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Review

The Role of Endogenous Brassinosteroids in the Mechanisms Regulating Plant Reactions to Various Abiotic Stresses

by
Rong Miao
1,
Caijuan Li
1,
Ziliang Liu
1,
Xiangyan Zhou
1,*,
Sijin Chen
1,
Dan Zhang
1,
Jiaqi Luo
2,
Wenhui Tang
3,
Cuiling Wang
1,
Jiling Wu
1 and
Zhengjun Chen
1
1
College of Life Science and Technology/State Key Laboratory of Aridland Crop Science, Gansu Agricultural University, Lanzhou 730070, China
2
Qinzhou District Agricultural Technology Comprehensive Service Center, Tianshui 741000, China
3
Zhuanglang Agricultural Technology Extension Center, Pingliang 744600, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(2), 356; https://doi.org/10.3390/agronomy14020356
Submission received: 15 December 2023 / Revised: 5 February 2024 / Accepted: 7 February 2024 / Published: 9 February 2024
(This article belongs to the Section Farming Sustainability)
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Abstract

:
Plants are vulnerable to many abiotic stresses, resulting in reduced plant productivity. Its adaptation to unfavorable environments relies on transmitting external stress signals into internal signaling pathways. A series of stress response mechanisms have been developed. Among them, brassinosteroids (BRs) are a class of steroid hormones that are widely involved in plant growth, development, and stress response. Via genetics, proteomics, and genomics studies, the major components of signaling and signaling pathways through a series of phosphorylation cascade reactions have been identified in model plants such as Arabidopsis. Numerous studies have shown that BRs play important roles in plant responses to drought, temperature, salt, heavy metals, and other environmental stresses. The application of BRs to improve plant stress resistance has become the focus of research in recent years, especially the regulation of stress via endogenous BRs. Therefore, this paper systematically summarizes the research progress related to endogenous BR levels and provides an overview of BR biosynthesis and the signaling pathway, as well as the function of endogenous BRs in the response to abiotic stresses.

1. Introduction

In nature, plants are always exposed to many environmental stresses. These stresses fall into two main categories: biotic stresses, mainly including insect pests and fungal and viral infections, and abiotic stresses, such as drought, high temperature, cold damage, heavy metals, salinity, and other stresses [1,2,3]. When plants are under abiotic stress, their growth and development are affected to different degrees, such as by the inhibition of photosynthesis, changes in endogenous hormones, the production of large amounts of reactive oxygen species via osmotic stress, etc. Abiotic stresses can slightly affect plant growth and development or lead to the death of the whole plant in serious cases [4]. Studies have shown that the dry and fresh weight of roots and above-ground parts of maize is significantly reduced under drought stress [5]. High temperatures inhibited seed vigor, delayed seedling emergence, accelerated leaf senescence, and inhibited stem and root growth [6]. Low temperatures significantly reduced the height, main root length, and dry and fresh mass of above- and below-ground parts of plant seedlings and significantly increased the malondialdehyde (MDA) content. The contents of soluble sugars (SSs), soluble protein (SP), and proline (Pro) were also affected under low-temperature stress [7]. Treating pepper with the heavy metal Cd had significant inhibitory effects on photosynthetic pigments and reduced CAT and APX activities [8]. Salt stress had significant effects on membrane lipid peroxidation and inhibited growth in rice seedlings [9].
Phytohormones, also known as endogenous plant hormones, play a significant role in plant growth and development and the plant’s response to abiotic stresses. Brassinosteroids (BRs) are biologically active phytosteroid hormones that were first isolated from the pollen of rapeseed and are the sixth major class of endogenous plant hormones in addition to auxin, ethylene (ETH), abscisic acid (ABA), gibberellins (GAs), and cytokinins (CTKs) [10,11]. At present, more than 70 BR-related compounds have been identified. Among them, 24-epibrassinolide (24-EBR) and 28-homobrassinolide (28-HBR) are the two most active ones, which play a key role in BR function and signal transduction [12,13]. In addition to endogenous plant-synthesized BRs, highly active analogs have been artificially synthesized due to the needs of production and scientific research practice. BRs play crucial roles in the regulation of seed germination, fruit ripening, plant productivity, and tolerance to abiotic stresses such as drought, high temperatures, salt, and heavy metals [14,15,16]. When plants suffer from abiotic stress, BRs directly induce the expression of response genes via signal transduction. Meanwhile, the resistance response of plants is indirectly induced via the second messenger, such as ROS/NO, the MAPK cascade, co-action with other endogenous hormones, etc. For example, MAPK was activated at high temperatures to regulate HSP expression [1]. NO and ROS mediated the process by which BRs regulate the cold tolerance of cucumbers [17].
Most studies have focused on the external application of BRs to promote plant growth, improve crop yield, and increase plant resistance to abiotic stresses [18,19,20]. For example, the application of 24-epibrassinolide on cucumber leaf surfaces promoted an increase in roots and stems and improved the resistance to cadmium stress [21]. However, the entire growth and development process of plants cannot be separated from the coordinated action between endogenous plant hormones and external environmental signals. Therefore, this paper reviews the biosynthesis of BRs, signaling, and the roles of endogenous BRs in regulating the plant’s response to abiotic stresses.

