Effects of BRs on plants subjected to salt stress Dashes indicate that there are no results in study.
Abstract
This chapter covers the advances in establishment and optimization of brassinosteroids (BRs) in the alleviation of abiotic stresses such as water, salinity, temperature, and heavy metals in plant system, especially roots. Plant roots regulate their developmental and physiological processes in response to various internal and external stimuli. Studies are in progress to improve plant root adaptations to stress factors. BRs are a group of steroidal hormones that play important roles in a wide range of developmental phenomena, and recently they became an alleviation agent for stress tolerance in plants. This review is expected to provide a resource for researchers interested in abiotic stress alleviation with BRs.
Keywords
- Water stress
- salt stress
- temperature stress
- heavy metal stress
1. Introduction
Abiotic stress responses in plants occur at various organ levels among which the root-specific processes are of particular importance. Under normal growth condition, root absorbs water and nutrients from the soil and supplies them throughout the plant body, thereby playing pivotal roles in maintaining cellular homeostasis. However, this balanced system is altered during the stress period when roots are forced to adopt several structural and functional modifications. Examples of these modifications include molecular, cellular, and phenotypic changes such as alteration of metabolism and membrane characteristics, hardening of cell wall, and reduction of root length [1, 2]. The root system has the crucial role of extracting nutrients and water through a complex interplay with soil biogeochemical properties and of maintaining these functions under a wide range of stress scenarios to ensure plant survival and reproduction [3].
Water stress is characterized by a reduction of water content and leaf water potential, closure of stomata, and decreased growth. Severe water stress may result in the arrest of photosynthesis, disturbance of metabolism, and finally the death of plant [4]. This water loss causes a loss of turgor pressure that may be accompanied by a decrease in cell volume depending on the hardness of the cell wall [5]. The cells of the root must activate processes to limit water loss and mitigate its harmful effects.
Salinity also affects plant growth, activity of major cytosolic enzymes by disturbing intracellular potassium homeostasis, causing oxidative stress and programmed cell death, reducing nutrient uptake, genetic and epigenetic effects, metabolic toxicity, inhibition of photosynthesis, decreasing CO2 assimilation, and reducing root respiration [6, 7, 8, 9]. Salt stress affects the root in all developmental zones. Cell division decreases in the meristematic zone and cell expansion attenuates in the elongation zone, resulting in reduced overall growth [10]. Cells also expand radially in the elongation zone [11], and root hair outgrowth suppresses in the differentiation zone [12]. Salt stress additionally results in agravitropic growth [13] as well as reduced lateral root number under high-salt conditions and enhanced lateral root number under moderate-salt conditions [14, 15]. Salt stress developes from excessive concentrations of salt, especially sodium chloride (NaCl) in soil. Root is the primary organ of exposure and hence responds rapidly [16]. Salt stress is known to increase Na+/K+ ratio in the root that leads to cell dehydration and ion imbalance [17, 18, 19].
High temperature increases the permeability of plasma membrane [20], and also reduces water availability [21]. Moreover, low temperature (chilling and frost stress) is also a major limiting factor for productivity of plant indigenous to tropical and subtropical climates [22]. Chilling stress has a direct impact on the photosynthetic apparatus, essentially by disrupting the thylakoid electron transport, carbon reduction cycle, and stomatal control of CO2 supply, together with an increased accumulation of sugars, peroxidation of lipids, and disturbance of water balance [23].
Heavy metal contamination in soil could result in inhibition of plant growth and yield reduction and even poses a great threat to human health via food chain [24]. Among heavy metals, Cadmium (Cd) in particular causes increasingly international concern [25]. Cd-contaminated soil results in considerable accumulation of Cd in edible parts of crops, and then it enters the food chain through the translocation and accumulation by plants [26, 27]. Another metal, chromium (Cr III or VI), is not required by plants for their normal plant metabolic activities. On the contrary, excess of Cr (III or VI) in agricultural soils causes oxidative stress for many crops. Reactive oxygen species (ROS), like hydrogen peroxide (H2O2), hydroxyl radical (OH⋅), and superoxide radical (O2−) generated under Cr-stress, are highly reactive and cause oxidative damages to DNA, RNA, proteins, and pigments [28, 29]. Nickel (Ni) is one of the most abundant heavy metal contaminants of the environment due to its release from mining and smelting practices. It is classified as an essential element for plant growth [30]. However, at higher concentrations, nickel is an important environmental pollutant. Ni2+ ions bind to proteins and lipids such as specific subsequences of histones [31] and induce oxidative damage. Copper (Cu) is also an essential micronutrient for most biological organisms. It is a cofactor for a large array of proteins involved in diverse physiological processes, such as photosynthesis, electron transport chain, respiration, cell wall metabolism, and hormone signaling [32, 33]. Cu has emerged as a major environmental pollutant in the past few decades because of its excessive use in manufacturing and agricultural industries [34]. Zinc (Zn) is one of the other essential microelement, the second most abundant transition metal, and plays roles in many metabolic reactions in plants [35, 36]. However, high concentrations of Zn are toxic, induce structural disorders, and cause functional impairment in plants. At organism level, Zn stress reduces rooting capacity, stunted growth, chlorosis, and at cellular level alters mitotic activity [37, 38].
The key to find out abiotic stress tolerance resides in understanding the plant’s capacity to accelerate/maintain or repress growth. Most plant hormones play a role in development and have been implicated in abiotic stress responses. One of these hormones, BRs, are a group of steroidal hormones that play significant roles in a wide range of developmental phenomena including cell division and cell elongation in stems and roots, photo-morphogenesis, reproductive development, leaf senescence, and also in stress responses [39]. Mitchell et al. [40] discovered BRs which were later extracted from the pollen of
BRs increase adaptation to various abiotic stresses such as light [43, 44], low or high temperature [45], drought [46, 47, 48], salt stress [9], and heavy metal stress [49, 50]. BRs may be applied/supplied to plants at different stages of their life cycle such as meiosis stage [51], anthesis stage [52], and root application [9, 53].
In this chapter, the potential role of BRs in alleviating the adverse effects of water, salt, low/high temperature stresses, and heavy metals on plants, especially roots, were discussed.
2. Water stress
Water shortage is predicted as one of the most important environmental problem for the 21st century that limits crop production [54]. Although drought stress inhibites the plant–water relations, exogenous application of BRs maintaines tissue–water status [55] by stimulating the proton pumping [56], activating nucleic acid and protein synthesis [57] and regulation of genes expressions [58]. It has been shown that 24-epibrassinolide (24-epiBL)-treated
Root nodulation is a fundamental developmental event in leguminous crops, and is sensitive to water shortage [61, 62, 63]. As endogenous hormones play an important role in the organogenesis and initial growth of nodules in roots, attempts have been made to increase root nodulation by growth regulator treatments [64, 65]. The potential of BRs in the improvement of root nodulation and yield have been reported in groundnut [66]. Upreti and Murti [67] also studied the effects of two BRs, epibrassinolide (EBL) and homobrassinolide (HBL), on root nodulation and yield in
Several researchers have found that increased proline levels can protect plants from water stress. BR treatment increased the contents of proline and protein under water stress [68]. Zhang et al. [69] also indicated that BR treatment promoted the accumulation of osmoprotectants, such as soluble sugars and proline. It may be due to the fact that BRs activated the enzymes of proline biosynthesis, which caused an additive effect on the proline content [70].
