Hydrogen Peroxide Signaling in Plant Development and Abiotic Responses: Crosstalk with Nitric Oxide and Calcium

Hydrogen peroxide (H₂O₂), as a reactive oxygen species, is widely generated in many biological systems. It has been considered as an important signaling molecule that mediates various physiological and biochemical processes in plants. Normal metabolism in plant cells results in H₂O₂ generation, from a variety of sources. Also, it is now clear that nitric oxide (NO) and calcium (Ca²⁺) function as signaling molecules in plants. Both H₂O₂ and NO are involved in plant development and abiotic responses. A wide range of evidences suggest that NO could be generated under similar stress conditions and with similar kinetics as H₂O₂. The interplay between H₂O₂ and NO has important functional implications to modulate transduction processes in plants. Moreover, close interaction also exists between H₂O₂ and Ca²⁺ in response to development and abiotic stresses in plants. Cellular responses to H₂O₂ and Ca²⁺ signaling systems are complex. There is quite a bit of interaction between H₂O₂ and Ca²⁺ signaling in responses to several stimuli. This review aims to introduce these evidences in our understanding of the crosstalk among H₂O₂, NO, and Ca²⁺ signaling which regulates plant growth and development, and other cellular and physiological responses to abiotic stresses.

Introduction

Hydrogen peroxide (H₂O₂), a form of reactive oxygen species, is regarded as a common cellular metabolite. H₂O₂ is continually synthesized through various sources including enzyme and non-enzyme pathways in plants. To date, it has become accepted that H₂O₂ plays important roles in plant developmental and physiological processes including seed germination (Barba-Espín et al., 2011), programmed cell death (PCD; Cheng et al., 2015; Vavilala et al., 2015), senescence (Liao et al., 2012b), flowering (Liu et al., 2013), root system development (Liao et al., 2009; Ma et al., 2014; Hernández-Barrera et al., 2015), stomatal aperture regulation (Ge et al., 2015) and many others. It is now clear that H₂O₂ functions as a signaling molecule which may respond to various stimuli in plant cells. These results suggest that H₂O₂ may be involved in cellular signaling transduction pathways and gene expression modulations in plants.

Nitric oxide (NO), as a small signaling molecule, appears to be involved in plant developmental and physiological processes such as seed germination (Wang et al., 2015), ripening and senescence (Shi Y. et al., 2015) as well as stomatal closure (Shi K. et al., 2015) and pollen tube growth (Wang et al., 2009). Meanwhile, NO signaling may have a vital role in the disease resistance (Kovacs et al., 2015) and response to abiotic stresses such as cold (Fan et al., 2015), salt (Liu W. et al., 2015) and drought (Shan et al., 2015). Calcium ion (Ca²⁺) signaling is also a core regulator of plant physiological process and stress adaption such as cell polarity regulation (Zhou et al., 2014), leaf de-etiolation (Huang et al., 2012), stomatal closure (Zou et al., 2015). Additionally, Ca²⁺ signaling is also involved in various responses to abiotic stimuli, including light (Hu et al., 2015) and heavy metal (Li et al., 2016).

A large amount of research show that H₂O₂, NO and Ca²⁺ as signaling are involved in plant growth and development as well as response to abiotic stresses. In this review, we focus on H₂O₂ signaling activities and its cross-talk with Ca²⁺ and NO in plants.

H₂O₂ Homeostasis

H₂O₂ Generation

H₂O₂ is a byproduct of aerobic metabolism in plants (Mittler, 2002). Figure 1 shows that H₂O₂ in plants can be synthesized either enzymatically or non-enzymatically. There are numerous routes of H₂O₂ production in plant cells, such as photorespiration, electron transport chains (ETC), and redox reaction.

