一氧化氮对植物重金属胁迫抗性的影响研究进展

一氧化氮(NO)作为一种重要的信号分子,在调节植物重金属胁迫抗性方面上起着非常重要的作用。综述了NO在植物体内的产生途径,重金属胁迫下植物体内内源NO含量的变化以及外源NO与内源NO对植物重金属胁迫抗性的影响。大量研究表明外源NO能够增强植物对重金属胁迫的抗性,一方面是通过增强植物细胞的抗氧化系统或直接清除活性氧,另一方面是通过影响植物对重金属的吸收以及重金属在植物细胞内的分布。然而内源NO在调节植物重金属胁迫抗性上的功能角色仍存在争议。有些研究表明内源NO是有益的,能够缓解重金属胁迫诱导的毒性;但是也有证据表明内源NO是有害的,能够通过促进植物对重金属的吸收以及对植物螯合素进行S-亚硝基化弱化其解毒功能,从而参与重金属诱导的毒害反应和细胞凋亡过程。     

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.     

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。     

Regulation of physiological aspects in plants by hydrogen sulfide and nitric oxide under challenging environment

Plants are exposed to a plethora of abiotic stresses such as drought, salinity, heavy metal and temperature stresses at different stages of their life cycle, from germination to seedling till the reproductive phase. As protective mechanisms, plants release signaling molecules that initiate a cascade of stress-signaling events, leading either to programmed cell death or plant acclimation. Hydrogen sulfide (H₂S) and nitric oxide (NO) are considered as new ‘gasotransmitter’ molecules that play key roles in regulating gene expression, posttranslational modification (PTM), as well as cross-talk with other hormones. Although the exact role of NO in plants remains unclear and is species dependent, various studies have suggested a positive correlation between NO accumulation and environmental stress in plants. These molecules are also involved in a large array of stress responses and act synergistically or antagonistically as signaling components, depending on their respective concentration. This study provides a comprehensive update on the signaling interplay between H₂S and NO in the regulation of various physiological processes under multiple abiotic stresses, modes of action and effects of exogenous application of these two molecules under drought, salt, heat and heavy metal stresses. However, the complete picture of the signaling cascades mediated by H₂S and NO is still elusive. Recent researches indicate that during certain plant processes, such as stomatal closure, H₂S could act upstream of NO signaling or downstream of NO in response to abiotic stresses by improving antioxidant activity in most plant species. In addition, PTMs of antioxidative pathways by these two molecules are also discussed.     

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。     

Nitric oxide and hydrogen sulfide crosstalk during heavy metal stress in plants

Gases such as ethylene, hydrogen peroxide (H₂O₂), nitric oxide (NO), carbon monoxide (CO) and hydrogen sulfide (H₂S) have been recognized as vital signaling molecules in plants and animals. Of these gasotransmitters, NO and H₂S have recently gained momentum mainly because of their involvement in numerous cellular processes. It is therefore important to study their various attributes including their biosynthetic and signaling pathways. The present review provides an insight into various routes for the biosynthesis of NO and H₂S as well as their signaling role in plant cells under different conditions, more particularly under heavy metal stress. Their beneficial roles in the plant's protection against abiotic and biotic stresses as well as their adverse effects have been addressed. This review describes how H₂S and NO, being very small-sized molecules, can quickly pass through the cell membranes and trigger a multitude of responses to various factors, notably to various stress conditions such as drought, heat, osmotic, heavy metal and multiple biotic stresses. The versatile interactions between H₂S and NO involved in the different molecular pathways have been discussed. In addition to the signaling role of H₂S and NO, their direct role in posttranslational modifications is also considered. The information provided here will be helpful to better understand the multifaceted roles of H₂S and NO in plants, particularly under stress conditions.     

Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants

Nitric oxide (NO) acts in a concentration and redox-dependent manner to counteract oxidative stress either by directly acting as an antioxidant through scavenging reactive oxygen species (ROS), such as superoxide anions (O₂^?*), to form peroxynitrite (ONOO^?) or by acting as a signaling molecule, thereby altering gene expression. NO can interact with different metal centres in proteins, such as heme-iron, zinc–sulfur clusters, iron–sulfur clusters, and copper, resulting in the formation of a stable metal–nitrosyl complex or production of varied biochemical signals, which ultimately leads to modification of protein structure/function. The thiols (ferrous iron–thiol complex and nitrosothiols) are also involved in the metabolism and mobilization of NO. Thiols bind to NO and transport it to the site of action whereas nitrosothiols release NO after intercellular diffusion and uptake into the target cells. S-nitrosoglutathione (GSNO) also has the ability to transnitrosylate proteins. It is an NO˙ reservoir and a long-distance signaling molecule. Tyrosine nitration of proteins has been suggested as a biomarker of nitrosative stress as it can lead to either activation or inhibition of target proteins. The exact molecular mechanism(s) by which exogenous and endogenously generated NO (or reactive nitrogen species) modulate the induction of various genes affecting redox homeostasis, are being extensively investigated currently by various research groups. Present review provides an in-depth analysis of the mechanisms by which NO interacts with and modulates the activity of various ROS scavenging enzymes, particularly accompanying ROS generation in plants in response to varied abiotic stress.     

