Integrating full-length transcriptomics and metabolomics reveals the regulatory mechanisms underlying yellow pigmentation in tree peony (Paeonia suffruticosa Andr.) flowers

Abstract

Tree peony (Paeonia suffruticosa Andr.) is a popular ornamental plant in China due to its showy and colorful flowers. However, yellow-colored flowers are rare in both wild species and domesticated cultivars. The molecular mechanisms underlying yellow pigmentation remain poorly understood. Here, petal tissues of two tree peony cultivars, “High Noon” (yellow flowers) and “Roufurong” (purple–red flowers), were sampled at five developmental stages (S1–S5) from early flower buds to full blooms. Five petal color indices (brightness, redness, yellowness, chroma, and hue angle) and the contents of ten different flavonoids were determined. Compared to “Roufurong,” which accumulated abundant anthocyanins at S3–S5, the yellow-colored “High Noon” displayed relatively higher contents of tetrahydroxychalcone (THC), flavones, and flavonols but no anthocyanin production. The contents of THC, flavones, and flavonols in “High Noon” peaked at S3 and dropped gradually as the flower bloomed, consistent with the color index patterns. Furthermore, RNA-seq analyses at S3 showed that structural genes such as PsC4Hs, PsDFRs, and PsUFGTs in the flavonoid biosynthesis pathway were downregulated in “High Noon,” whereas most PsFLSs, PsF3Hs, and PsF3’Hs were upregulated. Five transcription factor (TF) genes related to flavonoid biosynthesis were also upregulated in “High Noon.” One of these TFs, PsMYB111, was overexpressed in tobacco, which led to increased flavonols but decreased anthocyanins. Dual-luciferase assays further confirmed that PsMYB111 upregulated PsFLS. These results improve our understanding of yellow pigmentation in tree peony and provide a guide for future molecular-assisted breeding experiments in tree peony with novel flower colors.

PrMYB5 activates anthocyanin biosynthetic PrDFR to promote the distinct pigmentation pattern in the petal of Paeonia rockii

“…Total RNAs were extracted and reverse transcribed into first-strand cDNA for real-time quantitative PCR (qRT-PCR) using the PrimeScript TM RT Master MIX reverse transcription kit (TaKaRa, Beijing, China). qRT-PCR was conducted using SYBR ® Premix Ex Taq TM II (Perfect Real Time) Kit (TaKaRa, Beijing, China) on a Bio-Rad CFX96 TM Real-Time system (Bio-Rad, Hercules, CA, USA) according to the reaction conditions mentioned previously (Luo et al, 2021 ). The transcription levels of genes were normalized to the PsUbiquitin expression level and calibrated to the expression level in P. ostii petal background at S1.…”

“…Flavonoids were detected in tree peony petals and tobacco petals using the high-performance liquid chromatography (HPLC) method, as previously reported (Luo et al, 2021). First, each sample was ground into powder in liquid nitrogen.…”

“…Previous research demonstrated that the spot formation at the petal base of tree peony was primarily attributed to the spatial biosynthesis of cyanidin (Cy) and peonidin (Pn) anthocyanins (Zhang et al, 2015 ; Shi et al, 2017 ). The anthocyanin structural genes and anthocyanin regulatory MYBs have been identified in tree peony cultivars, including PsMYB114L, PsMYB12L, PsMYB12, PsMYB111, PsMYB4, PsMYB57 , and PsMYB58 (Gu et al, 2019 ; Zhang et al, 2019 , 2020a , b ; Luo et al, 2021 ). Among them, PsMYB12 directly activated the expression of PsCHS by forming an MBW regulatory complex with bHLH and WD40 proteins, which were specific to the petal blotch in tree peony cultivar “Qing Hai Hu Yin Bo” (Gu et al, 2019 ).…”

Integrative analysis of transcriptome and metabolome reveals flavonoid biosynthesis regulation in Rhododendron pulchrum petals

“…Flavonoids produce a variety of colors ranging from pale yellow to deep blue [ 3 ], which have been divided into flavonoids, flavonols, anthocyanins, isoflavones, flavan-3-ols, dihydroflavonols, dihydroflavones, and chalcons [ 4 , 5 ]. Among these, chalcones were reported in deep yellow color, while flavones and flavonols in faintly yellow or almost colorless [ 6 ]. A variety of colors can be produced by anthocyanins [ 7 ].…”

“…Recent studies have used integrated multi-omics analyses to identify and analyze traits related genes and pathways in plants [5,6,[37][38][39][40][41]. A combined analysis of transcriptomes and metabolomes can directly and accurately reflect organismal change.…”