Nitric Oxide 42 (2014) 40–43
Contents lists available at ScienceDirect
Nitric Oxide j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y n i o x
Review
The role of carbon monoxide signaling in the responses of plants to abiotic stresses Huyi He a,b,*, Longfei He a a b
College of Agronomy, Guangxi University, Nanning 530004, China Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China
A R T I C L E
I N F O
Article history: Received 27 May 2014 Revised 26 August 2014 Available online 29 August 2014 Keywords: Abiotic stress Carbon monoxide Nitric oxide H2O2 Oxidative damage Reactive oxygen species Signal transduction
A B S T R A C T
Whether carbon monoxide (CO) exerts toxic or protective effect is dependent on the concentration and location of CO in animals. Similarly, it has been increasingly evident that CO also is involved in diverse physiological processes in plants, from seed germination and dormancy to stomatal closure to regulation of multiple environmental stresses. In this review, we focus on CO synthesis and the role of CO in plant responses to abiotic stresses, such as salinity, drought, cadmium and mercury. In general, abiotic stresses induce CO production in plants. CO can alleviate oxidative damage by improving the activities of antioxidative enzymes and antioxidant metabolism. In addition, cross talk between CO signaling and other signaling molecules including nitric oxide (NO) and hydrogen peroxide (H2O2) also is discussed. © 2014 Published by Elsevier Inc.
Contents 1. 2. 3. 4. 5.
Introduction ........................................................................................................................................................................................................................................................... Synthesis of CO in plants .................................................................................................................................................................................................................................. Role of CO in abiotic stresses .......................................................................................................................................................................................................................... Cross talk between CO signaling and other signaling molecules ....................................................................................................................................................... Conclusions and perspectives ......................................................................................................................................................................................................................... Source of funding ................................................................................................................................................................................................................................................ References ..............................................................................................................................................................................................................................................................
1. Introduction Carbon monoxide (CO) is the most common cause of fatal poisoning in the world. Although the acute exposure to CO gas via the incomplete combustion of domestic gas has been well known for a long time, chronic exposure also occurs by means of cigarette smoking. In animals, endogenous CO production and heme oxygenase (HO EC 1.14.99.3) induction are stimulated by different stress responses, including heat shock, oxidants, metals, lipopolysaccharides, hypoxia, hyperoxia and reactive oxygen species (ROS) [1–3]. Similarly, CO plays a major role in a number of physiological processes
* Corresponding author. Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, No. 174 Daxue East Road, Nanning 530007, China. Fax: +86 771 3244229. E-mail address: [email protected] (H. He). http://dx.doi.org/10.1016/j.niox.2014.08.011 1089-8603/© 2014 Published by Elsevier Inc.
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such as growth and developmental regulation, stomatal closure, and adaptation responses to environmental stresses in plants [4–10]. As an important positive regulator, CO also is involved in seed germination and dormancy breaking [11,12], and adventitious rooting [10,13]. Low concentration of CO can stimulate seed germination and dormancy [11]. Exogenous CO induces adventitious rooting of hypocotyl cuttings (primary roots removed) from mung bean (Vigna radiata) seedlings [13]. CO produced by HO might mediate the induction of growth elongation of wheat root segments by IAA [14]. Basipetal transport of auxin induces a CO burst synthesized by HO in the basal region of hypocotyls, thus leading to adventitious root formation. This pathway might be mediated by the expression of DnaJ-1 and calcium-dependent protein kinase (CDPK) genes [10]. Abiotic stresses are major constraint to agricultural productivity in the world. The harm of abiotic stresses includes the disruption of cellular redox homeostasis, ROS production and oxidative stress. Plants have evolved tolerance mechanisms in responses to
H. He, L. He/Nitric Oxide 42 (2014) 40–43
41
Table 1 Reports on CO-mediated effects during abiotic stresses in plants. Plant species
Tissue
Abiotic stress
CO production
CO-mediated effect
CO-regulated gene
Reference
Triticum aestivum
Root
Salt
+
Seed
Salt
+
APX, DHAR, Mn-SOD, Cu/Zn-SOD, H+-ATPase α-amylase, CAT, Cu/Zn-SOD, HO-1
[9]
Oryza sativa
Maintain ion homeostasis/enhance antioxidant system Alleviate oxidative damage
Triticum aestivum Triticum aestivum Glycine max
Leaf Seed Root nodule Root
Salt Salt Salt
+ + +