铜、镉胁迫下外源NO介导的番茄解毒途径

一氧化氮(NO)作为信号分子,在抵御重金属胁迫中起重要作用,但对不同离子胁迫下的解毒机制尚缺乏研究.本研究采用营养液培养法,研究了铜(Cu)、镉(Cd)单一或复合胁迫下,番茄幼苗对Cu、Cd的吸收转运特性及对外源NO的响应机制.结果表明: 50 μmol·L^-1的Cu²⁺、Cd²⁺均显著抑制番茄植株的生长,其中Cd胁迫对生长的抑制效应远高于Cu胁迫.Cu、Cd单一或复合胁迫均使番茄根系Cu、Cd含量显著升高,但根系对Cu、Cd吸收存在严格选择性.根细胞对必需元素Cu表现出“奢侈吸收”的现象,而对毒性较强的Cd则吸收相对较少,胞内Cd浓度仅为Cu的1/10左右.外源NO处理可不同程度地缓解Cu、Cd胁迫,其中缓解Cd胁迫的效能更强.番茄对被动进入细胞的Cu、Cd具有相似的解毒机制:一方面,Cu、Cd胁迫诱导细胞质中产生谷胱甘肽(GSH)、植物螯合肽(PCs)和金属硫蛋白(MTs),络合过多的Cu、Cd离子,降低其生物毒性;另一方面,过多的Cu、Cd离子或螯合物被转运至液泡区隔化.外源NO通过调控GSH-GSSG(氧化型谷胱甘肽)氧化还原状态及GSH-PCs代谢方向的改变,促进Cu、Cd离子转运至液泡区隔化来缓解胁迫抑制;NO还可诱导植株叶片或根系表达更多的金属硫蛋白、GSH和PCs,而且上述响应普遍存在叠加效应.这可能是NO介导番茄对Cu、Cd胁迫的另一主要解毒途径.     

Nitric Oxide Alleviates Photochemical Damage Induced by Cadmium Stress in Pea Seedlings

Cadmium (Cd), a life threatening hazardous heavy metal is abundant in nature. Cd amounts are greater in leaves than other plant parts, and it shows considerable effects on photosynthesis. Nitric oxide (NO), a free radical present in living organisms, is now known as an important signaling molecule playing various physiological processes in plants. In this study, the possible ameliorative effect of NO on photosynthesis was examined on pea seedlings grown under Cd stress. Results showed that chlorophyll, net photosynthetic rate, transpiration rate, stomatal conductance, photochemical efficiency of Photosystem II and Photosystem I decreased, and Fo and non-photochemical parameters for PSII and PSI significantly increased due to Cd stress. This suggests that Cd affects the photochemistry efficiency at both the PSII and PSI levels. Nitric oxide supplementation through SNP ameliorated Cd stress by enhancing all the above mentioned parameters but causing a reduction in the Fo, and non-photochemical parameters of PSII and PSI in pea plants. These data indicate that the exogenous application of NO was useful in mitigating Cd-induced damage to photosynthesis in pea seedling.     

Nano carriers for nitric oxide delivery and its potential applications in plant physiological process: A mini review

Nitric oxide (NO) plays a key role in plant growth and defense. Since NO is a small molecule, devoid of charge and relatively lipophilic, it easily crosses cell membranes, acting as an important signaling messenger. Recently, several papers described the beneficial effects due to application of small molecular weight NO donors in plants. Exogenous NO donors break seed dormancy, stimulate plant germination and greening, control iron homeostasis in plants, and improve plant tolerance to salinity, metal toxicity, temperature and drought stress. However, these NO donors are thermally and photochemically unstable. A promising strategy that has been successfully used in biomedical applications is the combination of NO donors with nanomaterials. The encapsulation of NO donors in nanoparticles/nanotubes is able to control the release of therapeutic amounts of NO, thus improving its beneficial effects. Although nanomaterials have been used successfully to carry agrochemicals in plants, the delivery of NO is still to be studied. In this context, the present review highlights the advantages of applications of NO donors in plants, the uses of nanotechnology in agriculture, and the necessity to develop new strategies based on the combination of NO and nanomaterials in agriculture. Therefore, this review hopes to open up new perspectives in the area of nanobiotechnology, NO and agriculture.     