FIGURE 1

Figure 1. The various routes of hydrogen perioxide (H₂O₂) production and H₂O₂ removal in plant cells. Enzymatic production of H₂O₂ in plants requires several enzymes including cell wall peroxidases (Francoz et al., 2015), oxalate (Hu et al., 2003), amine oxidases and flavin-containing enzymes (Cona et al., 2006), glucose oxidases, glycolate oxidases (Chang and Tang, 2014), and sulfite oxidases (Brychkova et al., 2012). In these enzymes, some of them may convert O${}_2^{-}$ to H₂O₂ and O₂. And others may oxidize their each substrates to generate H₂O₂in biocatalysis processes. Several non-enzymatic reactions are also known to produce H₂O₂. In peroxisome, H₂O₂ synthesis is associated with glycolate oxidation during photosynthetic carbon oxidation cycle (Foyer and Noctor, 2003). In chloroplasts, H₂O₂ production can be produced by the reduction of O${}_2^{-}$ by photosynthetic electron transport (PET) chain. H₂O₂ in chloroplast also may be detected at the manganese-containing, oxygen evolving complex which is the donor site of photosystem II. Moreover, H₂O₂ could be generated in mitochondria through aerobic respiration because O${}_2^{-}$ is produced from complexes I and III in the electron transport chain. H₂O₂-scavenging enzymes include catalase (CAT; Willekens et al., 1997), peroxidase (POX; Fan and Huang, 2012), ascorbate peroxidase (APX) and glutathione reductase (GR; Jahan and Anis, 2014). In non-enzymatic pathway, Ascorbate (AsA) and glutathione (GSH) are responsible for decreasing H₂O₂ level (Kapoor et al., 2015).

There is evidence for H₂O₂ production in plants through several enzymes includingcell wall peroxidases (Francoz et al., 2015), oxalate (Hu et al., 2003), amine oxidases and flavin-containing enzymes (Cona et al., 2006; Figure 1). Moreover, nicotinamide adenine dinucleotide phosphate (NADPH) oxidases may also increase H₂O₂ level through generating superoxide which could be converted to H₂O₂ by superoxide dismutases (SOD; Grivennikova and Vinogradov, 2013; Brewer et al., 2015). Remans et al. (2010) observed that ROS accumulation, especially H₂O₂ formation, is mostly related with the stimulation of NADPH oxidase in plants under heavy metal stresses. Moreover, H₂O₂ produced by NADPH oxidases may significantly increase proline accumulation in Arabidopsis thaliana under salt or mannitol stress (Ben Rejeb et al., 2015). Additionally, some other oxidases such as glucose oxidases, glycolate oxidases (Chang and Tang, 2014), and sulfite oxidases (Brychkova et al., 2012) may oxidize their own substrates to produce H₂O₂ (Figure 1).

Several non-enzymatic reactions are also known to produce H₂O₂. For example, many reactions involved in photosynthesis and respiration are responsible for H₂O₂ production. It is generated continually via electron transport reactions both in mitochondria and chloroplasts (Figure 1).

Peroxisomes

Peroxisome is considered to be the site of photorespiration in plant cell, which needs light-dependent uptake of O₂ and releases CO₂ accompanying with the generation of H₂O₂. It is suggested that H₂O₂ synthesis is associated with the oxidation of glycolate during the photosynthetic carbon oxidation cycle (Foyer and Noctor, 2003; Figure 1).

Chloroplasts

Chloroplast is the source of photosynthesis in plants. Chloroplasts are the crucial sites for H₂O₂ production during photosynthesis. H₂O₂ generation is associated with oxygen reduction in chloroplast (Figure 1). Mehler (1951) discovered that reduction of O₂ lead to the formation of H₂O₂ in the presence of light in chloroplast. Moreover, H₂O₂ production can also be produced by the reduction of O${}_2^{\stackrel{°}{-}}$ by photosynthetic electron transport (PET) chain components such as Fe–S centers, reduced thioredoxin (TRX), ferredoxin and reduced plastoquinone in the chloroplast (Dat et al., 2000). In addition, non-enzymatic production of H₂O₂ in chloroplast may be detected at the manganese-containing, oxygen evolving complex which is the donor site of photosystem II (Figure 1). But this process, in most cases, may probably be ignored under physiological conditions.

Mitochondria

One important source of endogenously produced H₂O₂ in plant cell is mitochondria (Dickinson and Chang, 2011). H₂O₂ is generated in mitochondria during aerobic respiration when O${}_2^{-}$ is produced from complexes I and III in the electron transport chain, which is then rapidly converted to H₂O₂ by the enzyme superoxide dismutase (Figure 1).

H₂O₂ Removal

The antioxidant systems that regulate H₂O₂ levels consist of both non-enzymatic and enzymatic H₂O₂ scavengers (Figure 1). H₂O₂-scavenging enzymes include catalase (CAT; Willekens et al., 1997), peroxidase (POX; Fan and Huang, 2012), ascorbate peroxidase (APX) and glutathione reductase (GR; Jahan and Anis, 2014). Some studies revealed that APX was found in the cytosol (Begara-Morales et al., 2013), chloroplasts (Asada, 2006), and mitochondria (Navrot et al., 2007). Meanwhile, CAT can decompose H₂O₂ in peroxisome (Nyathi and Baker, 2006). It is quite clear that these enzymes exist in different organelles and they might decrease H₂O₂ content efficiently and maintain the stability of membranes.