Alleviate oxidative stress Alleviate oxidative stress Protect nitrogen metabolism
– HO-1, GS, GOAT
Salt
+
Osmotic Cd Cd Hg Hg Hg
+ + + + + +
Mn-SOD, Cu/Zn-SOD, NADPH oxidase HO-1 HO-1 HO-1 HO-1, APX, GPX Cu-Zn SOD, CAT, POD HO-1, PCS1
[26]
Seed Root Root Root Root Root, shoot, leaf Leaf Root, shoot, leaf
Inhibit superoxide anion overproduction – Alleviate oxidative damage Enhance antioxidative capability Alleviate oxidative damage Prevent oxidative stress Attenuate oxidative injury
UV-B –Fe
+ +
Prevent oxidative stress Regulate iron homeostasis
HO-1, CAT, APX IRT1, FRO2, FIT1, FER1
[31] [32]
Triticum aestivum Triticum aestivum Medicago sativa Medicago sativa Medicago sativa Brassica juncea Brassica napus Glycine max Arabidopsis
alteration of environmental conditions. CO is able to strongly protect plants against oxidative damage caused by the overproduction of reactive oxygen species (ROS), suggesting that CO is a potent antioxidant in various abiotic and biotic stresses [15]. In this review, we focus on synthesis of CO and its role in plant responses to abiotic stresses such as salinity, drought, cadmium (Cd), mercury (Hg), iron deficiency, and ultraviolet-B (UV-B) radiation. Moreover, crosstalk between molecules signaling with CO and those signaling with other molecules such as nitric oxide (NO) and hydrogen peroxide (H2O2) is also discussed. 2. Synthesis of CO in plants CO is an odorless, tasteless, and colorless concomitant product of heme degradation catalyzed by HO [16]. To date three isozymes have been detected in mammals: the inducible isoform HO1, the constitutively expressed isozyme HO-2, and an isozyme with very low activity HO-3. Although the most investigated mechanism for CO production in animals involves HO, there are other ways in which CO can be generated [2] speculated that the action of CO in animals, including cytoprotection and cytotoxic effects, might be dependent on its concentration and the different experimental materials applied. The presence of CO biosynthesis in plants was first reported by Wilks [17]. In addition to the photo-production of CO in living plants [18,19], there is a significant light-independent source of CO gas among smaller plants associated with the soil surface and soil–air interface [18,20]. It also has been shown that CO is released from haem proteins during the generation of ferrous iron (Fe2+) and biliverdin-IXα (BV-IXα), which can be reduced to bilirubin by biliverdin reductase. CO exhibits the ability to bind to the iron atom of the heme moiety associated with soluble guanylate cyclase (sGC), thereby activating the enzyme and increasing production of the intracellular second messenger molecule cGMP [21]. Although the GC activity and cGMP content have been detected in some plants recently, whether cGMP signaling system exits in plants still has no sufficient evidence to confirm. 3. Role of CO in abiotic stresses Almost all abiotic stresses generate free radicals and other oxidants, resulting in oxidative damage in terms of an increased level of ROS in plant cells [22]. CO is induced rapidly by salinity, drought,
[12] [23] [24] [25]
[27] [7] [28] [6] [29] [30]
Cd, Hg, iron deficiency, and UV-B in plants and regulates the plant responses to abiotic stresses (Table 1). CO has profound effects on intracellular signaling processes such as the maintenance of ROS homeostasis under oxidative stress [33,34]. CO plays a vital role in intracellular redox signaling and activation of antioxidant resistance mechanisms. Soil salinity limits crop productivity and quality by affecting several key metabolic processes such as osmotic and ionic homeostasis. Salinity alters the activities of many enzymes involved in nitrate and sulfate assimilation pathways in plants, lowers their energy status, and increases the demand for nitrogen and sulfur [35]. Exogenous application of low levels of CO donor hematin may be advantageous against salt-induced oxidative damage in wheat seedling leaves [23]. Low concentrations of CO can attenuate the inhibition of seed germination produced by salinity stress and counteract lipid peroxidation in germinating wheat seeds [24]. CO had an advantageous effect on attenuation of inhibition of seed germination and seedling growth induced by salt stress, and alleviated oxidative damage by activating anti-oxidant enzymes [12]. NaCl triggers a biphasic burst of CO production in wheat seedling roots, suggesting CO may be a key component responsible for salinity tolerance. CO might confer an increased tolerance to salinity stress by maintaining ion homeostasis and enhancing antioxidant system parameters in wheat seedling roots, both of which were partially mediated by NO signaling [9]. Up-regulation of HO, as part of an antioxidant defense system, could be protecting the soybean nodule nitrogen fixation and assimilation under saline stress conditions [25]. CO might be involved in plant tolerance against salinity stress, and its alleviation of programmed cell death (PCD) and inhibition of root growth were related to the decrease of superoxide anion overproduction partially via up-regulation of SOD and down-regulation of NADPH oxidase expression [26]. Drought is one of the major constraints to food production because it limits growth and development of plants. Drought or osmotic stress induces the accumulation of ROS in plants [22]. Hematin (a CO donor) pretreatment (≤0.1 μM) could delay wheat leaf chlorophyll loss mediated by further treatment of H2O2 and paraquat in a dose- and even time-dependent manner [15]. The polyethylene glycol-6000 (PEG)-induced inhibitory effect on seed germination was ameliorated by CO. The endogenous HO/CO signal system is required for the alleviation of osmotic stress-induced wheat seed germination inhibition and lipid peroxidation, which might have a possible interaction with NO [27].