2. BR Biosynthetic Pathway and Key Genes

Since the isolation of the most active brassinolide (BL), researchers have identified more than 70 similar compounds, collectively known as BRs, either via chemical synthesis or isolation and purification from nature [22,23,24]. As shown in Figure 1, the BR biosynthetic pathway is initiated by campesterol (CR). According to whether campestanol (CN) is generated in the synthetic process, it can be divided into the CN-dependent pathway and the CN-independent pathway [25,26]. From CN, the CN-dependent pathway branches into the early C-6 oxidation pathway and the late C-6 oxidation pathway. In the early C-6 pathway, CN is first oxidized at C-6 to form 6-oxocampestanol (6-oxoCN), followed by the hydroxylation of C-22 to form cathasterone (CT), and then through a series of catalytic reactions to form castasterone (CS). In the late C-6 oxidation pathway, CN is first hydroxylated at C-22 to form 6-deoxocathasterone (6-deoxoCT), the non-oxidized form of CT, then undergoes a series of catalytic steps corresponding to those in the early C-6 oxidation pathway, then completes the oxidation of C-6 to form CS in the final step, and is finally converted into BL. The CN-independent pathway directly forms BL via a more abbreviated eight-step catalytic reaction. In this pathway, CR is catalyzed by DWF4 (Dwarf 4), CPD (Constitutive photomorphogenesis and dwarfism), DET2 (De-etiolated 2), ROT3/CYP90D1 (Rotundifolia 3/Cytochrome P450 90D1), CYP85A1/2 (Cytochrome P450 85A1/Cytochrome P450 85A2), and other enzymes to form BL [27,28,29].
BRs that act on plants in nature are gradually synthesized in plant cells via a series of biochemical reactions, which involve the actions of many vital enzymes. The key enzymes in BR biosynthesis have gradually been studied. The coding genes of key enzymes in the BR synthetic pathway, such as the DWF4 gene, encoding cytochrome oxidase CYP90B1, have been further studied. CYP90B1 catalyzes the rate-limiting step of the entire biosynthetic pathway [30,31,32]. Studies have also shown that DWF4 enhances drought and salt tolerance, increases the level and activity of plant physiological indicators, and enhances plant productivity [33].
The CPD gene is a gene encoding A1 in 90 subfamilies of the cytochrome P450 family. It mainly affects the growth of plant roots, stems, and leaves and is an indispensable and important gene in plant growth and development [34].
The DET2 gene encodes the steroid 5α-reductase. It was shown that the expression level of the DET2 gene could regulate the endogenous BR content by altering the expression level of DET2 in plants [35].
ROT3 is a gene encoding 3-epi-6-deoxocathasterone 23-monooxygenase. It was shown that ROT3 is a target gene of BZR1. ROT3 affects the growth of plant stems and is involved in regulating the growth direction of plant leaves [36,37,38].
CYP90D1 is a key gene in the BR synthesis pathway. It was shown to affect cell division and cell wall synthesis by regulating BR synthesis in the maize internode and further affecting internode development and plant height [39].
CYP85A1, a gene encoding oleuropein lactone 6-oxidase 1, was found to be the target gene of BZR1. Studies have shown that CYP85A1 plays an essential role in plants subjected to abiotic stress, as well as regulating plant growth and development [40,41,42].

