The molecular taste receptor, found in humans and rodents, responds to asparagine and aspartic acid . Asparagine is considered to serve as a nitrogen storage molecule and synthesized at night under low-carbon conditions . Asparagine and glutamate are synthesized from aspartate and glutamine through ASPARAGINE SYNTHETASE1 . Likewise, proline levels change in response to energy levels. PROLINE DEHYDROGENASE converts proline to glutamate . Recent studies demonstrate that S1-bZIPs directly regulate the expression of ProDH and ASN1 via binding to the C-boxes, ACT motifs , and G-boxes in their promoters, thereby influencing amino acid metabolism . Over expression of tbz17 mORF in tobacco significantly induces the expression of ASN, whereas silencing of tbz17 represses the expression of ProDH and ASN . One of the target genes of AtbZIP53 is ProDH2 . Over expression of SlbZIP1 and AtbZIP11 mORFs in the transgenic tomato and Arabidopsis significantly up-regulates the expression of ASN1 and ProDH2 and affects amino acid contents . For example, over expression of SlbZIP1 increases the content of alanine, aspartic acid, glutamate, serine, threonine, tyrosine, and total amino acid content. Energy deprivation induces the expression of ASN1 and ProDH, which contributes to the recycling of amino acids to mitigate deficits of carbon, nitrogen, and energy . Many amino acid catabolism related genes induced by AtbZIP11 are largely repressed by treatments with sugar . Moreover, under highsucrose conditions, the translation of AtbZIP11 is inhibited via a uORF . These findings indicate that ASN1 and ProDH are ultimately regulated in a sugar-dependent manner, blueberry pot with AtbZIP11 acting as the link between sugar signaling and amino acid/nitrogen metabolism .
Additionally, AtbZIP1 and AtbZIP53 are also involved in modulating amino acid metabolism during stress responses . In Arabidopsis, it has been demonstrated that AtbZIP53 preferentially forms heterodimers with group C-bZIP members like AtbZIP9, AtbZIP10, and AtbZIP25 for controlling the gene expression of ASN1 and ProDH . However, the interacting partners between the S1- and C-bZIPs are not identified in many other crops and need to be investigated in the future.Overexpression of S1-bZIP mORFs induces sugar-related gene expression and increases sugar content . Previous studies have shown that over expression of tbz17 and SlbZIP1 mORF up-regulates the expression level of genes encoding sucrose phosphate synthase and sucrose phosphate phosphatase , whereas silencing tbz17 down-regulates the expression of these genes . Furthermore, it has been demonstrated that constitutive expression of the S1-bZIP1s such as tbz17 and AtbZIP11 mORF significantly increases the sucrose concentration in transgenic lines . Interestingly, the contents of glucose and fructose were significantly increased and the citric acid content was significantly decreased in transgenic plants with over expression AtbZIP11 . The induction of the AtbZIP11 mORF also results in the up-regulation of genes associated with the metabolism of trehalose, myo-inositol and raffinose. Transgenic Arabidopsis lines over expressing AtbZIP11 showed decreased contents of the trehalose-6-phosphate , limiting the plant’s ability to use available sugars, thereby slowing plant growth. This growth inhibition in Arabidopsis cannot be reversed by the exogenous application of metabolizable sugars such as glucose and sucrose .
The use of the fruit-specific E8 promoter to drive over expression of SlbZIP1 increases the sugar contents in tomato while avoiding growth impairment . Remarkably, sucrose contents were approximately sixfold higher in transgenic lines with approximately 1.5-fold higher fructose, glucose, and total sugar contents than in wild type. Similar effects such as significantly increased glucose and fructose contents and significantly reduced citric acid content were observed in mutants with enhanced FvebZIP1.1 mORF protein expression due to the uORFs mutation . In a recent study, heterologous over expression of strawberry FvbZIP11 affects fruit quality and flavor in tomato . In comparison with wild type, the total soluble solid was significantly increased at the breaker, pink and red ripe stages in three transgenic tomato lines. The soluble sugar content was significantly accumulated at 30–50 days after anthesis in transgenic line 6. In addition, the titratable acid content was significantly reduced at 30 days after anthesis, while SS/TTA ratio was significantly increased from 20 to 50 days after anthesis in the transgenic tomato line . Taken together, these studies demonstrate that the S1-bZIPs play important roles in the regulation of sugar metabolism for quality improvement in plants.S1-bZIPs play an essential role in plant adaptation to unfavorable conditions . It has been documented that S1-bZIPs play important roles in plant innate immunity, especially against attack by various pathogens , and in response to abiotic stresses, such as cold , drought , and salinity . It has been demonstrated that the C-/S1-bZIP-SnRK1 complex participates in the reprogramming of primary metabolism related to carbohydrate and amino acid and induces salt stress tolerance through ABA-independent signaling in Arabidopsis roots .