Ascorbate (AsA) and glutathione (GSH), as non-enzymatic compounds, are constantly participated in regulating ROS level (Kapoor et al., 2015). AsA, a key antioxidant for elimination of H₂O₂, can react with H₂O₂ directly. GSH is a crucial antioxidant which may be associated with regenerating AsA, and rapidly oxidizes excess H₂O₂. Therefore, GSH is also involved in regulating H₂O₂ level and redox balance in plant cells (Krifka et al., 2012). In fact, H₂O₂ homeostasis seems to result in some biological effects on plant cells which may be as a signaling sign in signaling transduction pathway.

Responses to H₂O₂

Growth and Development

Table 1 shows that H₂O₂ mediates various developmental and physiological processes in plants. These findings indicate that H₂O₂ may affect different parts of plants by increasing endogenous H₂O₂ level or by regulating relative gene expression. Also, the change of H₂O₂ level may impact metabolic and antioxidant enzyme activity in favor of plant growth and development (Barba-Espín et al., 2011; Liu et al., 2013). However, the mechanisms that allow different H₂O₂ function in plants still require examination.

TABLE 1

Table 1. The developmental and physiological effects of H₂O₂ in plants.

Stress Condition

Recent studies have demonstrated that H₂O₂ is a key signaling molecule in the signaling pathway, which associated with abiotic stress response. A number of discussions showed that H₂O₂ could respond to abiotic stresses such as drought (Hameed and Iqbal, 2014; Ashraf et al., 2015), salinity (Sathiyaraj et al., 2014; Mohamed et al., 2015), cold (Orabi et al., 2015), high temperatures (Wang Y. et al., 2014; Wu et al., 2015), UV radiation (He et al., 2005), ozone (Oksanen et al., 2004), and heavy metal (Wen et al., 2013; Table 2). It is clear from these studies that H₂O₂ could enhance abiotic stress resistance through protecting organelle structure under abiotic stress conditions. For instance, H₂O₂ may protect chloroplast ultrastructure to preserve photosynthesis under abiotic stress. Similarly, to improve plant abiotic stress tolerance, H₂O₂ may modulate the expression of resistance genes and antioxidant enzyme activities during abiotic stress response.

TABLE 2

Table 2. Report on H₂O₂-mediated effect during stresses in plants.

H₂O₂ as a Signaling Molecule in Plant

Among ROS, H₂O₂ has comparatively long life span and small size, which permit it to traverse through cellular membranes to different cellular compartments. García-Mata and Lamattina (2013) found that H₂O₂ may move between cells through aquaporin channels for signaling transduction. Increasing evidences point out that H₂O₂ signaling may regulate various plant physiological processes. For example, H₂O₂ as signaling molecule may participate in nitrosative stress-triggered cell death in kimchi cabbage (Brassica rapa var. glabra Regel) seedlings (Kim et al., 2015). Also, Li et al. (2015) suggested that H₂O₂ is involved in signaling crosstalk between NO and hydrogen sulfide (H₂S) to induce thermotolerance in maize seedlings. Moreover, the interaction among H₂O₂, NO and Ca²⁺ could relieve copper stress in Ulva compressa (González et al., 2012). H₂O₂ signaling was also demonstrated to play a salient role in brassinosteroid-regulated stomatal movement (Shi C. et al., 2015). As stated above, H₂O₂ as an important signaling molecule may play a significant role at every stage of plant life and under various abiotic stress conditions. H₂O₂ signaling appears to crosstalk with many different signaling molecules such as hormones (Shi C. et al., 2015), protein kinase (González et al., 2012) and many other small signaling molecules (Li et al., 2015). H₂O₂ and these signaling molecules may influence each other through various positive and negative feedback loops. Thus, they co-regulate cell division and differentiation, antioxidant system as well as gene expression involved in plant development and defense.

