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Comparative Analysis of miRNA Expression Profiles Provides Insight into Regulation of Biosynthesis of Flavonoids and Terpenoids Between Two Varieties of Toona sinensis Sprouts

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Abstract

In this study, small RNA sequencing has been performed to identify the miRNAs and explore their regulatory mechanism in T. sinensis sprouts. From HPLC analysis, the flavonoid content was higher in the BYC2 (purple toon sprout) than in the GYC2 (green toon sprout), whereas the volatile terpenoids revealed an inverse change. Therefore, the small RNA libraries of two varieties were constructed, and 331 known miRNAs and 23 novel miRNAs were discovered. Differential gene expression analysis demonstrated the upregulation of 25 miRNAs and the downregulation of 27 miRNAs between BYC2 and GYC2. qRT-PCR analysis showed that nine miRNAs involved in the biosynthetic regulation of flavonoids were downregulated in the BYC2, whereas eight miRNAs related to the regulation of the biosynthesis of terpenoids were upregulated, when compared with GYC2. The results indicated that the differential expression of the miRNAs mentioned above played a crucial role in the regulation of the formation of the flavonoids and terpenoids in T. sinensis sprouts. The present study not only fills in the paucity of knowledge regarding the T. sinensis miRNA, it also provides more valuable information for the genetic improvement of T. sinensis cultivation for the future.

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Abbreviations

AACT:

Acetyl-CoA-acetyltransferase

ARF:

Auxin response factor

BYC2:

Black Youchun

CHS:

Chalcone synthase

C4H:

Cinnamic acid 4-hydroxylase

4CL:

4-Coumarate CoA ligase

DFR:

Dihydroflavonol 4- reductase

DXS:

1-Deoxy-d-xylulose-5-phosphate synthase

ERF:

Ethylene-responsive transcription factor

FAS:

(E)-β-farnesene synthase

F3H:

Flavanone 3-hydroxylase

FLS:

Flavonol synthase

FPPS:

Farnesyl diphosphate synthase

GDS:

(-)-Germacrene D synthase

GO:

Enrichment Gene Ontology enrichment

GYC2:

Green Youchun

MBW:

MYB-bHLH-WD40 (MBW) transcription complex

miRNA:

MicroRNA

MEP:

2-C-methyl-d-erythritol-4-phosphate

MYB:

Myeloblastosis

HMGR:

3-Hydroxy-3-methyl glutaryl coenzyme A reductase

HCT:

Shikimate O-hydroxycinnamoyltransferase

HDS:

4-Hydroxy-3-methylbut-2-enyl-diphosphate synthase

KEGG:

Pathway kyoto encyclopedia of genes and genomes pathway

LAR:

Leucoanthocyanidin reductase

KS:

Ent-kaur-16-ene synthase

LDOX:

Leucoanthocyanidin dioxygenase

LIS:

Linalool synthase

LS:

(R)-limonene synthase

MK:

Mevalonate kinase

PAL:

Phenylalanine ammonia lyase

PMK:

Phosphomevalonate kinase

qRT-PCR:

Quantitative real-time PCR

SE:

Squalene epoxidase

SQS:

Squalene synthase

sRNA:

Small RNA

SPL:

Squamosa promoter-binding protein-like

TPS:

Terpene synthases

UGT:

Anthocyanidin 3-O-glucosyltransferase

WRKY:

WRKY transcription factor

ZIP:

Homeodomain leucine zipper

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Acknowledgements

We would like to thank Dr. Gopal Patel’s help to revise the manuscript from Laboratory of Medicinal Plant Biotechnology, Pharmacy College, Zhejiang Chinese Medicine University. We are also grateful to Postgraduate San Peng Fan, Dawei You, and Man Xu for their help to improve the experiment operation from Laboratory of Medicinal Plant Biotechnology, Pharmacy College, Zhejiang Chinese Medicine University. We thank Novogene Technologies (Beijing, China) for supplying small RNA sequencing service.

Funding

This work was supported by grants from the Natural Science Key Foundations of the Anhui Bureau of Education and institution of higher education outstanding top talent cultivation funding project of the Anhui Bureau of Education (No. KJ2019A0515, gxgwfx2020049), the Natural Science Key Foundation of Fuyang normal university (No. 2020FSKJ01ZD), the Innovation Program for College Students (No. 202010371013), the Open Fund of Advantaged and Characteristic Disciplines (Traditional Chinese Medicine of Zhejiang Chinese Medical University) for Key Construction Universities in Zhejiang Province (No. ZYAOX2018027).

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Authors and Affiliations

  1. Biology and Food Engineering College, Fuyang Normal University, Fuyang, 236037, Anhui, China

    Hu Zhao, Xiaopu Shi, Cheng Shen, Caifeng Chen & Changqing Qu

  2. Engineering Technology Research Center of Anti-Aging Chinese Herb, Fuyang Normal University, Fuyang, 236037, Anhui, China

    Hu Zhao, Caifeng Chen & Changqing Qu

  3. Laboratory of Medicinal Plant Biotechnology, Pharmacy College, Zhejiang Chinese Medicine University, Hangzhou, 311402, Zhejiang, China

    Gopal Patel, Wei Zhou & Guoyin Kai

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  1. Hu Zhao
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  2. Xiaopu Shi
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  3. Cheng Shen
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  4. Caifeng Chen
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  5. Changqing Qu
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  6. Gopal Patel
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  7. Wei Zhou
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  8. Guoyin Kai
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Contributions

HZ, WZ, and GK conceived and designed this experiment. HZ drafted the manuscript. WL and CQ collected samples of toon sprouts. YC and SF extracted and assayed flavonoid components and volatile terpenoid compounds. PG, HZ and WZ carried out qRT-PCR experiments and analyzed the data. All authors read and approved the manuscript.

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Correspondence to Hu Zhao.

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The authors declare no conflict of interest.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 26 KB) . Transcript counts of miRNAs in four small RNA libraries of toon sprouts

12374_2021_9321_MOESM2_ESM.jpg

Supplementary file2 (JPG 1392 KB) Figure S1. Predicted secondary structures of potential novel miRNAs from toon sprouts. Sequences indicated in red correspond to predicted miRNA

12374_2021_9321_MOESM3_ESM.xlsx

Supplementary file3 (XLSX 30344 KB) Table S2. Target prediction results of miRNAs from toon sprouts. Table S2. Target prediction results of miRNAs from toon sprouts.

Supplementary file4 (XLSX 888 KB) Table S3. Potential target numbers of miRNAs from toon sprouts

Supplementary file5 (XLSX 47 KB) Table S4. GO enrichment analysis of predicted target unigenes

Supplementary file6 (XLSX 17 KB) Table S5. KEGG pathway analysis of predicted target unigenes

Supplementary file7 (XLSX 54 KB) Table S6. Differential expression levels of miRNAs from toon sprouts

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Zhao, H., Shi, X., Shen, C. et al. Comparative Analysis of miRNA Expression Profiles Provides Insight into Regulation of Biosynthesis of Flavonoids and Terpenoids Between Two Varieties of Toona sinensis Sprouts. J. Plant Biol. 65, 291–310 (2022). https://doi.org/10.1007/s12374-021-09321-6

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