42
H. He, L. He/Nitric Oxide 42 (2014) 40–43
Heavy metal toxicity resulting from contamination is known to affect the biosphere. And this leads to health hazards for animals and plants. Cd is a non-essential and toxic metal, rapidly taken up by roots and accumulated in various plant tissues, which hampers crop growth and productivity worldwide. Hematin can markedly boost the HO/CO system, which exhibits a vital role in protecting the plant against Hg-induced oxidative damage [6]. Exogenous Cd increased CO production. As a signal element, CO release alleviated Cd-induced oxidative damage by modulating glutathione (GSH) and ascorbic acid (AsA) homeostasis in the roots of alfalfa [7]. Cdinduced HO-1 gene expression is associated with depletion of GSH in the roots of Medicago sativa, leading to enhanced antioxidative capability transiently [28]. CO-mediated enhancement of Hg tolerance was closely related to the accumulation of proline and reduced non-protein thiols [29]. Overexpression of BnHO-1 resulted in less accumulation of Hg in some lines of transformants than in untransformants [30]. Deeper understanding of CO production and action helps to evaluate the effects and remedy of different concentrations of the same metal or the concentrations of different metals in plants. Due to the depletion of the stratospheric ozone layer, UV-B radiation (280–320 nm) has deleterious effects on plants, including decreased biomass formation, reduced photosynthesis and damaged DNA. UV-B perception increases O2− generation and NO production of plants. NO and H2O2 participate in the signaling required for HO-1 up-regulation, which mediates the enhancement in HO activity. CO is produced by HO-mediated heme catabolism [31]. CO can regulate iron-homeostasis in iron-starved Arabidopsis and exogenous CO can prevent iron deficiency-induced chlorosis and improve chlorophyll accumulation [32]. Like the case of mammals, it is very important to know the concentration range and production rate of CO under abiotic stress conditions in plants. However, plant cells are not surrounded by abundant heme proteins in the tissues. In terms of CO diffusion, plants physical inter-cellular environments are entirely different from that of animal tissues. In mammalian systems, the concentration and localization of CO production are clear. Contrasting with the mammalian systems, the concentration and localization of CO production in plants remain to be elucidated. 4. Cross talk between CO signaling and other signaling molecules CO and NO all bind to the heme of hemoglobins, thereby disturbing energy transduction systems including respiration. Also, CO might exert its biological effects by its synergism with NO (Fig. 1).
Abiotic stresses
Thom et al. [36] discovered that exposure of endothelial cells to low levels of CO (10–110 nmol/L) led to an increase in steady-state NO and NO-derived oxidants peroxynitrite, suggesting that competition from CO for intracellular NO-binding sites contributes to the elevation of the NO level. The rate of superoxide production is enhanced by slowing the terminal transfer rate of electrons to molecular O2 by CO binding at cytochrome c oxidase (and NO in some cases). NO reversibly inhibits the activities of tobacco catalase (CAT) and ascorbate peroxidase (APX) [37]. Because CO and NO are able to activate sGC, they share many properties and CO may serve as a neuronal messenger molecule similar to NO [38]. It is becoming increasingly clear that these two gases do not always work independently, but rather can modulate each other’s activity in animals [3,38]. NO donor SNP alleviates Cd-caused chlorophyll loss through argumentation of HO-1 transcript levels [39]. As shown in animals, CO induces LR formation probably mediated by the NO/ NOS pathway and NO may act downstream of CO signaling [5]. NO is required for CO-induced guard cell closure [4,8]. CO might mediate the induction of growth elongation of wheat (Triticum aestivum) root segments by IAA, which might be related to NO/cGMP-dependent pathways [10,14]. Wheat seedling roots treated daily with exogenous CO could synthesize NO, indicating that NO may be a part of the downstream signal molecule of CO action [9]. A balance between NO and ROS is essential in order to trigger the antioxidant response against oxidative stress [31]. Endogenous CO level was increased in Arabidopsis under iron-deficiency and CO exposure induced NO accumulation in root tips, indicating that CO may play an important role in improving plant adaptation to iron deficiency or cross-talking with NO [32]. In addition, CO could inhibit excessive NO generation and suppress the catalytic activity of cytochrome P450 monooxygenases, enzyme systems that account for endogenous generation of ROS. The increase in free iron induces the up-regulation of ferritin which in turn causes overall reduction of free iron and thereby attenuates oxidative susceptibility [40]. By application of H2O2 or AsA, heme methylene bridges can be broken and CO released [2]. CO protects endothelial cells from various stimuli-induced apoptosis by inhibiting ROS formation, and ROS modulated by CO can influence the activity of several transcription factors and kinases such as NF-kB and p38 [41,42]. CO likely activates p38 mitogen-activated protein kinase (MAPK) by generating oxidant [34]. ABA-induced H2O2 production activates a 46-kD MAPK, which in turn induces the expression and the activities of CAT, cAPX and GR1. The activation of MAPK also enhances the H2O2 production, forming a positive feedback loop [43]. CO aqueous solution induced CAT and superoxide dismutase (SOD) activities, resulting in the alleviation of oxidative damage [12]. CO and H2O2 exhibit a similar regulation role in the stomatal movement. CO-induced stomatal closure probably involves H2O2 signaling and CO is involved in darkness-induced HO synthesis in Vicia faba guard cells [44]. CO prevented GA-induced PCD by enhancing the activities or transcripts of CAT and APX [45].
NO 5. Conclusions and perspectives
CO
CAT/APX
H2O2
CAT/SOD
cGMP
MAPK Cascades
Plant responses Fig. 1. A model for carbon monoxide-mediated signaling in plant responses to abiotic stresses.