Crosstalk Between H₂O₂ and No

NO is a diatomic free radical gas. Previous studies suggested that NO could take part in a wide range of physiological processes such as vasorelaxation, nervous system, defense against pathogens in animals (Mayer and Hemmens, 1998). In mammals, NO is synthesized via three different isoforms of NO synthase (NOS) including inducible NOS (iNOS; Nathan and Hibbs, 1991), endothelial NOS (eNOS) and neuronal NOS (nNOS; Förstermann et al., 1994). In plants, NO could be synthesized through enzymatic and non-enzymatic pathways (Figure 2). The enzymatic pathway includes nitrate reductase (NR; Rockel et al., 2002), nitric oxide-like (NOS-like) synthase (Guo et al., 2003), Nitrite-NO reductase (Ni-NOR; Stöhr et al., 2001) and xanthine oxidase (XOR; Corpas et al., 2004) pathways. The non-enzymatic generation of NO includes nitrification or de-nitrification processes (Skiba et al., 1993, Figure 2).

FIGURE 2

Figure 2. Summary of the main NO systhetic pathways and NO functions in plant growth, development and defense processes. NO may be synthesized by enzymatically and non-enzymatically pathways. In enzymatic pathway, nitrate reductase (NR; Rockel et al., 2002), Nitrite-NO reductase (Ni-NOR; Stöhr et al., 2001) and xanthine oxidase (XOR; Corpas et al., 2004) could convert NO${}_3^{-}$ and NO${}_2^{-}$ to NO. Meanwhile, because of NOS-like enzyme (Guo et al., 2003), L-Arginine may be catalyzed to NO. In non-enzymatic pathway, N${}_2^{-}$ could be transformed to NO through nitrification and denitrification (Skiba et al., 1993). NO plays an important signaling molecule in plant. It could regulate developmental and physiological processes such as seed germination (Wang et al., 2015), root development (Liao et al., 2011) and stomatal closure (Shi C. et al., 2015). Also, it may be involved in response to abiotic stresses such as cold (Fan et al., 2015), salt (Liu W. et al., 2015) and drought (Shan et al., 2015).

A plethora of evidences suggest that NO, as a versatile signaling molecule, is involved in regulating every aspect of plant growth and developmental processes such as seed germination (Fan et al., 2013; Wang et al., 2015), flowering (Liu W. W. et al., 2015), root growth and development (Liao et al., 2011; Wu et al., 2014; Xiang et al., 2015), ripening and senescence (Liao et al., 2013; Shi Y. et al., 2015). Meanwhile, as a physiological regulator, NO signaling is involved in mediating stomatal closure (Noelia et al., 2015; Shi K. et al., 2015; Chen et al., 2016), pollen tube growth (Wang et al., 2009). Also, NO plays an essential role in plant disease resistance (Rasul et al., 2012; Kovacs et al., 2015) and responses to various abiotic stresses such as cold (Fan et al., 2015), heat (Yu et al., 2015), salt (Liu W. et al., 2015), drought (Shan et al., 2015), UV-B (Esringu et al., 2015) and heavy metal (Alemayehu et al., 2015; Chen et al., 2015; Kaur et al., 2015). These studies have paved the way to understand the signaling roles of NO which may affect cell metabolism, cellular redox balance and gene expression in plants. The relative target receptor may receive signaling activated by various stimuli. As a result, NO may activate regulatory mechanism to promote developmental and physiological processes and regulate abiotic stress response in plants.

Interaction in Growth and Development

To date, the interaction between H₂O₂ and NO has been demonstrated clearly in plants. The signaling crosstalk between H₂O₂ and NO has been considered to be an essential factor to influence plant developmental and physiological processes such as leaf cell death (Lin et al., 2012), delay senescence (Iakimova and Woltering, 2015), root growth and development (Liao et al., 2010, 2011), stomatal closure (Huang et al., 2015; Shi K. et al., 2015), and pollen tube growth (Serrano et al., 2012). Table 3 shows the interaction of H₂O₂ and NO at different levels in a great number of developmental and physiological processes in plants. On the one side, H₂O₂ may act as a cofactor to promote endogenous NO synthesis. For example, Lin et al. (2012) implied that H₂O₂ may stimulate NO production through increasing NR activity in leaves of noe1 plants under high light. Shi C. et al. (2015) reported that Gα-activated H₂O₂ production may induce NO synthesis. The research found that NO could modulate stomatal closure in H₂O₂ mutants AtrbohF and AtrbohD AtrbohF and in the wild type treated with H₂O₂ scavenger and inhibitor. However, H₂O₂ did not close or reduce the stomatal closure in mutants Nia1-2 and Nia2-5 Nia1-2, and in the wild type treated c-PTIO or tungstate (Shi C. et al., 2015). These results clearly show that H₂O₂ might induce NO synthesis in stomatal closure. On the other side, NO may induce H₂O₂ generation in plants. Liao et al. (2011) reported cPTIO or L-NAME could inhibit the endogenous H₂O₂ generation implying that NO was required for the production of H₂O₂ during adventitious rooting. Meanwhile, NO could mediate antioxidant enzyme activities to influence the H₂O₂ level (Zhang et al., 2007). Thus, the interaction of H₂O₂ and NO may trigger a serious of physiological and biological response in plant cells.