Drought stress causes increment in H2O2 due to decrease in antioxidative enzyme activities [71]. Plants have improved various defense mechanisms to respond and adapt to water stress [72]. Vardhini et al. [73] studied with sorghum seedlings grown under PEG-imposed water stress and investigated the effects of HBL and 24-epiBL on the activities of four oxidizing enzymes: superoxide dismutase (SOD), glutathione reductase (GR), IAA oxidase, and polyphenol oxidase (PPO). They found that supplementation of both the BRs resulted in enhanced SOD and GR but lowered IAA oxidase and PPO. Li and Feng [68] also reported that treatment of brassinolide significantly increased peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX) activities of seedlings under normal water and mild water stress. Therefore, increment in enzyme activities provided tolerance of
3. Salt stress
Salinity stress is one of the most serious abiotic stress factors. It causes morphological, biochemical, cytogenetic, and molecular changes in plants [9, 76, 77, 78]. Root lengths, shoot lengths, and root numbers decrease in plants exposed to salt stress [7]. Moreover, salinity also induces oxidative stress in plants due to production ROS [79, 80]. These ROS are produced in the cell and interacted with a number of vital cellular molecules and metabolites, thereby leading to a number of destructive processes causing cellular damage [81].
BRs reduce impacts of salt stress on ROS, gene expression, mitotic index, nutrient uptake, and growth [9, 82, 83–88]. There are lots of studies to analyse alleviation of salt stress by using BRs. In these studies, different parameters have been investigated to understand the mechanism of BRs on salt stress (Table 1).
|
[9] | [84] | [85] | [86] | [87] | [88] |
|
--- | --- | --- | --- | Increased but reduced |
--- |
|
Increased | --- | Increased | --- | Increased | --- |
|
Increased SOD and CAT activities | Increased CAT, GR, POX and SOD activities | Increased POX and SOD activities | Increased SOD and POD activities | Showed varying results depending on 24-epiBL concentration for SOD, APX, CAT, GR |
Increased CAT, POX and SOD activities |
|
Increased | Increased | Increased | Increased | Increased | Increased |
|
Seeds were grown under both 150–250 mM salt concentrations and 0.5 and 1 µM HBR at 48 h and 72 h. | Plants received 100 mM NaCl as well as 0.01 µM of HBL during 18 days after sowing | 25, 50, 100, and 150 mM NaCl were applied and then sprayed twice with 0.05 ppm brassinolide during 25 days. At 45 days from sowing, the plants were collected | Seedlings were exposed to 90 mM NaCl with 0, 0.025, 0.05, 0.10, and 0.20 mg dm–3 24-epiBL for 10 days | Seeds were soaked for 8 h in different concentrations of 24-epiBL (10–11, 10-9 and 10–7 M). After 24-epiBL application, The seeds were sown in autoclaved sand moistened with different concentrations of NaCl (0, 75, 100, 125 mM) during 12 days | The 15-day-old plants were exposed to 100 mM NaCl and they were subsequently treated by exogenous 24-epiBL (10–8 M). The plants were harvested after 30 days of growth |
|
|
|
|
|
|
|
4. Temperature stress
4.1. High temperature
In general, a transient elevation in temperature (usually 10–15oC above environment) causes heat shock or heat stress [89]. High-temperature effects can be seen at the biochemical and molecular level in plant organs (especially leaves). Heat stress induces decrease in duration of developmental phases, leading to fewer organs, smaller organs, reduce light perception over the shortened life cycle, and finally play an important role in losing the product [90, 91, 92].
High-temperature stress often induces the overproduction of ROS [93] which can cause membrane lipid peroxidation, protein denaturation, and nucleic acid damage [94, 95]. Many studies have demonstrated that ROS scavenging mechanisms play an important role in protecting plants from high-temperature stress [96, 97]. BRs applications decrease ROS levels and increase antioxidant enzyme activities to provide thermotolerance to elevated temperatures [98].
4.2. Low temperature
Chilling and frost stresses affect growth, development, survival, and crop productivity in plants [99, 100, 101]. However, BRs treatments enhance seedling tolerance to chilling stress [101] and increase the height, root length, root biomass, and total biomass of rice under low-temperature conditions [102, 103]. In another study, Krishna [104] reported the same results in maize. They postulated that treatments with BRs promoted growth recovery of maize seedlings following chilling treatment (0–3°C).
Chilling stress increases the proline, betaine, soluble protein, soluble sugar contents of plants [79, 105]. Studies showed that BRs treatment enhanced proline content and therefore increased plant chilling resistance and cell membrane stability [99, 100, 106, 107].
Chilling stress could trigger the production of antioxidant enzymes in plants to prevent the chilling injury [108]. In the previous investigations, it was reported that treatment with BRs further increased the activities of antioxidant enzymes under chilling stress as well [99, 100, 107, 109]. The enhanced activities of the antioxidative enzymes as a result of BRs applications may occur with increasing de novo synthesis or activation of the enzymes, which is mediated through transcription and/or translation of specific genes to gain tolerance [57].
5. Heavy metal stresses
5.1. Cd stress
Cd toxicity has emerged as one of the major agricultural problems in many soils around the world [110]. It has been shown to interfere with the uptake, transport, and utilization of essential nutrients and water, change enzyme activities, cause symptoms (chlorosis, necrosis), decrease in fresh and dry mass of root and shoot and also their lengths [110, 111, 112].
There are lots of studies to investigate the effects of BRs on Cd stress in plant species [110, 113, 114]. In these studies, results showed that BRs change different parameters such as germination, plant dry biomass, protein content, and antioxidant enzyme activities (Table 2). It is proposed that the changes induced by BRs are mediated through the repression and/or de-repression of specific genes [58]. Microarray experiments evaluating gene expression changes in
5.2. Cr stress
Cr (III or VI) is not required by plants for their normal plant metabolic activities [117]. The entry of Cr into a plant system occurs through roots via using the specialized uptake systems of essential metal ions required for normal plant metabolism [118]. On the contrary, excess of Cr (III or VI) in agricultural soils causes oxidative stress to many crops. Reduced seed germination, disturbed nutrient balance, wilting, and plasmolysis in root cells and thus effects on root growth of plants have been documented in plants under Cr stress [118, 119].
Choudhary et al. [120] reported that EBL treatment improved seedlings growth under Cr (VI) stress. Ability of EBL to increase seedling growth under this metal stress could be attributed to the capacity of BRs to regulate cell elongation and divisional activities, by enhancing the activity of cell wall loosening enzymes (xyloglucan transferase/hydrolase, XTH) [121]. Studies also indicated that increment in antioxidant activities as a result of BRs application (Table 2) provide plant tolerance to grow under Cr stress.