Preliminary advances in the knowledge of CO role in the regulation of plant growth and development, and tolerance of plants to environmental stresses have been achieved, but the current situation of CO research in plants is at an early stage. Due to the technological obstacle of CO detection, so far the biochemical and molecular details of precise CO biosynthetic pathway have not been fully understood. For example, it is not clear for nonenzymatic pathways and functions of CO in plants. At present, most studies of CO signaling are based on pharmacological methods as plant NO research. Although the effects of chemical donors and fluorescence probes may be subjected to technical limitations, there is no question about the involvement of CO in plant responses to abiotic
H. He, L. He/Nitric Oxide 42 (2014) 40–43
stresses. On the one hand, CO might protect plants against ROScaused oxidative damage by improving the activities of antioxidative enzymes and antioxidant metabolism. On the other hand, as a signaling molecule, CO plays important roles in responses to environmental stresses via cross talk with other hormones together. However, it is uncertain how these identified pathways interact with each other in plants. With the screening of relevant HO mutants and application of reverse genetics, proteomics, transcriptomes, and functional genomics, it will be revealed how CO metabolism is governed. Crop yield depends on the capacity of plants to tolerate increases in ROS. Application of chemical CO donors helps to improve crop productivity. The identification of CO targets and deeper understanding of CO signaling transduction will provide novel biochemical and physiological evidence on CO function in the responses of plants to abiotic stresses. Source of funding This study was funded by the National Natural Science Foundation of China (Nos. 30960181 and 31260296) and 2011 Guangxi Innovation Program for Graduates (GXU11T31076). References [1] C.A. Piantadosi, Biological chemistry of carbon monoxide, Antioxid. Redox Signal. 4 (2002) 259–270. [2] J. Dulak, A. Jozkowicz, Carbon monoxide: a “new” gaseous modulator of gene expression, Acta Biochim. Pol. 50 (2003) 31–47. [3] R.N. Watts, P. Ponka, D.R. Richardson, Effects of nitrogen monoxide and carbon monoxide on molecular and cellular iron metabolism: mirror-image effector molecules that target iron, Biochem. J. 369 (2003) 429–440. [4] Z.Y. Cao, B.K. Huang, Q.Y. Wang, W. Xuan, T.F. Ling, B. Zhang, et al., Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway, Chin. Sci. Bull. 52 (2007a) 2365–2373. [5] Z.Y. Cao, W. Xuan, Z.Y. Liu, X.N. Li, N. Zhao, P. Xu, et al., Carbon monoxide promotes lateral root formation in rapeseed, J. Integr. Plant Biol. 49 (2007b) 1070–1079. [6] Y. Han, W. Xuan, T. Yu, W.B. Fang, T.L. Lou, Y. Gao, et al., Exogenous hematin alleviates mercury-induced oxidative damage in the roots of Medicago sativa, J. Integr. Plant Biol. 49 (2007) 1703–1713. [7] Y. Han, J. Zhang, X. Chen, Z. Gao, W. Xuan, S. Xu, et al., Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa, New Phytol. 177 (2008) 155–166. [8] X.G. Song, X.P. She, B. Zhang, Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis, Physiol. Plant. 132 (2008) 514–525. [9] Y.J. Xie, T.F. Ling, Y. Han, K.L. Liu, Q.S. Zheng, L.Q. Huang, et al., Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots, Plant Cell Environ. 31 (2008) 1864–1881. [10] W. Xuan, F.Y. Zhu, S. Xu, B.K. Huang, T.F. Ling, J.F. Qi, et al., The heme oxygenase/ carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process, Plant Physiol. 148 (2008) 881–893. [11] J. Dekker, M. Hargrove, Weedy adaptation in Setaria spp. V. Effects of gaseous environment on giant foxtail (Setaria faberii) (Poaceae) seed germination, Am. J. Bot. 89 (2002) 410–416. [12] K.L. Liu, S. Xu, W. Xuan, T.F. Ling, Z.Y. Cao, B.K. Huang, et al., Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa, Plant Sci. 172 (2007) 544–555. [13] J. Xu, W. Xuan, B.K. Huang, Y.H. Zhou, T.F. Ling, S. Xu, et al., Carbon monoxideinduced adventitious rooting of hypocotyls cutting from mung bean seedling, Chin. Sci. Bull. 51 (2006) 668–674. [14] W. Xuan, L.Q. Huang, M. Li, B.K. Huang, S. Xu, H. Liu, et al., Induction of growth elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants?, Plant Growth Regul. 52 (2007) 41–51. [15] Z.S. Sa, L.Q. Huang, G.L. Wu, J.P. Ding, X.Y. Chen, T. Yu, et al., Carbon monoxide: a novel antioxidant against oxidative stress in wheat seedling leaves, J. Integr. Plant Biol. 49 (2007) 638–645. [16] M.D. Maines, The heme oxygenase system: a regulator of second messenger gases, Annu. Rev. Pharmacol. Toxicol. 37 (1997) 517–554. [17] S.S. Wilks, Carbon monoxide in green plants, Science 129 (1959) 964–966.
