Genome-wide Identification and Expression Analysis of Auxin Response Factor Genes in Arabian Jasmine

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Xin Huang College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Haigang Guo College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Lili Yin College of Life Science, Shanxi Datong University, Datong 037009, Shanxi, China

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Ruigang Wu College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Xingwen Zhou College of Architecture and Urban Planning, Fujian University of Technology, Fuzhou 350118, Fujian, China

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Abstract

Auxin response factors (ARFs) are an important family of auxin-mediated proteins that have key roles in various physiological and biochemical processes. To the best of our knowledge, no genome-wide identification of the ARF gene family in Arabian jasmine (Jasminum sambac) has been conducted to date. During this study, 24 ARF genes were identified in the Arabian jasmine genome. A phylogenetic analysis suggested that the 24 Arabian jasmine ARFs (JsARFs) were clustered into seven groups and distributed on 11 of the 13 Arabian jasmine chromosomes. The promoter regions of these ARFs were rich in cis-responsive elements related to hormone responses, light responses, and biotic and abiotic stresses. A collinearity analysis showed that certain genes arose by duplication, such as JsARF6 and JsARF19 and JsARF7 and JsARF24. A subsequent analysis of expression profiles based on RNA sequencing data showed that most genes had differential expression patterns among different tissues. The expression levels of 11 genes under indole-3-acetic acid hormone treatment were determined using quantitative real-time polymerase chain reaction, and the results demonstrated that the expression levels of nine JsARF genes were downregulated. Our findings provide valuable information to create the foundation for further functional investigations of the roles of ARF genes in Arabian jasmine growth and development.

Jasminum is a genus comprising erect or climbing shrubs in the Oleaceae family, which includes ∼60 species in China that can be divided into single-leaved, double-leaved, and multi-petaled types (Tang et al. 2016). Arabian jasmine (Jasminum sambac) has high ornamental, economic, edible, and medicinal values (Mourya et al. 2017). Most species are resistant to abiotic stress, and the deciduous vine is extremely hardy and drought-tolerant (Reshma et al. 2021). Auxin is widely distributed in plants and has an important role in plant growth and development, including seed germination, inflorescence formation, fruit development, leaf formation, and root structure formation and differentiation (Wang et al. 2007). Auxin can directly regulate the process of cell division, differentiation, and expansion through interactions with the recipient cell membrane or via other signaling pathways (Tiwari et al. 2004). Auxins can also bind directly to auxin-response elements [AuxREs (5′-TGTCTC-3′)] at the promoters of auxin-inducible genes to mediate auxin-dependent transcriptional regulation (Hagen and Guilfoyle 2002). Auxin response factors (ARFs) generally contain three domains: the DNA-binding domain, middle region, and C-terminal dimerization domain. Among them, the N-terminal B3-like DNA-binding domain is highly conserved and can bind to AuxREs in the promoters of auxin-responsive genes (Ulmasov et al. 1999). The middle region can activate or inhibit target genes depending on their amino acid composition (Xing et al. 2011). The C-terminal dimerization domain contains motifs III and IV, which are also present in auxin/indoleacetic acid (Aux/IAA) proteins; both can mediate heterodimerization of ARFs and Aux/IAAs and prevent ARFs from binding to AuxREs under low auxin concentrations (Ulmasov et al. 1999). However, under high auxin concentrations, Aux/IAA proteins are degraded via the ubiquitination pathway, and ARFs are released and bound to AuxREs in the promoters of these genes to activate or repress gene expression (Finet et al. 2013).

The functions of some ARFs in arabidopsis (Arabidopsis thaliana) (Okushima et al. 2005), tomato (Solanum lycopersicum) (Kumar et al. 2011), apple (Malus domestica) (Luo et al. 2014), rice (Oryza sativa) (Wang et al. 2007), sugar beet (Beta vulgaris) (Cui et al. 2020), and longan (Dimocarpus longan) (Peng et al. 2020) have been studied. In arabidopsis, several ARF genes are involved in the regulation of plant morphological growth, such as apical bud formation, pollen wall synthesis, vascular bundle development, tropical hypocotyl movement, and adventitious root formation (Hardtke et al. 2004). Among these, AtARF2 and AtARF19 are considered key genes in the auxin and ethylene signaling pathways (Mallory et al. 2005). AtARF6 and AtARF8 regulate the expression of the jasmonate ZIM-domain/TAFY10A, which is controlled by jasmonic acid (Schruff et al. 2006). The formation of lateral roots is severely impaired in the arf7 arf19 double knockout mutants (Okushima et al. 2007). This phenotype could be restored through overexpression of lateral organ boundaries-domain16/asymmetric leaves2-like18 (LBD16/ASL18) and LBD29/ASL16 in the double mutant, suggesting that AtARF7 and AtARF19 regulate lateral root formation via direct activation of ligand binding domain (LBD)/argininosuccinate lyases in arabidopsis (Tiwari et al. 2003). AtARF5 maintains apical meristem development by directly regulating AtARF7 and AtARF15, and it also regulates leaf vascular bundle tissue development by regulating AtARF8 (Tiwari et al. 2004). Regarding rice, OsARF12 (i.e., an auxin response factor) may have a role in regulating phosphate homeostasis (Qi et al. 2012). Regarding wheat (Triticum aestivum), TaARF15-A.1 may contribute to the development of roots and leaves during the vegetative growth stage (Qiao et al. 2018). Notably, ARF genes have also shown complex responses to abiotic stresses such as drought, cold, and salt (Hu et al. 2015).

