen species can result in the

degradation of cellular constituents such as carbohydrates, lipids, and pro-

teins (Ahmad et al., 2010, 2011; Koyro et al., 2012). Oxidative stress can

also have unfavorable effects on chlorophyll and carotenoid resistance, pre-

venting the plant photosynthetic efficiency and respiratory processes (Yao

et al., 2009). Plants respond by activating different signaling pathways and

hence producing antioxidants molecules, which are able to degrade the pro-

ducts of cellular stress such as reactive oxygen species (Foyer and Shigeoka,

2011; Zhang et al., 2011). Enzymes such as superoxide dismutase, catalase

and glutathione peroxidase are required for cellular activities and their

enhanced levels under stress can catabolize the products of oxidative stress

including the active oxygen species, resulting in the alleviation of stress

(Sajedi et al., 2011; Ahmad et al., 2010, 2011; Koyro et al., 2012).

However, it has been indicated that low amounts of reactive oxygen spe-

cies can act as signal molecules regulating plant response under stress by

affecting Ca21 signaling and hence ABA and stomata activity (Pei et al.,

2000; Desikan et al., 2001; Zhang et al., 2001; Miller et al., 2008). ABA is

able to affect plant response to stress by regulating the gene network of reac-

tive oxygen species including catalase, ascorbate peroxidase and superoxide

dismutase (Jiang and Zhang, 2002; Zhang et al., 2011; Fujita et al., 2013).

Different stresses including salinity, drought, cold, heat, high light, etc.

may result in the production of reactive oxygen species, such as oxygen


(O2), superoxide radical (O2�2), hydroperoxyl radical, hydroxyl radical and

hydrogen peroxide (H2O2), in plants and can regulate the activity of different

transcription factors. However, at high amounts they adversely affect plant

growth. Under stress, proxidases are produced, and hence the plant may

respond by producing antioxidant enzymes as mentioned earlier (Mittler,

2002; Jones, 2006).

Airaki et al. (2012) investigated the effects of suboptimal temperature

(8 �C) on the growth of pepper (Capsicum annum L.) and determined differ-

ent reactive nitrogen and oxygen species, which were significantly affected

by suboptimal temperature. They found that the production of products such

as glutathione and ascorbate can help the plant to alleviate the stress by

affecting cell redox potential.

18.4 STRESS AND HORMONAL SIGNALING

Plant hormones, including auxin, cytokinins, abscisic acid (ABA), gibberellins,

ethylene, jasmonates, brassinosteroids and strigolactones, are able to regulate

different functions in plant at cellular and molecular levels. There are different

signaling pathways and interactions related to plant hormones, among which

the role of hormonal signaling under stress can be of the greatest importance

(Hirayama and Shinozaki, 2010; Miransari, 2012; Miransari et al., 2014). The

response of plants under stress is regulated by plant hormones indicating that

the presence of hormones can increase plant tolerance to stress. Production of

hormones in plants may result in activation of different genes in plant and

hence the regulation of different activities such as: 1) activation of different

signaling pathways, 2) cell cycling, 3) plant water behavior, 4) plant response

to stress, etc. (Wang et al., 2007a; Tuteja, 2007; Rahman, 2013).

The effects of auxin under stress can be through the induction of plant

transcription factors related to genes such as Aux/IAA, GH3, and small

auxin-up RNA (SAUR) genes. The auxin signaling pathways is mostly

induced and regulated by transcription factors including auxin response fac-

tors (ARFs) and the Aux/IAA repressors (Han et al., 2009; Jain and

Khurana, 2009).

The role of ABA under stress has also been indicated. Stresses such as

salinity and drought result in the production of ABA. The activity of stomata

under different conditions including stresses is regulated by ABA, which is

its most important function in plants (Jia and Davies, 2007). Due to the vari-

ous functions of ABA in plants it could be the most important signaling mol-

ecule among hormones. The expression of different genes by ABA and

hence the subsequent plant response can result in the alleviation of stress in

plants. For example, the expression of nced genes in plant is induced by

ABA under stress (Wan and Li, 2006). The adverse effects on small RNA

induce the production of ABA, indicating that there is a link between small

RNA pathways and ABA signaling pathways in plant (Zhang et al., 2008).


The gene that produces cytokinin is ipt resulting in the production of iso-

pentyl transferase and isopentenyladenosine-50-monophosphate (McGraw,

1987). Among the important functions of cytokinin is the protection of photo-

synthesis under stress by interacting with the receptor proteins and activation

of related signaling pathway. As a result the genes are expressed and

miRNAs, electrons, carbon, photosynthesis related proteins, and the enzyme

ribulose bisphosphate carboxylase/oxygenase are produced. By using the gene

ipt it is possible to genetically modify plant response under drought stress as

the process of leaf senescence is delayed (Rivero et al., 2007, 2009).