Similarly, C-/S1-bZIP-SnRK1 signaling is involved in defenses against biotic stresses, which are also energy-consuming processes that require metabolic readjustment in plants . Research in our laboratory has suggested that petunia PhOBF1, a homolog of AtbZIP11, is involved in plant defenses against a wide range of viral pathogens . In the study, silencing PhOBF1 resulted in the reduction of RNA silencing-related gene expression, including RNA-dependent RNA polymerases, Dicer-like RNase III enzymes, and Argonaut. PhOBF1-RNAi plants displayed a compromised resistance to tobacco rattle virus and tobacco mosaic virus . On the other hand, over expression of PhOBF1 in petunia enhances resistance to these virus infections. Interestingly, PhOBF1-silenced petunia lines produced much lower levels of the compounds associated with the shikimate and phenylpropanoid pathways such as free salicylic acid , salicylic acid glucoside, and phenylalanine, but much higher levels of those were detected in PhOBF1 over expressing plants . Intriguingly, PhbZIP44, a paralog of PhOBF1 appears to be unable to participate in this antiviral process, suggesting functional diversity and specificity among the S1-bZIPs . In Arabidopsis, S1-bZIPs AtbZIP11/ATB2, AtbZIP44, AtbZIP2/GBF5, and AtbZIP53 can bind to a 6-bp cis-acting element located in the promoter of ProDH , which is responsive to hypoosmolarity and proline. AtbZIP53 directly and strongly promotes hypoosmolarity induced transcription of ProDH, which is enhanced by the synergistic interplay between AtbZIP53 and the group C member AtbZIP10 . Analysis of transcriptome data has revealed the complexity of the response to abiotic stresses by S1-AtbZIPs. For instance, the transcript level of AtbZIP53 was found to be strongly up-regulated by salt stress in roots and by osmotic stress in green tissues. Cold, osmotic, and salt elicitors were found to remarkably increase the expression of AtbZIP1 in roots and AtbZIP11 in green tissues but inhibit the expression of AtbZIP2 in green tissues. AtbZIP44 shows a solid and specific response to cold stress in the root and to salinity in green tissues . The expression of AtbZIP1 in roots was significantly induced by salt treatment. Arabidopsis bzip1 bzip53 double mutant reprograms carbohydrate and amino acid metabolism to help roots adapt to salt stress. Furthermore, AtbZIP1 binds the promoter of BCAT2 and TAT7 and plays a role as a signalling module of SnRK1-bZIP1 under salt stress. This pathway is independent of ABA-SnRK2-AREB signaling pathways, whereas bZIP53 transcription partially depends on the SnRK2/AREB pathway . In tomato, SlbZIP1 increases salt tolerance by increasing the gene expression related to ABA biosynthesis and signal transduction . In response to water deficiency, two cucumber S1-bZIP member transcripts accumulated in the root but decreased in leaves . Likewise, in sweet potato, the expression of IbbZIP1 is highly induced by treatments with NaCl and ABA. Abiotic stress-related genes are significantly up-regulated in the transgenic Arabidopsis over expressing IbbZIP1, suggesting the role of IbbZIP1 in salt and drought tolerance . In apple, an S1-bZIP, MdbZIP80, has been shown to negatively regulate cytokinin-mediated drought and salt tolerance . This study shows that MdbZIP80 specifically heterodimerizes with C-bZIPs MdbZIP2 and MdbZIP39. The formed C-/S1-bZIP complex then binds to the ACTCAT motif in the promoter of MdIPT5b, a gene encoding the rate-limiting enzyme isopentenyltransferase in the cytokinin biosynthesis pathway, thereby suppressing its expression. This leads to drought and salt stress response through the cytokinin pathway by delaying drought-induced premature leaf senescence by reducing oxidative damage and maintaining plant growth . Another study demonstrates that low temperature stress induces mlipl5 expression, nursery pots and the protein subsequently binds to the promoter region of Adh1 . Interestingly, mechanical damage in tea leaves leads to the activation of S1-bZIPs such as CsbZIP2, −11, −14, −16, −20, −21, −28 and −30 . Overall, it appears that the expression levels of these S1-bZIPs respond to stress signals in a tissue-specific manner. The members of S1-bZIP share partially redundant functions but play a role in unique regulatory mechanisms. Generally, the S1- and C-AtbZIPs heterodimerize to mediate stress signal transduction cascades. For example, S1-bZIP AtbZIP53 forms heterodimers with group C-bZIP members such as AtbZIP10 or AtbZIP25 and increases DNA binding activity, resulting in strong activation of the target genes. These heterodimers can also form tertiary complexes with the non-bZIP protein ABI3 to play a synergistic role in target gene expression ; however, it needs to be demonstrated whether other members of S1-bZIP such as AtbZIP1 heterodimers are formed under stress conditions .