3. Signal Transduction Pathway of BRs

The BR signaling pathway has been intensively studied in recent years (Figure 2), and these studies have established a complex BR transduction pathway that plays a significant role in plant growth and development. BRs are recognized on the cell surface, and their receptor, BR-insensitive-1 (BRI1), is a single-transmembrane leucine-rich repeat sequence receptor-like protein kinase with an N-terminus that possesses a BR-binding structural domain at the N-terminus and a phosphokinase structural domain at the C-terminus [43,44]. When BRs are absent in plants, the activity of BRI1 is inhibited by BKI1, and, therefore, the activities of BRI1-associated receptor kinase 1 (BAK1), BR signaling kinases 1 (BSK1), and BRI1 suppressor 1 (BSU1), which are located downstream of the BR signaling pathway, are also inhibited by BKI1 [45,46]. BIN2 is a glycogen synthase kinase 3 (GSK3)-like kinase that is negatively regulated in the BR signaling pathway. In addition, brassinazole resistant 1 (BZR1) and BRI1 ems suppressor 1 (BES1) are core transcription factors downstream of the BR signaling pathway and are homologous genes [47]. BIN2 phosphorylates the transcription factors BZR1 and BES1 and reduces their transcriptional activity. The 14-3-3 proteins (a highly conserved family of cytosolic proteins that are widely expressed in all eukaryotes and bind to a wide range of functional signaling proteins and are, therefore, also known as ‘bridge proteins’ for protein interactions) induce the translocation of phosphorylated BZR1 and BES1 from the nucleus to the cytoplasm, where they are degraded by the 26S proteasome. At the same time, the protein phosphatase protein phosphate 2A (PP2A) dephosphorylates the phosphorylated transcription factors BZR1 and BZR2. The dephosphorylated BZR1 has high DNA-binding activity, which regulates BR biosynthesis and the expression of downstream target genes either directly or synergistically with other proteins, ultimately regulating plant growth and development [31]. When the level of BRs is high, the extracellular domain of the receptor protein BRI1 binds to the BRs, and then BRI1 immediately disassociates from BKI1, thus activating BAK1 [48]. Activated BRI1 phosphorylates BSK1, causing BSK1 to detach from the receptor complex. In addition, BRI1 phosphorylates the receptor-like cytoplasmic kinase constitutive differential growth 1 (CDG1) through the Ser 234 position. After that, BSK1 and CDG1 phosphorylate and activate BSU1, and BSU1 inactivates BIN2 by dephosphorylating the Tyr 200 residue of BIN2. Ultimately, BSU1 promotes the activity and stability of plant-specific transcription factors BZR1 and BES1 so that they can enter the nucleus and bind to DNA to induce the expression of target genes of BR signaling, thus regulating the growth and development processes of plants as well as the response to abiotic stresses [49,50].

4. Responses of Endogenous BRs to Different Abiotic Stresses

The upregulation or downregulation of key enzyme genes and transcription factors in BR biosynthesis and signaling pathways directly regulate the levels of endogenous BRs to adjust plant responses to abiotic stresses. The regulated mechanisms and biological functions of endogenous BRs in plants responding to adversity presented in previous studies are summarized in Table 1.

4.1. Drought Stress and BRs

Water is vital to plant growth and development, and drought stress is a serious threat to the yield and quality of crops [89,90]. When plants become water-deprived, the leaves first wilt, the leaf area decreases, and the root system develops to improve water absorption. When the water deficit increases, crop growth and development are inhibited, the yield declines, and the plant dries out and dies [91,92,93]. Under normal circumstances, reactive oxygen species (ROS) in plants are in a relatively balanced state. When plants are subjected to drought stress, the balance between the accumulation of ROS and the antioxidant defense system is destroyed. To cope with ROS damage to cells or tissues, the antioxidant system in plants is activated, and these protection systems coordinate with each other to reduce the damage [94]. The osmoregulatory substances gradually increase with increasing drought levels [95,96]. Chlorophyll is a vital pigment involved in photosynthesis, which is one of the most significant anabolic processes in plants and is the first physiological process to be affected by drought stress [97]. Under drought conditions, the chlorophyll content decreases, the photosynthetic capacity declines, and photosynthesis weakens due to leaf wilting [98,99].
