Differentially evolved glucosyltransferases determine natural variation of rice flavone accumulation and UV-tolerance

Abstract

Decoration of phytochemicals contributes to the majority of metabolic diversity in nature, whereas how this process alters the biological functions of their precursor molecules remains to be investigated. Flavones, an important yet overlooked subclass of flavonoids, are most commonly conjugated with sugar moieties by UDP-dependent glycosyltransferases (UGTs). Here, we report that the natural variation of rice flavones is mainly determined by OsUGT706D1 (flavone 7-O-glucosyltransferase) and OsUGT707A2 (flavone 5-O-glucosyltransferase). UV-B exposure and transgenic evaluation demonstrate that their allelic variation contributes to UV-B tolerance in nature. Biochemical characterization of over 40 flavonoid UGTs reveals their differential evolution in angiosperms. These combined data provide biochemical insight and genetic regulation into flavone biosynthesis and additionally suggest that adoption of the positive alleles of these genes into breeding programs will likely represent a potential strategy aimed at producing stress-tolerant plants.

Apigenin produced by maize flavone synthase I and II protects plants against UV‐B‐induced damage

“…Different reports and our previous studies have shown that maize plants accumulate O ‐glycosyl flavones in different tissues, in addition to the predominant C ‐glycosyl flavones (Casas et al, ; Falcone Ferreyra et al, ; Peng et al, ; Ren et al, ; Wen et al, ). The biosynthesis pathway of O ‐glycosyl flavones has been elucidated in rice, involving first the formation of the flavone aglycones, and then their O ‐glycosylation (Brazier‐Hicks et al, ; Lam et al, ).…”

“…Arabidopsis plants that overexpress Zm FNSI and Zm FNSII accumulate less CPDs after the UV‐B treatment (~580–600 IOD vs. ~700–720 IOD in WT and dmr6‐1 mutants), providing evidence of protective roles of flavones against DNA damage induced by UV‐B. It is worth mentioning that, as dmr6‐1 mutant plants, WT plants do not accumulate apigenin in 21‐day‐old rosette leaves (Falcone Ferreyra et al, ; Peng et al, ), the tissue used for dot blot experiments. We also previously reported that AtDMR6 transcript levels in rosette leaves of WT plants are much lower than those in cauline and senescing leaves, the latter being the only tissues where apigenin was detected.…”

“…Although C ‐glycosyl flavones accumulate in leaves from high‐altitude landraces, suggesting that they can protect plants against UV‐B damage, our present results suggest that flavones, and probably their corresponding O ‐glycosides, can also play protective roles against deleterious effects of UV‐B radiation. Accordingly, it was recently reported that apigenin 5‐ O‐ glucoside has a more protective function than apigenin 7‐ O ‐glucoside in the UV‐B tolerance of rice plants (Peng et al, ). These authors suggested that Zm UGT707A8 could be the flavone 5‐ O ‐glucosyltransferase responsible for 5‐ O‐ glucoside biosynthesis in maize whereas Zm UGT707A19 seems to be responsible for apigenin 7‐ O ‐glucoside biosynthesis.…”

Metabolic GWAS‐based dissection of genetic bases underlying the diversity of plant metabolism

“…to the interaction with various environmental stimuli (abiotic or biotic stresses), have been comprehensively studied with GWAS (Figure ). Generally, the variation of agricultural traits are limited (Huang et al ., ; Si et al ., ), while the content of a large proportion of detectable metabolites displays tremendous variation (Matsuda et al ., ; Wen et al ., ; Peng et al ., ). QTLs for agricultural performance in crops identified by GWAS tend to be of moderate or low effect (Huang et al ., ; Si et al ., ), which might partially result from the limited variation in targeted end‐phenotypes.…”

“…QTLs for agricultural performance in crops identified by GWAS tend to be of moderate or low effect (Huang et al ., ; Si et al ., ), which might partially result from the limited variation in targeted end‐phenotypes. In contrast, genetic variants controlling natural variation in accumulation of metabolites are much easier to be identified by GWAS (Matsuda et al ., ; Wen et al ., ; Peng et al ., ), because of the tremendous diversity across experimental populations and accurate evaluation of metabolite contents.…”