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Contents lists available at ScienceDirect
Nitric Oxide j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / y n i o x
Review
The role of carbon monoxide signaling in the responses of plants to abiotic stresses Huyi He a,b,*, Longfei He a a b
College of Agronomy, Guangxi University, Nanning 530004, China Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, Nanning 530007, China
A R T I C L E
I N F O
Article history: Received 27 May 2014 Revised 26 August 2014 Available online 29 August 2014 Keywords: Abiotic stress Carbon monoxide Nitric oxide H2O2 Oxidative damage Reactive oxygen species Signal transduction
A B S T R A C T
Whether carbon monoxide (CO) exerts toxic or protective effect is dependent on the concentration and location of CO in animals. Similarly, it has been increasingly evident that CO also is involved in diverse physiological processes in plants, from seed germination and dormancy to stomatal closure to regulation of multiple environmental stresses. In this review, we focus on CO synthesis and the role of CO in plant responses to abiotic stresses, such as salinity, drought, cadmium and mercury. In general, abiotic stresses induce CO production in plants. CO can alleviate oxidative damage by improving the activities of antioxidative enzymes and antioxidant metabolism. In addition, cross talk between CO signaling and other signaling molecules including nitric oxide (NO) and hydrogen peroxide (H2O2) also is discussed. © 2014 Published by Elsevier Inc.
Contents 1. 2. 3. 4. 5.
Introduction ........................................................................................................................................................................................................................................................... Synthesis of CO in plants .................................................................................................................................................................................................................................. Role of CO in abiotic stresses .......................................................................................................................................................................................................................... Cross talk between CO signaling and other signaling molecules ....................................................................................................................................................... Conclusions and perspectives ......................................................................................................................................................................................................................... Source of funding ................................................................................................................................................................................................................................................ References ..............................................................................................................................................................................................................................................................
1. Introduction Carbon monoxide (CO) is the most common cause of fatal poisoning in the world. Although the acute exposure to CO gas via the incomplete combustion of domestic gas has been well known for a long time, chronic exposure also occurs by means of cigarette smoking. In animals, endogenous CO production and heme oxygenase (HO EC 1.14.99.3) induction are stimulated by different stress responses, including heat shock, oxidants, metals, lipopolysaccharides, hypoxia, hyperoxia and reactive oxygen species (ROS) [1–3]. Similarly, CO plays a major role in a number of physiological processes
* Corresponding author. Cash Crops Research Institute, Guangxi Academy of Agricultural Sciences, No. 174 Daxue East Road, Nanning 530007, China. Fax: +86 771 3244229. E-mail address: [email protected] (H. He). http://dx.doi.org/10.1016/j.niox.2014.08.011 1089-8603/© 2014 Published by Elsevier Inc.
40 41 41 42 42 43 43
such as growth and developmental regulation, stomatal closure, and adaptation responses to environmental stresses in plants [4–10]. As an important positive regulator, CO also is involved in seed germination and dormancy breaking [11,12], and adventitious rooting [10,13]. Low concentration of CO can stimulate seed germination and dormancy [11]. Exogenous CO induces adventitious rooting of hypocotyl cuttings (primary roots removed) from mung bean (Vigna radiata) seedlings [13]. CO produced by HO might mediate the induction of growth elongation of wheat root segments by IAA [14]. Basipetal transport of auxin induces a CO burst synthesized by HO in the basal region of hypocotyls, thus leading to adventitious root formation. This pathway might be mediated by the expression of DnaJ-1 and calcium-dependent protein kinase (CDPK) genes [10]. Abiotic stresses are major constraint to agricultural productivity in the world. The harm of abiotic stresses includes the disruption of cellular redox homeostasis, ROS production and oxidative stress. Plants have evolved tolerance mechanisms in responses to
H. He, L. He/Nitric Oxide 42 (2014) 40–43
41
Table 1 Reports on CO-mediated effects during abiotic stresses in plants. Plant species
Tissue
Abiotic stress
CO production
CO-mediated effect
CO-regulated gene
Reference
Triticum aestivum
Root
Salt
+
Seed
Salt
+
APX, DHAR, Mn-SOD, Cu/Zn-SOD, H+-ATPase α-amylase, CAT, Cu/Zn-SOD, HO-1
[9]
Oryza sativa
Maintain ion homeostasis/enhance antioxidant system Alleviate oxidative damage
Triticum aestivum Triticum aestivum Glycine max
Leaf Seed Root nodule Root
Salt Salt Salt
+ + +