Endogenous hormones play a primary role in drought stress [100,101]. Under drought conditions, plants show an overall decrease in the levels of hormones that promote plant growth and an increase in the levels of hormones that inhibit plant growth [100].
When plants are subjected to drought stress, BRs regulate the expression of some drought-resistant genes and the content of related proteins in plants to enhance drought resistance (Figure 3). The BHLH protein is involved in the regulation of the BR signaling pathway. BEE3, a bHLH family gene, is an early BR response gene. In cotton, BRs activated GhBZR1 to inhibit the expression of GhBEE3-Like, and the results showed that knocking out the GhBEE3-Like gene increased the expression of stress-related genes GhERD10, GhCDPK1, and GhRD26 and enhanced drought resistance [52]. RD26 is a drought-responsive transcription factor, which is a key component of the drought-responsive transcriptional pathway in BRs. Under normal conditions, BR signaling suppresses the drought response pathway by repressing the expression of RD26. Under drought stress, RD26 was upregulated to inhibit BR-induced growth, thereby increasing drought tolerance [102]. Moreover, RD26 interacted with BES1 and BZR1 and repressed BR levels [53,103,104]. The overexpression of TaBZR2 and TaBES1 can improve the drought tolerance of wheat, and studies suggest that BRs can positively regulate drought tolerance in plants [54,55]. Overexpression of the DWF4 gene increased seed yield in the oilseed crop plant Brassica napus, and transgenic plants showed an increase in root biomass and root length and significantly enhanced tolerance to drought stress compared with the wild-type [33]. We found that interference with StCPD expression enhanced the damage to the membrane system and reduced the resistance to drought stress [56,105]. Overexpression of the CYP85A1 gene promoted root development, increased the accumulation of proline, decreased H2O2 levels, and enhanced drought resistance in transgenic tobacco [42].
On the contrary, under drought stress, BRs can negatively regulate the drought tolerance of plants after the mutation of the key genes in BR synthesis and signaling. In tomatoes, the overexpression of the BR receptor gene BRI1 improved the content of plant ABA and the activities of SOD and POD enzymes, thus negatively regulating plant drought tolerance [57]. An essential transcription factor in BR signaling, BES1, interacted with WRKY46/54/70 to repress drought-induced gene expression, thus negatively regulating drought tolerance [58]. Loss of BEH3 (BES1/BZR1 homolog 3) reduced MDA and ROS contents and increased Pro accumulation in Arabidopsis, thereby enhancing the drought-insensitive properties of the atrzf1 mutant [59]. BRs can inhibit the transcriptional activity of PLTs related to the root development of Arabidopsis thaliana via BZR1/BES1, thereby negatively regulating the drought resistance of plants [60]. In the loss-of-function BdBRI1 mutant of short-stalked grass with significantly higher expression of the drought-related genes BdP5CS, BdERD1, BdRD26, and BdCOR47, the plant height and leaves area were reduced, and the mutant showed greater drought tolerance [61]. BRs can also co-regulate drought tolerance in plants by interacting with other endogenous hormones, such as ABA [95,106]. TINY (a dehydration response element-binding protein in the Arabidopsis AP2/ERF family) promoted ABA-induced stomatal closure, activated drought-responsive gene expression, and inhibited BRs-mediated growth via TINY-BES1 antagonism, and BIN2 prevented an unnecessary stress response under normal conditions via phosphorylation [62].

