Summary of representative reports on the interaction of nitric oxide with phytohormones during various abiotic stresses.
Plants, being sessile, are concurrently exposed to various biotic and abiotic stresses. The perception of stress signals in plants involves a wide spectrum of signal transduction pathways that interact to induce tolerance against adverse environmental conditions. This functional overlapping among various stress signaling cascades also leads to the expression of genes that regulate biosynthesis or action of other hormones. Phytohormonal signals, activated by both developmental and environmental responses, play a crucial role to develop stress tolerance in plants. Nitric oxide (NO) is one of the major players in plant signaling networks. Emerging evidence supports that NO interplays with signaling pathways of auxins, gibberellins, abscisic acid, ethylene, jasmonic acid, brassinosteroids, and other plant hormones to control metabolism, growth, and development in plants. This chapter focuses on the current state of knowledge of cross talk between signaling pathways of NO and phytohormones in plants exposed to various abiotic stresses.
- nitric oxide
- abiotic stresses
- signaling cascades
- plant growth
Exposure to a wide array of environmental stresses is one of the most crucial factors that negatively influence plant growth and productivity worldwide. Plants respond to such adverse conditions through perception of endogenous and exogenous stress factors via hormone signaling networks along with the coordination of several downstream signal transduction mechanisms involving cyclic nucleotides, calcium ions, and reactive oxygen (such as hydrogen peroxide) or nitrogen (e.g., nitric oxide) species. Acclimation to abiotic stresses is achieved through turgor maintenance , accumulation of osmolytes , regulation of photosynthetic and transpiration rate, and activation of antioxidant machinery . Moreover, stress-induced alterations in gene expression and metabolism stimulate several anti-stress compounds, which help to modify physiology, phenology, growth, and reproduction of plants exposed to adverse environmental conditions .
Nitric oxide (NO) is an important metabolite and stress signaling molecule that influences multitude of physiological and developmental functions in plants. It serves as a key component of the signaling cascades involved in plant growth, metabolism, and adaptive responses to various biotic and abiotic stresses. It is well established that NO regulates a plethora of physiological processes ranging from seed germination to plant senescence. Emerging evidence suggests this potential plant growth regulator interplays with various phytohormones (PHs) to control metabolism, growth, and development in plants.
During the last few years, extensive research has been carried out to explore the multiple and diversified mechanisms underlying PHs interactions with NO. There is virtually no doubt that NO acts either upstream or downstream of PHs [5, 6]. It seems that NO modulates the biosynthesis, distribution, degradation, and conjugation of elements involved in PHs transport and signaling [7–11]. However, further studies are required to explain how NO concomitantly interacts with hormone-related proteins at post-transcriptional or even translational level. Similarly, the understanding of mechanisms underlying intersection of NO signaling with signaling cascades of auxins (AUXs), gibberellins (GBs), cytokinins (CKs), ethylene (ETs), absicic acid (ABA), salicylic acid (SA), jasmonic acid (JA), polyamines (PAs), brassinosteroids (BRs), and strigolactones (SLs) under abiotic stress conditions remains elusive. Considering the common function played by these plant growth regulations in enhancing plant tolerance to biotic and abiotic stresses, it can be speculated that PHs-mediated stress responses are linked with NO synthesis. Therefore, this chapter would focus on the current state of knowledge of cross talk between signaling pathways of NO and PHs in plants exposed to various abiotic stresses ( Table 1 ).
