EFFECTS OF FLAVONOID METABOLISM ON PLANT RESPONSE TO STRESS TOLERANCE
Flavonoids are a class of secondary metabolites of polyphenols with C6-C3-C6 as the basic structure or phenyl-benzopyran structure. Flavonoids also are a large class of secondary metabolites formed by plants in the long-term ecological adaptation process to withstand the stress of harsh ecological conditions, animals, and microorganisms. They are widely distributed in the plant kingdom and are abundant in flowers, fruits and leaves of many plants (Du et al., 2010). Based on the different oxygen rings and conformations of the basic molecular structure of flavonoids, flavonoids are generally divided into six categories: flavone, flavonol, isoflavone, flavanone, flavanol and anthocyanidin (Rice-Evans et al., 2010). The starting substrate for plant flavonoid biosynthesis is derived from coumaroyl-CoA of the phenylpropane metabolic pathway and malonyl-CoA from acetyl-coenzymes. Under the action of chalcone synthase (CHS), they first form chalcone (Aoki et al., 2000), and then the naringenin is formed by the catalytic action of chalcone isomerase (CHI) (McKhann and Hirsch, 1994). Under the catalysis of cytochrome P450 monooxygenase (CPM) and other enzymes, naringen can be used as a major intermediate metabolite to synthesize other flavonoids (Akashi et al., 1999; Falcone Ferreyra et al., 2012; Lam et al., 2014; Liu et al., 2003; Uchida et al., 2015).
More than 10,000 plant flavonoids have been discovered (Aoki et al., 2000; Jiang et al., 2010). They play very important roles in plant resistance to various stress tolerances (Agati et al., 2012; Yamasaki et al., 1997; Yan, et al., 2014). They could remove free radicals under ultraviolet radiation (Li et al., 1993; Treutter et al., 2005), improve seed storage capacity and prolong life (Debeaujon et al., 2000), change petal color (Mola et al., 1998), interfere with the polar distribution of auxin (Buer et al., 2004), affect the accumulation and composition of fatty acids (Lian et al., 2017), etc.
Early studies on the mechanism of flavonoids involved in stress resistance mainly focused on their regulations on response to ultraviolet radiation (Mellway et al., 2009; Tattini et al., 2006). Later, flavonoids were found with strong antioxidant activity (Agati et al., 2007; Hernández et al., 2009; Pourcel et al., 2007; Treutter et al., 2006). Since various stresses can cause excessive peroxide to accumulate in plants, the significant role of flavonoids in plants’ stress resistance attracts increasing interests (Fasano et al., 2014; Qiu et al., 2008; Rai et al, 2016; Watkins et al., 2014). Tattini et al. (2004) reported that European privet flavonoids as antioxidants respond to strong light and drought stress. Li et al. (2011) found a conserved trans-acting element (G-box, CACGTG) in the promoter region of the chalcone synthase family gene (AtCHS ) in Arabidopsis thaliana , which regulates the accumulation of H2O2 by responding to cGMP signals (Abu Zahra et al., 2014). Yan et al. (2014) found that the cytochrome P450 monooxygenase GmFNSII/GmCPM in soybean was beneficial to the accumulation of flavonoid aglycones in plants and the reduction of H2O2 content. In previous studies, we found that the content of flavonoids such as quercimeritrin in salt-tolerant soybeans is relatively higher than that of salt-sensitive soybeans, which is beneficial for soybeans to adapt to salt stress (Lu et al., 2013). With the deepening of research, we further discovered that enzymes related to the flavonoid metabolism pathway are important salt stress response factors, and they can significantly regulate the salt tolerance of plants such as Arabidopsis thaliana and soybean (Pi et al., 2016). We recently found that the salt-triggered phosphorylation of GmMYB173, subsequent elevates the transcription ofGmCHS5 for enhancing the accumulation of dihydroxy B-ring flavonoids (such as cyaniding-3-arabinoside chloride) (Pi et al., 2018); while salt-inhibited phosphorylation of GmMYB183 subsequently decreases the transcription of GmCYP81E11 for reducing monohydroxy B-ring flavonoids (such as ononin) (Pi et al., 2019). Actually, both GmMYB173 phosphorylation and GmMYB183 dephosphorylation contribute to soybean salt tolerance.
The abovementioned studies showed that flavonoids played a very important role in the response of plants to stress. However, there is no direct evidence been found to show us whether bZIP could regulate flavonoid accumulation for plant adaption to these stresses.
CONCLUDING REMARKS Due to their significant roles in plant tolerances to various stress, the bZIP transcription factors have been comprehensively studied, including their categorization and regulatory mechanisms of target genes. However, there is at least one interesting issue worthy of further investigation: Whether bZIP transcription factor regulates plant stress tolerance by modulating the synthesis of flavonoids.
To date, plenty of literatures show that bZIPs regulate plant tolerances to various abiotic stresses, such as low temperature, drought, and high salt. Besides, there are many reports reveal that flavonoids participate in various stress responses. Moreover, a lot of researches have now confirmed that bZIP transcription factors play an important role in the synthesis of flavonoids. Specially, bZIPs in subfamily H could bind to G-box in promoter of cold responsive genes (Table I and II); members of this subfamily also could modulate the synthesis of some flavonoids (Table III). Since members in this group shares similar conversed protein motifs (supplemental Figure S1 and S2), it is reasonable to hypothesize that plant bZIPs in subfamily H could bind to G-box of cold-responsive genes to further regulate the synthesis of flavonoids. Similarly, it also makes sense that bZIPs in subfamily A could regulate the synthesis of flavonoids by binding to G-box or ABRE of genes involved in cold, salinity, drought and osmotic stresses; subfamily S could regulate the synthesis of flavonoids by bind to G-box or C-box or A-box or ABRE of genes involved in cold, salinity and drought stresses (Table I, II and III). However, these hypotheses are still needed to be further verified.
ACKNOWLEDGEMENTS
This work was supported by the grants 31970286 and 31301053 from the National Science Foundation of China, LY17C020004 from the Natural Science Foundation of Zhejiang Province.