TABLE 3

Table 3. The developmental and physiological effects of crosstalk between H₂O₂ and NO in plants.

Interaction during Abiotic Stress

Recently, the roles of H₂O₂and NO signaling and their crosstalk in mediating plant response to abiotic stresses have been largely established (Table 4).

TABLE 4

Table 4. Reports on interaction between H₂O₂ and NO involved in abiotic stresses in plants.

Drought

Drought stress is a major environmental factor that affects plant growth and development. As reported by Liao et al. (2012a), both H₂O₂ and NO could protect mesophyll cells ultrastructure and improve the photosynthetic level of leaves under drought stress during adventitious rooting in marigold explants. Similarly, the interplay between H₂O₂ and NO signaling may increase the activity of myo-inositol phosphate synthase to alleviate drought stress (Tan et al., 2013). Additionally, Lu et al. (2009) suggested that endogenous NO and H₂O₂ may be involved in ABA-induced drought tolerance of bermudagrass by increasing antioxidant enzyme activities. NO may be considered to be upstream or downstream signaling molecule of H₂O₂ (Lu et al., 2009; Liao et al., 2012a). Thus, the interaction between H₂O₂ and NO may alleviate drought stress through up-regulating antioxidant defense system to protect cell membrane and maintain ion homeostasis in plants.

Salt

The interaction between H₂O₂ and NO plays an important role in plant tolerance to salt stress (Zhang et al., 2007; Tan et al., 2013). Tanou et al. (2009) suggested that H₂O₂ and NO pre-treatments could alleviate salinity-induced protein carbonylation in citrus. The authors suggested an interaction between H₂O₂ and NO during salt stress response. Furthermore, H₂O₂- and NO-responsive proteins have been identified which may further reveal a protein interaction network between H₂O₂ and NO signaling under salt stress (Tanou et al., 2010).

UV-B

UV-B, a key environmental signal, initiates diverse responses in plants (Jansen and Bornman, 2012). UV-B radiation can also influence plant growth, development, and productivity. It has been shown that the crosstalk between H₂O₂ and NO could be involved in the response to UV-B stress. There was an interrelationship among Gα protein, H₂O₂, and NO during UV-B-induced stomatal closure in Arabidopsis leaves (He et al., 2013). This study found that there was a significant increase in H₂O₂ or NO levels which associated with stomatal closure in the wild type by UV-B stress. However, these effects were abolished by double mutants of AtrbohD and AtrbohF or Nia1 mutants. These results strongly suggested that the crosstalk between H₂O₂ and NO signaling might play an essential role during UV-B-induced stomatal closure in guard cells. Recently, Tossi et al. (2014) also showed a mechanism involving both H₂O₂ and NO generation in response to UV-B exposure. Therefore, the crosstalk between H₂O₂ and NO can regulate stomatal movement to reduce UV-B stress damage to plant cells.

Cold

Cold stress adversely influences plant growth and development. Guo et al. (2014) reported that the interaction of H₂O₂ and NO may affect cold-induced S-adenosylmethionine synthetase and increase cold tolerance through up-regulating polyamine oxidation in Medicago sativa subsp. falcate. Moreover, signaling interplay of H₂O₂ and NO was essential for cold-induced gene expression of falcata myo-inositol phosphate synthase (MfMIPS), which improved tolerance to cold stress (Tan et al., 2013). Thus, the interaction between H₂O₂ and NO may initiate different mechanisms to response to cold stresses.

Heat

Recently, many studies have been conducted to investigate the relationship between H₂O₂ and NO under heat stress. Li et al. (2015) reported that a signaling crosstalk between H₂O₂ and NO may be involved in inducing thermotolerance in maize seedlings. Moreover, H₂O₂ may be upstream signaling of NO in the heat shock pathway in Arabidopsis seedlings (Wang L. et al., 2014). In addition, treatment with low level of H₂O₂ or NO could increase seedling viability under heat resistance (Karpets et al., 2015). These studies support the existence of crosstalk between H₂O₂ and NO in heat responses in plants.