|Type of stress||Phytohormone||Plant species||Response||Relation with NO||References|
|Drought stress||ABA||Increased expression of ABA biosynthetic gene ||+||Zhang et al. |
|AUX||Development of adventitious roots||+||Liao et al. |
|SA||Increased tolerance against osmotic stress||+||Alavi et al. |
|CK||Regulation of photosynthetic machinery||+||Shao et al. |
|Cd toxicity||ET||Promoted the Cd-induced senescence processes||−||Rodríguez-serrano et al. |
|PAs||Inhibition of root growth||+||Groppa et al. |
|AUX||Stabilization of AUX repressor protein IAA17 through suppression of AUX carriers PIN1/3/7||−||Yuan and Huang |
|Improved antioxidative capacity and reduced degradation of AUX in roots||+||Xu et al. |
|SA||Increased activities of antioxidative enzymes||+||Wang et al. |
|Restricted Cd distribution to organelles||+||Xu et al. |
|Ni toxicity||SA||Enhanced chlorophyll contents and reduced lipid peroxidation and proline accumulation||+||Kazemi et al. |
|Cu toxicity||BR||Increased ABA synthesis resulted in improved tolerance||+||Choudhary et al. |
|Al toxicity||GA||Promoted apical root growth||+||He et al. |
|Salinity stress||ABA||Decreased salt-induced leaf senescence by regulating the expression of ABA biosynthesis genes (||−||Kong et al. |
|ET||Reduced ROS levels and blocked ET synthesis resulting in lower dead cell ratio in cell suspension cultures||−||Poór and Tari |
|AUX||Repressed AUX signaling through stabilization of AUXIN RESISTANT3 (AXR3)/INDOLE-3-ACETIC ACID17 (IAA17)||−||Liu et al. |
|SA||Reduced H2O2 accumulation, limited Na2+ uptake and increased influx of H+-ATPase to plasma membrane||+||Dong et al.|
|PAs||Reduced free putrescine, spermidine and polyamine oxidase (PAO) activity||−||Fan et al. |
|Temperature stress||ABA||Improved the thermotolerance of plant calluses||+||Song et al. |
|Enhanced ||+||Guo et al. |
|PAs||Increased putrescine and spermidine levels and stimulated the expression of genes encoding Spd synthase (||+||Diao et al. |
|Conversion of putrescine into spermidine or spermine conferred cold tolerance||+||Li et al. |
|SA||Increased NR activity reduced chilling injury||+||Aydin and Nalbantoğlu |
|JA||Increased CAT activity to scavenge H2O2, leading to reduced chilling injury||+||Liu et al. |
2. NO-phytohormone cross talk under drought stress
Drought stress is one of the major limiting factors affecting multiple aspects of plant growth and productivity . The typical mechanism of plants response to water stress, frequently caused by drought, is closure of stomata to conserve water. NO and ABA are the two most important stress-related molecules that intensively cross talk during environmental challenges like drought to induce plant adaptive responses such as stomatal closure and activation of antioxidant machinery [5, 11]. Evidence suggests that NO acts downstream of ABA as decreased NO synthesis reduces ABA-induced responses in plant tissues exposed to stress conditions [12, 13]. However, NO is also reported to counteract ABA during events not linked to stress adaptation such as breaking of seed dormancy [14, 15]. It indicates a certain level of specificity in NO-ABA cross talk mechanisms, which seems to depend on the type of plant cell, tissue or organ studied, or nature of physiological event under analysis.
Generation of ROS (H2O2) under adverse environmental conditions triggers NO-mediated ABA responses such induction of stomatal closure , activation of antioxidant enzymes , and up-regulation of transcription factors . In addition, cGMP and type 2C protein phosphatases (PP2Cs) have also been identified to participate in downstream of NO-mediated ABA signal transduction and upstream of cytosolic Ca2+ during the regulation of stomatal apparatus [19–21]. Moreover, the calcium/calmodulin system and mitogen-activated protein kinases (MAPKs) have also been demonstrated as key downstream elements involved in ABA or H2O2-induced NO signaling during plant antioxidant defense mechanisms [22, 23]. Cross talk between NO and ABA in the ABA-dependant signaling network up-regulated the cytosolic Ca2+ to regulate Crassulacean acid metabolism (CAM) expression in bromeliads that significantly improved plant tolerance in a water-limited environment [21, 24]. It seems that ABA-induced NO production is associated with increased nitrate reductase (NR) activity that controls stomatal movements in
Interestingly, NO serves as a second messenger in the signaling cascades of various plant hormones such as GA, JA, ET, CK, and AUX involved in the regulation of stomata under environmental stress conditions [27, 28]. Interactions between NO and AUX signaling pathways are complex and need to be explored in plants exposed to water-limited environment. It is well established that both NO and AUX interplay during growth and development of plant roots [29, 30]. Association of AUX with ET to regulate root morphology and development is considered a key aspect of drought tolerance in plants . Development of adventitious roots in cucumber hypocotyl cuttings involves the cross talk between AUX and NO signaling networks activated by Ca2+ dependent protein kinase activity . Since NO is intensively involved in lateral root formation during drought stress , it may be speculated that AUX and NO signaling cascades interact and influence the architecture and development of root hair and root meristem size [34, 35] for the extraction of more water under drought stress conditions.