The development of genomic data regarding Arabian jasmine provides the opportunity to annotate and classify the entire genome of this species and conduct comparative genomic studies (Wang et al. 2022). To the best our knowledge, no detailed systematic study of Arabian jasmine ARFs (JsARFs) has yet been conducted. During this study, the sequences of ARF genes in Arabian jasmine were identified via data mining of the existing genome and transcriptome. Furthermore, comprehensive analyses of the ARF gene structure, motif composition, cis-acting regulatory elements, and expression profiles in different tissues were performed. This work creates the foundation for the functional characterization of JsARF genes.

Materials and Methods

Identification and characterization of ARF family members in the J. sambac genome.

The genome assembly, annotation files, and additional functional annotations are publicly available in the Github database (Shen 2023). To effectively identify the ARF family members of Arabian jasmine, candidate protein sequences were downloaded from the Pfam ARF Hidden Markov Model map (PF06507). The whole-genome HMMER software (version 3.2.12) (Mistry et al. 2013) was used for Hidden Markov Model screening of Arabian jasmine. Based on the Pfam results, further examination of the ARF-like protein sequences was performed, and redundancy of the ARF protein was identified on different servers, including the National Center for Biotechnology Information (Bethesda, MD, USA) using Conserved Domain Search (Wheeler et al. 2006). A subcellular localization prediction was performed using Subcellular Localization Predictor (Yu et al. 2006). The isoelectric points and molecular weights of the proteins were calculated using JavaScript programs (Stothard 2000).

Chromosomal distribution of ARF genes.

The location of JsARF members on chromosomes was extracted from the genome annotation files (Shen 2023), and the density of the whole chromosome was determined. Visual analysis was performed using TBtools software (Chen et al. 2020), and the distribution of JsARF family members on chromosomes was displayed.

Analysis of conserved motifs and domains.

A conserved motif analysis of the ARF protein sequences was performed using the classical motif discovery model of MEME-suite 5.3.3 (Bailey et al. 2006). The parameter of the optimum motif was set at 6 to 200, and the maximum number of motifs was set to 10. The conserved domain analysis was performed using TBtools.

Analysis of cis-regulatory elements.

To identify cis-regulatory elements (CREs) in ARF genes, a 2000-bp region upstream of the translation start was identified by aligning the coding sequences with the genomic sequences. From these, regulatory elements were predicted using the PlantCARE database (Magali et al. 2002) and plotted using TBtools software.

Collinearity analysis of JsARF genes.

To investigate the mechanisms mediating ARF gene family evolution, MCScanX (Wang et al. 2012) was used to analyze tandem, proximal, and dispersed duplications. A collinearity analysis of the Arabian jasmine genomes was conducted using the TBtools software package to map the genes to their chromosomal locations (Xie et al. 2018). Collinearity caused by segmental duplicate events and tandem duplicates caused by gene duplication events were identified. According to the alignment results, if a pair of alignment sequences was connected on the chromosome, then MCScanX considered that one of the two sequences was generated via duplication of the other sequence (i.e., gene duplication event). Because clusters also exist on chromosomes, MCScanX software could help to confirm whether a group of multiple pairs of sequences was produced by the replication of another group (i.e., fragment duplication event).

Phylogenetic analysis of ARF proteins.

The phylogenetic relationship between ARF proteins in Arabian jasmine, arabidopsis, and rice has been investigated (Wang et al. 2007). A phylogenetic tree of 23 AtARF, 25 OsARF, and 24 JsARF proteins was constructed using the neighbor-joining method. The coding sequences of the full-length genes were aligned through multiple gene alignment using fast Fourier transform (Kazutaka et al. 2019). A comparison of protein sequences and generation of phylogenetic trees were performed using MEGA7 software (Arizona State University, Tempe, AZ, USA) with 1000 bootstrap replicates. The ARF protein sequences of arabidopsis and rice were downloaded from the arabidopsis (Philippe et al. 2012) and rice (Kawahara et al. 2013) databases to construct a phylogenetic tree, and figures were generated using the iTOL website (Ivica and Bork 2019).