5.3. Ni stress
The heavy metals that affect (either positively or negatively) plants include Fe, Cu, Zn, Mn, Co, Ni, Pb, Cd, and Cr, but out of them, nickel has recently been defined as an essential micronutrient, because of its involvement in urease activity in legumes [122]. Excess Ni causes different problems. These symptoms include the inhibition in root elongation, photosynthesis and respiration, and interveinal chlorosis [123]. Moreover, the toxic concentration of Ni also inhibits enzyme activities and protein metabolism [124]. This metal also accelerates the activities of antioxidative enzymes [125, 126].
BRs effect on Ni stress in plants has been studied to understand the relationship between BRs and this stress (Table 2). One of these studies was carried out by Yusuf et al. [49]. They showed that seed germination and seedling growth were significantly reduced by Ni treatment, but HBL treatment enhanced germination percentage as well as shoot and root lengths in Ni-stressed seedlings. BRs confer tolerance against heavy metals either by reducing their uptake or by stimulating the antioxidative enzymes in
5.4. Cu stress
Among the pollutants of agricultural soils, Cu has become increasingly hazardous due to its involvement in fungicides, fertilizers, and pesticides [130]. In addition, Cu present in excess has been known to decrease root biomass and alter plant metabolism [131, 132]. Sharma and Bhardwaj [127] demonstrated decrease in growth parameters of
Effects of exogenous application of BRs were studied on
5.5. Zn stress
Zn is an essential microelement, the second most abundant transition metal after iron (Fe), and has a role in many metabolic reactions in plants [35, 36]. However, high concentrations of Zn are toxic, induce structural disorders, and cause functional problems in plants. At organism level, Zn stress causes reduced rooting capacity, growth, and at cellular level alters mitotic activity [37, 38]. It induces oxidative stress by promoting ROS production as a result of indirect consequence of Zn toxicity [142].
Application of BRs on plants alleviates Zn stress via increasing protein content and antioxidant enzyme activities (Table 2). Çağ et al. [143] reported that EBL application effectively enhanced the protein content in
|
[114] | [146] | [30] | [147] | [141] | [145] |
|
--- | --- | --- | --- | --- | --- |
|
--- | Increased | Decreased protein content | --- | Showed varying results | --- |
|
Increased CAT, POX and SOD activities | Decreased CAT level | Decreased SOD but increased POD activities | Increased SOD, CAT and POX activities | Showed varying results | Increased |
|
Alleviated | Improved | Improved | Improved | Increased | Increased |
|
Soil amended with 50 µM Cd and foliage sprayed with 10-8 M HBL at 20 days after sowing. The plants were sampled at 30 days after sowing | Seeds were treated with eEBL (10-9 M) and 1.2 mM Cr(VI) (K2CrO4) solution at 7 days | Seeds were soaked for 8 h in different concentrations of 24-epiBL (0, 10-7, 10-9 and 10-11 M). Then, seeds were grown under different (0, 0.5, 1.0, 1.5, and 2.0 mM) Ni concentrations | Seeds were grown in different levels of Cu2+ (50 or 100 mg kg-1 of soil. At 15 and 20 days stage, 10-5 mM HBL was applied. At 45 days, plants were collected |
Seeds were grown under both 30 µM – 40 µM Cu and 2 µM HBR at 48 h and 72 h |
EBR (0.5, 1, and 2 µM) and 5 mM of Zn were applied to seeds. Seven day old seedlings were collected |
|
|
|
L. |
|
|
|
|
|
|
|
|
6. Conclusion
Roots are very important plant organs whose architecture is determined by endogenous and environmental conditions to adjust water and nutrient uptake from soil [148, 149]. BRs, one of the plant hormones, have both positive and negative effects on root growth related to hormone concentrations [150]. Experimental condition is one of the most important factors for analysing BRs effects on root development. The procedures using BRs to alleviate abiotic systems generally are easy, time saving, and one of the most reliable systems [53]. Therefore, BRs open up new approaches for plant tolerance against hazardous environmental conditions [151]. Morphological, biochemical, and molecular analyses have been performed to analyse the effects of BRs. However, detailed analyses should be performed to investigate the relationship between abiotic stresses and BRs, especially gene expression studies will provide knowledge about interaction at molecular level in plants [152]. We tried to cite as many papers as possible. Yet we apologize to authors whose works are gone unmentioned in this chapter.
Acknowledgments
We are grateful to the Research Fund of Istanbul University for financial support (Projects 39824, 43403, and UDP54481).
References
- 1.
Gowda VRP, Henry A, Yamauchi A, Shashidhar HE, Serraj R. Root biology and genetic improvement for drought avoidance in rice. Field Crops Res 2011;122:1–13. DOI: 10.1016/j.fcr.2011.03.001 - 2.
Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 2012; 63:3523–3543. DOI: 10.1093/jxb/ers100 - 3.
Ahmadi N, Audebert A, Bennett MJ. The roots of future rice harvests. Rice 2014;7:29. DOI: 10.1186/s12284-014-0029-y - 4.
Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R. Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloids Surfaces B: Biointerf 2008;61:298–303. DOI: 10.1016/j.colsurfb.2007.09.008 - 5.
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu, JK. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 2006;45:523–39. DOI: 10.1111/j.1365-313X.2005.02593.x - 6.
Abogadallah GM. Antioxidative defense under salt Stress. Plant Signal Behavior 2010;5:369-374. DOI: 10.4161/psb.5.4.10873 - 7.
Demirkiran A, Marakli S, Temel A, Gozukirmizi N. Genetic and epigenetic effects of salinity on in vitro growth of barley. Genet Molecul Biol 2013;36(4):566–70. DOI: 10.1590/S1415-47572013000400016 - 8.
Liu J, Gao H, Wang X, Zheng Q, Wang C, Wang X, Wang Q. Effects of 24-epibrassinolide on plant growth, osmotic regulation and ion homeostasis of salt stressed canola. Plant Biol 2014;16(2):440–50. DOI: 10.1111/plb.12052 - 9.
Marakli S, Temel A, Gozukirmizi N. Salt stress and homobrassinosteroid interactions during germination in barley roots. Not Bot Horti Agrobo 2014;42:446–52. DOI: 10.15835/nbha4229461 - 10.
West G, Inze D, Beemster GTS. Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 2004;135:1050–8. DOI: 10.1104/pp.104.040022 - 11.
Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inze D, Verbruggen N. Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana . Planta 2000;211:632–40. DOI: 10.1007/s004250000334 - 12.
Halperin SJ, Gilroy S, Lynch JP. Sodium chloride reduces growth and cytosolic calcium, but does not affect cytosolic pH, in root hairs of Arabidopsis thaliana L. J Exp Bot 2003;54:1269–80. DOI: 10.1093/jxb/erg134 - 13.