Alleviate oxidative stress Alleviate oxidative stress Protect nitrogen metabolism
– HO-1, GS, GOAT
Salt
+
Osmotic Cd Cd Hg Hg Hg
+ + + + + +
Mn-SOD, Cu/Zn-SOD, NADPH oxidase HO-1 HO-1 HO-1 HO-1, APX, GPX Cu-Zn SOD, CAT, POD HO-1, PCS1
[26]
Seed Root Root Root Root Root, shoot, leaf Leaf Root, shoot, leaf
Inhibit superoxide anion overproduction – Alleviate oxidative damage Enhance antioxidative capability Alleviate oxidative damage Prevent oxidative stress Attenuate oxidative injury
UV-B –Fe
+ +
Prevent oxidative stress Regulate iron homeostasis
HO-1, CAT, APX IRT1, FRO2, FIT1, FER1
[31] [32]
Triticum aestivum Triticum aestivum Medicago sativa Medicago sativa Medicago sativa Brassica juncea Brassica napus Glycine max Arabidopsis
alteration of environmental conditions. CO is able to strongly protect plants against oxidative damage caused by the overproduction of reactive oxygen species (ROS), suggesting that CO is a potent antioxidant in various abiotic and biotic stresses [15]. In this review, we focus on synthesis of CO and its role in plant responses to abiotic stresses such as salinity, drought, cadmium (Cd), mercury (Hg), iron deficiency, and ultraviolet-B (UV-B) radiation. Moreover, crosstalk between molecules signaling with CO and those signaling with other molecules such as nitric oxide (NO) and hydrogen peroxide (H2O2) is also discussed. 2. Synthesis of CO in plants CO is an odorless, tasteless, and colorless concomitant product of heme degradation catalyzed by HO [16]. To date three isozymes have been detected in mammals: the inducible isoform HO1, the constitutively expressed isozyme HO-2, and an isozyme with very low activity HO-3. Although the most investigated mechanism for CO production in animals involves HO, there are other ways in which CO can be generated [2] speculated that the action of CO in animals, including cytoprotection and cytotoxic effects, might be dependent on its concentration and the different experimental materials applied. The presence of CO biosynthesis in plants was first reported by Wilks [17]. In addition to the photo-production of CO in living plants [18,19], there is a significant light-independent source of CO gas among smaller plants associated with the soil surface and soil–air interface [18,20]. It also has been shown that CO is released from haem proteins during the generation of ferrous iron (Fe2+) and biliverdin-IXα (BV-IXα), which can be reduced to bilirubin by biliverdin reductase. CO exhibits the ability to bind to the iron atom of the heme moiety associated with soluble guanylate cyclase (sGC), thereby activating the enzyme and increasing production of the intracellular second messenger molecule cGMP [21]. Although the GC activity and cGMP content have been detected in some plants recently, whether cGMP signaling system exits in plants still has no sufficient evidence to confirm. 3. Role of CO in abiotic stresses Almost all abiotic stresses generate free radicals and other oxidants, resulting in oxidative damage in terms of an increased level of ROS in plant cells [22]. CO is induced rapidly by salinity, drought,
[12] [23] [24] [25]
[27] [7] [28] [6] [29] [30]
Cd, Hg, iron deficiency, and UV-B in plants and regulates the plant responses to abiotic stresses (Table 1). CO has profound effects on intracellular signaling processes such as the maintenance of ROS homeostasis under oxidative stress [33,34]. CO plays a vital role in intracellular redox signaling and activation of antioxidant resistance mechanisms. Soil salinity limits crop productivity and quality by affecting several key metabolic processes such as osmotic and ionic homeostasis. Salinity alters the activities of many enzymes involved in nitrate and sulfate assimilation pathways in plants, lowers their energy status, and increases the demand for nitrogen and sulfur [35]. Exogenous application of low levels of CO donor hematin may be advantageous against salt-induced oxidative damage in wheat seedling leaves [23]. Low concentrations of CO can attenuate the inhibition of seed germination produced by salinity stress and counteract lipid peroxidation in germinating wheat seeds [24]. CO had an advantageous effect on attenuation of inhibition of seed germination and seedling growth induced by salt stress, and alleviated oxidative damage by activating anti-oxidant enzymes [12]. NaCl triggers a biphasic burst of CO production in wheat seedling roots, suggesting CO may be a key component responsible for salinity tolerance. CO might confer an increased tolerance to salinity stress by maintaining ion homeostasis and enhancing antioxidant system parameters in wheat seedling roots, both of which were partially mediated by NO signaling [9]. Up-regulation of HO, as part of an antioxidant defense system, could be protecting the soybean nodule nitrogen fixation and assimilation under saline stress conditions [25]. CO might be involved in plant tolerance against salinity stress, and its alleviation of programmed cell death (PCD) and inhibition of root growth were related to the decrease of superoxide anion overproduction partially via up-regulation of SOD and down-regulation of NADPH oxidase expression [26]. Drought is one of the major constraints to food production because it limits growth and development of plants. Drought or osmotic stress induces the accumulation of ROS in plants [22]. Hematin (a CO donor) pretreatment (≤0.1 μM) could delay wheat leaf chlorophyll loss mediated by further treatment of H2O2 and paraquat in a dose- and even time-dependent manner [15]. The polyethylene glycol-6000 (PEG)-induced inhibitory effect on seed germination was ameliorated by CO. The endogenous HO/CO signal system is required for the alleviation of osmotic stress-induced wheat seed germination inhibition and lipid peroxidation, which might have a possible interaction with NO [27].
