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.     

Overexpression of an Arabidopsis magnesium transport gene, AtMGT1, in Nicotiana benthamiana confers Al tolerance

Aluminium (Al) toxicity is the most important limiting factor for crop production in acid soil environments worldwide. In some plant species, application of magnesium (Mg(2+)) can alleviate Al toxicity. However, it remains unknown whether overexpression of magnesium transport proteins can improve Al tolerance. Here, the role of AtMGT1, a member of the Arabidopsis magnesium transport family involved in Mg(2+) transport, played in Al tolerance in higher plants was investigated. Expression of 35S::AtMGT1 led to various phenotypic alterations in Nicotiana benthamiana plants. Transgenic plants harbouring 35S::AtMGT1 exhibited tolerance to Mg(2+) deficiency. Element assay showed that the contents of Mg, Mn, and Fe in 35S::AtMGT1 plants increased compared with wild-type plants. Root growth experiment revealed that 100 microM AlCl(3) caused a reduction in root elongation by 47% in transgenic lines, whereas root growth in wild-type plants was inhibited completely. Upon Al treatment, representative transgenic lines also showed a much lower callose deposition, an indicator of increased Al tolerance, than wild-type plants. Taken together, the results have demonstrated that overexpression of ATMGT1 encoding a magnesium transport protein can improve tolerance to Al in higher plants.     

Nitric oxide enhances aluminum tolerance by affecting cell wall polysaccharides in rice roots

Nitric oxide (NO) is a key signal molecule involved in many physiological processes in plants. To study the mechanisms of exogenous NO contribution to alleviate the aluminum (Al) toxicity, roots of rice (Oryza sativa) seedlings pre-treated with sodium nitroprusside (SNP, a NO donor) were used to investigate the effect of Al in this study. Results indicated that NO alleviated the lipid peroxidation induced by Al and promoted the root elongation, whereas butylated hydroxyanisole (BHA), an efficient lipophilic antioxidant, alleviated the lipid peroxidation only. Rice seedling roots pre-treated with SNP followed by Al treatment had lower contents of pectin and hemicellulose, lower Al accumulation in root tips and cell walls, higher degree of methylation of pectin and lower wall Al-binding capacity than the roots with Al treatment only. Therefore, the decreased Al accumulation in the cell walls of rice roots is likely to be the reason for the NO-induced increase of Al tolerance in rice, and it seems that exogenous NO enhanced Al tolerance in rice roots by decreasing the contents of pectin and hemicellulose, increasing the degree of methylation of pectin, and decreasing Al accumulation in root cell walls.     

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.     

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。     

The combined treatment of Mn and Al alleviates the toxicity of Al or Mn stress alone in barley

Aluminum (Al) and manganese (Mn) toxicity commonly coexists in acid soil, so the crop cultivars suitable for planting in acid soil should show high tolerance to both elements simultaneously. However, it is still not clear if the toxicity of Mn and Al on plant growth is antagonistic or synergistic, and the plants with Al tolerance are also tolerant to Mn toxicity. In this study, three barley genotypes (one Tibetan wild and two cultivated), differing in Al tolerance, were characterized for growth and physiological responses to Al or Mn toxicity as well as the combined treatment of the two toxic elements. Interestingly, it has been found that the combined treatment of both metals was less affected in comparison with Al or Mn treatment alone, in terms of plant growth, Al or Mn concentration in plant tissues, and photosynthetic parameters, indicating antagonistic interaction of Al and Mn for their effect on plant growth and physiological traits. The results also showed that there was a dramatic difference among barley genotypes in Mn toxicity tolerance and XZ16 showed much higher tolerance than other two genotypes. High Mn tolerance is mainly described to less Mn uptake and lower Mn concentration in plants, and Mn tolerance is independent of Al tolerance.     

Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos

Aluminum (Al) is toxic to plants when solubilized into Al(3+) in acidic soils, and becomes a major factor limiting plant growth. However, the primary cause for Al toxicity remains unknown. Nitric oxide (NO) is an important signaling molecule modulating numerous physiological processes in plants. Here, we investigated the role of NO in Al toxicity to Hibiscus moscheutos. Exposure of H. moscheutos to Al(3+) led to a rapid inhibition of root elongation, and the inhibitory effect was alleviated by NO donor sodium nitroprusside (SNP). NO scavenger and inhibitors of NO synthase (NOS) and nitrate reductase had a similar inhibitory effect on root elongation. The inhibition of root elongation by these treatments was ameliorated by SNP. Aluminum inhibited activity of NOS and reduced endogenous NO concentrations. The alleviation of inhibition of root elongation induced by Al, NO scavenger and NOS inhibitor was correlated with endogenous NO concentrations in root apical cells, suggesting that reduction of endogenous NO concentrations resulting from inhibition of NOS activity could underpin Al-induced arrest of root elongation in H. moscheutos.     