Sun F, Zhang W, Hu H, Li B, Wang Y, Zhao Y, Li K, Liu M, Li X. Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis . Plant Physiol 2008;146:178–188. DOI: 10.1104/pp.107.109413 - 14.
Wang Y, Li K, Li X. Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana . J Plant Physiol 2009;166:1637–45. DOI: doi:10.1016/j.jplph.2009.04.009 - 15.
Zolla G, Heimer YM, Barak S. Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J Exp Bot 2010;61:211–224. DOI: 10.1093/jxb/erp290 - 16.
Ghosh D, Xu J. Abiotic stress responses in plant roots: a proteomics perspective, Front Plant Sci 2014;5:6. DOI: 10.3389/fpls.2014.00006 - 17.
Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Annal Bot 2003;91:503–27. DOI: 10.1093/aob/mcg058 - 18.
Cavalcanti FR, Santos Lima JPM, Ferreira-Silva SL, Viegas RA, Silveira JAG, Roots and leaves display contrasting oxidative response during salt stress and recovery in cowpea. J Plant Physiol 2007;164:591–600. DOI: 10.1016/j.jplph.2006.03.004 - 19.
Munns R, Tester M. Mechanisms of salinity tolerance. Ann Rev Plant Biol 2008;59:651–81. DOI: 10.1146/annurev.arplant.59.032607.092911 - 20.
Zhang JH, Huang WD, Liu YP, Pan QH. Effects of temperature acclimation pretreatment on the ultrastructure of mesophyll cells in young grape plants ( Vitis vinifera L. cv. Jingxiu) under cross-temperature stresses. J Integrat Plant Biol 2005;47:959–70. DOI: 10.1111/j.1744-7909.2005.00109.x - 21.
Simoes-Araujo JL, Rumjanek NG, Margis-Pinheiro M. Small heat shock proteins genes are differentially expressed in distinct varieties of common bean. Brazil J Plant Physiol 2003;15:33–41. DOI: 10.1590/S1677-04202003000100005 - 22.
Salveit ME. Chilling injury is reduced in cucumber and rice seedlings in tomato pericarp discs by heat-shocks applied after chilling. Postharvest Biol Technol 2001;21:169–77. DOI: doi:10.1016/S0925-5214(00)00132-0 - 23.
Allen DJ, Ort DR. Impact of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 2001;6:36–42. DOI: doi:10.1016/S1360-1385(00)01808-2 - 24.
Lux A, Martinka M, Vaculik M, White PJ. Root responses to cadmium in the rhizosphere: a review. J Exp Bot 2011;62:21–37. DOI: 10.1093/jxb/erq281 - 25.
Mulligan CN, Yong RN, Gibbs BF. Remediation technologies for metal-contaminated soils and groundwater: an evaluation. Eng Geol 2001;60:193–207. DOI: doi:10.1016/S0013-7952(00)00101-0 - 26.
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S. Root-to-shoot cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 2009;60:2677–88. DOI: 10.1093/jxb/erp119 - 27.
Cai Y, Cao F, Wei K, Zhang G, Wu F. Genotypic dependent effect of exogenous glutathione on cd-induced changes in proteins, ultrastructure and antioxidant defense enzymes in rice seedlings. J Hazard Mater 2011;192:1056–66. DOI: 10.1016/j.jhazmat.2011.06.011 - 28.
Ali S, Bai P, Zeng F, Cai S, Shamsi IH, Qui B, Wu F, Zhang G. The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance. Environ Exp Bot 2011;70:185–91. DOI: 10.1016/j.envexpbot.2010.09.002 - 29.
Sharma I, Pati PK, Bhardwaj R. Effect of 28-homobrassinolide on antioxidant defence system in Raphanus sativus L. under chromium toxicity. Ecotoxicol 2011;20:862–74. DOI: 10.1007/s10646-011-0650-0 - 30.
Kanwar MK, Bhardwaj R, Chowdhary SP, Arora P, Sharma P, Kumar S. Isolation and characterization of 24-Epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense ofBrassica plants and in vitro cytotoxicity. Acta Physiol Plant 2013;35:1351–62. DOI: 10.1007/s11738-012-1175-8 - 31.
Bal W, Kasprzak KS. Induction of oxidative damage by carcinogenic metal. Toxicol Lett 2002;127:55–62. DOI: doi:10.1016/S0378-4274(01)00483-0 - 32.
Bhakuni G, Dube B.K, Sinha P, Chatterjee C. Copper stress affects metabolism and reproductive yield of chickpea. J Plant Nutri 2009;32:703–11. DOI: 10.1080/01904160902743258 - 33.
Andre CM, Larondelle Y, Evers D. Dietary antioxidants and oxidative stress from a human and plant perspective: a review. Curr Nutri Food Sci 2010;6:2–12. DOI: 10.2174/157340110790909563 - 34.
Bouazizi H, Jouili H, Geitmann A, El Ferjani E. Cell wall accumulation of Cu ions and modulation of lignifying enzymes in primary leaves of bean seedlings exposed to excess copper. Biol Trace Element Res 2011;139:97–107. DOI: 10.1007/s12011-010-8642-0 - 35.
Gayor A, Srivastava PS, Iqbal M. Morphogenic and biochemical responses of Bacopa monniera cultures to zinc toxicity. Plant Sci 1999;143:187–93. DOI: 10.1016/S0168-9452(99)00032-1 - 36.
Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A. Comparative study of responses in four datura species to zinc stress. Chemosphere 2005;59:1005–13. DOI: 10.1016/j.chemosphere.2004.11.030 - 37.
Castiglione S, Franchin C, Fossat T, Lingua G, Torrigiani P, Biondi S. High zinc concentrations reduce rooting capacity and alter metallothionein gene expression in white poplar ( Populus alba L. cv. Villafranca). Chemosphere 2007;67:1117–26. DOI: 10.1016/j.chemosphere.2006.11.039 - 38.
Tewari RK, Kumar P, Sharma PN. Morphology and physiology of zinc-stressed mulberry plants. J Plant Nutri Soil Sci 2008;171:286–94. DOI: 10.1002/jpln.200700222 - 39.
Choudhary SP, Yu JQ, Yamaguchi-Shinozaki K, Shinozaki K, Phan Tran L-S. Benefits of brassinosteroid crosstalk. Trends Plant Sci 2012;17:594–605. DOI: 10.1016/j.tplants.2012.05.012 - 40.
Mitchell JW, Mandava NB, Worley JE, Plimmer JR, Smith MV. Brassins: a family of plant hormones from rape pollen. Nature 1970;225:1065–66. DOI: 10.1038/2251065a0 - 41.
Grove MD, Spencer GF, Rohwededer WK, Mandava N, Worley JF, Warthen JR JD, Steffens GL, Flippen-Anderson JL, Cook JR JC. Brassinolide, a plant promoting steroid isolated from Brassica napus pollen. Nature 1979;281:216–7. DOI: 10.1038/281216a0 - 42.