4.2. Temperature Stress and BRs

Temperature is a major environmental factor that affects crop growth, development, and yield. For most crops, 15–28 °C is the optimum temperature for growth. Irreversible damage is caused to the growth and development of the crop when the ambient temperature exceeds a certain limit, and this environmental factor is known as high-temperature stress [107,108]. Under high-temperature stress, plant growth and development are hindered [109]. The cell membrane plays an essential role in the process of temperature sensing in plants. High temperatures disrupt the cell membrane’s permeability and the intracellular exudation of primary substances, inducing a sharp rise in the content of ROS radicals, inducing oxidative stress [110,111]. Plants accumulate osmoregulators to avoid or minimize heat damage. The accumulation of endogenous hormones helps maintain the stability of plant cell membranes under high-temperature stress and enhances the photosynthetic capacity of the plant’s photosynthetic system, thereby increasing the ability of plants to tolerate high temperatures.
When plants are exposed to high temperatures, they adapt to high-temperature stress by maintaining membrane stability, transmitting heat signals, inducing the expression of heat response genes, and regulating heat response genes by interacting with hormones. Heat stress proteins (HSPs) play a crucial role in plant tolerance to heat stress [112]. When the ambient temperature is 10–15 °C above the plant’s appropriate temperature, the plant quickly activates the defense mechanism, such as synthesizing a large number of HSPs, ROS scavenging enzymes, Pro, and other osmotic protective substances [113,114].
BRs can improve the heat resistance of plants (Figure 4). Recent studies have found that BES1 is rapidly dephosphorylated and activated via heat stress; BES1 directly binds to the heat shock element (HSE) on the HSP70/90 promoter and activates the transcription of the latter; and HsfA1s promotes this activation activity and increases heat stress resistance [63,115]. Under heat stress, the bes1 mutants show decreased photosynthesis, increased lipid peroxide and ABA contents, and increased sensitivity to high temperatures [116]. A study showed that the knock-down of TaBRI1 expression showed a decreased yield and decreased tolerance to intense light and high-temperature stress [64]. BRs can also play a role in heat stress via the transcription factor BZR1 [65]. In the tomato bzr1 mutant, ROS-scavenging enzyme activity and gene expression were inhibited, and BR-induced high-temperature stress tolerance was reduced. At the same time, BZR1 positively regulated heat stress via the FER gene [117]. Ethylene-responsive factors (ERFs) are nodes of ethylene signaling pathways involved in various biological processes and responses to stress [66]. Studies have shown that BRs can improve the heat resistance of plants by inhibiting the expression of ERF49 via BZR1 [67,118]. BIN2 also plays a regulatory role in BR signaling, heat stress BR signaling, and heat stress. BIN2 inhibited BZR1′s dephosphorylation by PP2A and increased the accumulation and activity of ABI5, thereby reducing the heat tolerance of plants [119]. In addition, BIN2 negatively affected heat resistance via the phosphorylation of the activator HsfA1d [68]. In conclusion, BR receptors and their downstream signaling molecules play a significant role in regulating the growth response under temperature stress.
When the environmental temperature is 0–15 °C, plant growth and development and crop production are also limited, and this environmental factor is called low-temperature stress [120,121]. Low-temperature stress is an important environmental factor affecting plant growth and development. The most immediate changes in plants when subjected to low-temperature stress are manifested physiologically. Low temperatures cause leaf stoma to close, reducing the plant’s photosynthetic and respiratory processes and root water uptake, with leaves gradually turning yellow. In severe cases, the plant dies of water deprivation [122,123]. Low temperatures alter the structure of cell membranes, causing damage to cell membranes and the loss of selective permeability in the membrane system, resulting in ionic imbalance, the accumulation of large amounts of ROS in the plant, and inducing the production of toxic O2− and H2O2 in the plant cells [69,124].
Studies have shown that the C-repeat binding factor or dehydration-responsive element-binding protein 1 (CBF/DREB1) plays an essential role in the plant cold response [125]. It contains the AP2/ERF conserved domain, which binds to the cis-elements in the cold-responsive gene (COR) gene promoter to activate gene expression, thereby enabling the accumulation of protective substances in plant cells, such as penetrants and cryoprotective proteins, and improving frost resistance in plants [121,126]. Some transcription factors positively or negatively regulate the expression of CBF under low-temperature stress (Figure 5). For example, the inducer of CBF expression 1 (ICE1) and its homologous ICE2 can positively regulate the expression of the CBF gene and plant frost resistance [121,127]. BRs are involved in the regulation of plant cold resistance. Studies have shown that BIN2 can negatively regulate the expression of the CBF gene via the transcription factors ICE1, BZR1, and CESTA. In the early stage of cold stress, BIN2 kinase activity is inhibited, resulting in the maximum induction of the CBF gene, thereby improving the frost resistance of plants. BIN2 activity then increases, and CBF expression decreases [70,128]. The overexpression of DWARF in tomatoes reduced protein oxidation and lipid peroxidation and upregulated GRX expression, thereby improving cold tolerance [71]. The overexpression of DWF4 in Arabidopsis upregulated the cold response gene COR15A and improved cold resistance [72]. The overexpression of the BZR1 gene in tomatoes improved tolerance under low-temperature stress and increased ABA synthesis by activating NCED1. BIN2 negatively regulated BZR1 protein accumulation and cold tolerance by inhibiting ABA biosynthesis [74]. The overexpression of SlBRI1 regulated ROS levels, phytohormone biosynthesis and signaling, and the expression of CBF and COR genes, thereby positively regulating plant tolerance to low-temperature stress [73]. In Arabidopsis, gain-of-function mutants of the transcription factors BZR1 and BES1, the core transcription factors in BR signaling, significantly decreased electrolyte leakage under cold stress, indicating that they positively regulated the plant’s freezing tolerance. BZR1 directly acts on the promoters of CBF1 and CBF2, regulating their expression both extracellularly and intracellularly. BZR1 also regulated other COR genes not coupled to CBF, thereby regulating the plant’s response to cold stress. These results suggest that BZR1 positively regulates plant cold tolerance via the CBF-dependent and CBF-independent pathways [75].