Ced-9 inhibits Al-induced programmed cell death and promotes Al tolerance in tobacco

Our previous data showed that apoptotic suppressors inhibit aluminum (Al)-induced programmed cell death (PCD) and promote Al tolerance in yeast cells, however, very little is known about the underlying mechanisms, especially in plants. Here, we show that the Caenorhabditis elegans apoptotic suppressor Ced-9, a Bcl-2 homologue, inhibited both the Al-induced PCD and Al-induced activity of caspase-like vacuolar processing enzyme (VPE), a crucial executioner of PCD, in tobacco. Furthermore, we show that Ced-9 significantly alleviated Al inhibition of root elongation, decreased Al accumulation in the root tip and greatly inhibited Al-induced gene expression in early response to Al, leading to enhancing the tolerance of tobacco plants to Al toxicity. Our data suggest that Ced-9 promotes Al tolerance in plants via inhibition of Al-induced PCD, indicating that conserved negative regulators of PCD are involved in integrated regulation of cell survival and Al-induced PCD by an unidentified mechanism.     

低磷和铝毒胁迫条件下菜豆有机酸的分泌与累积

以水培方式研究了低磷、铝毒胁迫条件下,不同菜豆基因型根系有机酸的分泌及其在植穆不同部位的累积,结果表明,低磷,铝毒胁迫诱导菜豆有机酸的分泌与累积存在显著的基因差异。低磷、铝毒胁迫诱导菜豆主要分泌柠檬酸、酒石酸和乙酸,其中,50μmol/LAl^3 诱导柠檬酸分泌量最高;低磷（小于20μmol/LH2PO4^－）胁迫诱导柠榨菜酸分泌量显著高于高磷处理,但低磷处理之间差异不明显,铝毒胁迫诱导菜豆有机酸的分泌与累积显著高于低磷胁迫处理,低磷,铝毒胁迫植株不同部位有机酸的含量为叶片大小根系,低磷,铝毒胁迫时,G842菜豆型柠檬酸有机酸分泌总量显著高于273、AFR和ZPV,其干重和磷吸收明明显于大G273,AFR和ZPV,且铝吸收量小于G273,AFR和ZPV,说明,G482菜豆基因型对低磷,铝毒的适应能力强于G273,AFR和ZPV基因型,菜豆有机酸,,尤其柠檬酸的分泌是其适应低磷、铝毒胁迫的重要生理反应。     

Molecular and physiological strategies to increase aluminum resistance in plants

Aluminum (Al) toxicity is a primary limitation to plant growth on acid soils. Root meristems are the first site for toxic Al accumulation, and therefore inhibition of root elongation is the most evident physiological manifestation of Al toxicity. Plants may resist Al toxicity by avoidance (Al exclusion) and/or tolerance mechanisms (detoxification of Al inside the cells). The Al exclusion involves the exudation of organic acid anions from the root apices, whereas tolerance mechanisms comprise internal Al detoxification by organic acid anions and enhanced scavenging of free oxygen radicals. One of the most important advances in understanding the molecular events associated with the Al exclusion mechanism was the identification of the ALMT1 gene (Al-activated malate transporter) in Triticum aestivum root cells, which codes for a plasma membrane anion channel that allows efflux of organic acid anions, such as malate, citrate or oxalate. On the other hand, the scavenging of free radicals is dependent on the expression of genes involved in antioxidant defenses, such as peroxidases (e.g. in Arabidopsis thaliana and Nicotiana tabacum), catalases (e.g. in Capsicum annuum), and the gene WMnSOD1 from T. aestivum. However, other recent findings show that reactive oxygen species (ROS) induced stress may be due to acidic (low pH) conditions rather than to Al stress. In this review, we summarize recent findings regarding molecular and physiological mechanisms of Al toxicity and resistance in higher plants. Advances have been made in understanding some of the underlying strategies that plants use to cope with Al toxicity. Furthermore, we discuss the physiological and molecular responses to Al toxicity, including genes involved in Al resistance that have been identified and characterized in several plant species. The better understanding of these strategies and mechanisms is essential for improving plant performance in acidic, Al-toxic soils.     

