**1. Introduction**

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

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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 [1], accumulation of osmolytes [2], regulation of photosynthetic and transpiration rate, and activation of antioxidant machinery [3]. 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 [4].

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**).


Cross Talk between Nitric Oxide and Phytohormones Regulate Plant Development during Abiotic Stresses http://dx.doi.org/10.5772/intechopen.69812 119

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 [1], accumulation of osmolytes [2], regulation of photosynthetic and transpiration rate, and activation of antioxidant machinery [3]. 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

118 Phytohormones - Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses

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

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

**Phytohormone Plant species Response Relation** 

ABA biosynthetic gene *vp14*

Increased tolerance against

adventitious roots

osmotic stress

machinery

ABA *Zea mays* Increased expression of

CK *Zea mays* Regulation of photosynthetic

AUX *Tagetes erecta* Development of

*aestivum*

SA *Triticum* 

**with NO**

**References**

+ Zhang et al. [26]

+ Liao et al. [33]

+ Alavi et al. [41]

+ Shao et al. [42]

(PHs) to control metabolism, growth, and development in plants.

adverse environmental conditions [4].

abiotic stresses (**Table 1**).

**Type of stress**

Drought stress



**Table 1.** Summary of representative reports on the interaction of nitric oxide with phytohormones during various abiotic stresses.

## **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 [2]. 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 (H2 O2 ) under adverse environmental conditions triggers NO-mediated ABA responses such induction of stomatal closure [16], activation of antioxidant enzymes [17], and up-regulation of transcription factors [18]. 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 H2 O2 -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 *Arabidopsis* [19] and CAM expression in bromeliads [24]. The expression of CYP707A2 gene, induced by NO biosynthesis, during seed germination initiated ABA catabolism and increased ABA levels to enhance plant resistance against drought stress [11, 25]. BR treatment of water-stressed *Zea mays* leaves induced NO generation in mesophyll cells and up-regulated the expression of ABA biosynthetic gene *vp14* to enhance water stress tolerance in *Zea mays* [26].

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 [31]. 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 [32]. Since NO is intensively involved in lateral root formation during drought stress [33], 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.

**2. NO-phytohormone cross talk under drought stress**

cell, tissue or organ studied, or nature of physiological event under analysis.

Generation of ROS (H2

**Type of stress**

stresses.

Temperature stress

ABA *Phragmites* 

PAs *Lycopersicon* 

*australis*

*esculentum*

O2

Drought stress is one of the major limiting factors affecting multiple aspects of plant growth and productivity [2]. 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

**Phytohormone Plant species Response Relation** 

120 Phytohormones - Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses

of plant calluses

*Medicago sativa* Enhanced *MfSAMS1* expression

cold stress

tolerance

chilling injury

scavenge H2

**Table 1.** Summary of representative reports on the interaction of nitric oxide with phytohormones during various abiotic

*Zingiber officinale* Conversion of putrescine

SA *Spinacia oleracea* Increased NR activity reduced

JA *Cucumis sativus* Increased CAT activity to

Improved the thermotolerance

to increase acclimation against

Increased putrescine and spermidine levels and stimulated the expression of genes encoding Spd synthase (*LeSPDS*), arginine decarboxylase (*LeADC. LeADC1*) and ornithine decarboxylase (*LeODC*) to improve chilling stress

into spermidine or spermine conferred cold tolerance

O2

reduced chilling injury

, leading to

**with NO**

**References**

+ Song et al. [109]

+ Guo et al. [123]

+ Diao et al. [121]

+ Li et al. [124]

+ Aydin and

+ Liu et al. [129]

Nalbantoğlu [128]

ABA responses such induction of stomatal closure [16], activation of antioxidant enzymes [17], and up-regulation of transcription factors [18]. In addition, cGMP and type 2C protein

) under adverse environmental conditions triggers NO-mediated

Drought stress influences the signaling of various JA-associated genes [36]. JA stimulates CDPK production by increasing Ca2+ influx and the resultant signal cascade results in ABAregulated stomatal closure. A rapid loss in turgor and subsequent reduction in stomatal aperture were noted in excised *Arabidopsis* leaves treated with either ABA or methyl JA (MeJA) [37]. Suppression of MeJA-induced Ca2+ oscillations in guard cells of ABA-deficient mutants [38] implies that MeJA cross talk with ABA involves Ca2+ signal transduction pathways. Moreover, treatment with ABA or MeJA induces the formation of NO and ROS in guard cells [37]. Studies involving *Arabidopsis* revealed that ABA mediated Ca2+ influx into cytoplasm involves CPK6, which acts downstream of NO and ROS signaling and therefore may be a target of NO-stimulated Ca2+ influx into the cytoplasm [39]. In 2008, Palmieri et al. demonstrated that NO treatment up-regulated several genes involved in the JA biosynthetic pathway, indicating a potential regulation of JA signaling through the ROS/NO pathway [40]. NO also acts downstream of SA signaling to scavenge ROS in water-stressed plants. Coordinated action of NO and SA was found to alleviate the damaging effects of polyethylene (PEG)-induced osmotic stress in *Triticum aestivum* seedlings [41].

A positive interaction between NO and CK under water-limited environment was reported by Shao et al. [42]. 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 *Zea mays* [42]. Contrasting reports indicate antagonistic interaction between NO and CK, for example, CK-induced reduction in NO levels promoted stomatal opening in dark grown *Vicia fabia* seedlings [43]. Presumably, CKs activate plasma membrane H1-ATPase through decreasing NO levels in guard cells, and then stimulate stomatal opening in darkness. Wilhelmova et al. [44] reported similar results in transgenic tobacco plants. Negative interaction between NO and CKs was evident during leaf development as increased NO production reduced CKs level in aging leaves. Evidence suggests that reaction of zeatin with peroxynitrite, a NO derivative, reduces its availability in plants [45].