The gaseous plant hormone, ethylene, with the simplest structure as com-

pared to other plant hormones, has some important functions in plants

including the germination of seed, abscission and tissue senescence. Based

on the related signaling pathways, ethylene is interactive with the ethylene

receptors, which are two-component histidine protein kinases, located on the

plasma membrane (Mount and Chang, 2002; Miransari and Smith, 2014).

The ethylene signaling pathway is among the best-known signaling

pathways and has the important transcription factor ETHYLENE

INSENSITIVE3. Under stress the production of the stress hormone ethylene

increases, adversely affecting plant growth. Interestingly, it has been indi-

cated that the use of plant growth promoting rhizobacteria (PGPR) may

result in decreased production of ethylene by the production of the enzyme

1-aminocyclopropane-1-carboxylate (ACC) deaminase (Glick et al., 2007;

Jalili et al., 2009).

The production of gibberellins in plants is catalyzed by the enzymes

monooxygenases, dioxygenases and cyclases. The enhancing effect of gibber-

ellins on plant growth is by degradation of DELLA proteins (Griffiths et al.,

2006). DELLA proteins are able to modify plant response to stress by affect-

ing the combined response of plant hormones to stress (Miransari, 2012).

Brassinosteroids are steroid products affecting different plant functions,

including plant growth and development. So far about 70 brassinosteroids

(Sasse, 2003; Yu et al., 2008) have been identified. During the production of

brassinosteroids, molecular oxygen is required, indicating that this hormone

can modify the effects of hypoxia on plant growth and development. The

hormone is able to alleviate the unfavorable effects of different stresses in

plants (Miransari, 2012).

The lipid hormones, jasmonates, are able to affect plant systemic resis-

tance as well as plant growth and development (Schaller and Stintzi, 2009).

Jasmonates are able to affect plant growth under stress by interacting with

the other plant hormones, controlling the production of reactive oxygen spe-

cies, calcium influx, and activating nitrogen protein kinase (Hu et al., 2009).

The hormone has an important role in the process of nodulation in legumi-

nous plants (Sun et al., 2006).

Among the most important effects of salicylic acid on plant

growth is the regulation of plant systemic resistance, by the following


mechanisms: 1) expression of different genes including the PAL and priming

genes, 2) activation of phytoalexin related pathways, 3) deposition of callose

and phenolic products, and 4) affecting the auxin signaling pathway (Chen

et al., 2009).

Strigolactones are a new class of plant hormones affecting: 1) mycor-

rhizal fungi symbiosis with its plant host as hyphal branching factors, 2)

shoot branching, and 3) germination of parasitic weed Striga. The important

factor affecting the production of the hormone in plant is phosphorous star-

vation (Akiyama et al., 2005; Lopez-Raez et al., 2008; Miransari, 2011).

18.5 STRESS AND ROLE OF MIRNAS AND SIRNAS

Small RNAs, including the two major classes of microRNAs (miRNAs) and

short-interfering RNAs (siRNAs), can regulate different plant functions includ-

ing growth and development, phytohormone signaling, and flowering as well as

plant adaptation to abiotic and biotic stresses (Chen, 2005; Yang et al., 2007;

Shukla et al., 2008; Lelandais-Briere et al., 2011; Cuperus et al., 2011; Li et al.,

2011). For the diverse performance of biological processes, they must be

precisely regulated (Ji and Chen, 2012). The length of a mature miRNA ranges

from 19 to 24 nucleotide and it can regulate the activity of post-transcriptional

gene through paring with mRNA and the subsequent cleavage (Guo and Lu,

2010). Their structure can be modified and stabilized by the small RNA trans-

ferase and the methylate transferase (as its homologue) and siRNAs as well as

the proteins bound to RNA (Chen et al., 2011; Ji and Chen, 2012).

Presently, miRNAs and their sequences have been indicated in 41 plant

species (Griffiths-Jones, 2004; 2006). For the first time Subramanian et al.

(2008) found 35 novel miRNA families in soybean [Glycine max (L.)

Merrill] and researched their role in the symbiotic process between rhizo-

bium and soybean. The presence of miRNAs has been reported by different

workers, but very few have investigated their role under abiotic and biotic

stresses (Wang et al., 2009; Chen et al., 2009).