ARF protein–protein interaction analysis.

To predict the interactions between JsARF proteins, ARF protein sequences were submitted to STRING (version 10) (Damian et al. 2015). Then, the protein–protein interaction networks were visualized using Cytoscape (version 3.7.2) (Shannon et al. 2003).

Tissue-specific expression analysis of JsARF genes.

The RNA sequencing (RNA-seq) data were submitted to the National Center for Biotechnology Information SRA database under accession number SRR14317414-SRR14317417. This included the data of different tissues, including roots, stems, leaves, and flowers of 3-month-old Arabian jasmine. Furthermore, the expression levels of 24 JsARF genes were collected and compiled, and a heat map of gene expression was generated using TBtools.

JsARF gene expression analysis in response to IAA.

Seeds of Arabian jasmine were sown on the experimental field of Hebei University of Engineering (Handan, Hebei, China). Branches of 3-month-old Arabian jasmine were immersed in 100 μM IAA solution for 0, 1, 6, and 12 h. Then, leaves were collected and immediately frozen in liquid nitrogen and stored at −80 °C before RNA extraction and quantitative real-time polymerase chain reaction (qRT-PCR) analysis. Three biological replicates were used for each treatment. All genes were analyzed using an algorithm based on variances calculated using the cross-gene error model (±SD) in GraphPad Prism (version 9.0; GraphPad, San Diego, CA, USA).

The RC411–01 kit (Vazyme Biotech Co., Ltd., Nanjing, China) was used to extract RNA from the samples. Total RNA was reverse-transcribed and subjected to the qRT-PCR analysis using Taq Pro Universal SYBR qPCR Master Mix (Q712–02; Vazyme Biotech Co., Ltd.). Data were analyzed using the 2−ΔΔ CT method. Specific primers for fluorescence determined using qRT-PCR were designed with Primer3 software (Koressaar and Remm 2007) according to the candidate gene sequence, and the amplicons generated using these primers were 150 to 300 bp long. The primer sequences used are listed in Supplemental Table 1.

Results

Identification of the ARF gene family in Arabian jasmine.

Two different methods were used to identify all ARF family members in the Arabian jasmine genome. Twenty-four unique ARF genes were selected to identify candidate ARF family protein sequences. Details of these genes (chromosome identity document, name, gene name, predicted subcellular location, chromosome location, protein amino acid length, and basic data of the derived peptides) are provided in Table 1. The amino acid length of the JsARF proteins ranged between 136 and 1085. The predicted molecular weight of the identified ARF proteins ranged between 15.0 and 119.9 kDa, and the isoelectronic points of JsARFs ranged between 5.4 and 8.99. Subcellular localization of the 24 JsARF proteins was identified. According to the predicted results, except for two ARF proteins (JsARF4 and JsARF10) predicted to be localized in the cytoplasm, others were predicted to be localized in the nucleus.

Table 1.

Physical and chemical characteristics and subcellular localization prediction of putative Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) proteins. Number of encoded amino acids, theoretical molecular weight (wt), and isoelectric points were calculated using JavaScript programs (Stothard 2000). The subcellular localization was predicted using Subcellular Localization Predictor (Yu et al. 2006).

Table 1.

Distribution of JsARF genes on Arabian jasmine chromosomes.

The chromosomal locations of the 24 identified JsARFs were precisely mapped based on the available genome sequences (Fig. 1). The distribution of ARF genes on the 13 Arabian jasmine chromosomes was not uniform, and the length of each chromosome also varied. Only one JsARF gene was present on chromosomes 9, 11, and 13; two were distributed on chromosomes 2, 4, and 8; three were distributed on chromosomes 1, 3, 5, 6, and 12; and none was present on chromosomes 7 and 10.

Fig. 1.
Fig. 1.

Chromosomal locations of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes. The scaffold number of chromosomes (Chr) is shown on the left side of each bar chart. The scaffold size is indicated by its relative length using the information. The color gradient from blue to red on the chromosomes indicates low to high gene density.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Analyses of gene structure, CREs, and conserved protein domains of JsARFs.

The 24 identified JsARF protein sequences were used to construct the phylogenetic tree (Fig. 2A). Subsequently, 10 motifs were identified in JsARF protein domains (Fig. 2B). Most B3 domains consisted of motifs 1, 2, 3, and 7; the AuxRE domain was composed of motifs 5, 6, 8, and 10; and the Aux/IAA protein domain consisted of motifs 4 and 9. Among them, most motifs occurred only once in the JsARF protein sequence; however, motif 4 was present twice in certain regions of JsARF16.

Fig. 2.
Fig. 2.