4.3. Salt Stress and BRs

Salt stress seriously affects crop development and survival. Salt stress is mainly caused by neutral salts such as NaCl and Na2SO4 [129,130]. Plants generally maintain a high K+, low Na+ state [131]. When more salt ions enter a plant, salt stress leads to ion imbalance, resulting in increased toxicity of Na+, inducing ion stress in the plant, damaging the cell membrane structure, and changing the normal physiological metabolism levels [132]. With the accumulation of soluble salt in the soil, a high concentration of Na+ reduces the soil water potential and makes it difficult for roots to absorb water, resulting in osmotic stress and physiological drought [133]. At the same time, Na+ absorbed by roots accumulates in stems and leaves via transpiration, which reduces the plant’s yield. In addition, osmotic stress can cause ABA accumulation. A significant protective structure of plant cells is the cell membrane, which can regulate the ion balance in the cell [129]. Under salt stress, plants produce a large number of ROS, which can not only continuously induce lipid peroxidation but also lead to protein denaturation and, thus, the denaturation of cell membranes and even cell damage or death [134,135]. When the salt concentration increases, plant photosynthesis also changes, including the destruction of the chloroplast structure and the reduction in the photosynthetic pigment content and photosynthetic enzyme activity, and, finally, plant growth is inhibited [136].
Under salt stress, plants regulate their physiological and biochemical status as well as the expression of related genes to maintain their normal growth, and BR signaling can regulate stomatal density and conductance to regulate tissue water loss under high salt conditions (Figure 6). Studies have shown that the overexpression of the DET2 gene in tobacco improves membrane lipid peroxidation and increases enzyme activity under salt stress, thereby increasing the tolerance of tobacco to salt stress [76]. We found that the overexpression of the StDWF4 gene in potatoes enhanced salt tolerance [77]. The overexpression of PeCPD in woody plants enhanced gene expression during BR synthesis and metabolism and improved plant growth and salt tolerance [78]. BZR1 positively regulated salt tolerance and upregulated the expression of various stress-related genes in tomatoes [79]. The overexpression of the BZR1 gene in tobacco enhanced the BR signaling and response in tobacco, reduced the levels of H2O2 and O2− accumulation in the body under salt stress, alleviated cell damage, and ultimately improved the salt tolerance of transgenic tobacco [80]. The ZmBES1/BZR1-5 protein reduced the sensitivity of plants to ABA and increased their tolerance to osmotic stress by regulating the expression of many downstream genes, which ultimately led to an increase in salt tolerance [81]. In addition, Arabidopsis growth was inhibited under salt stress by promoting the accumulation of the BZR1-targeted SUMO protease ULP1a, which desulfonylated BZR1 in the cytoplasm [82]. Different GSK3-like kinases can regulate different abiotic stress responses by phosphorylating different proteins. BIN2, a typical GSK3-like kinase, acts as a rate-limiting regulator that avoids the over-activation of SOS2 under salt stress and as an inhibitory factor that suppresses the activity of SOS2 via SOS3 and SCaBP8 during the recovery period after salt stress, as well as promoting plant growth [70,83]. Studies have shown that BIN2 negatively regulates the salt stress signaling pathway in Arabidopsis by activating the AGL16 protein [84]. In addition, HOP1 and HOP2 promoted the accumulation of BIN2 and HSP90; BZR1 was also accumulated in the cells; and the BR content was significantly increased to stimulate plant growth under salt stress [85]. In conclusion, BRs can regulate plant salt tolerance via the synergistic action of related genes and transcription factors and the interaction between BRs and other hormone signals.

4.4. Heavy Metal Stress and BRs

Soil is a principal part of the ecological environment and an essential material basis for human survival and development. Heavy metals are easily stored in the soil, seriously threatening the sustainable use of soil resources and food security [137,138]. Pollution caused by heavy metals is long-term, irreversible, and hidden once it enters the environment [139,140]. After heavy metals enter the soil, they mainly enter plants via the root system, pass through the xylem, and then distribute to different tissues in above-ground parts [141]. Heavy metal stress can inhibit the division of the nuclei of the root tip cells of the plant and affect root elongation and growth. Numerous studies have shown that, when plants are subjected to heavy metal stress, root vitality is reduced and roots grow slowly or even decay, hindering water transportation from the root system to the above-ground parts of the plant, interfering with the normal physiological metabolic process, and directly affecting the growth and development of the plant [142,143]. When heavy metals enter the plant, the plant cell nuclei have a synergistic effect, changing the internal structure of the chloroplasts. The content of photosynthetic enzymes within the chloroplasts is reduced, the leaf stomata close, and the photosynthetic intensity is reduced [144]. Subjecting a plant to heavy metal stress results in a reduction in the selective permeability of the plasma membrane, the exudation of ions and organic matter out of the cell membrane, and the entry of harmful substances into the cells, which leads to physiological dysfunctions [145]. At the cellular level, heavy metals can stimulate ROS production and cause oxidative stress, resulting in cell membrane damage and the inactivation of antioxidant enzymes, thus affecting the function and viability of plant cells [146]. The plant root system will secrete some characteristic substances, such as organic acids, amino acids, soluble sugars, etc. Under heavy metal stress, changes in the quantity and composition of plant root secretions can influence the mobility of heavy metals and microbial activity, thus reducing the entry of heavy metals into the plant [147,148].
BRs can alleviate the damage to plants under heavy metal stress. Results show that heterogeneic overexpression of PeDWF4 significantly increases the biomass of transgenic tobacco plants. Osmotic regulation of transgenic tobacco lines under CuSO4 stress was mainly achieved by increasing the contents of proline and soluble proteins. The resistance to CuSO4 stress was improved by increasing SOD and POD contents and reducing chlorophyll loss. This may be due to the allogeneic overexpression of the PeDWF4 gene, which enhanced the endogenous BR synthesis ability of tobacco and increased the endogenous brassinolide content, thus improving the tolerance of transgenic tobacco lines to heavy metal stress [86]. By analyzing the expression pattern of the PscCYP716A1 gene and measuring the endogenous BR content, it was proved that PscCYP716A1 mediated endogenous BR biosynthesis, enhanced the osmoregulation ability, and strengthened the antioxidant system by maximizing the endogenous BR content. In addition, when the PscCYP716A1 gene was overexpressed, the accumulation and transport capacity of cadmium in poplar were also improved [87]. The BRI1 activation signal cascade upregulates the expression of transcription factors, thereby enhancing the transcription of brassinosteroid genes [149,150]. The increased expression of these genes increases endogenous BR levels, which help alleviate heavy metal stress. The interaction between BRs and GA is complex. The DELLA protein plays a blocking role in GA signal transduction. Under heavy metal stress, the activity of ROS-scavenging enzymes is increased due to the interaction between the DELLA protein and BRZ1, thus improving the resistance of plants to heavy metals [88]. BR-mediated transcription factors regulate heavy metal stress, and crosstalk with other plant hormones under heavy metal stress has been studied. Nevertheless, the regulatory mechanisms involved are poorly understood and will provide new directions for the study of plant stress.

