NO and ROS implications in the organization of root system architecture

Over the past decades the role of nitric oxide (NO) and reactive oxygen species (ROS) in signaling and cellular responses to stress has witnessed an exponential trend line. Despite advances in the subject, our knowledge of the role of NO and ROS as regulators of stress and plant growth and their implication in signaling pathways is still partial. The crosstalk between NO and ROS during root formation offers new domains to be explored, as it regulates several plant functions. Previous findings indicate that plants utilize these signaling molecules for regulating physiological responses and development. Depending upon cellular concentration, NO either can stimulate or impede root system architecture (RSA) by modulating enzymes through post-translational modifications. Similarly, the ROS signaling molecule network, in association with other hormonal signaling pathways, control the RSA. The spatial regulation of ROS controls cell growth and ROS determine primary root and act in concert with NO to promote lateral root primordia. NO and ROS are two central messenger molecules which act differentially to upregulate or downregulate the expression of genes pertaining to auxin synthesis and to the configuration of root architecture. The investigation concerning the contribution of donors and inhibitors of NO and ROS can further aid in deciphering their role in root development. With this background, this review provides comprehensive details about the effect and function of NO and ROS in the development of RSA.     

植物一氧化氮信号分子的研究进展

一氧化氮(NO)作为一种重要的信号分子,不仅参与植物的种子休眠和萌发以及根的形态建成等生长发育过程,还参与调节植物细胞的气孔运动以及植物抗逆应答反应。该文结合最新研究成果,总结了植物NO信号调控机理的研究进展,主要包括NO合成途径、信号转导途径及其与其它信号分子之间的交叉反应和对植物抗逆的调控作用等。     

The diversity of nitric oxide function in plant responses to metal stress

Nitric oxide (NO) emerges as signalling molecule, which is involved in diverse physiological processes in plants. High mobility metal interferes with NO signaling. The exogenous NO alleviates metal stress, whereas endogenous NO contributes to metal toxicity in plants. Owing to different cellular localization and concentration, NO may act as multifunctional regulator in plant responses to metal stress. It not only plays a crucial role in the regulation of gene expression, but serves as a long-distance signal. Through tight modulation of redox signaling, the integration among NO, reactive oxygen species and stress-related hormones in plants determines whether plants stimulate death pathway or activate survival signaling.     

NO是植物应激反应的信号分子

根据NO的性质和可能的产生途径,略述了生物胁迫(病原菌侵害)和干旱胁迫、盐胁迫、极端温度、机械损伤、臭氧和紫外辐射等各种非生物胁迫信号与NO信号分子的偶联及其信号的级联途径,概括了NO可能介导的生物过程,讨论了NO通过其下游信号过程对与细胞的生理影响以及该下游信号过程所涉及到的cGMP、cADPR的产生和NO与其它信号分子(ROS、SA、ABA等)的协同作用,表明胁迫诱导的NO爆发是激发、启动和装备植物细胞的重要信号级联环节,这个环节能使植物细胞处于应激状态,并迅速作出反应,形成一系列适应机制。     

Extracellular ATP and nitric oxide signaling pathways regulate redox-dependent responses associated to root hair growth in etiolated Arabidopsis seedlings

Extracellular ATP (eATP) and nitric oxide (NO) have emerged as crucial players in plant development, stress responses and cell viability. Glutathione (GSH) is an abundant reducing agent with proposed roles in plant growth, development and stress physiology. In a recent publication, we demonstrated that eATP and NO restore hypocotyl elongation of etiolated Arabidopsis seedlings treated with GSH. Here it is reported that exogenous ATP also restores root hair growth suggesting a role for ATP and NO in the regulation of redox balance associated to specific processes of plant morphogenesis. A tentative model integrating redox-, eATP- and NO-signaling pathways during root hair growth in Arabidopsis seedlings is presented.Key words: Arabidopsis thaliana, extracellular ATP signaling, nitric oxide, redox system, root hair     

Pharmacological and genetical evidence supporting nitric oxide requirement for 2,4-epibrassinolide regulation of root architecture in Arabidopsis thaliana

Brassinosteroids (BRs) regulate various physiological processes, such as tolerance to stresses and root growth. Recently, a connection was reported between BRs and nitric oxide (NO) in plant responses to abiotic stress. Here we present evidence supporting NO functions in BR signaling during root growth process. Arabidopsis seedlings treated with BR 24-epibrassinolide (BL) show increased lateral roots (LR) density, inhibition of primary root (PR) elongation and NO accumulation. Similar effects were observed adding the NO donor GSNO to BR-receptor mutant bri1-1. Furthermore, BL-induced responses in the root were abolished by the specific NO scavenger c-PTIO. The activities of nitrate reductase (NR) and nitric oxide synthase (NOS)-like, two NO generating enzymes were involved in BR signaling. These results demonstrate that BR increases the NO concentration in root cells, which is required for BR-induced changes in root architecture.     

Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L

Nitric oxide (NO) as a key signaling molecule has been involved in mediation of various biotic and abiotic stress-induced physiological responses in plants. In the present study, we investigated the effect of NO on Cassia tora L. plants exposed to aluminum (Al). Plants pre-treated for 12 h with 0.4 mM sodium nitroprusside (SNP), an NO donor, and subsequently exposed to 10 microM Al treatment for 24 h exhibited significantly greater root elongation as compared with the plants without SNP treatment. The NO-promoted root elongation was correlated with a decrease in Al accumulation in root apexes. Furthermore, oxidative stress associated with Al treatment increased lipid peroxidation and reactive oxygen species, and the activation of lipoxygenase and antioxidant enzymes was reduced by NO. Such effects were confirmed by the histochemical staining for the detection of peroxidation of lipids and loss of membrane integrity in roots. The ameliorating effect of NO was specific, because the NO scavenger cPTIO [2-(4-carboxy-2-phenyl)-4,4,5,5-tetramethylinidazoline-1-oxyl-3-oxide] completely reversed the effect of NO on root growth in the presence of Al. These results indicate that NO plays an important role in protecting the plant against Al-induced oxidative stress.     

Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana

Nitric oxide (NO) participates in the regulation of diverse functions in plant cells. However, different NO concentrations may trigger different pathways during the plant development. At basal levels of NO, plants utilize the NO signaling transduction pathway to facilitate plant growth and development, whereas higher concentrations trigger programmed cell death (PCD). Our results show that NO lower than the levels causing PCD, but higher than the basal levels induce DNA damage in root cells in Arabidopsis as witnessed by a reduction in root growth, rather than cell death, since cells retain the capacity to differentiate root hairs. The decrease in meristematic cells and increase in DNA damage signals in roots in responses to NO are in a dose dependent manner. The restraint of root growth is due to cell cycle arrest at G1 phase which is caused by NO induced DNA damage, besides a second arrest at G2/M existed in NO supersensitive mutant cue1. The results indicate that NO restrain root growth via DNA damage induced cell cycle arrest.     

植物细胞一氧化氮信号转导研究进展

一氧化氮(nitric oxide, NO)作为重要的信号分子, 调控植物的种子萌发、根形态建成和花器官发生等许多生长发育过程, 并参与气孔运动的调节以及植物对多种非生物胁迫和病原体侵染的应答过程。已经知道, 精氨酸依赖的NOS途径和亚硝酸盐依赖的NR途径是植物细胞NO产生的主要酶促合成途径。NO及其衍生物能够直接修饰底物蛋白的金属基团、半胱氨酸和酪氨酸残基, 通过金属亚硝基化、巯基亚硝基化和Tyr-硝基化等化学修饰方式, 调节靶蛋白的活性, 并影响cGMP和Ca²⁺信使系统等下游信号途径, 调控相应的生理过程。最新的一些研究结果也显示, MAPK级联系统与NO信号转导途径之间存在复杂的交叉调控。此外, 作为活跃的小分子信号, NO和活性氧相互依赖并相互影响, 共同介导了植物的胁迫应答和激素响应过程。文章综述了植物NO信号转导研究领域中一些新的研究进展, 对NO与活性氧信号途径间的交叉作用等也作了简要介绍。     

The message of nitric oxide in cadmium challenged plants

During the last decade it has been found that cadmium (Cd), one of the most toxic elements occurring in polluted environments, interferes with nitric oxide (NO), a multifunctional signaling molecule in living organisms. The formation of NO has been demonstrated in vivo in various plant tissues exposed to Cd stress, but unfortunately, the time and intensity of NO generation, relatively frequently shows conflicting data. What is more, there is still limited information regarding the functional role of endogenously produced NO in plants challenged with heavy metals. The first pharmacological approaches revealed that exogenously applied NO can alleviate cadmium toxicity in plants, promoting the direct scavenging of reactive oxygen species (ROS) or activating antioxidant enzymes. However, recent reports have indicated that NO even contributes to Cd toxicity by promoting Cd uptake and participates in metal-induced reduction of root growth. In view of this heterogeneous knowledge, much more puzzling if we consider results first obtained using exogenous NO sources, this review is focused mainly on the implication of endogenous NO in plant response to Cd exposure. Furthermore, a basic draft for NO mode of action during cadmium stress is proposed.     