The S1-bZIP gene low-temperature-induced protein 19 is significantly induced by low temperature in monocots . The LIP19 protein appears to be unable to form homodimers and bind to DNA in rice . However, the counterpart of LIP19 proteins in maize and wheat can form homodimers and bind to cis-elements in DNA sequences . The WLIP19 can heterodimerize with wheat TaOBF1, another low temperature-responsive S1-bZIP member. The stable heterodimerization between LIP19-type and OBF1-type proteins seems to induce the expression of target genes in response to different abiotic stresses, especially cold stress . However, there is no definitive evidence showing that the formation of heterodimers or homodimers between WLIP19 and TaOBF1 directly affects the expression of the downstream stress-responsive genes including COR and LEA genes . Recent research indicates that a group C-bZIP TabZIP6 dimerizes with WLIP19, TaOBF1, or itself and then binds to the promoters of genes encoding CBFs , resulting in inhibition of their expression. These dimers can also inhibit the expression of some COR genes . Rice S1-bZIP plays a vital role in ABA-mediated drought and salt stress response. One of the S1-bZIPs, OsbZIP71, appears to be able to form homodimers and heterodimers with group C-bZIP members OsbZIP15, OsbZIP20, OsbZIP33, and OsbZIP88. It has been speculated that these heterodimers help OsbZIP71 bind to the promoters of its target genes, OsNHX1, and COR413-TM1 because OsbZIP71 on its own has weak DNA-binding activity to the G-box element and no transcriptional activation activity . Thus, the interplay between C-group and S1-subgroup is proposed to affect plant response to stress.Plant growth and development are tightly interlinked with the control of metabolism, especially energy homeostasis. Transient energy deprivation causes plants to adjust their metabolism to adapt to daily light/dark cycles and unpredictable environmental changes. It has been proposed that the Snf1- related kinase 1 and Target of Rapamycin kinase function to reprogram plant metabolism in response to the energy status . Evidence suggests that SnRK1 mediates the phosphorylation of S1-bZIPs to control plant growth and development under starvation and nutrient-replete conditions . As the transcriptional regulators downstream of SnRK1, AtbZIP11 can directly control a subset of SnRK1-dependent genes via binding to G-box elements in their promoter regions . Furthermore, heterodimerization between group C- and S1- bZIPs is enhanced by the phosphorylation of group C-bZIPs by SnRK1. Phosphorylation of AtbZIP63 provides the structural basis for forming the AtbZIP63-AtbZIP1-SnRK1/AtbZIP63- AtbZIP11-SnRK1 complex and ultimately leads to the adjustment of metabolism to ensure plant survival under low energy conditions . Notably, the formation of the complex is dependent on the SnRK1-specific phosphorylation sites, which are pivotal for the function of AtbZIP1 and AtbZIP53 . Additionally, the identification of many SnRK1-independent genes regulated by AtbZIP11 indicates a function of AtbZIP11 beyond SnRK1 signaling . It seems that heterodimers within the C-/S1- bZIP network function as a hub to integrate SnRK1-dependent and -independent signals to adjust growth/development and stress responses . Recent studies showed that S1-bZIPs regulate the root apical meristem size through controlling polar auxin flux . Under low energy conditions, AtbZIP2, AtbZIP11, and AtbZIP44 directlyactivate the transcription of INDOLE-3-ACETIC ACID PROTEIN 3/SHORT HYPOCOTYL 2 , a negative regulator of auxin signaling, which leads to the down-regulation of PIN-FORMED genes, limiting polar auxin transport to the root tip and blocking auxin-driven primary root growth .