Abstract

Tree peony is an economically important crop that is widely used in the food, floriculture, and pharmaceutical industries. However, the buds of tree peony are susceptible to low temperature stress. To elaborate the metabolic and transcriptional changes during bud sprouting, we performed metabolite and transcriptome analyses of the buds of Paeonia suffruticosa cultivar ‘Yulouchun’ at three developmental stages under low temperature treatment. The results showed that the contents of anthocyanin and α-linolenic acid (ALA) increased, concomitant with increased production of sucrose, gibberellic acid, indolylacetic acid, trans -zeatin riboside, and jasmonic acid as well as reduced accumulation of abscisic acid. Transcriptome profiling revealed 6355 differentially expressed genes (DEGs) during bud growth. We identified many structural DEGs whose expression was correlated with the accumulation of anthocyanin, ALA, sucrose, and hormones. In particular, the expression of transcription factors (TFs) PsMYB113 and PsMYB123 was found to be positively correlated with anthocyanin biosynthetic genes flavonoid 3′,5′-Hydroxylase , dihydroflavonol 4-reductase ( DFR ), anthocyanidin synthase ( ANS ), and two UDP-glycosylatransferase s. A positive correlation between a bZIP TF PsDPBF3 and an ALA biosynthetic gene fatty acid desaturase3 ( FAD3 ) was also found. Transcript abundances of these TFs and structural genes changed under sucrose and hormone treatments. Silencing of PsMYB113 and PsMYB123 resulted in decreased anthocyanin production and tolerance to freezing in tree peony buds. In addition, PsDPBF3 -silenced buds displayed reduced ALA levels and low temperature hardiness. In vivo promoter-binding assays verified that both PsMYB113 and PsMYB123 trans-activated the expression of DFR and ANS , while PsDPBF3 specifically regulated the transcription of FAD3 . Taken together, our data suggest that the production of anthocyanin and polyunsaturated fatty acid is closely implicated in cold tolerance of tree peony buds. • Cold stress increased various metabolite contents during bud sprouting of tree peony. • Transcriptome profiling revealed 6355 DEGs in cold-treated tree peony buds. • Silencing of PsMYB113 , PsMYB123 , and PsDPBF3 led to reduced tolerance to cold stress. • PsMYB113 and PsMYB123 bound to the promoters of anthocyanin-related DFR and ANS. • PsDPBF3 specifically trans-activated the expression of PUFA-associated FAD3 .

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