Heavy Metal Stress

Alberto et al. (2012) suggested that the signaling interaction between H₂O₂ and NO was involved in alleviating copper stress of Ulva compressa through mediating antioxidant enzyme activities and activating relative gene expression. Besides, the interplay of NO and H₂O₂ in wheat seedlings participated in regulating root growth under zinc stress and alleviated zinc stress through increasing antioxidant system, decreasing lipid peroxidation as well as up-regulating resistance gene expression (Duan et al., 2015). Obviously, the crosstalk of H₂O₂ and NO has been found under heavy metal stress condition, which may trigger a variety of antioxidant responses in plants.

As stated above, the physiological effect of H₂O₂ and NO is similar and synergetic. In different cases, these forms of interaction are various. However, the form of H₂O₂ and NO crosstalk depend on plant species and environmental stresses. H₂O₂ and NO could modulate each other through regulating antioxidant enzymes activities and relative gene expression in plants. Meanwhile, H₂O₂ and NO may synergistically regulate many common target genes which were related to signaling transduction, defense reaction, plant hormone interactions, protein transport and metabolism. Therefore, it has a significant meaning to elaborate the mechanism of the interaction between H₂O₂ and NO in plant developmental processes and response to abiotic stresses.

Crosstalk Between H₂O₂ and Ca²⁺

Ca²⁺ is a widespread signaling molecule in plants. When plants receive stimuli, the change of intracellular Ca²⁺ concentration may transfer signaling to regulate a series of cellular processes in plants (Kong et al., 2015; Tang et al., 2015). There are various types of Ca²⁺ receptors and channels in plants such as Ca²⁺-ATPases (Pászty et al., 2015), Ca²⁺-binding sensor protein (Wagner et al., 2015), inositol-1,4,5-trisphosphate (IP₃; Serrano et al., 2015) and cyclic ADP-ribose (cADPR, Gerasimenko et al., 2015). It is well known that Ca²⁺ is involved in plant growth and development such as seed germination (Kong et al., 2015), pollen tube growth (Zhou et al., 2014), leaf de-etiolation (Huang et al., 2012), root growth and development (Liao et al., 2012a; Han et al., 2015) and other physiological processes including cell polarity regulation (Zhou et al., 2014; Himschoot et al., 2015), stomatal closure (Zou et al., 2015) and immune response (Seybold et al., 2014). Furthermore, variations in cytosolic free Ca²⁺ concentration have been demonstrated to response to a wide range of environmental stresses such as heat shock (Urao et al., 1994), drought (Zou et al., 2015), light (Hu et al., 2015), salt (Tepe and Aydemir, 2015), and heavy metal (Li et al., 2016). Because of Ca²⁺ has various receptors and channels in plants, it may receive different upstream signaling molecules quickly and then respond to abiotic stress.

Interaction in Growth and Development

Crosstalk between H₂O₂ and Ca²⁺ occurs in plant cells (Table 5). For example, exogenous H₂O₂ caused transiently dose-dependent increase in Ca²⁺ influx in Arabidopsis thaliana root epidermis (Demidchik et al., 2007). Two Ca²⁺ channels could be regulated by H₂O₂ level in root elongation zone. Han et al. (2015) demonstrated that H₂O₂ signaling could induce root elongation by mediating Ca²⁺ influx in the plasma membrane of root cells in Arabidopsis seedlings. Richards et al. (2014) also suggested that Annexin 1, a Ca²⁺ transport protein, may regulate H₂O₂-induced Ca²⁺ signature in Arabidopsis thaliana roots to promote root growth and development. Additionally, Ca²⁺ signaling was involved in H₂O₂-induced adventitious rooting in marigold because removal of Ca²⁺ could inhibit H₂O₂-induced adventitious root development (Liao et al., 2012a). Interestingly, Wu et al. (2010)'s findings strongly suggested that spermidine oxidase (Spd)-derived H₂O₂ signaling may mediate Ca²⁺ influx. Spd was probably related to downstream induction of H₂O₂ signaling and then H₂O₂ activated Ca²⁺-permeable channels during pollen tube growth (Wu et al., 2010). Cross talk between Ca²⁺–Calmodulin (CaM) and H₂O₂ also played a significant role in antioxidant defense in ABA signaling in maize leaves (Hu et al., 2007; Table 5). Thus, the signaling crosstalk between H₂O₂ and Ca²⁺ may affect every stage of plant development by modulating cell elongation and division, antioxidant enzyme activity and gene expression. H₂O₂ may activate Ca²⁺ receptors and target proteins to increase [Ca²⁺]_cyt level and Ca²⁺ may induce endogenous H₂O₂ generation during plant growth and development.