Phylogenetic tree diagram, motif, domain composition, distributions of cis-regulatory elements (CREs) in the promoter regions, and structure of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) candidate genes. (A) Phylogenetic relationship of JsARFs. (B) Identified conserved motifs of JsARFs; 10 motifs were found and are illustrated in different colors. (C) Conserved domain of JsARFs are represented by three different colors. (D) The 2000-bp upstream sequences were used to analyze 15 specific phytohormone and abiotic stress-related cis elements. (E) Exon–intron structures of JsARF genes. Exons and introns are shown as green color and black lines, respectively. The left and right ends are untranslated regions and are indicated with yellow color.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

According to the conserved protein domain analysis results (Fig. 2C), most JsARF proteins, such as JsARF3, JsARF5, JsARF9, JsARF11, JsARF12, JsARF13, JsARF16, JsARF17, JsARF18, JsARF19, JsARF20, JsARF22, JsARF23, and JsARF24, contained three domains: AuxRE, B3, and auxin/indole-3-acetic acid (Aux/IAA). Two domains (AuxRE and B3) were present in some JsARFs, including JsARF1, JsARF2, JsARF6, JsARF7, JsARF10, JsARF14, and JsARF15. JsARF8 contained AuxRE and Aux/IAA domains, whereas JsARF4 and JsARF21 each contained only the AuxRE domain.

The occurrence and distribution of CREs in JsARF gene promoter sequences were analyzed using PlantCARE (Fig. 2D). The results showed that the promoters of JsARFs contained numerous CREs, which can be classified into different functional groups. Among them, the most abundant CREs were consensus GC receptor (GR)-responsive elements (GRE) related to light responses, including the MEX-3 recognition element motif, GT1 motif (GGT TAA), G-box, and lamp element. The group representing the second highest number of CREs comprised elements involved in the jasmonic acid methyl ester response. Additionally, several CREs associated with biological and abiotic stresses, including wound, drought, defense, and stress responses, as well as CREs related to salicylic acid, gibberellin, abscisic acid, and auxin responses, were found in the promoter regions of 24 JsARFs. In particular, JsARF4, JsARF19, and JsARF21 contained elements related to auxin response, suggesting that these genes may respond to auxin.

The structures of the 24 JsARF genes were analyzed based on their intron/exon arrangement (Fig. 2E), and the results showed that the coding sequences of all JsARF genes were disrupted by introns, with the numbers varying between 2 and 14.

Collinearity analysis of JsARFs.

Based on the collinearity analysis, gene duplication events were analyzed to clarify the amplification pattern of JsARFs (Fig. 3). The results showed a collinearity relationship between JsARF7 and JsARF24, JsARF5 and JsARF17, and JsARF11 and JsARF13. Furthermore, collinearity among JsARF6, JsARF16, and JsARF19 was observed.

Fig. 3.
Fig. 3.

Collinear relationship of auxin response factor (ARF) genes on Arabian jasmine (Jasminum sambac) chromosomes. Each of the 13 chromosomes of Arabian jasmine is marked with a different color, and each Arabian jasmine ARF (JsARF) gene is shown above the corresponding chromosome. Light grey lines indicate all synteny blocks between each chromosome, and thick red lines indicate duplicated ARF gene pairs. The scale bar marked on the chromosome represents the chromosome length (megabases).

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Phylogenetic analysis of JsARFs.

To classify the phylogenetic relationships among JsARFs, the protein sequences of ARFs in Arabian jasmine, arabidopsis, and rice were used to construct a phylogenetic tree (Fig. 4). Based on the classification of ARFs in arabidopsis, these proteins were divided into seven groups (Guilfoyle et al. 1998): group I, group II, group III A, group III B, group IV, group V, and group VI. Group I included two JsARFs (JsARF2 and JsARF16). Group II was the largest group and included six JsARFs (JsARF1, JsARF4, JsARF6, JsARF10, JsARF15, and JsARF19). Group III A contained three JsARFs (JsARF5, JsARF12, and JsARF17). Group III B contained four JsARFs (JsARF3, JsARF11, JsARF13, and JsARF14). Group IV included only one JsARF (JsARF23). Group V included five JsARFs (JsARF9, JsARF18, JsARF20, JsARF21, and JsARF22). Group VI included three JsARFs (JsARF7, JsARF8, and JsARF24).

Fig. 4.
Fig. 4.

Phylogenetic analysis of auxin response factor (ARF) proteins from Arabian jasmine (Jasminum sambac), arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). ARFs were divided into seven clades, with each represented by a different color. Arabian jasmine ARFs (JsARFs) are indicated in red.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Interaction analysis of JsARF family proteins.