High level of reduced glutathione contributes to detoxification of lipid peroxide‐derived reactive carbonyl species in transgenic Arabidopsis overexpressing glutathione reductase under aluminum stress

Lipid peroxide‐derived reactive carbonyl species (RCS), generated downstream of reactive oxygen species (ROS), are critical damage‐inducing species in plant aluminum (Al) toxicity. In mammals, RCS are scavenged primarily by glutathione (reduced form of glutathione, GSH), but in plant Al stress, contribution of GSH to RCS detoxification has not been evaluated. In this study, Arabidopsis plants overexpressing the gene AtGR1 (accession code At3g24170), encoding glutathione reductase (GR), were generated, and their performance under Al stress was examined. These transgenic plants (GR‐OE plants) showed higher GSH levels and GSH/GSSG (oxidized form of GSH) ratio, and an improved Al tolerance as they suffered less inhibition of root growth than wild‐type under Al stress. Exogenous application of 4‐hydroxy‐2‐nonenal, an RCS responsible for Al toxicity in roots, markedly inhibited root growth in wild‐type plants. GR‐OE plants suffered significantly smaller inhibition, indicating that the enhanced GSH level increased the capacity of RCS detoxification. The generation of H₂O₂ due to Al stress in GR‐OE plants was lower by 26% than in wild‐type. Levels of various RCS, such as malondialdehyde, butyraldehyde, phenylacetaldehyde, (E)‐2‐heptenal and n‐octanal, were suppressed by more than 50%. These results indicate that high levels of GSH and GSH/GSSG ratio by GR overexpression contributed to the suppression of not only ROS, but also RCS. Thus, the maintenance of GSH level by overexpressing GR reinforces dual detoxification functions in plants and is an efficient approach to enhance Al tolerance.     

Toxicity and tolerance of aluminum in plants: tailoring plants to suit to acid soils

Aluminum (Al) stress is one of the serious limiting factors in plant productivity in acidic soils, which constitute about 50 % of the world’s potentially arable lands and causes anywhere between 25 and 80 % of yield losses depending upon the species. The mechanism of Al toxicity and tolerance has been examined in plants, which is vital for crop improvement and enhanced food production in the future. Two mechanisms that facilitate Al tolerance in plants are Al exclusion from the roots and the ability to tolerate Al in the symplast or both. Although efforts have been made to unravel Al-resistant factors, many aspects remain unclear. Certain gene families such as MATE, ALMT, ASR, and ABC transporters have been implicated in some plants for resistance to Al which would enhance the opportunities for creating crop plants suitable to grow in acidic soils. Though QTLs have been identified related to Al-tolerance, no crop plant that is tolerant to Al has been evolved so far using breeding or molecular approaches. The remarkable changes that plants experience at the physiological, biochemical and molecular level under Al stress, the vast array of genes involved in Al toxicity-tolerance, the underlying signaling events and the holistic image of the molecular regulation, and the possibility of creating transgenics for Al tolerance are discussed in this review.     

Involvement of putrescine and nitric oxide in aluminum tolerance by modulating citrate secretion from roots of red kidney bean

Background and Aims

Polyamines and nitric oxide (NO) are two important molecules modulating numerous environment stresses in plants. This study was to investigate the roles of polyamines and NO in aluminum (Al) tolerance in red kidney bean.

Methods

The interaction between putrescine (Put) and NO under Al stress was examined. NO donor and scavenger were used to further examine the role of NO in Al-induced citrate secretion from roots by high performance liquid chromatography.

Results

Al stress caused increase of endogenous free Put, and exogenous Put alleviated Al-induced inhibition of root elongation and Al accumulation. In addition, Put induced NO production and nitrate reductase (NR) activity under Al stress. Al- and Put-induced NO production could be reversed by NR inhibitor. Furthermore, Al stress stimulated citrate secretion from roots, and this response was stimulated by NO donor, whereas NO scavenger inhibited Al-induced citrate secretion from roots. Concomitantly, NO donor reduced Al accumulation in root apexes, while NO scavenger further enhanced Al accumulation. Al-induced inhibition of root growth was significantly improved by exogenous citrate treatment.

Conclusions

Put and NO enhanced Al tolerance by modulating citrate secretion from roots, and NO may act downstream of Put in red kidney bean under Al stress.     