5. Conclusions

As important plant hormones, BRs have a large and complex signaling regulatory network. In this study, it was concluded that up-regulation or down-regulation of BR-related genes and transcription factors directly regulated endogenous BR levels, thereby regulating plant responses to abiotic stress. In addition, the structure of BRs and the significant components and molecular mechanisms involved in these processes have been understood. However, it is undeniable that there are still many knowledge blind spots and details that must be further investigated. For example, BRs can regulate abiotic stresses in plants, but the mechanisms of stress resistance have not been fully explored. In addition, BRs can crosstalk with other plant endogenous hormones, such as ABA, ETH, etc., to jointly regulate abiotic stress, but the mechanism of their interactions with other signaling pathways has not been fully investigated. Therefore, with the development of biotechnology, exploring the regulatory network and potential mechanisms of BRs to improve crop yield and resistance to abiotic stress will provide a new direction for future research.

Author Contributions

X.Z. provided the study idea. R.M. wrote the original draft. C.L., Z.L., D.Z., S.C., J.L., W.T., C.W., J.W. and Z.C. collected the data and constructed the graphs. S.C., C.W. and J.W. reviewed and edited the manuscript. X.Z. made the final revisions to the paper. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (no. 31960443)/the Research Program Sponsored by the State Key Laboratory of Aridland Crop Science, Gansu Agricultural University (no. GSCS-2018-4)/the Research Program Sponsored by the Youth Mentor Fund, and Gansu Agricultural University (no. GSAU-QDFC-2021-14).