Zhao B, Li J. Regulation of brassinosteroid biosynthesis and inactivation. J Integrat Plant Biol 2012;54:746–59. DOI: 10.1111/j.1744-7909.2012.01168.x. - 43.
Wang M, Jiang WJ, Yu HJ. Effects of exogenous epibrassinolide on photosynthetic characteristics in tomato ( Lycopersicon esculentum Mill) seedlings under weak light stress. J Agricult Food Chem 2010;58:3642–5. DOI: 10.1021/jf9033893 - 44.
Kurepin LV, Joo SH, Kim S-K, Pharis RP, Back TG. (2012). Interaction of brassinosteroids with light quality and plant hormones in regulating shoot growth of young sunflower and Arabidopsis seedlings. J Plant Growth Regulat 2012;31:156–64. DOI: 10.1007/s00344-011-9227-7 - 45.
Wang Q, Ding T, Gao L, Pang J, Yang N. Effect of brassinolide on chilling injury of green bell pepper in storage. Sci Horticult 2012;144:195–200. DOI: 10.1016/j.scienta.2012.07.018 - 46.
Anjum SA, Wang LC, Farooq M, Hussain M, Xue LL, Zou CM. Brassinolide application improves the drought tolerance in maize through modulation of enzymatic antioxidants and leaf gas exchange. J Agronomy Crop Sci 2011;197:177–85. - 47.
Li YH, Liu YJ, Xu XL, Jin M, An LZ, Zhang H, Effect of 24-epibrassinolide on drought stress-induced changes in Chorispora bungeana . Biol Plant 2012;56:192–6. DOI: 10.1007/s10535-012-0041-2 - 48.
Mahesh B, Parshavaneni B, Ramakrishna B, Rao SSR. Effect of brassinosteroids on germination and seedling growth of radish ( Raphanus sativus L.) under PEG-6000 induced water stress. Am J Plant Sci 2013;4:2305–13. DOI: 10.4236/ajps.2013.412285 - 49.
Yusuf M, Fariduddin Q, Hayat S, Hasan SA, Ahmad A. Protective responses of 28-Homobrssinolide in cultivars of Triticum aestivum with different levels of nickel. Arch Environ Contam Toxicol 2011;60:68–76. DOI: 10.1007/s00244-010-9535-0 - 50.
Yusuf M, Fariduddin Q, Ahmad A. 24-Epibrassinolide modulates growth, nodulation, antioxidant system, and osmolyte in tolerant and sensitive varieties of Vigna radiate under different levels of nickel: a shotgun approach. Plant Physiol Biochem 2012;57:143–53. DOI: 10.1016/j.plaphy.2012.05.004 - 51.
Saka H, Fujii S, Imakawa A.M, Kato N, Watanabe S, Nishizawa T, Yonekawa S. Effect of brassinolide applied at the meiosis and flowering stages on the levels of endogenous plant hormones during grain filling in rice plant ( Oryza sativa L.). Plant Prod Sci 2003;6:36–42. DOI: 10.1626/pps.6.36 - 52.
Liu H, Guo T, Zhu Y, Wang C, Kang G. Effects of Epibrassinolide (epi-BR) application at anthesis on starch accumulation and activities of key enzymes in wheat grains. Acta Agronom Sinica 2006;32:924–30. - 53.
Kartal G, Temel A, Arican E, Gozukirmizi N. Effects of brassinosteroids on barley root growth, antioxidant system and cell division. Plant Growth Regulat 2009;58:261–7. DOI: 10.1007/s10725-009-9374-z - 54.
Yuan G-F, Jia C-G, Li Z, Sun B, Zhang L-P, Liu N, Wang Q-M. Effect of brassinosteroids on drought resistance and abscisic acid concentration in tomato under water stress. Sci Horticult 2010;126:103–8. DOI: 10.1016/j.scienta.2010.06.014 - 55.
Farooq M, Wahid A, Basra SMA, Islam-ud-Din. Improving water relations and gas exchange with brassinosteroids in rice under drought stress. J Agron Crop Sci 2009;195:262–9. DOI: 10.1111/j.1439-037X.2009.00368.x - 56.
Khripach VA, Zhabinski VN, Khripach NB. New practical aspects of brassinosteroids and results of their ten year agricultural use in Russia and blakanes. In: Hayat S, Ahmad A, editors. Brassinosteroids; Bioactivity and Crop Productivity. Kluwer Academic Publisher, Dordrecht; 2003. pp. 189–230. - 57.
Bajguz A. Effect of brassinosteroids on nucleic acid and protein content in cultured cells of Chlorella vulgaris. Plant Physiol Biochem 2000;38:209–15. DOI: 10.1016/S0981-9428(00)00733-6 - 58.
Felner M. Recent progress in brassinosteroid research: hormone perception and signal transduction. In: Hayat S, Ahmad A, editors. Brassinosteroids: Bioactivity and Crop Productivity. Kluwer Academic Publishers, Dordrecht; 2003. pp. 69–86. - 59.
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P. Brassinosteroid confers tolerance in Arabidopsis thaliana andBrassica napus to a range of abiotic stresses. Planta 2007;225:353–64. DOI: 10.1007/s00425-006-0361-6 - 60.
Vardhini BV, Rao SSR. Amelioration of osmotic stress by brassinosteroids on seed germination and seedling growth of three varieties of sorghum. Plant Growth Regulat 2003;41:25–31. DOI: 10.1023/A:1027303518467 - 61.
Bordeleau LM, Prevost D. Nodulation and nitrogen fixation in extreme environments. Plant Soil 1994;161:115–25. DOI: 10.1007/BF02183092 - 62.
Ramos MLG, Gordon AJ, Minchin FR, Sprent JI, Parsons R. Effect of water stress on nodule physiology and biochemistry of a drought tolerant cultivar of common bean ( Phaseolus vulgaris L.). Annals Bot 1999;83:57–63. DOI: 10.1006/anbo.1998.0792 - 63.
Serraj R, Sinclair TR, Purcell LC. Symbiotic N2 fixation response to drought. J Exp Bot 1999;50:143–55. DOI: 10.1093/jxb/50.331.143 - 64.
Singh T, Kumar V. Nodulation and plant growth as influenced by growth regulators in some legumes. Acta Bot Ind 1989;17:177–81. - 65.
Fedorova EE, Zhiznevskaya GY, Al’zhapparova ZK, Izmailov SF. Phytohormones in nitrogen-fixing nodules of leguminous plants. Fiziologiya I Biokhimiya Kul'Turnykh Rastenii. 1991;23:426–38. - 66.
Vardhini BV, Rao SSR. Effect of brassinosteroids on nodulation and nitrogenase activity in groundnut ( Arachis hypogaea L.). Plant Growth Regulat 1999;28:165–7. DOI: 10.1023/A:1006227417688 - 67.