NO says more than ‘YES’ to salt tolerance: Salt priming and systemic nitric oxide signaling in plants

Nitric oxide (NO) is now recognized as an important signaling molecule and there has been an increasing bulk of studies regarding the various functions of NO in plants exposed to environmental stimulus. There is also emerging evidence, although not extensive, that NO plays systemic signaling roles during the establishment of salt tolerance in many plant species. In this mini-review, we highlight several candidate mechanisms as being functional in this NO systemic signaling action. In addition, we outline data supporting that plants possess prime-like mechanisms that allow them to memorize previous NO exposure events and generate defense responses following salt stress.Key words: nitric oxide, nitrosative stress, priming, salinity, systemic signaling     

Interactions between nitric oxide and plant hormones in aluminum tolerance

Nitric oxide (NO) is involved, together with plant hormones, in the adaptation to Al stress in plants. However, the mechanism by which NO and plant hormones interplay to improve Al tolerance are still unclear. We have recently shown that patterns of plant hormones alteration differ between rye and wheat under Al stress. NO may enhance Al tolerance by regulating hormonal equilibrium in plants, as a regulator of plant hormones signaling. In this paper, some unsolved issues are discussed based on recent studies and the complex network of NO and plant hormones in inducing Al tolerance of plants are proposed.     

植物MPK信号通路与信号分子H2O2和NO之间的相互关系

促分裂原活化蛋白激酶(MPK)级联途径是真核细胞中普遍存在且保守的信号传导通路,广泛参与植物生长发育和植物抵抗生物和非生物胁迫的防御反应。过氧化氢(H2O2)和一氧化氮(NO)作为重要的信使分子也广泛参与植物生长发育和防御反应的信号传导。近年来,研究也表明MPK信号通路与信号分子H2O2和NO之间存在着多种复杂的关系。一方面,在一些刺激的信号传递过程中,MPK信号通路参与了信号分子H2O2和NO的产生、清除或其信号的向下传递等过程;另一方面,在有些刺激的信号传递过程中,它们位于不同的信号传递途经中,行使不同的功能。本文就目前植物MPK信号通路与H2O2和NO之间相互关系的研究现状进行了综述和分析,并指出了该研究领域存在的问题。     

Nitric Oxide Modulates the Expression of Proteins and Promotes Epiphyllous Bud Differentiation in Kalanchoe pinnata

Nitric oxide (NO), a recent addition to the signaling molecules in plants, plays an important role in mediating both biotic and abiotic stress responses. The occurrence of reproductive/vegetative structures, known as epiphylly, on the surface of leaves is a stress survival mechanism exhibited by some plants, including Kalanchoe pinnata. In the present study the role of NO during epiphyllous bud differentiation was investigated. NO donors l-arginine, NaNO₂, and SNP promoted epiphyllous bud differentiation in a dose-dependent manner, whereas NO inhibitors reversed the effect, suggesting the involvement of NO in the process. Albeit numerous physiological processes are reported to be modulated by NO, but their correlation with NO-responsive genes and proteins needs to be established. To address this issue, NO-responsive proteins (NORPs) were identified using 2D-PAGE and MS analysis. Major NORPs that were identified belonged to photosynthesis, oxidative phosphorylation, signaling, and stress metabolism, aptly indicating their probable role in this stress-induced growth process. The present study clearly indicates the role of NO in this stress survival mechanism, thus strongly affirming its role in stress responses.     

H2S与Ca^2＋协同增强谷子对Cr^6＋胁迫的耐受

继一氧化氮（NO）和一氧化碳（CO）之后,第三种气体信号分子硫化氢（H2S）对植物体生长发育和环境胁迫应答的调控正在受到越来越多的关注。钙离子（Ca2＋）是重要的第二信使,参与植物对多种胁迫的响应。该实验以谷子这种抗逆性较强的作物为材料,对其响应六价铬（Cr6＋）胁迫过程中H2S和Ca2＋45号的互作进行了研究。结果表明,Cr6＋胁迫显著激活谷子幼苗的H2s产生系统,外源H2S预处理能明显降低Cr6＋胁迫对谷子根尖细胞的损伤,而H2S的合成抑制剂羟胺（HA）预处理,使得Cr6＋对谷子的毒害增强;进一步实验发现,H2S能激活Ca2＋信号下游相关基因的表达,同时Ca＋能增强H2S的产生,表明在植物体内H2S和Ca＋信号存在复杂的联系。该研究也证明,H2S和ca2＋可以通过调节重金属离子转运蛋白增强谷子对Cr6＋的耐受。     

