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Genome-wide analysis of ARF transcription factors reveals HcARF5 expression profile associated with the biosynthesis of β-ocimene synthase in Hedychium coronarium

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Abstract

Key message

Herein, 37 ARF genes were identified and analyzed in Hedychium coronarium and HcARF5 showed a potential role in the regulation of HcTPS3.

Abstract

Auxin is an important plant hormone, implicated in various aspects of plant growth and development processes especially in the biosynthesis of various secondary metabolites. Auxin response factors (ARF) belong to the transcription factors (TFs) gene family and play a crucial role in transcriptional activation/repression of auxin-responsive genes by directly binding to their promoter region. Nevertheless, whether ARF genes are involved in the regulatory mechanism of volatile compounds in flowering plants is largely unknown. β-ocimene is a key floral volatile compound synthesized by terpene synthase 3 (HcTPS3) in Hedychium coronarium. A comprehensive analysis of H. coronarium genome reveals 37 candidate ARF genes in the whole genome. Tissue-specific expression patterns of HcARFs family members were assessed using available transcriptome data. Among them, HcARF5 showed a higher expression level in flowers, and significantly correlated with the key structural β-ocimene synthesis gene (HcTPS3). Furthermore, transcript levels of both genes were associated with the flower development. Under hormone treatments, the response of HcARF5 and HcTPS3, and the emission level of β-ocimene contents were evaluated. Subcellular and transcriptional activity assay showed that HcARF5 localizes to the nucleus and possesses transcriptional activity. Yeast one-hybrid (Y1H) and dual-luciferase assays revealed that HcARF5 directly regulates the transcriptional activity of HcTPS3. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays showed that HcARF5 interacts with scent-related HcIAA4, HcIAA6, and HcMYB1 in vivo. Overall, these results indicate that HcARF5 is potentially involved in the regulation of β-ocimene synthesis in H. coronarium.

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Abbreviations

AbA:

Aureobasidin A

ABA:

Abscisic acid

Aux/IAA:

Auxin/Indole-3-Acetic Acid

cDNA:

Complementary DNA

GC–MS:

Gas chromatography-mass spectrometer

GFP:

Green fluorescent protein

DBD:

DNA-binding domain

ERE:

Ethylene responsive elements

MeJA:

Methyl jasmonate

qRT-PCR:

Quantitative reverse transcription PCR

MEME:

Multiple Em for Motif Elicitation

NJ:

Neighbor-Joining

ORF:

Open reading frame

PlantTFDB:

Plant Transcription Factor Database

RNA-seq:

RNA-sequencing

SMART:

Simple Modular Architecture Research Tool

TAIR:

The Arabidopsis Information Resource

ABRE:

ABA-responsive element

CDS:

Coding domain sequence

Ka:

Non-synonymous substitution rate

Ks:

Synonymous substitution rate

Mya:

Million years ago

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Funding

This work was supported by the Research Projects in Key-Areas of Guangdong Province (Grant no. 2020B20220007), National Natural Science Foundation of China to Y. F. (Grant no. 31770738), People’s Livelihood Science and Technology Projects of Guangzhou to Yanping Fan (Grant no. 201903010054) and National Natural Science Foundation of China to Rangcai Yu (Grant no. 31870690).

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Author notes

  1. Farhat Abbas and Yanguo Ke contributed equally.

Authors and Affiliations

  1. The Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, 510642, China

    Farhat Abbas, Yanguo Ke, Yiwei Zhou, Yunyi Yu, Xinyue Li & Yanping Fan

  2. College of Life Sciences, South China Agricultural University, Guangzhou, 510642, China

    Rangcai Yu

  3. College of Economics and Management, Kunming University, Kunming, 650214, China

    Yanguo Ke

  4. College of Horticulture, South China Agricultural University, Guangzhou, 510642, China

    Muhammad Waseem

  5. Department of Botany, Division of Science and Technology, University of Education, Lahore, 54770, Punjab, Pakistan

    Umair Ashraf

  6. Guangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, 510642, China

    Yanping Fan

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  1. Farhat Abbas
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Contributions

FA, YF, RY conceived and design the concept. FA, YK and YZ performed the experiment. FA, MW, YZ and UA analyze the data. YY and XL did the formal analysis. FA, KG and MW drafted the manuscript. FA, RY and YF revised and finalized the manuscript. All authors endorse the final version of the manuscript.

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Correspondence to Yanping Fan.

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The authors declare no conflict of interest.

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Communicated by Sukhpreet Sandhu.

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Supplementary Information

Below is the link to the electronic supplementary material.

299_2021_2709_MOESM1_ESM.jpg

Supplementary file 1: Figure 1: Phylogenetic relationships, gene structure, and conserved domain analysis of HcARF TFs (JPG 762 KB)

Supplementary file 2: Figure 2: Multiple sequence alignment of 37 HcARF proteins (PDF 862 KB)

299_2021_2709_MOESM3_ESM.jpg

Supplementary file 3: Figure 3: Sequence alignment of HcARF5 with AtARF1, OsARF7, SlARF1, and VvARF1 proteins (JPG 1201 KB)

299_2021_2709_MOESM4_ESM.tif

Supplementary file 4: Figure 4: The schematic representation of the individual motifs found in HcARF genes (TIF 3086 KB)

299_2021_2709_MOESM5_ESM.jpg

Supplementary file 5: Figure 5: The correlation analysis between the expression pattern of HcARF5 and HcTPS3 gene and emission of β-ocimene contents (JPG 298 KB)

299_2021_2709_MOESM6_ESM.xlsx

Supplementary file 6: Table 1: Detailed characteristics of HcARF genes. Table 2: Primer used in the experiments. Table 3: The Ka/Ks ratios and estimated divergence time for segmentally and tandemly duplicated HcARF genes. Table 4: Numbers of known stress-related elements in the promoter regions of HcARF genes. Table 5: List of ARF gene ids from different species. Table 6: Coding sequences of 37 HcARF genes. Table 7: Protein sequences of 37 HcARFs (XLSX 69 KB)

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Abbas, F., Ke, Y., Zhou, Y. et al. Genome-wide analysis of ARF transcription factors reveals HcARF5 expression profile associated with the biosynthesis of β-ocimene synthase in Hedychium coronarium. Plant Cell Rep 40, 1269–1284 (2021). https://doi.org/10.1007/s00299-021-02709-1

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