An analysis of potential interactions between the 24 identified JsARFs based on protein structure was performed (Fig. 5). The results showed that JsARF12 and JsARF16 were predicted to interact with six JsARFs. JsARF11, JsARF14, JsARF15, and JsARF23 were predicted to interact with five JsARFs. JsARF20 and JsARF21 were predicted to interact with three JsARFs. However, the remaining 16 JsARFs showed no predicted interactions with any other JsARFs.

Fig. 5.
Fig. 5.

Predicted protein–protein interaction networks of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) proteins. Different genes are shown in different colors, and the lines illustrate the way in which they interacted.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Expression of JsARF genes in various tissues.

The expression details of all 24 JsARF genes in the roots, stems, leaves, and flowers were obtained from the Arabian jasmine transcriptomic data (Fig. 6). The results showed that JsARF4 and JsARF14 were not expressed in any of the analyzed tissues; however, other genes were expressed in at least one tissue. The expression of JsARF5 in roots was significantly higher than that in leaves and flowers, and that of JsARF12 was relatively high in all tissues. Based on these results, there were significant differences in the expression levels of JsARFs in different tissues.

Fig. 6.
Fig. 6.

Relative expression levels of auxin response factor (ARF) genes in flower, leaves, root, and stem tissues of Arabian jasmine (Jasminum sambac). The color scale on the right represents the log2 expression values, with blue and red indicating low and high levels of transcript abundance. Gene names are listed on the right side. Expression-based hierarchical clustering of genes is shown.

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Effect of IAA treatment on the expression of JsARF genes in leaves.

The expression levels of JsARF1, JsARF19, and JsARF23 were significantly different after IAA treatment, and this change gradually decreased with the increasing treatment time (Fig. 7). The expression levels of JsARF2, JsARF3, JsARF5, JsARF8, and JsARF11 initially decreased and then gradually increased. JsARF21 expression decreased to a stable level. JsARF18 expression at 12 h was significantly different from that at 0 h. JsARF20 expression decreased to a stable level after a rapid increase at 6 h.

Fig. 7.
Fig. 7.

Expression of 10 Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes after 0, 1, 6, and 12 h under indoleacetic acid (IAA) treatment. Asterisks indicate statistically significant differences as determined using an analysis of variance (*P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001).

Citation: Journal of the American Society for Horticultural Science 148, 4; 10.21273/JASHS05276-22

Discussion

The ARF family is an important transcription factor family in many plants (Guilfoyle et al. 1998) and has key roles in leaf development, flowering, and fruiting. Furthermore, ARFs participate in lateral root development, leaf growth, and flower development (Kumar et al. 2011; Zouine et al. 2014). In this study, 24 ARF genes in the Arabian jasmine genome were identified, and the main features of their gene structure and conserved function domain were analyzed. The expression levels of JsARFs in different tissues and their response to auxin were also examined.

Most ARF proteins contain three main conserved domains: the unique B3 domain at the N-terminus, the repressor/activation domain ARF in the middle, and the Aux/IAA dimer domain at the C-terminus. Among the 24 JsARF genes, 15 were found to contain these three conserved domains. JsARF1, JsARF2, JsARF6, JsARF7, JsARF10, JsARF14, and JsARF15 had only two conserved domains (B3 and ARF). JsARF4 and JsARF21 had only B3 conserved domains. During a previous study of arabidopsis, all but 4 of the 23 AtARFs contained the three conserved domains (Liscum and Reed 2002). In sorghum (Sorghum bicolor), 21 of the 46 SbARFs contained the three conserved domains; however, all genes encoded proteins with B3 and ARF domains. These results also suggested that the JsARF protein contained Aux/IAA, B3, and ARF domains; however, the number of domains was lower than that in other examined plants. Additionally, the number of introns in the different groups was different, which indicated diverse functions. Similar conclusions have been drawn for tomato (Kumar et al. 2011) and arabidopsis (Reed 2001).

Subsequently, the phylogenetic relationships of the 24 JsARF proteins were analyzed and subsequently divided into seven subfamilies. The members of AtARFs were mainly distributed in group III B, whereas the members of rice and Arabian jasmine were mainly distributed in group II. Based on the phylogenetic relationship between Arabian jasmine and arabidopsis ARFs, JsARF5/12/17 were found to be closely related to AtARF1 and AtARF2 (Ellis et al. 2005), suggesting that these proteins might be involved in the growth of Arabian jasmine leaves and flowers. JsARF23 is closely related to AtARF5, suggesting an association with hypocotyl formation and microtubule growth in Arabian jasmine (Nagpal et al. 2005). We also found that the expression levels of JsARF1, JsARF4, JsARF10, and JsARF14 were very low, or that these genes were not expressed in all tissues, implying that they may have lost their function in tissue development during evolution (Lanctot et al. 2020).