TABLE 5

Table 5. The developmental and physiological effects of crosstalk between H₂O₂ and Ca²⁺ in plants.

Interaction in Abiotic Stress

Clearly, correlations also exist between H₂O₂ and Ca²⁺ in response to abiotic stresses in plants (Table 6). Shoresh et al. (2011) investigated that supplemental Ca²⁺ had a significant effect on H₂O₂ metabolism and regulating leaves and roots growth in maize under salt stress. The authors indicated that extracellular Ca²⁺ may modulate endogenous H₂O₂ levels through activating polyamine oxidase activity. Also, salt stress may induce H₂O₂ accumulation in Ca²⁺-dependent salt resistance pathway in Arabidopsis thaliana roots (Li et al., 2011). Moreover, Lu et al. (2013) suggested that exogenous H₂O₂ and Ca²⁺ may mediate root ion fluxes in mangrove species under NaCl stress. Obviously, H₂O₂ may interact with Ca²⁺ under salt stress in plants through mediating root ion balance, increasing antioxidant enzymatic activity and up-regulating the expression of related genes. Moreover, H₂O₂ and Ca²⁺ signaling were also involved in ABA responses to drought stress in Arabidopsis thaliana through Ca²⁺-dependent protein kinase8 (CPK8) which could regulate catalase3 (CAT3) activity mediating stomatal movement (Zou et al., 2015). In addition, Qiao et al. (2015) reported that a Ca²⁺-binding protein (rice annexin OsANN1) could enhance heat stress tolerance by modulating H₂O₂ production. Over production of H₂O₂ induced by heat stress increased OsANN1 expression and up-regulated the level of SOD and CAT expression, which constructed a signaling mechanism for stress defense in plants (Qiao et al., 2015). Until now, the signaling crosstalk between H₂O₂ and Ca²⁺ may regulate various responses to abiotic stresses in plants. It may be connected with the regulation of antioxidant system. Thus, the interaction between H₂O₂ and Ca²⁺ may increase antioxidant enzyme activities such as APX, SOD, and GR. These antioxidant enzymes may alleviate stress damages in plants. In addition, the crosstalk between H₂O₂ and Ca²⁺ could regulate gene expression level and induce protein interactions.

TABLE 6

Table 6. Reports on interaction between H₂O₂ and Ca²⁺ involved in abiotic stresses in plants.

It appears that the interrelationship between H₂O₂ and Ca²⁺ may be involved in various aspects of plant growth and development processes and abiotic stress responses. In fact, the change of Ca²⁺ concentration is closely related to H₂O₂ burst in plant cells. The combination of H₂O₂ and Ca²⁺ may play crucial roles in plants. Different plants even different parts of the same plant may have different modulation mechanisms. Thus, relationship between H₂O₂ and Ca²⁺ signaling in plants is very complex. The interplay of H₂O₂, Ca²⁺ and its mechanism need to be illustrated clearly in the future.

Crosstalk Among H₂O₂, No and Ca²⁺

It has been suggested that there is a connection among H₂O₂, NO, and Ca²⁺ in plants. H₂O₂, NO, and Ca²⁺ may act as essential signaling molecules which may form a complex signaling network to regulate different developmental and physiological processes in plants (Figure 3). For instance, during adventitious rooting of mung bean, Ca²⁺ signaling played a pivotal role and functioned as a downstream molecule of H₂O₂ and NO signal pathway (Li and Xue, 2010; Figure 3). Similarly, there is a possible relationship among H₂O_2,NO and Ca²⁺/CaM during adventitious rooting in marigold explants (Liao et al., 2012a). The authors found that exogenous NO and H₂O₂ promoted adventitious root development in marigold explants through increasing endogenous Ca²⁺ and CaM levels. Moreover, H₂O₂, NO and Ca²⁺ were also involved in oligochitosan-induced programmed cell death in tobacco suspension cells (Zhang et al., 2012). Pharmacological experiments revealed that Ca²⁺ signaling induced NO accumulation through inducing H₂O₂ generation during stomatal closure in Arabidopsis guard cells (Li et al., 2009). Furthermore, Wang et al. (2011) suggested a functional correlationship among H₂O₂, calcium-sensing receptor (CAS) and NO in Ca²⁺-dependent guard cell signaling. It was shown that CAS may transduce Ca²⁺ signaling through activating its downstream target NO and H₂O₂ signaling pathway (Wang et al., 2011). Therefore, it is thus clear that the interplay of H₂O₂, NO, and Ca²⁺ may have an significant effect on plant growth and physiological processes through promoting cell proliferation, controlling cell metabolism, meanwhile, regulating modes of cell death. Moreover, Vandelle et al. (2006) has reported that NO and H₂O₂ synthesis could also act upstream to increase cytosolic Ca²⁺ concentration during hypersensitive response (HR) through activating plasma membrane- and intracellular membrane-associated Ca²⁺ channels. Besides, the interaction among H₂O₂, NO, and Ca²⁺ signaling may regulate ABA-induced antioxidant defense in maize (Ma et al., 2012). Obviously, the mutual effect among H₂O₂, NO and Ca²⁺ may increase antioxidant system and induce disease defense in plants.