Metabolic and Physiological Changes Induced by Nitric Oxide and Its Impact on Drought Tolerance in Soybean

Nitric oxide (NO) is an important signaling molecule that plays a pivotal role in stress tolerance. To study the role of NO in drought tolerance and elucidate the underlying mechanisms, NO (0 and 100 μM) was applied to drought-treated soybean plants. Drought stress was imposed by PEG (5% (W/V) of PEG 6000. Nitric oxide improved growth of soybean plants under drought as evidenced by enhanced dry weight (30%). Nitric oxide caused a remarkable increase in activities of catalase and superoxide dismutase (SOD) and SOD expression (14.8-fold), which led to a significant decline in malondealdehyde content under drought conditions. Nitric oxide induced proline biosynthesis due to enhancing pyrroline-5- carboxylate synthetase (P5CS) expression (43.66-fold). The growth-promoting effect of NO application in soybean plants was concomitant with change in metabolic profile (phenolic acid and flavonoid compounds). Nitric oxide up-regulated of phenylalanine ammonia-lyase (PAL) expression in drought-treated plants and may influence on the phenylpropanoid production. Nitric oxide increased salicylic acid (SA) content in soybean plants under stress. So, NO and SA are jointly responsible for boosted tolerance to drought stress in soybean plants. The decrease in unsaturated fatty acid through NO application might reflect a reduction in oxidative damage. These results propose a multifaceted contribution of NO through regulation of physiological and metabolic processes in response to drought stress.

     

Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings

Salicylic acid (SA) and nitric oxide (NO) are reported to alleviate the damaging effects of stress in plants rather similarly when applied at appropriate low concentrations. An experiment was therefore conducted to study the impact of SA, sodium nitroprusside (SNP; as NO donor), and methylene blue (MB; as a guanylate cyclase inhibitor) on wheat seedling performance under osmotic stress. Osmotic stress significantly reduced shoot fresh weight (SFW), chlorophyll contents (Chla, Chlb, total Chl), and membrane stability index (MSI) and also increased malondialdehyde (MDA) level, lipoxygenase (LOX) activity, and hydrogen peroxide production. Moreover, enzymatic antioxidant activities including superoxide dismutase, guaiacol peroxidase, and glutathione reductase activity were enhanced under osmotic stress. On the contrary, SA or SNP pretreatment reduced the damaging effects of osmotic stress by further enhancing the antioxidant activities that led to increased SFW, Chl, and MSI and reduced MDA level and LOX activity. However, pretreatment of plants with MB reversed or reduced the protective effects of SA and SNP suggesting that the protective effects were likely attributed to NO signaling. Therefore, NO may act as downstream of SA signaling in reduction of induced oxidative damage in wheat seedlings.     

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.     

Revealing on hydrogen sulfide and nitric oxide signals co-ordination for plant growth under stress conditions

In the recent times, plants are facing certain types of environmental stresses, which give rise to formation of reactive oxygen species (ROS) such as hydroxyl radicals, hydrogen peroxides, superoxide anions and so on. These are required by the plants at low concentrations for signal transduction and at high concentrations, they repress plant root growth. Apart from the ROS activities, hydrogen sulfide (H₂S) and nitric oxide (NO) have major contributions in regulating growth and developmental processes in plants, as they also play key roles as signaling molecules and act as chief plant immune defense mechanisms against various biotic as well as abiotic stresses. H₂S and NO are the two pivotal gaseous messengers involved in growth, germination and improved tolerance in plants under stressed and non-stress conditions. H₂S and NO mediate cell signaling in plants as a response to several abiotic stresses like temperature, heavy metal exposure, water and salinity. They alter gene expression levels to induce the synthesis of antioxidant enzymes, osmolytes and also trigger their interactions with each other. However, research has been limited to only cross adaptations and signal transductions. Understanding the change and mechanism of H₂S and NO mediated cell signaling will broaden our knowledge on the various biochemical changes that occur in plant cells related to different stresses. A clear understanding of these molecules in various environmental stresses would help to confer biotechnological applications to protect plants against abiotic stresses and to improve crop productivity.     

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。