Data Availability Statement

Data are contained within the article. No data were generated or analyzed in this research.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. The biosynthetic pathway of BRs, showing the CN-dependent pathway and the CN-independent pathway.
Figure 1. The biosynthetic pathway of BRs, showing the CN-dependent pathway and the CN-independent pathway.
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Figure 2. Model of the signaling pathway of brassinosteroids (adopted from Chaudhuri’s study [51]).
Figure 2. Model of the signaling pathway of brassinosteroids (adopted from Chaudhuri’s study [51]).
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Figure 3. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to drought stresses. Note: Agronomy 14 00356 i001 represents a promoted function; Agronomy 14 00356 i002 represents an inhibited function, same as below.
Figure 3. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to drought stresses. Note: Agronomy 14 00356 i001 represents a promoted function; Agronomy 14 00356 i002 represents an inhibited function, same as below.
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Figure 4. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to high-temperature stresses.
Figure 4. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to high-temperature stresses.
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Figure 5. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway under cold stresses.
Figure 5. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway under cold stresses.
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Figure 6. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to salt stress.
Figure 6. The working model of major genes and transcription factors in BR biosynthesis and signaling pathway responding to salt stress.
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Table 1. Responses of brassinosteroids to different abiotic stresses in plants.
Table 1. Responses of brassinosteroids to different abiotic stresses in plants.
Abiotic StressesBiological FunctionPlant SpecieReference
Drought stressGhBZR1 inhibited GhBEE3-Like gene expression and improved drought resistanceGossypium hirsutum L.[52]
BZR1 and BES1 inhibited RD26 expression and drought toleranceArabidopsis thaliana[53]
Overexpression of TaBZR2 and TaBES1 increased drought resistance Triticum aestivum L.[54,55]
Under the drought, overexpression of the DWF4 increased the yield Brassica napus[33]
Interference expression of the StCPD reduced resistance to drought stress Solanum tuberosum[56]
Overexpression of the CYP85A1 enhanced drought resistanceNicotiana tabacum L.[42]
The SlBRI1 gene expression negatively regulated drought resistanceSolanum lycopersicum L.[57]
BES1 interacts with WRKY46, 54 and 70 to negatively regulated drought toleranceArabidopsis thaliana[58]
Loss of the BEH3 gene in Arabidopsis improved drought resistanceArabidopsis thaliana[59]
BZR1/BES1 inhibited the transcriptional activity of PLTs and negatively regulated drought resistanceArabidopsis thaliana[60]
Down-regulation of the BdBRI1 gene increased drought resistanceBrachypodium distachyon[61]
The TINY interacted with and antagonized the BES1 to improve drought resistanceArabidopsis thaliana[62]
Temperature stressBES1 and HSFA1 interacted to enhance heat resistanceArabidopsis thaliana[63]
The bes1 mutant increased sensitivity to high temperatureArabidopsis thaliana[64]
The TaBRI1 knock-down mutant reduced tolerance to high-temperature stressTriticum aestivum L.[65]
The BZR1 positively regulated heat stressSolanum lycopersicum L.
Arabidopsis thaliana		[66,67]
The BIN2 inhibited heat resistance by activating ABI5 and HSFA1SArabidopsis thaliana[68,69]
The BIN2 inhibited cold tolerance by down-regulating CBF expressionArabidopsis thaliana[70]
Overexpression of the DWRF enhanced the expression of GRX to improve cold toleranceSolanum lycopersicum L.[71]
Overexpression of DWF4 enhanced the expression of COR15A to improve cold toleranceArabidopsis thaliana[72]
Overexpression of the SlBRI1 increased plant tolerance to low temperature stressSolanum lycopersicum L.[73]
The BZR1 positively regulated low temperature stress Solanum lycopersicum L.
Arabidopsis thaliana		[74,75]
Salt stressOverexpression of the DET2 increased salt toleranceNicotiana tabacum L.[76]
Overexpression of the StDWF4 enhanced salt toleranceSolanum tuberosum[77]
Overexpression of the PeCPD improved plant growth and salt tolerancePopulus tomentosa[78]
Overexpression of BZR1 increased salt tolerance Nicotiana tabacum L.
Solanum lycopersicum L.		[79,80]
ZmBES1/BZR1-5 improved salt tolerance Arabidopsis thaliana[81]
Reduction in salt tolerance by deSUMOylation of BZR1Arabidopsis thaliana[82]
BIN2 and the SOS3/ SCaBP8-SOS2 module interacted to coordinate salt stressArabidopsis thaliana[83]
The BIN2 negatively regulated salt stressArabidopsis thaliana[84]
HOP enhanced salt tolerance by promoting BIN2-HSP complex accumulation. Arabidopsis thaliana[85]
Heavy metal stressOverexpression of the DWF4 improved the resistance of CuSO4 stress Nicotiana tabacum L.[86]
Overexpression of the PscCYP716A1 improved the accumulation and transport capacity of CdPopulus[87]
DELLA protein interacted with the BRZ1 to enhance plant resistance to heavy metalsArabidopsis thaliana[88]
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Miao, R.; Li, C.; Liu, Z.; Zhou, X.; Chen, S.; Zhang, D.; Luo, J.; Tang, W.; Wang, C.; Wu, J.; et al. The Role of Endogenous Brassinosteroids in the Mechanisms Regulating Plant Reactions to Various Abiotic Stresses. Agronomy 2024, 14, 356. https://doi.org/10.3390/agronomy14020356

AMA Style

Miao R, Li C, Liu Z, Zhou X, Chen S, Zhang D, Luo J, Tang W, Wang C, Wu J, et al. The Role of Endogenous Brassinosteroids in the Mechanisms Regulating Plant Reactions to Various Abiotic Stresses. Agronomy. 2024; 14(2):356. https://doi.org/10.3390/agronomy14020356

Chicago/Turabian Style

Miao, Rong, Caijuan Li, Ziliang Liu, Xiangyan Zhou, Sijin Chen, Dan Zhang, Jiaqi Luo, Wenhui Tang, Cuiling Wang, Jiling Wu, and et al. 2024. "The Role of Endogenous Brassinosteroids in the Mechanisms Regulating Plant Reactions to Various Abiotic Stresses" Agronomy 14, no. 2: 356. https://doi.org/10.3390/agronomy14020356

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