一氧化氮在植物体内的来源和功能

一氧化氮(nitric oxide,NO)是生物体内重要的活性分子。NO参与了动物体内血管松弛、神经传递及免疫防御反应等一系列生理功能而被认为是可扩散的多功能第二信使。在植物体内NO也是一种广泛存在的信号分子,参与调节了许多重要的生理过程如生长、发育、抗病防御反应、细胞程序性死亡和抗逆反应。对NO在植物体内的来源、信号转导、调节植物生长发育和对胁迫的响应方面所发挥的作用进行了综述,并讨论了其潜在的一些功能。     

Nitric oxide as a key component in hormone-regulated processes

Nitric oxide (NO) is a small gaseous molecule, with a free radical nature that allows it to participate in a wide spectrum of biologically important reactions. NO is an endogenous product in plants, where different biosynthetic pathways have been proposed. First known in animals as a signaling molecule in cardiovascular and nervous systems, it has turned up to be an essential component for a wide variety of hormone-regulated processes in plants. Adaptation of plants to a changing environment involves a panoply of processes, which include the control of CO₂ fixation and water loss through stomatal closure, rearrangements of root architecture as well as growth restriction. The regulation of these processes requires the concerted action of several phytohormones, as well as the participation of the ubiquitous molecule NO. This review analyzes the role of NO in relation to the signaling pathways involved in stomatal movement, plant growth and senescence, in the frame of its interaction with abscisic acid, auxins, gibberellins, and ethylene.     

Nitric oxide signaling in plant-pathogen interactions

Nitric oxide (NO), first characterized as an endothelium-derived relaxation factor, is involved in diverse cellular processes including neuronal signaling, blood pressure homeostasis, and immune response. Recent studies have also revealed a role for NO as a signaling molecule in plants. As a developmental regulator, NO promotes germination, leaf extension and root growth, and delays leaf senescence and fruit maturation. Moreover, NO acts as a key signal in plant resistance to incompatible pathogens by triggering resistance-associated hypersensitive cell death. In addition, NO activates the expression of several defense genes (e.g. pathogenesis-related genes, phenylalanine ammonialyase, chalcone synthase) and could play a role in pathways leading to systemic acquired resistance.     

The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots

Nitric oxide (NO) is a signaling molecule involved in plant responses to abiotic and biotic stresses. While there is evidence for NO accumulation during legume nodulation, almost no information exists for arbuscular mycorrhizas (AM). Here, we investigated the occurrence of NO in the early stages of Medicago truncatula–Gigaspora margarita interaction, focusing on the plant response to fungal diffusible molecules. NO was visualized in root organ cultures and seedlings by confocal microscopy using the specific probe 4,5-diaminofluorescein diacetate. Five-minute treatment with the fungal exudate was sufficient to induce significant NO accumulation. The specificity of this response to AM fungi was confirmed by the lack of response in the AM nonhost Arabidopsis thaliana and by analyzing mutants impaired in mycorrhizal capacities. NO buildup resulted to be partially dependent on DMI1, DMI2, and DMI3 functions within the so-called common symbiotic signaling pathway which is shared between AM and nodulation. Significantly, NO accumulation was not induced by the application of purified Nod factor, while lipopolysaccharides from Escherichia coli, known to elicit defense-related NO production in plants, induced a significantly different response pattern. A slight upregulation of a nitrate reductase (NR) gene and the reduction of NO accumulation when the enzyme is inhibited by tungstate suggest NR as a possible source of NO. Genetic and cellular evidence, therefore, suggests that NO accumulation is a novel component in the signaling pathway that leads to AM symbiosis.     

植物一氧化氮生物学的研究进展

一氧化氮(NO)是植物中的一种关键的信号分子.在植物中,NO的潜在来源包括一氧化氮合成酶、硝酸还原酶、黄嘌呤氧化还原酶和非酶促途径.NO能促进植物生长,延缓叶片、花和果实衰老,促进休眠和需光种子的萌发,能与植物激素相互作用调节气孔运动,诱导程序性细胞死亡和防御相关基因的表达,并在逆境中作为一种抗氧化剂起作用.NO的细胞内信号反应包括环鸟苷酸、环腺苷二磷酸核糖的产生和细胞质Ca2 浓度的增加,其信号转导途径及其生物化学和细胞学本质还不十分清楚.     