Protein interaction networks are composed of different proteins involved in various life processes, such as biological signaling, regulation of gene expression, energy and material metabolism, and cell cycle regulation, through interactions with each other (Damian et al. 2015). During gene mechanism research, the search for interacting proteins is a process used to deeply explore gene functions. Based on the prediction results of the protein interactions, we found that only eight of these genes had protein–protein interactions.

When growth hormones are absent or present at low concentrations, ARF binds to the Aux/IAA protein to form a nonactivated heterodimer, thus preventing early gene transcription; therefore, there is no growth hormone response. In contrast, when the growth hormone concentration is high, the Aux/IAA protein repressor can be recognized by the SKP-Cullin-F-boxTIR (SCFTIR) complex, and the ubiquitin ligase is activated. This leads to ubiquitination of the Aux/IAA protein and its subsequent degradation by the 26S proteasome. Thus, a homodimer is formed that binds to the growth hormone response element of the early gene promoter and activates early gene transcription. This regulates the expression of downstream genes, resulting in a series of growth hormone-related responses and subsequent physiological functions (Grones and Friml 2015). Because the ARF gene is a transcription factor that regulates auxin-responsive genes, it is important to determine how the JsARF gene responds to IAA treatment. It has been reported that AtARF4/5/16/19 and rice OsARF1/23 transcript levels increased after treatment with auxin, whereas OsARF5/14/21 level decreased (Wang et al. 2007). In our study, IAA also had complex promoting and inhibitory effects on JsARF gene levels. As a transcription factor, ARF can regulate the expression of auxin response genes, which has been adequately demonstrated by previous studies (Hardtke et al. 2004). The expression levels of JsARF5, JsARF12, and JsARF17 were highly induced, indicating that these genes might have an important role in the growth and development of this species. Although the role of JsARFs in these processes is unclear, because of their similarity to AtARFs, the possibility of JsARFs participating in these different developmental processes in Arabian jasmine cannot be ruled out.

Conclusions

In the present study, 24 JsARF genes were identified in Arabian jasmine. The JsARF genes were randomly located on different chromosomes and divided into seven subfamilies according to a phylogenetic analysis of their encoded protein sequences. Their properties were analyzed using gene replication, expression profiles, cis elements, and protein–protein interaction networks. Different types of JsARF partners could interact with each other, and RNA-seq data revealed that most JsARF genes were expressed differently in different tissues. JsARF5, JsARF12, and JsARF17 were strongly expressed in roots, stems, leaves, and flowers. These highly expressed genes might have important roles in plant growth. Additionally, the external application of IAA has an inhibitory or promoting effect on JsARF genes. Although the function of ARFs in Arabian jasmine is currently unknown, the expression profile and analysis of conserved motifs in this study can provide a valuable foundation for future research in this field.

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Supplemental Table 1.

Gene-specific primers were designed for the expression analysis of 23 Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes under indoleacetic acid (IAA) treatment by quantitative real-time polymerase chain reaction (qRT-PCR). JsACTIN2 was used as a loading control, and three biological and three technical replicates were performed for each qRT-PCR.

Supplemental Table 1.
  • Fig. 1.

    Chromosomal locations of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes. The scaffold number of chromosomes (Chr) is shown on the left side of each bar chart. The scaffold size is indicated by its relative length using the information. The color gradient from blue to red on the chromosomes indicates low to high gene density.

  • Fig. 2.

    Phylogenetic tree diagram, motif, domain composition, distributions of cis-regulatory elements (CREs) in the promoter regions, and structure of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) candidate genes. (A) Phylogenetic relationship of JsARFs. (B) Identified conserved motifs of JsARFs; 10 motifs were found and are illustrated in different colors. (C) Conserved domain of JsARFs are represented by three different colors. (D) The 2000-bp upstream sequences were used to analyze 15 specific phytohormone and abiotic stress-related cis elements. (E) Exon–intron structures of JsARF genes. Exons and introns are shown as green color and black lines, respectively. The left and right ends are untranslated regions and are indicated with yellow color.

  • Fig. 3.

    Collinear relationship of auxin response factor (ARF) genes on Arabian jasmine (Jasminum sambac) chromosomes. Each of the 13 chromosomes of Arabian jasmine is marked with a different color, and each Arabian jasmine ARF (JsARF) gene is shown above the corresponding chromosome. Light grey lines indicate all synteny blocks between each chromosome, and thick red lines indicate duplicated ARF gene pairs. The scale bar marked on the chromosome represents the chromosome length (megabases).

  • Fig. 4.

    Phylogenetic analysis of auxin response factor (ARF) proteins from Arabian jasmine (Jasminum sambac), arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). ARFs were divided into seven clades, with each represented by a different color. Arabian jasmine ARFs (JsARFs) are indicated in red.