Upreti KK, Murti GSR. Effects of brassinosteroids on growth, nodulation, phytohormone content and nitrogenase activity in French bean under water stress. Biologia Plant 2004;48:407–11. DOI: 10.1023/B:BIOP.0000041094.13342.1b - 68.
Li KR, Feng CH. Effects of brassinolide on drought resistance of Xanthoceras sorbifolia seedlings under water stress. Acta Physiol Plant 2011;33:1293–300. DOI: 10.1007/s11738-010-0661-0 - 69.
Zhang M, Zhai Z, Tian X, Duan L, Li Z. Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean ( Glycine max L.). Plant Growth Regulat 2008;56:257–64. DOI: 10.1007/s10725-008-9305-4 - 70.
Fariduddin Q, Khanam S, Hasan SA, Ali B, Hayat S, Ahmad A. Effect of 28-homobrassinolide on the drought stress-induced changes in photosynthesis and antioxidant system of Brassica juncea L. Acta Physiol Plant 2009;31:889–97. DOI: 10.1007/s11738-009-0302-7 - 71.
Reddy AR, Chaitanya KV, Vivekanandan M. Drought induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 2004;161:1189-1202. DOI:10.1016/j.jplph.2004.01.013 - 72.
Xiong L, Schumaker KS, Zhu JK. Cell signaling during cold, drought, and salt stress. Plant Cell 2002;14:S165–83. DOI: 10.1105/tpc.000596 - 73.
Vardhini BV, Sujatha E, Rao SSR. Brassinosteroids: alleviation of water stress in certain enzymes of sorghum seedlings. J Phytol 2011;3(10):38–43. - 74.
Mazorra LM, Nunez M, Hechavarria M, Coll F, Sanchez-Blanco MJ. Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. Biol Plant 2002;45:593–6. DOI: 10.1023/A:1022390917656 - 75.
Cao S, Xu Q, Cao Y, Qian K, An K, Zhu Y, Binzeng, H, Zhao H, Kuai B. Loss of function mutation in DET2 gene lead to an enhanced resistance to oxidative stress inArabidopsis . Physiol Plant 2005;123:57–66. DOI: 10.1111/j.1399-3054.2004.00432.x - 76.
Eraslan F, Inal A, Gunes A, Alpaslan A. Impact of exogenous salicylic acid on the growth, antioxidant activity and physiology of carrot plants subjected to combined salinity and boron toxicity. Sci Horticult 2007;113:120–8. DOI: 10.1016/j.scienta.2007.03.012 - 77.
Tuteja N. Mechanisms of high salinity tolerance in plants. Methods Enzymol 2007;428:419–38. DOI: 10.1016/S0076-6879(07)28024-3 - 78.
Munns R, Tester M. Mechanisms of salinity tolerance. Ann Rev Plant Biol 2008;59:651–81. DOI: 10.1146/annurev.arplant.59.032607.092911 - 79.
Ashraf M, Foolad MR. Improving plant abiotic-stress resistance by exogenous application of osmoprotectants glycinebetaine and proline. Environ Exp Bot 2007;59:206–16. - 80.
Daneshmand F, Arvin MJ, Kalantari KM. Acetylsalicylic acid ameliorates negative effects of NaCl or osmotic stress in Solanum stoloniferum in vitro. Biol Plant 2010;54:781–4. DOI: 10.1007/s10535-010-0142-8 - 81.
Ashraf M. Biotechnological approach of improving plant salt tolerance using antioxidants as markers. Biotechnol Adv. 2009;27:84–93. DOI: 10.1016/j.biotechadv.2008.09.003 - 82.
Talaat NB, Shawky BT. 24-Epibrassinolide alleviates salt-induced inhibition of productivity by increasing nutrients and compatible solutes accumulation and enhancing antioxidant system in wheat ( Triticum aestivum L.). Acta Physiol Plant 2013;35:729–40. DOI: 10.1007/s11738-012-1113-9 - 83.
Divi UK, Rahman T, Krishna P. Gene expression and functional analyses in brassinosteroid-mediated stress tolerance. Plant Biotechnol J 2015, DOI: 10.1111/pbi.12396. - 84.
Hayat S, Hasan SA, Yusuf M, Hayat Q, Ahmad A. Effect of 28-homobrassinolide on photosynthesis, fluorescence and antioxidant system in the presence or absence of salinity and temperature in Vigna radiata . Environ Exp Bot 2010;69:105–12. DOI: 10.1016/j.envexpbot.2010.03.004 - 85.
El-Mashad AAA, Mohamed HI. Brassinolide alleviates salt stress and increases antioxidant activity of cowpea plants ( Vigna sinensis ). Protoplasma 2012;249:625–35. DOI: 10.1007/s00709-011-0300-7 - 86.
Ding H-D, Zhu X-H, Zhu Z-W, Yang S-J, Zha D-S, Wu X-X. Amelioration of salt-induced oxidative stress in eggplant by application of 24-epibrassinolide. Biol Plant 2012;56(4):767–70. DOI: 10.1007/s10535-012-0108-0 - 87.
Sharma I, Ching E, Saini S, Bhardwaj R, Pati PK. Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. Plant Physiol Biochem 2013;69:17–26. DOI: 10.1016/j.plaphy.2013.04.013 - 88.
Fariduddin Q, Mir BA, Yusuf M, Ahmad A. 24-epibrassinolide and/or putrescine trigger physiological and biochemical responses for the salt stress mitigation in Cucumis sativus L. Photosynthetica 2014;52(3):464–74. DOI: 10.1007/s11099-014-0052-7 - 89.
Bajguz A. Brassinosteroid enhanced the level of abscisic acid in Chlorella vulgaris subjected to short-term heat stress. J Plant Physiol 2009;166:882–6. DOI: 10.1016/j.jplph.2008.10.004 - 90.
Stone P. The effects of heat stress on cereal yield and quality. In: Basra AS. (Ed.) Crop Responses and Adaptations to Temperature Stress. Binghamton, NY: Food Products Press; 2001. p. 302. - 91.
Rane J, Chauhan H. Rate of grain growth in advanced wheat (Triticum aestivum) accession under late-sown environment. Ind J Agricult Sci 2002;72:581–5. - 92.
Hussain SS, Mudasser M. Prospects for wheat production under changing climate in mountain areas of Pakistan: an econometric analysis. Agricult Sys 2007;94:494–501. DOI: 10.1016/j.agsy.2006.12.001 - 93.
Janeczko A, Oklestkova J, Pociecha E, Koscielniak J, Mirek M. Physiological effects and transport of 24-epibrassinolide in heat-stressed barley. Acta Physiol Plant 2011;33:1249–59. DOI: 10.1007/s11738-010-0655-y - 94.
Yin H, Chen QM, Yi MF. Effects of short-term heat stress on oxidative damage and responses of antioxidant system in Lilium longiflorum . Plant Growth Regulat 2008;54:45–54. DOI: 10.1007/s10725-007-9227-6 - 95.
Bartwal A, Mall R, Lohani P, Guru SK, Arora S. Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regulat 2012;32:216–32. DOI: 10.1007/s00344-012-9272-x - 96.