Li et al. (2011) found new miRNAs, in Populus euphratica, which were

responsive to drought stress. The sequencing of miRNA indicated the upreg-

ulation of 104 miRNAs and the downregulation of 27 miRNAs under

drought stress. Such a finding can lead to the production of resistant plants

under adverse environmental conditions. Under drought stress 22 miRNA

were upregulated and 10 miRNA were downregulated. The substrates of

miRNAs controlled different activities in plant including growth, protein

functioning, nutrient conditions, etc. (Wang et al., 2011).

Using deep sequencing and data analysis Yu et al. (2011) reported five

responsive miRNAs in Brassica rapa under heat stress. This indicates the

important role of miRNAs in Brassica rapa under heat stress. The role of

miRNAs under high levels of aluminum was investigated by Chen et al.

(2012) in the model legume plant Medicago truncatula. The sequencing of


miRNA showed that there were 23 responsive miRNAs under unfavorable

levels of Al, most of which were downregulated by stress.

18.6 STRESS AND PLANT PROTEOMICS

It is important to indicate which genes and hence proteins are activated,

expressed, and produced under stress so that the alleviation of stress and pro-

duction of more tolerant plants become possible. Accordingly, different tech-

niques have been developed and used including the use of “omics” such as

“proteomics.” Using proteomics, it may be possible to identify which pro-

teins are produced under stress and hence how plants may respond under

stress. The use of proteomic techniques under different conditions including

stress has been investigated by many workers (Zhang et al., 2009; Zorb

et al., 2009; Agrawal et al., 2012).

The use of the helix loop (OrbHLH2) improved the ability of Arabidopsis

thaliana under salt and osmotic stress (Zhou et al., 2009). Swami et al.

(2011) investigated the behavior of sorghum proteins in the leaf under salt

stress (200 mM NaCl for 96 h). The expressed proteins under the stress were

of signaling, transcriptional, metabolic and functioning significance. They

recognized different proteins under the stress including RNA binding protein,

putative inorganic pyrophosphatase, serine/threonine protein kinase, and indi-

cated that under salt stress the plant has a special mechanism to alleviate the

stress.

Using proteomics, Ford et al. (2011) investigated the expression of 159

wheat proteins under drought stress. With respect to the physiological prop-

erties and the level of tolerance in the tested cultivars, different numbers of

proteins were changed during the stress. Yao et al. (2011) investigated the

effects of phosphorous deficiency (concentration less than 5µM) on the pro-

tein collection of Brassica napus using proteomics. Proteins related to the

transcription of genes, translation of proteins, metabolism of carbon, transfer

of energy and plant growth were downregulated as a result of stress.

However, root related proteins were upregulated.

The effects of cold and salt stress on the growth of potato (Solanum

tuberosum L.) were investigated in a growth chamber experiment at both

transcriptomic and proteomic levels. While a high number of genes were reg-

ulated by cold stress, salt stress resulted in significantly high number of pro-

teins. Under both stresses the photosynthesis genes were downregulated, but

cell rescue and transcriptional related genes were upregulated (Evers et al.,

2012; Mansour, 2013).

Under stress plant response can be indicated by gene and protein expres-

sion; the production of reactive oxygen species and subsequent production of

antioxidant enzymes is also a mechanism used by plants to alleviate the

stress. Hence, relating plant behavior under stress at transcriptomic and


proteomic level to the production of reactive oxygen species may be a good

method to determine plant tolerance.

18.7 CONCLUSIONS

Plants are able to survive under stress as they modify their morphological

and physiological mechanisms. Many signaling pathways such as mitogen-

activated protein kinase signaling, reactive oxygen species and redox signal-

ing, and hormonal signaling, as well as the small RNAs, are activated during

stress. Use of appropriate techniques such as proteomics can also be impor-

tant for the evaluation of plant response under stress. Indicating the activated

signaling pathways and the related genes and proteins can be useful for the

production of tolerant plants under stress.

The role of signaling under stress is of great importance and must be elu-

cidated so that the production of tolerant plants may be likely at large scale.

This chapter discussed some of the most important details regarding plant

signaling pathways under stress. Accordingly, the related cellular compo-

nents, genes and proteins, which are activated under stress have also been

explained. However, for future prospects, biologists have to make the results

of their research work more applicable: 1) The precision of new and sug-

gested methods must be tested regularly so that the related signaling

pathways are exactly elucidated; 2) cellular behavior, expressed genes and

proteins must be investigated and evaluated precisely to make the use of alle-

viating strategies more applicable; 3) the cross talk and interactions between

different signaling pathways can importantly indicate plant response under

stress as well as the subsequent use of effective and required techniques; 4)

the use of more sophisticated and precise instruments can be a useful tool to

make the modification of plants under stress more possible; and 5) the litera-

ture being presented by researchers is also very effective, speeding up the

rate of progress of scientific knowledge.

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