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H. He, L. He/Nitric Oxide 42 (2014) 40–43
Heavy metal toxicity resulting from contamination is known to affect the biosphere. And this leads to health hazards for animals and plants. Cd is a non-essential and toxic metal, rapidly taken up by roots and accumulated in various plant tissues, which hampers crop growth and productivity worldwide. Hematin can markedly boost the HO/CO system, which exhibits a vital role in protecting the plant against Hg-induced oxidative damage [6]. Exogenous Cd increased CO production. As a signal element, CO release alleviated Cd-induced oxidative damage by modulating glutathione (GSH) and ascorbic acid (AsA) homeostasis in the roots of alfalfa [7]. Cdinduced HO-1 gene expression is associated with depletion of GSH in the roots of Medicago sativa, leading to enhanced antioxidative capability transiently [28]. CO-mediated enhancement of Hg tolerance was closely related to the accumulation of proline and reduced non-protein thiols [29]. Overexpression of BnHO-1 resulted in less accumulation of Hg in some lines of transformants than in untransformants [30]. Deeper understanding of CO production and action helps to evaluate the effects and remedy of different concentrations of the same metal or the concentrations of different metals in plants. Due to the depletion of the stratospheric ozone layer, UV-B radiation (280–320 nm) has deleterious effects on plants, including decreased biomass formation, reduced photosynthesis and damaged DNA. UV-B perception increases O2− generation and NO production of plants. NO and H2O2 participate in the signaling required for HO-1 up-regulation, which mediates the enhancement in HO activity. CO is produced by HO-mediated heme catabolism [31]. CO can regulate iron-homeostasis in iron-starved Arabidopsis and exogenous CO can prevent iron deficiency-induced chlorosis and improve chlorophyll accumulation [32]. Like the case of mammals, it is very important to know the concentration range and production rate of CO under abiotic stress conditions in plants. However, plant cells are not surrounded by abundant heme proteins in the tissues. In terms of CO diffusion, plants physical inter-cellular environments are entirely different from that of animal tissues. In mammalian systems, the concentration and localization of CO production are clear. Contrasting with the mammalian systems, the concentration and localization of CO production in plants remain to be elucidated. 4. Cross talk between CO signaling and other signaling molecules CO and NO all bind to the heme of hemoglobins, thereby disturbing energy transduction systems including respiration. Also, CO might exert its biological effects by its synergism with NO (Fig. 1).
Abiotic stresses
Thom et al. [36] discovered that exposure of endothelial cells to low levels of CO (10–110 nmol/L) led to an increase in steady-state NO and NO-derived oxidants peroxynitrite, suggesting that competition from CO for intracellular NO-binding sites contributes to the elevation of the NO level. The rate of superoxide production is enhanced by slowing the terminal transfer rate of electrons to molecular O2 by CO binding at cytochrome c oxidase (and NO in some cases). NO reversibly inhibits the activities of tobacco catalase (CAT) and ascorbate peroxidase (APX) [37]. Because CO and NO are able to activate sGC, they share many properties and CO may serve as a neuronal messenger molecule similar to NO [38]. It is becoming increasingly clear that these two gases do not always work independently, but rather can modulate each other’s activity in animals [3,38]. NO donor SNP alleviates Cd-caused chlorophyll loss through argumentation of HO-1 transcript levels [39]. As shown in animals, CO induces LR formation probably mediated by the NO/ NOS pathway and NO may act downstream of CO signaling [5]. NO is required for CO-induced guard cell closure [4,8]. CO might mediate the induction of growth elongation of wheat (Triticum aestivum) root segments by IAA, which might be related to NO/cGMP-dependent pathways [10,14]. Wheat seedling roots treated daily with exogenous CO could synthesize NO, indicating that NO may be a part of the downstream signal molecule of CO action [9]. A balance between NO and ROS is essential in order to trigger the antioxidant response against oxidative stress [31]. Endogenous CO level was increased in Arabidopsis under iron-deficiency and CO exposure induced NO accumulation in root tips, indicating that CO may play an important role in improving plant adaptation to iron deficiency or cross-talking with NO [32]. In addition, CO could inhibit excessive NO generation and suppress the catalytic activity of cytochrome P450 monooxygenases, enzyme systems that account for endogenous generation of ROS. The increase in free iron induces the up-regulation of ferritin which in turn causes overall reduction of free iron and thereby attenuates oxidative susceptibility [40]. By application of H2O2 or AsA, heme methylene bridges can be broken and CO released [2]. CO protects endothelial cells from various stimuli-induced apoptosis by inhibiting ROS formation, and ROS modulated by CO can influence the activity of several transcription factors and kinases such as NF-kB and p38 [41,42]. CO likely activates p38 mitogen-activated protein kinase (MAPK) by generating oxidant [34]. ABA-induced H2O2 production activates a 46-kD MAPK, which in turn induces the expression and the activities of CAT, cAPX and GR1. The activation of MAPK also enhances the H2O2 production, forming a positive feedback loop [43]. CO aqueous solution induced CAT and superoxide dismutase (SOD) activities, resulting in the alleviation of oxidative damage [12]. CO and H2O2 exhibit a similar regulation role in the stomatal movement. CO-induced stomatal closure probably involves H2O2 signaling and CO is involved in darkness-induced HO synthesis in Vicia faba guard cells [44]. CO prevented GA-induced PCD by enhancing the activities or transcripts of CAT and APX [45].
NO 5. Conclusions and perspectives
CO
CAT/APX
H2O2
CAT/SOD
cGMP
MAPK Cascades
Plant responses Fig. 1. A model for carbon monoxide-mediated signaling in plant responses to abiotic stresses.
