RrMYB5‐ and RrMYB10‐regulated flavonoid biosynthesis plays a pivotal role in feedback loop responding to wounding and oxidation in Rosa rugosa

Abstract

Summary Flavonoids play critical roles in plant responses to various stresses. Few studies have been reported on what the mechanism of activating flavonoid biosynthesis in plant responses to wounding and oxidation is. In this study, flavonoid metabolites and many MYB transcript factors from Rosa rugosa were verified to be induced by wounding and oxidation. RrMYB5 and RrMYB10, which belong to PA1‐ and TT2‐type MYB TFs, respectively, showed extremely high induction. Overexpression of RrMYB5 and RrMYB10 resulted in an increased accumulation of proanthocyanidins in R. rugosa and tobacco by promoting the expression of flavonoid structural genes. Transcriptomic analysis of the transgenic plants showed that most genes, involved in wounding and oxidation response and ABA signalling modulation, were up‐regulated by the overexpression of RrMYB10, which was very much similar to that observed in RrANR and RrDFR overexpression transgenics. RrMYB5 and RrMYB10 physically interacted and mutually activated each other's expressions. They solely or synergistically activated the different sets of flavonoid pathway genes in a bHLH TF EGL3‐independent manner. Eventually, the accumulation of proanthocyanidins enhanced plant tolerance to wounding and oxidative stresses. Therefore, RrMYB5 and RrMYB10 regulated flavonoid synthesis in feedback loop responding to wounding and oxidation in R. rugosa. Our study provides new insights into the regulatory mechanisms of flavonoid biosynthesis by MYB TFs and their essential physiological functions in plant responses to wounding and oxidative stresses.

Advances in Biosynthesis and Biological Functions of Proanthocyanidins in Horticultural Plants

“…The transcriptional level of LoMYB29 in Larix olgensis was upregulated by wounding, high light intensity, NaCl, PEG6000, methyl jasmonate (MeJA), and abscisic acid (ABA) treatments, and ectopic overexpression of LoMYB29 enhanced the PAs to accumulate in Arabidopsis leaves [159]. This is in agreement that wounding, oxidative stress and salicylic acid (SA) can trigger the upregulated expression of RrMYB5, RrMYB10 (Rosa rugosa), and RcMYBPA2 (Rosa chinensis), which can then activate the promoter of PAs structural genes and result in accumulation of PAs in roses [31,160]. PAs are known as a powerful antioxidant that has been proved to increase the antioxidant capacity of plants [6].…”

“…A-type PAs are mainly found in bilberry, peanuts, plums, cranberries, curry, and cinnamon [46][47][48][49]. accumulation of PAs is associated with the resistance of plants against various biotic and abiotic stimuli, such as low temperature [27,28], drought [29], wounding [30,31], UV radiation [30], and fungal pathogens [32][33][34]. Therefore, increasing attention has been focused on the metabolic engineering and regulatory mechanism of PAs in horticultural plants.…”

“…The MBW complex in Arabidopsis, composed of AtMYB123 (TT2), AtbHLH42 (TT8), and TTG1 proteins, was reported to activate the expression of DFR, LDOX, and ANR (BAN) genes, which lead to the accumulation of PAs in the seed coat [93,94]. A large number of homologs of TT2, TT8, and TTG1 have been identified in various plants, such as FaMYB9/11, FabHLH3, and FaTTG1 in strawberry [95], LjTT2a/2b/2c in Lotus japonicus [96], VvMYBPA2/PAR in Vitis vinifera [97], TaMYB14 in Trifolium arvense [98], TaMYB10-A1/-B1/-D1 in wheat [99], HvMYB10 in Hordeum vulgare [100], Tc-MYBPA in Theobroma cacao [101], MtMYB5/14 in M. truncatula [102], MdMYB9/11/12 in apple [27], PtMYB115 in poplar [34], CsMYB60 in cucumber [103,104], RrMYB10 in Rosa rugosa [31], AabHLH1 in Anthurium andraeanum [105], DkMYB2/4, DkMYC1, and DkWDR1 in persimmon [24,106,107], MtWD40-1 in M. truncatula [108], FhTTG1 in Freesia hybrida [109], and SlAN11 in tomato [110]. These factors are transcriptional activators of PAs biosynthetic pathways, suggesting that the MBW complexes are well conserved in higher plants [87,94].…”

“…PAs are known as a powerful antioxidant that has been proved to increase the antioxidant capacity of plants [6]. Overexpression of RrMYB5 and RrMYB10 in rose somatic embryos and seedlings, not only increased PAs content, but also enhanced the activity of catalase, peroxidase and superoxide dismutase of plants/tissues to low accumulation MDA and scavenge ROS, which improved tolerance to the stresses [31,160,161]. This means that PAs improve plant tolerance to environmental stresses by regulating the antioxidant system to facilitate ROS scavenging.…”

Transcriptional Factors Regulate Plant Stress Responses Through Mediating Secondary Metabolism

“…Moreover, accumulation of proanthocyanins also elevated the resistance against wounding and oxidative stress in Rosa rugosa, which was regulated by RrMYB5 and RrMYB10. Two proanthocyanin biosynthetic genes, RrANR and RrDFR were consequently upregulated or downregulated in RrMYB5/RrMYB10 overexpression or knockout R.rugosa lines, respectively [95].…”