Hu WH, Xiao YA, Zeng JJ, Hu XH. Photosynthesis, respiration and antioxidant enzymes in pepper leaves under drought and heat stresses. Biol Plant 2010;54:761–5. DOI: 10.1007/s10535-010-0137-5 - 97.
Asthir B, Koundal A, Bains NS. Putrescine modulates antioxidant defense response in wheat under high temperature stress. Biol Plant 2012;56:757–61. DOI: 10.1007/s10535-012-0209-1. - 98.
Wu X, Yao X, Chen J, Zhu Z, Zhang H, Zha D. Brassinosteroids protect photosynthesis and antioxidant system of eggplant seedlings from high-temperature stress. Acta Physiol Plant 2014;36:251–61. DOI: 10.1007/s11738-013-1406-7 - 99.
Liu Y, Zhao Z, Si J, Di C, Han J, An L. Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana . Plant Growth Regulat 2009;59:207–14. DOI: 10.1007/s10725-009-9405-9 - 100.
Liu YJ, Jiang HF, Zhao ZG, An LZ. Abscisic acid is involved in brassinosteroids-induced chilling tolerance in the suspension cultured cells from Chorispora bungeana . J Plant Physiol 2011;168:853–62. DOI: 10.1016/j.jplph.2010.09.020 - 101.
Wang B, Zeng G. Effect of epibrassinolide on the resistance of rice seedlings to chilling injury. J Plant Physiol Molecul Biol 1993;19:38–42. - 102.
Kim KS, Sa JG. Effects of plant growth regulator, brassinolide, on seedling growth in rice ( Oryza sativa L). Res Rep Rural Develop Admin Rice 1989;31(1):49–53. - 103.
Hirai K, Fujii S, Honjo K. The effect of brassinolide on ripening of rice plants under low temperature condition. Japan J Crop Sci 1991;60(1):29–35. - 104.
Krishna P. Brassinosteroid-mediated stress responses. J Plant Growth Regulat 2003;22:289–97. DOI: 10.1007/s00344-003-0058-z - 105.
Burbulis N, Jonytiene V, Kupriene R, Blinstrubiene A. Changes in proline and soluble sugars content during cold acclimation of winter rapeseed shoots in vitro. J Food, Agricult Environ 2011;9:371–4. - 106.
Hu WH, Wu Y, Zeng JZ, He L, Zeng QM. Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 2010;48:537–44. DOI: 10.1007/s11099-010-0071-y - 107.
Fariduddin Q, Yusuf M, Chalkoo S, Hayat S, Ahmad A. 28-homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. Photosynthetica 2011;49(1):55–64. DOI: 10.1007/s11099-011-0022-2 - 108.
Oidaira H, Sano S, Koshiba T, Ushimaru T. Enhancement of antioxidative enzyme activities in chilled rice seedlings. J Plant Physiol 2000;156:811–3. DOI: 10.1016/S0176-1617(00)80254-0 - 109.
Ahammed GJ, Yuan HL, Ogweno JO, Zhou YH, Xia XJ, Mao WH, Shi K, Yu JQ. Brassinosteroid alleviates phenanthrene and pyrene phytotoxicity by increasing detoxification activity and photosynthesis in tomato. Chemosphere 2012;86:546–55. DOI: 10.1016/j.chemosphere.2011.10.038 - 110.
Hasan SA, Hayat S, Ahmad A. Brassinosteroids protect photosynthetic machinery against the cadmium induced oxidative stress in two tomato cultivars. Chemosphere 2011;84:1446–51. DOI: 10.1016/j.chemosphere.2011.04.047 - 111.
López-Millán AF, Sagardoy R, Solanas M, Abadía A, Abadía J. Cadmium toxicity in tomato ( Lycopersicon esculentum ) plants grown in hydroponics. Environ Exp Bot 2009;65:376–85. DOI: 10.1016/j.envexpbot.2008.11.010 - 112.
Hayat S, Alyemeni MN, Hasan SA. Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi J Biol Sci 2012;19:325–35. DOI: 10.1016/j.sjbs.2012.03.005 - 113.
Cao F, Liu L, Ibrahim W, Cai Y, Wu F. Alleviating effects of exogenous glutathione, glycinebetaine, brassinosteroids and salicylic acid on cadmium toxicity in rice seedlings ( Oryza sativa ). Agrotechnology 2013;2:107. DOI:10.4172/2168-9881.1000107 - 114.
Hayat S, Khalique G, Wani AS, Alyemeni MN, Ahmad A. Protection of growth in response to 28-homobrassinolide under the stress of cadmium and salinity in wheat. Int J Biol Macromolecul 2014;64:130–6. DOI: 10.1016/j.ijbiomac.2013.11.021 - 115.
Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette M-LM, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J, Renou J-P, Vavasseur A, Leonhardt N. Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 2006;88:1751–65. DOI: 10.1016/j.biochi.2006.04.018 - 116.
Villiers F, Jourdain A, Bastien O, Leonhardt N, Fujioka S, Tichtincky G, Parcy F, Bourguignon J, Hugouvieux V. Evidence for functional interaction between brassinosteroids and cadmium response in Arabidopsis thaliana. J Exp Bot 2012;63:1185–200. DOI: 10.1093/jxb/err335 - 117.
Gill A, Sagoo MIS. Mutagenic potential and nutritive quality of turnip plants raised over chromium amended soils. Int J Bot 2010;6:127–31. - 118.
Shanker AK, Cervantes TC, Loza-Tavera H, Avudainayagam S. Chromium toxicity in plants. Environ Int 2005;31:739–53. DOI: 10.1016/j.envint.2005.02.003 - 119.
Panda SK, Choudhury S. Chromium stress in plants. Brazil J Plant Physiol 2005;17(1):95–102. DOI: 10.1590/S1677-04202005000100008 - 120.
Choudhary SP, Kanwar M, Bhardwaj R, Gupta BD, Gupta RK. Epibrassinolide ameliorates Cr (VI) stress via influencing the levels of indole-3-acetic acid, abscisic acid, polyamines and antioxidant system of radish seedlings. Chemosphere 2011;84:592–600. DOI: 10.1016/j.chemosphere.2011.03.056 - 121.
Sun Y, Veerabomma S, Abdel-Mageed HA, Fokar M, Asami T, Yoshida S, Allen RD. Brassinosteroid regulates fiber development on cultured cotton ovules. Plant Cell Physiol 2005;46:1384–91. DOI: 10.1093/pcp/pci150 - 122.
Welch RM. Micronutrient nutrition of plants. Crit Rev Plant Sci 1995;14:49–82. DOI: 10.1080/07352689509701922 - 123.
Marschner H. Mineral Nutrition of Higher Plants. 2nd Ed. Academic Press, London 1995. - 124.
Kevrešan S, Petrovič N, Popovič M, Kandrač M. Effect of heavy metals on nitrate and protein metabolism in sugar beet. Biol Plant 1998;41:235–40. DOI: 10.1023/A:1001818714922 - 125.