FIGURE 3

Figure 3. Schematic model of the interaction among H₂O₂, NO, Ca²⁺ in different plant physiological and defense processes. H₂O₂, NO and Ca²⁺ may receive various stimuli through signaling sensors. They might interact via cross-regulation and transduce signaling to downstream molecules by activating phosphokinase like MAPKs, or relative enzyme activity in order to regulate plant development and growth and abiotic stress responses.

Furthermore, the interplay among H₂O₂, NO, and Ca²⁺ also have an effect on abiotic stress response in plants. For example, Lang et al. (2014) reported that NO likely interacted with Ca²⁺ and H₂O₂ in Aegiceras corniculatum to up-regulate Na⁺/H⁺ antiport system of plasma membrane under salt stress. There were species-specific interactions between H₂O₂, Ca²⁺, NO, and ATP in salt-induced reduction of K⁺ efflux (Lang et al., 2014). Moreover, there was a crosstalk among H₂O₂, NO, and Ca²⁺ when Ulva compressa exposed to copper excess and the interaction had a significant effect on transcriptional activation of target genes (Alberto et al., 2012). The H₂O₂-induced NO generation could be inhibited by Ca²⁺ channel blockers, implicating that Ca²⁺ may mediate the effect of H₂O₂ on NO production. Furthermore, Ca²⁺ release through different type of Ca²⁺ channels was also shown to be activated by NO and H₂O₂ (Alberto et al., 2012; Figure 3). The interrelationship between H₂O₂, NO and Ca²⁺ may provide additional layers of responses to abiotic stresses through controlling ion transport, increasing antioxidant enzyme activities and affecting expression of resistance genes, indicating a feedback mechanism between H₂O₂, NO and Ca²⁺ under abiotic stresses. In a word, the combination of these findings strongly supports the view that there has an interaction among H₂O₂, NO, and Ca²⁺ signaling pathway in plant growth, development and abiotic stress responses. During signaling transduction, Ca²⁺ signaling could be activated by H₂O₂ and NO; it could also regulate H₂O₂ and NO signaling. Ca²⁺ may act as a point of signaling convergence between H₂O₂ and NO signaling pathways in plants. However, the network of H₂O₂, NO, and Ca²⁺ seems to be intricate and multidimensional. Therefore, considerably more work will need to be done to determine the interaction among H₂O₂, NO and Ca²⁺ signaling in plants.

Conclusion

H₂O₂ was once considered as a poisonous molecule in plants. Based on current studies, H₂O₂ may be a vital signaling molecule which controls plant growth and development. Interestingly, NO and Ca²⁺ which also act as the key component of signaling transduction in plants seem to be as upstream or downstream signaling molecules of H₂O₂. Meanwhile, H₂O₂ modulates NO and Ca²⁺ signaling pathways. There is a complex interactive network among H₂O₂, NO, and Ca²⁺ in plants. Moreover, the interplay among them has functional implications for regulating developmental and physiological processes which may increase the possibility of signal reception and transduction in plants. Future work will need to focus on the molecular mechanism of the interplay among H₂O₂, NO, and Ca²⁺ during signaling transduction in plants.

Author Contributions

LN wrote the paper. WL provided the idea and revised the paper.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This research was supported by the National Natural Science Foundation of China (Nos. 31160398 and 31560563), the Post Doctoral Foundation of China (Nos. 20100470887 and 2012T50828), the Key Project of Chinese Ministry of Education (No. 211182), the Research Fund for the Doctoral Program of Higher Education (No. 20116202120005), the Natural Science Foundation of Gansu References Province, China (Nos. 1308RJZA179 and 1308RJZA262), and the Fundamental Research Funds for Universities in Gansu, P. R. China.

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