  • Fig. 5.

    Predicted protein–protein interaction networks of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) proteins. Different genes are shown in different colors, and the lines illustrate the way in which they interacted.

  • Fig. 6.

    Relative expression levels of auxin response factor (ARF) genes in flower, leaves, root, and stem tissues of Arabian jasmine (Jasminum sambac). The color scale on the right represents the log2 expression values, with blue and red indicating low and high levels of transcript abundance. Gene names are listed on the right side. Expression-based hierarchical clustering of genes is shown.

  • Fig. 7.

    Expression of 10 Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes after 0, 1, 6, and 12 h under indoleacetic acid (IAA) treatment. Asterisks indicate statistically significant differences as determined using an analysis of variance (*P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001).

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  • Hardtke CS, Ckurshumova W, Vidaurre DP, Singh SA, Stamatiou G, Tiwari SB, Hagen G, Guilfoyle TJ, Berleth T. 2004. Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4. Development. 131(5):10891100. https://doi.org/10.1242/dev.00925.

    • Search Google Scholar
    • Export Citation
  • Hu W, Zuo J, Hou X, Yan Y, Wei Y, Liu J, Li M, Xu B, Jin Z. 2015. The auxin response factor gene family in banana: Genome-wide identification and expression analyses during development, ripening, and abiotic stress. Front Plant Sci. 6:742. https://doi.org/10.3389/fpls.2015.00742.

    • Search Google Scholar
    • Export Citation
  • Ivica L, Bork P. 2019. Interactive Tree Of Life (iTOL) v4: Recent updates and new developments. Nucleic Acids Res. 47(W1):W256W259. https://doi.org/10.1093/nar/gkz239.

    • Search Google Scholar
    • Export Citation
  • Kawahara Y, de la Bastide M, Hamilton JP, Kanamori H, McCombie WR, Ouyang S, Schwartz DC, Tanaka T, Wu J, Zhou S, Childs KL, Davidson RM, Lin H, Quesada-Ocampo L, Vaillancourt B, Sakai H, Lee SS, Kim J, Numa H, Itoh T, Buell CR, Matsumoto T. 2013. Improvement of the Oryza sativa Nipponbare reference genome using next generation sequence and optical map data. Rice (N Y). 6:4. https://doi.org/10.1186/1939-8433-6-4.

    • Search Google Scholar
    • Export Citation
  • Kazutaka K, Rozewicki J, Yamada KD. 2019. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 20(4):11601166. https://doi.org/10.1093/bib/bbx108.

    • Search Google Scholar
    • Export Citation
  • Koressaar T, Remm M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics. 23(10):12891291. https://doi.org/10.1093/bioinformatics/btm091.

    • Search Google Scholar
    • Export Citation
  • Kumar R, Tyagi AK, Sharma AK. 2011. Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics. 285(3):245260. https://doi.org/10.1007/s00438-011-0602-7.

    • Search Google Scholar
    • Export Citation
  • Lanctot A, Taylor-Teeples M, Oki EA, Nemhauser JL. 2020. Specificity in auxin responses is not explained by the promoter preferences of activator ARFs. Plant Physiol. 182(4):15331536. https://doi.org/10.1104/pp.19.01474.

    • Search Google Scholar
    • Export Citation
  • Liscum E, Reed JW. 2002. Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol. 49(3):387400. https://doi.org/10.1023/A:1015255030047.

    • Search Google Scholar
    • Export Citation
  • Luo XC, Sun MH, Xu RR, Shu HR, Wang JW, Zhang SZ. 2014. Genomewide identification and expression analysis of the ARF gene family in apple. Forensic Genom. 93(3):785797. https://doi.org/10.1007/s12041-014-0462-0.

    • Search Google Scholar
    • Export Citation
  • Magali L, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30(1):325327. https://doi.org/10.1093/nar/30.1.325.

    • Search Google Scholar
    • Export Citation
  • Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell. 17(5):13601375. https://doi.org/10.1105/tpc.105.031716.

    • Search Google Scholar
    • Export Citation
  • Mistry J, Finn RD, Eddy SR, Bateman A, Punta M. 2013. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41(12):e121. https://doi.org/10.1093/nar/gkt263.

    • Search Google Scholar
    • Export Citation
  • Mourya N, Bhopte D, Sagar R. 2017. A review on Jasminum sambac: A potential medicinal plant. IntJ Ind Herbs Drugs. 2(5):1316.

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JM. 2005. Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development. 132(18):41074118. https://doi.org/10.1242/dev.01955.

    • Search Google Scholar
    • Export Citation
  • Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. 2007. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell. 19(1):118130. https://doi.org/10.1105/tpc.106.047761.

    • Search Google Scholar
    • Export Citation
  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A. 2005. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell. 17(2):444463. https://doi.org/10.1105/tpc.104.028316.