Schickler H, Caspi H. Response of antioxidative enzymes to nickel and cadmium stresss in hyperaccumulator plants of the genus Alyssum . Physiol Plant 1999;105:39–44. DOI: 10.1034/j.1399-3054.1999.105107.x - 126.
Prasad SM, Dwivedi R, Zeeshan M. Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress. Photosynthetica 2005;43:177–85. DOI: 10.1007/s11099-005-0031-0 - 127.
Sharma P, Bhardwaj R. Effects of 24-epibrassinolide on growth and metal uptake in Brassica juncea L. under copper metal stress. Acta Physiol Plant 2007;29:259–63. DOI: 10.1007/s11738-007-0032-7 - 128.
Kanwar MK, Bhardwaj R, Arora P, Choudhary SP, Sharma P, Kumar S. Plant steroid hormones produced under Ni stress are involved in the regulation of metal uptake and oxidative stress in Brassica juncea L. Chemosphere 2012;86:41–9. DOI: 10.1016/j.chemosphere.2011.08.048 - 129.
Sharma I, Pati PK, Bhardwaj R. Effect of 24-epibrassinolide on oxidative stress markers induced by nickel-ion in Raphanus sativus L. Acta Physiol Plant 2011;33:1723–35. DOI: 10.1007/s11738-010-0709-1 - 130.
Chen LM, Lin CC, Kao CH. Copper toxicity in rice seedlings: changes in antioxidative enzyme activities, H2O2 level and cell wall peroxidase activity in roots. Bot Bull Acad Sin 2000;41:99–103. - 131.
Sheldon AR, Menzies NW. The effect of copper toxicity on the growth and root morphology of Rhode grass ( Chloris gayana Knuth.) in resin buffered solution culture. Plant Soil 2005;278:341–9. DOI: 10.1007/s11104-005-8815-3 - 132.
Chatterjee C, Sinha P, Dube BK, Gopal R. Excess copper induced oxidative damages and changes in radish physiology. Commun Soil Sci Plant Anal 2006;37:2069–76. DOI: 10.1080/00103620600770425 - 133.
Alaoui-Sossé B, Genet P, Vinit-Dunand F, Toussaint ML, Epron D, Badot PM. Effect of copper on growth in cucumber plants ( Cucumis sativus ) and its relationships with carbohydrate accumulation and changes in ion contents. Plant Sci 2004;166:1213–8. DOI: 10.1016/j.plantsci.2003.12.032 - 134.
Maksymiec W, Krupa Z. Effects of methyl jasmonate and excess copper on root and leaf growth. Biol Plant 2007;51:322–6. DOI: 10.1007/s10535-007-0062-4 - 135.
Ducic T, Polle A. Transport and detoxification of manganese and copper in plants. Brazil J Plant Physiol 2005;17:103–12. DOI: 10.1590/S1677-04202005000100009 - 136.
Choudhary SP, Bhardwaj R, Gupta BD, Dutt P, Gupta RK, Kanwar M, Biondi S. Enhancing effects of 24-epibrassinolide and Putrescine on the antioxidant capacity and free radical scavenging activity of Raphanus sativus seedlings under Cu ion stress. Acta Physiol Plant 2011;33:1319–33. DOI: 10.1007/s11738-010-0665-9 - 137.
Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana . Proc Nat Acad Sci USA 2009;106:7648–53. DOI: 10.1073/pnas.0812346106 - 138.
Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, Cano-Delgado AI. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 2011;138:849–59. DOI: 10.1242/dev.057331 - 139.
Gudesblat GE, Russinova E. Plants grow on brassinosteroids. Curr Opin Plant Biol 2011;14:530–7. DOI: 10.1016/j.pbi.2011.05.004 - 140.
Filová A, Sytar O, Krivosudská E. Effects of brassinosteroid on the induction of physiological changes in Helianthus annuus L. under copper stress. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 2013;61:623–9. DOI: 10.11118/actaun201361030623 - 141.
Betul Burun K, Marakli S, Gozukirmizi N. Alleviation of copper stress with brassinosteroid in germinating sunflower roots. J Animal Plant Sci 2015; in press. - 142.
Vázquez MN, Guerrero YR, González LM, de la Noval WT. Brassinosteroids and plant responses to heavy metal stress. An overview. Open J Metal 2013;3:34–41. DOI: 10.4236/ojmetal.2013.32A1005. - 143.
Çağ S, Gören-Sağlam N, Çıngıl-Barış Ç, Kaplan E. The effect of different concentration of epibrassinolide on chlorophyll, protein and anthocyanin content and peroxidase activity in excised red cabbage ( Brassica oleraceae L.) cotyledons. Biotechnol Biotechnol Equip 2007;21:422–5. DOI: 10.1080/13102818.2007.10817487 - 144.
Sharma P, Bhardwaj R, Arora N, Arora HK. Effect of 28- homobrassinolide on growth, Zn metal uptake and antioxidative enzyme activities in Brassica juncea L. seedlings. Brazil J Plant Physiol 2007;19(3):203–10. DOI: 10.1590/S1677-04202007000300004 - 145.
Ramakrishna B, Rao SSR. 24-Epibrassinolide alleviated zinc-induced oxidative stress in radish ( Raphanus sativus L.) seedlings by enhancing antioxidative system. Plant Growth Regulat 2012;68:249–59. DOI: 10.1007/s10725-012-9713-3 - 146.
Choudhary SP, Kanwar M, Bhardwaj R, Yu J-Q, Pan Tran L-S. Chromium stress mitigation by polyamine-brassinosteroid application involves phytohormonal and physiological strategies in Raphanus sativus L. PLoS ONE 2012;7(3):e33210. DOI: 10.1371/journal.pone.0033210 - 147.
Fariduddin Q, Khan TA, Yusuf M. Hydrogen peroxide mediated tolerance to copper stress in the presence of 28-homobrassinolide in Vigna radiata . Acta Physiol Plant 2014;36:2767–78. DOI: 10.1007/s11738-014-1647-0 - 148.
Malamy JE. Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 2005;28:67–77. - 149.
Vriet C, Russinova E, Reuzeau C. Boosting crop yields with plant steroids. Plant Cell 2012;24:842–57. DOI: 10.1105/tpc.111.094912 - 150.
Müssig C, Shin G-H, Altmann T. Brassinosteroids promote root growth in Arabidopsis . Plant Physiol 2003;133:1261–71. DOI: 10.1104/pp.103. - 151.
Bajguz A, Hayat S. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 2009;47:1–8. DOI:10.1016/j.plaphy.2008.10.002 - 152.
Shu H, Ni W, Guo S, Gong Y, Shen X, Zhang X, Xu P, Guo Q. Root-applied brassinolide can alleviate the NaCl injuries on cotton. Acta Physiol Plant 2015;37:75. DOI 10.1007/s11738-015-1823-x