植物一氧化氮生物学的研究进展

一氧化氮 (NO) 是植物中的一种关键的信号分子。在植物中, NO的潜在来源包括一氧化氮合成酶、硝酸还原酶、黄嘌呤氧化还原酶和非酶促途径。NO能促进植物生长, 延缓叶片、花和果实衰老, 促进休眠和需光种子的萌发, 能与植物激素相互作用调节气孔运动, 诱导程序性细胞死亡和防御相关基因的表达, 并在逆境中作为一种抗氧化剂起作用。 NO的细胞内信号反应包括环鸟苷酸、环腺苷二磷酸核糖的产生和细胞质Ca2+浓度的增加, 其信号转导途径及其生物化学和细胞学本质还不十分清楚。     

Nitric oxide-induced salt stress tolerance in plants: ROS metabolism,signaling, and molecular interactions

Nitric oxide (NO), a non-charged, small, gaseous free-radical, is a signaling molecule in all plant cells. Several studies have proposed multifarious physiological roles for NO, from seed germination to plant maturation and senescence. Nitric oxide is thought to act as an antioxidant, quenching ROS during oxidative stress and reducing lipid peroxidation. NO also mediates photosynthesis and stomatal conductance and regulates programmed cell death, thus providing tolerance to abiotic stress. In mitochondria, NO participates in the electron transport pathway. Nitric oxide synthase and nitrate reductase are the key enzymes involved in NO-biosynthesis in aerobic plants, but non-enzymatic pathways have been reported as well. Nitric oxide can interact with a broad range of molecules, leading to the modification of protein activity, GSH biosynthesis, S-nitrosylation, peroxynitrite formation, proline accumulation, etc., to sustain stress tolerance. In addition to these interactions, NO interacts with fatty acids to form nitro-fatty acids as signals for antioxidant defense. Polyamines and NO interact positively to increase polyamine content and activity. A large number of genes are reprogrammed by NO; among these genes, proline metabolism genes are upregulated. Exogenous NO application is also shown to be involved in salinity tolerance and/or resistance via growth promotion, reversing oxidative damage and maintaining ion homeostasis. This review highlights NO-mediated salinity-stress tolerance in plants, including NO biosynthesis, regulation, and signaling. Nitric oxide-mediated ROS metabolism, antioxidant defense, and gene expression and the interactions of NO with other bioactive molecules are also discussed. We conclude the review with a discussion of unsolved issues and suggestions for future research.     

Involvement of salicylic acid and nitric oxide in protective reactions of wheat under the influence of heavy metals

This article studies the effect of salicylic acid (SA) and nitric oxide (NO) on Triticum aestivum L. wheat plants exposed to the influence of high concentrations of copper and zinc compounds. It is shown that heavy metals (HMs) caused a decrease in the growth parameters in the overground and underground plant parts and contributed to a sharp deterioration in the energy balance and the situation regarding oxidative stress. SA and NO exerted a protective effect, which was expressed in the increased ability to accumulate shoot and root mass, stabilize the energy balance, and reduced lipid peroxidation. Resemblance of protective reactions of wheat plants affected by SA and NO appeared as the alteration of energy (Rtot/Pnet and alternative respiration) and antioxidant (MDA) balance of studied plants was identified. The resemblance possibly evidences of common signaling pathway for SA and NO caused by effect of toxic concentrations of heavy metals.     

Nitric oxide-mediated regulation of oxidative stress in plants under metal stress: a review on molecular and biochemical aspects

Given their sessile nature, plants continuously face unfavorable conditions throughout their life cycle, including water scarcity, extreme temperatures and soil pollution. Among all, metal(loid)s are one of the main classes of contaminants worldwide, posing a serious threat to plant growth and development. When in excess, metals which include both essential and non-essential elements, quickly become phytotoxic, inducing the occurrence of oxidative stress. In this way, in order to ensure food production and safety, attempts to enhance plant tolerance to metal(loid)s are urgently needed. Nitric oxide (NO) is recognized as a signaling molecule, highly involved in multiple physiological events, like the response of plants to abiotic stress. Thus, substantial efforts have been made to assess NO potential in alleviating metal-induced oxidative stress in plants. In this review, an updated overview of NO-mediated protection against metal toxicity is provided. After carefully reviewing NO biosynthetic pathways, focus was given to the interaction between NO and the redox homeostasis followed by photosynthetic performance of plants under metal excess.