Drought stress influences the signaling of various JA-associated genes . JA stimulates CDPK production by increasing Ca2+ influx and the resultant signal cascade results in ABA-regulated stomatal closure. A rapid loss in turgor and subsequent reduction in stomatal aperture were noted in excised
A positive interaction between NO and CK under water-limited environment was reported by Shao et al. . Treatment of plants with CK plus NO scavenger (Hemoglobin) revealed that CK promoted NO signaling, probably mainly through a NR source in plants exposed to water stress conditions. CK interaction with NO signaling cascades regulated photosynthetic machinery and increased the adaptability to drought stress in
3. NO-phytohormone cross talk under heavy metals stress
Heavy metals (HMs) are phytotoxic elements that can damage plant growth and metabolism at very low concentrations . The involvement of plant hormones such as IAA, CK, and ET to alleviate HMs-induced toxicity is well reported [47–49]. Some recent studies suggest that NO acts in concert with signaling pathways of phytohormones to induce tolerance against excess elements [50, 51]. However, the exact nature of NO-hormone interactions still needs to be explored and is largely dependent on the species, the plant organ as well as concentration of metal and duration of stress .
Cadmium is one of the most widely distributed HM in agricultural soils . Cd-induced increase in endogenous levels of NO is associated with its role as a bioactive molecule to quench ROS . Alterations in hormonal homeostasis are potential signals that directly affect plant responses to Cd stress, including interplay between hormones and the whole plant signaling network, such as the ROS , MAPK , and NO signaling pathways . Exposure to short-term Cd stress revealed an interrelation of ET with NO generation, polyamine metabolism, and MAPK cascades in young
Interplay between NO and GA has been reported to influence a wide spectrum of physiological processes, including seed germination, primary root growth, and inhibition of hypocotyl elongation [8, 29]. Interaction of NO with GA was observed to promote apical root growth in
Combined NO and SA application was observed to counteract the toxic effects of Ni in
Cross talk between plant hormones and NO is also considered critical for Fe-deficiency signaling . Evidence obtained in
4. NO-phytohormone cross talk under salinity stress
Salinity stress is considered one of the most harmful stresses due to its high magnitude and worldwide distribution . Phytohormones play a key role in enhancing the tolerance and adaptability of plants against salinity stress. Some recent studies suggest that NO acts in concert with signaling pathways of phytohormones to induce tolerance against salt stress [85, 86]. Presumably, plant hormones such as ABA, ET, and AUX are transported from salt-treated roots to leaves to trigger NO synthesis or transport throughout the plant . NO-induced alleviation of oxidative damage in salt-stressed plants is associated with increased antioxidant activities and decreased thiobarbituric acid reactive substances content . ABA stimulates H2O2 accumulation that results in increased NO generation, leading to the activation of MAPK and up-regulation of genes associated with antioxidant enzymes [17, 18] in plants exposed to abiotic stresses like salinity. However, NO does not always positively interplay with ABA. In cotton, exogenous NO supply (using SNP as NO donor) reduced salt-induced leaf senescence by decreasing ABA content and down regulating the expression of ABA biosynthesis genes (
In general, it is believed that ET biosynthesis corresponds to increased damage in plants. However, recent studies indicate ET as a stress-signaling hormone that interacts with signaling cascades of other phytohormones to enhance tolerance against various biotic/abiotic stresses [70, 86]. Studies involving tobacco seedlings showed that transcriptional activation of ethylene response factor (ERF) in ethylene-signaling process improved salt stress tolerance by decreasing ROS accumulation . Treatment of
Participation of both NO and ROS in SA-induced stomatal closure is also reported in literature . Activation of a peroxidase (sensitive to the inhibitor salicylhydroxamic acid) by SA promotes ROS accumulation and NO generation in guard cells, leading to stomatal closure. Experiment with soybean seedlings showed that combined application of SNP (as NO donor) and SA alleviated the toxicity of NaCl-induced salt stress by increased proline accumulation and activation of CAT, APX, and GPX. Similar results were reported by Liu et al.  and Dong et al.  in
Sulfur (S) is a major component of metabolites such as reduced glutathione (GSH), coenzyme A, methionine, cysteine (Cys), sulfo-lipids, iron-sulfur (Fe-S) clusters, and thioredoxin system involved in regulation of physiological processes under salt stress conditions . Evidence suggests that NO promotes S-assimilation, which is linked to ET production through Cys synthesis . Hence, it may be speculated that NO and S interact to modulate ABA and ET levels in guard cells that may influence the stomatal and photosynthetic response under salt stress conditions. NO combines with GSH to generate S-nitrosoglutathione (GSNO), leading to enhanced S requirement of plants for improved tolerance under environmental stress conditions [99, 100]. Coordinated effect of NO and S regulated the utilization of S and GSH resulting in improved growth and photosynthetic activity in salt-stressed mustard plants . NO is a key regulatory signal that activates several biochemical processes and interacts with sulfhydryl groups and nitro groups in the process of nitration to enhance tolerance against salt stress . NO also cooperates with other signaling molecules such as H2S to enhance tolerance against salinity stress in plants. NO and H2S cross talk helped to maintain low Na+ levels with up-regulation of
