Abstract

Tea (Camellia sinensis) flowers are normally white, even though the leaves could be purple. We previously discovered a specific variety with purple leaves and flowers. In the face of such a phenomenon, researchers usually focus on the mechanism of color formation but ignore the change of aroma. The purple tea flowers contain more anthocyanins, which belong to flavonoids. Meanwhile, phenylalanine (Phe), derived from the shikimate pathway, is a precursor for both flavonoids and volatile benzenoid–phenylpropanoids (BPs). Thus, it is not clear whether the BP aroma was attenuated for the appearance of purple color. In this study, we integrated metabolome and transcriptome of petals of two tea varieties, namely, Zijuan (ZJ) with white flowers and Baitang (BT) with purple flowers, to reveal the relationship between color (anthocyanins) and aroma (volatile BPs). The results indicated that in purple petals, the upstream shikimate pathway promoted for 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase (DAHPS) was elevated. Among the increased anthocyanins, delphinidin-3-O-glucoside (DpG) was extremely higher; volatile BPs, including benzyl aldehyde, benzyl alcohol, acetophenone (AP), 1-phenylethanol, and 2-phenylethanol, were also enhanced, and AP was largely elevated. The structural genes related to the biosynthesis of volatile BPs were induced, while the whole flavonoid biosynthesis pathway was downregulated, except for the genes flavonoid 3′-hydroxylase (F3′H) and flavonoid 3′,5′-hydroxylase (F3′5′H), which were highly expressed to shift the carbon flux to delphinidin, which was then conjugated to glucoside by increased bronze-1 (BZ1) (UDP-glucose: flavonoid 3-O-glucosyltransferase) to form DpG. Transcription factors (TFs) highly related to AP and DpG were selected to investigate their correlation with the differentially expressed structural genes. TFs, such as MYB, AP2/ERF, bZIP, TCP, and GATA, were dramatically expressed and focused on the regulation of genes in the upstream synthesis of Phe (DAHPS; arogenate dehydratase/prephenatedehydratase) and the synthesis of AP (phenylacetaldehyde reductase; short-chain dehydrogenase/reductase), Dp (F3′H; F3′5′H), and DpG (BZ1), but inhibited the formation of flavones (flavonol synthase) and catechins (leucoanthocyanidin reductase). These results discovered an unexpected promotion of volatile BPs in purple tea flowers and extended our understanding of the relationship between the BP-type color and aroma in the tea plant.

Highlights

  • Benzenoids, especially phenylpropanoids, are the main sources of plant color and aroma

  • Except for methyl salicylate (MeSA), other common volatile Benzenoids and phenylpropanoids (BPs) were significantly elevated in purple flowers: 1-PE, Bald, and benzyl alcohol (Balc) were 2, 2.9, and 2.8 times higher, respectively; and 2-PE was even not detected in white flowers

  • In terms of the total amounts, the dominant aroma from BPs was changed in the purple tea flowers, where the phenylpropanoids (AP, 1-PE, and 2-PE) were higher than other benzenoids (Bald, Balc, and MeSA), while in the normal whiter flowers, it was opposite

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Summary

Introduction

Benzenoids, especially phenylpropanoids, are the main sources of plant color and aroma. It has been widely proved that these structure genes were influenced by many transcription factors (TFs), such as MYB, ERF, Abbreviations: BPs, benzenoids and phenylpropanoids; 1-PE, 1-phenylethanol; 2-PE, 2-phenylethanol; 4CL, 4-coumarate-CoA ligase; ADT, arogenate dehydratase/prephenate dehydratase; ANR, anthocyanidin reductase; ANS, anthocyanidin synthase; AP, acetophenone; Balc, benzyl alcohol; Bald, benzaldehyde; BPBT, benzyl alcohol O-benzoyltransferase; BT, Baitang; BZ1, bronze-1; C4H, cinnamate-4 hydroxylase; CHI, chalcone isomerase; CHS, chalcone synthase; Cy, cyanidin; DAHPS, 3-deoxy-D-arabino-heptulosonate 7-phosphate synthase; DFR, dihydroflavonol 4-reductase; Dp, delphinidin; DpG, delphinidin-3-O-glucoside; F3 5 H, flavonoid 3 ,5 -hydroxylase; F3H, flavanone 3-hydroxylase; F3 H, flavonoid 3 -hydroxylase; FLS, flavonol synthase; GA3P, glyceraldehyde 3-phosphate; GST, glutathione S-transferase; LAR, leucoanthocyanidin reductase; MATE, multidrug and toxin extrusion; MeSA, methyl salicylate; MRP, multidrug resistance-associated protein; Mv, malvidin; PAR, phenylacetaldehyde reductase; PEP, phosphoenolpyruvate; Pg, pelargonidin; Phe, phenylalanine; Pn, peonidin; Pt, petunidin; SAMT, salicylic acid carboxyl methyltransferase; SDR, short-chain dehydrogenase/reductase; TFs, transcription factors; TPM, Transcripts Per Kilobase of exon model per Million mapped reads; UFGT, UDP-glucose: flavonoid 3-O-glucosyltransferase; ZJ, Zijuan

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