Preliminary advances in the knowledge of CO role in the regulation of plant growth and development, and tolerance of plants to environmental stresses have been achieved, but the current situation of CO research in plants is at an early stage. Due to the technological obstacle of CO detection, so far the biochemical and molecular details of precise CO biosynthetic pathway have not been fully understood. For example, it is not clear for nonenzymatic pathways and functions of CO in plants. At present, most studies of CO signaling are based on pharmacological methods as plant NO research. Although the effects of chemical donors and fluorescence probes may be subjected to technical limitations, there is no question about the involvement of CO in plant responses to abiotic
H. He, L. He/Nitric Oxide 42 (2014) 40–43
stresses. On the one hand, CO might protect plants against ROScaused oxidative damage by improving the activities of antioxidative enzymes and antioxidant metabolism. On the other hand, as a signaling molecule, CO plays important roles in responses to environmental stresses via cross talk with other hormones together. However, it is uncertain how these identified pathways interact with each other in plants. With the screening of relevant HO mutants and application of reverse genetics, proteomics, transcriptomes, and functional genomics, it will be revealed how CO metabolism is governed. Crop yield depends on the capacity of plants to tolerate increases in ROS. Application of chemical CO donors helps to improve crop productivity. The identification of CO targets and deeper understanding of CO signaling transduction will provide novel biochemical and physiological evidence on CO function in the responses of plants to abiotic stresses. Source of funding This study was funded by the National Natural Science Foundation of China (Nos. 30960181 and 31260296) and 2011 Guangxi Innovation Program for Graduates (GXU11T31076). References [1] C.A. Piantadosi, Biological chemistry of carbon monoxide, Antioxid. Redox Signal. 4 (2002) 259–270. [2] J. Dulak, A. Jozkowicz, Carbon monoxide: a “new” gaseous modulator of gene expression, Acta Biochim. Pol. 50 (2003) 31–47. [3] R.N. Watts, P. Ponka, D.R. Richardson, Effects of nitrogen monoxide and carbon monoxide on molecular and cellular iron metabolism: mirror-image effector molecules that target iron, Biochem. J. 369 (2003) 429–440. [4] Z.Y. Cao, B.K. Huang, Q.Y. Wang, W. Xuan, T.F. Ling, B. Zhang, et al., Involvement of carbon monoxide produced by heme oxygenase in ABA-induced stomatal closure in Vicia faba and its proposed signal transduction pathway, Chin. Sci. Bull. 52 (2007a) 2365–2373. [5] Z.Y. Cao, W. Xuan, Z.Y. Liu, X.N. Li, N. Zhao, P. Xu, et al., Carbon monoxide promotes lateral root formation in rapeseed, J. Integr. Plant Biol. 49 (2007b) 1070–1079. [6] Y. Han, W. Xuan, T. Yu, W.B. Fang, T.L. Lou, Y. Gao, et al., Exogenous hematin alleviates mercury-induced oxidative damage in the roots of Medicago sativa, J. Integr. Plant Biol. 49 (2007) 1703–1713. [7] Y. Han, J. Zhang, X. Chen, Z. Gao, W. Xuan, S. Xu, et al., Carbon monoxide alleviates cadmium-induced oxidative damage by modulating glutathione metabolism in the roots of Medicago sativa, New Phytol. 177 (2008) 155–166. [8] X.G. Song, X.P. She, B. Zhang, Carbon monoxide-induced stomatal closure in Vicia faba is dependent on nitric oxide synthesis, Physiol. Plant. 132 (2008) 514–525. [9] Y.J. Xie, T.F. Ling, Y. Han, K.L. Liu, Q.S. Zheng, L.Q. Huang, et al., Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots, Plant Cell Environ. 31 (2008) 1864–1881. [10] W. Xuan, F.Y. Zhu, S. Xu, B.K. Huang, T.F. Ling, J.F. Qi, et al., The heme oxygenase/ carbon monoxide system is involved in the auxin-induced cucumber adventitious rooting process, Plant Physiol. 148 (2008) 881–893. [11] J. Dekker, M. Hargrove, Weedy adaptation in Setaria spp. V. Effects of gaseous environment on giant foxtail (Setaria faberii) (Poaceae) seed germination, Am. J. Bot. 89 (2002) 410–416. [12] K.L. Liu, S. Xu, W. Xuan, T.F. Ling, Z.Y. Cao, B.K. Huang, et al., Carbon monoxide counteracts the inhibition of seed germination and alleviates oxidative damage caused by salt stress in Oryza sativa, Plant Sci. 172 (2007) 544–555. [13] J. Xu, W. Xuan, B.K. Huang, Y.H. Zhou, T.F. Ling, S. Xu, et al., Carbon monoxideinduced adventitious rooting of hypocotyls cutting from mung bean seedling, Chin. Sci. Bull. 51 (2006) 668–674. [14] W. Xuan, L.Q. Huang, M. Li, B.K. Huang, S. Xu, H. Liu, et al., Induction of growth elongation in wheat root segments by heme molecules: a regulatory role of carbon monoxide in plants?, Plant Growth Regul. 52 (2007) 41–51. [15] Z.S. Sa, L.Q. Huang, G.L. Wu, J.P. Ding, X.Y. Chen, T. Yu, et al., Carbon monoxide: a novel antioxidant against oxidative stress in wheat seedling leaves, J. Integr. Plant Biol. 49 (2007) 638–645. [16] M.D. Maines, The heme oxygenase system: a regulator of second messenger gases, Annu. Rev. Pharmacol. Toxicol. 37 (1997) 517–554. [17] S.S. Wilks, Carbon monoxide in green plants, Science 129 (1959) 964–966.
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