Recently, it has been proposed that NO negatively regulates CK signaling by limiting phosphorelay activity via S-nitrosylation . Contrasting reports of Kong et al.  showed that foliar applied SNP (as NO donor) delayed salt-induced leaf senescence in cotton seedlings by up-regulating the expression of CK biosynthesis gene, isopentenyl transferase (
5. NO-phytohormone cross talk under temperature stress
Temperature stress negatively influences the vegetative and reproductive growth phases of plants. Coordinated action between NO and plant hormones (ABA, JA, GA, CK) induce thermotolerance in plants by activating the antioxidant machinery and up-regulating the expression of genes encoding heat shock proteins [104–106]. Studies involving
Low temperature severely restricts plant growth and causes both structural and metabolic damages in plants . Exposure to low temperature induces oxidative and nitrosative stress thereby promoting NO synthesis , which serves as a potential link between PA and ABA to induce stress responses in plants . Literature indicated extensive cross talk among NO, ABA, PAs, and H2O2 to modulate various physiological and stress responses under low temperature conditions [110, 121]. Interplay among NO, SA, and ABA was noted to enhance the antioxidative activities (CAT, SOD, POX) that contributed to improved chilling injury in
NR and NOS pathway are the most widely known NO sources in plants [19, 127]. Evidence obtained by Aydin and Nalbantoğlu  showed that SA pretreatment of
6. NO-phytohormone cross talk under other abiotic stresses
Ever increasing human population and industrial productivity has resulted in alarming rise in air pollutants, causing extensive damages to natural habitats of plant . Ozone is characterized as one of the most phytotoxic air pollutants severely restricting plant growth and development . Plants use many transportable chemical signals such as NO to turn the sensing of ozone from guard cells to adjacent epidermal and mesophyll cells . Presumably, NO generation in relation to ozone stress induces ET and ABA synthesis and interferes with stomatal ABA response, potentially by inhibiting K+ efflux at the guard cells . The involvement of alternative oxidase (
Destruction of ozone layer in upper atmosphere, as a result of increased concentrations of air pollutants, has exposed living organisms to UV-radiation particularly UV-B that induces oxidative stress in plants [138, 139]. Although it is well known that NO interacts with ABA, ET, MeJA to control guard cell signaling in response to various environmental stresses [140, 141], only few reports are available with regard to NO, ET, and ABA cross talk in stomatal regulation under UV-B stress . Studies involving
A transient NO burst is among the earliest responses to wounding . NO production in wounded parts involves several pathways including cross talk with signaling cascades of hormones and endogenous signals [146, 147]. It was shown that NO and AUX actively take part in wound-healing response in plants [145, 148]. Imanishi et al.  presented evidence for the involvement MeJA and mechanical wounding in expression of the
Initiation of senescence in plants is controlled by various factors such as nutrient supply, light conditions, leaf age, and environmental stress . Plant hormones such as ET and CK influence senescence by either promoting or delaying the process, respectively [155, 156]. Evidence supports the interaction of NO with other plant hormones to floral senescence and fruit maturation . Recently, Ji et al.  demonstrated that SA treatment at low concentrations induced NOA1-dependent NO signaling and activated antioxidant defense to counteract MeJA-induced leaf senescence. NO plays a conceivable role to counteract the ABA- and jasmonate-induced senescence in rice by inhibiting H2O2 accumulation and lipid peroxidation . Mishina et al.  found that delayed leaf senescence in
7. Conclusion and future perspectives
Although our understanding of NO interactions with plant hormones has increased dramatically in past few years, many pieces of the puzzle are still missing. It is well established that NO coordinates with plant hormones to regulate gene expression and activities of anti-oxidative enzymes under adverse environmental conditions. However, our current knowledge about NO-phytohormone interactions is derived chiefly from NO-induced posttranslational modifications of transcription factors and biosynthetic enzymes. Future work is needed to explore the interplay among NO, plant hormones, ROS, protein kinases, and cytoskeletal proteins in order to understand the complicated network of NO signaling under abiotic stress conditions. Interestingly, most of the studies related to NO-phytohormonal interactions involve experiments in controlled laboratory environments, very little is known about the cross talk between these signaling molecules during flower initiation or grain development. Moreover, plants growing under natural conditions face multiple stresses; hence, future studies will need to address how NO interacts with the signaling cascades of phytohormones in plants exposed to two or more abiotic stresses.