Organic acid anions:An effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils

Aluminum(Al) toxicity and phosphorous(P) deficiency are two major limiting factors for plant growth on acidic soils.Thus,the physiological mechanisms for Al tolerance and P acquisition have been intensively studied.A commonly observed trait is that plants have developed the ability to utilize organic acid anions(OAs;mainly malate,citrate and oxalate) to combat Al toxicity and P deficiency.OAs secreted by roots into the rhizosphere can externally chelate Al~(3+) and mobilize phosphate(Pi),while OAs synthesized in the cell can internally sequester Al~(3+) into the vacuole and release free Pi for metabolism.Molecular mechanisms involved in OA synthesis and transport have been described in detail.Ensuing genetic improvement for Al tolerance and P efficiency through increased OA exudation and/or synthesis in crops has been achieved by transgenic and marker-assisted breeding.This review mainly elucidates the crucial roles of OAs in plant Al tolerance and P efficiency through summarizing associated physiological mechanisms,molecular traits and genetic manipulation of crops.     

Overexpression of <Emphasis Type="Italic">Citrus junos</Emphasis> mitochondrial citrate synthase gene in <Emphasis Type="Italic">Nicotiana benthamiana</Emphasis> confers aluminum tolerance

Aluminum (Al) toxicity is one of the major factors that limit plant growth in acid soils. Al-induced release of organic acids into rhizosphere from the root apex has been identified as a major Al-tolerance mechanism in many plant species. In this study, Al tolerance of Yuzu (Citrus Junos Sieb. ex Tanaka) was tested on the basis of root elongation and the results demonstrated that Yuzu was Al tolerant compared with other plant species. Exposure to Al triggered the exudation of citrate from the Yuzu root. Thus, the mechanism of Al tolerance in Yuzu involved an Al-inducible increase in citrate release. Aluminum also elicited an increase of citrate content and increased the expression level of mitochondrial citrate synthase (CjCS) gene and enzyme activity in Yuzu. The CjCS gene was cloned from Yuzu and overexpressed in Nicotiana benthamiana using Agrobacterium tumefaciens-mediated methods. Increased expression level of the CjCS gene and enhanced enzyme activity were observed in transgenic plants compared with the wild-type plants. Root growth experiments showed that transgenic plants have enhanced levels of Al tolerance. The transgenic Nicotiana plants showed increased levels of citrate in roots compared to wild-type plants. The exudation of citrate from roots of the transgenic plants significantly increased when exposed to Al. The results with transgenic plants suggest that overexpression of mitochondrial CS can be a useful tool to achieve Al tolerance.     

拟南芥COPT家族蛋白研究进展

铜(Cu)是植物必需的微量元素, 作为多种酶的辅因子参与许多植物生理生化反应。Cu缺乏和过量均影响植物正常生长发育, 因此植物进化出精妙复杂的调控网络来严格控制植物体内的Cu含量。植物Cu转运蛋白COPT家族成员与Cu有很高的亲和力, 能够调节植物对Cu的吸收和转运, 在维持植物体内Cu稳态平衡过程中发挥重要作用。COPT蛋白涉及不同的Cu转运功能, 如从外界环境中摄取Cu、从细胞器中输出Cu、长距离运输Cu以及在不同器官间动用和再分配Cu。此外, COPT蛋白在其它离子的稳态平衡维持、昼夜节律性生物钟调控、植物激素合成和植物对激素信号的感受过程中也发挥重要作用。该文综述了模式植物拟南芥(Arabidopsis thaliana) COPT家族各成员的表达和定位、调控机制以及生物学功能等方面的最新进展。     

拟南芥COPT家族蛋白研究进展

铜(Cu)是植物必需的微量元素, 作为多种酶的辅因子参与许多植物生理生化反应。Cu缺乏和过量均影响植物正常生长发育, 因此植物进化出精妙复杂的调控网络来严格控制植物体内的Cu含量。植物Cu转运蛋白COPT家族成员与Cu有很高的亲和力, 能够调节植物对Cu的吸收和转运, 在维持植物体内Cu稳态平衡过程中发挥重要作用。COPT蛋白涉及不同的Cu转运功能, 如从外界环境中摄取Cu、从细胞器中输出Cu、长距离运输Cu以及在不同器官间动用和再分配Cu。此外, COPT蛋白在其它离子的稳态平衡维持、昼夜节律性生物钟调控、植物激素合成和植物对激素信号的感受过程中也发挥重要作用。该文综述了模式植物拟南芥(Arabidopsis thaliana) COPT家族各成员的表达和定位、调控机制以及生物学功能等方面的最新进展。