    • Search Google Scholar
    • Export Citation
  • Peng Y, Fang T, Zhang Y, Zhang M, Zeng L. 2020. Genome-wide identification and expression analysis of Auxin Response Factor (ARF) gene family in longan (Dimocarpus longan L.). Plants. 9(2):221. https://doi.org/10.3390/plants9020221.

    • Search Google Scholar
    • Export Citation
  • Philippe L, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E. 2012. The Arabidopsis Information Resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Res. 40(D1):D1202D1210. https://doi.org/10.1093/nar/gkr1090.

    • Search Google Scholar
    • Export Citation
  • Qi Y, Wang S, Shen C, Zhang S, Chen Y, Xu Y, Liu Y, Wu Y, Jiang D. 2012. OsARF12, a transcription activator on auxin response gene, regulates root elongation and affects iron accumulation in rice (Oryza sativa). New Phytol. 193(1):109120. https://doi.org/10.1111/j.1469-8137.2011.03910.x.

    • Search Google Scholar
    • Export Citation
  • Qiao LY, Zhang WP, Li XY, Zhang L, Zhang XJ, Li X, Guo HJ, Ren Y, Zheng J, Chang ZJ. 2018. Characterization and expression patterns of auxin response factors in wheat. Front Plant Sci. 9:1395. https://doi.org/10.3389/fpls.2018.01395.

    • Search Google Scholar
    • Export Citation
  • Reed JW. 2001. Roles and activities of Aux/IAA proteins in Arabidopsis. Trends Plant Sci. 6(9):420425. https://doi.org/10.1016/S1360-1385(01)02042-8.

    • Search Google Scholar
    • Export Citation
  • Reshma D, Anitha CT, Sheeja TT. 2021. Phytochemical and pharmacological properties of five different species of Jasminum. Plant Arch. 21:126136. https://doi.org/10.51470/PLANTARCHIVES.2021.v21.no2.022.

    • Search Google Scholar
    • Export Citation
  • Schruff MC, Spielman M, Tiwari S, Adams S, Fenby N, Scott RJ. 2006. The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development. 133(2):251261. https://doi.org/10.1242/dev.02194.

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Xin Huang College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Haigang Guo College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Lili Yin College of Life Science, Shanxi Datong University, Datong 037009, Shanxi, China

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Ruigang Wu College of Landscape and Ecological Engineering, Hebei University of Engineering, Handan 056038, Hebei, China

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Xingwen Zhou College of Architecture and Urban Planning, Fujian University of Technology, Fuzhou 350118, Fujian, China

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Contributor Notes

R.W. and X.Z. contributed equally to this work. This study was supported by the Youth Science Foundation of Hebei Province (C2019402255), the Key Program of Innovation and Entrepreneurship Training Program for College Students of Hebei College of Engineering (X202210076061), and the Handan Science and Technology Program (21422012321).

R.W. is the corresponding author. E-mail: wuruigang1986@126.com.

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  • Fig. 1.

    Chromosomal locations of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes. The scaffold number of chromosomes (Chr) is shown on the left side of each bar chart. The scaffold size is indicated by its relative length using the information. The color gradient from blue to red on the chromosomes indicates low to high gene density.

  • Fig. 2.

    Phylogenetic tree diagram, motif, domain composition, distributions of cis-regulatory elements (CREs) in the promoter regions, and structure of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) candidate genes. (A) Phylogenetic relationship of JsARFs. (B) Identified conserved motifs of JsARFs; 10 motifs were found and are illustrated in different colors. (C) Conserved domain of JsARFs are represented by three different colors. (D) The 2000-bp upstream sequences were used to analyze 15 specific phytohormone and abiotic stress-related cis elements. (E) Exon–intron structures of JsARF genes. Exons and introns are shown as green color and black lines, respectively. The left and right ends are untranslated regions and are indicated with yellow color.

  • Fig. 3.

    Collinear relationship of auxin response factor (ARF) genes on Arabian jasmine (Jasminum sambac) chromosomes. Each of the 13 chromosomes of Arabian jasmine is marked with a different color, and each Arabian jasmine ARF (JsARF) gene is shown above the corresponding chromosome. Light grey lines indicate all synteny blocks between each chromosome, and thick red lines indicate duplicated ARF gene pairs. The scale bar marked on the chromosome represents the chromosome length (megabases).

  • Fig. 4.

    Phylogenetic analysis of auxin response factor (ARF) proteins from Arabian jasmine (Jasminum sambac), arabidopsis (Arabidopsis thaliana), and rice (Oryza sativa). ARFs were divided into seven clades, with each represented by a different color. Arabian jasmine ARFs (JsARFs) are indicated in red.

  • Fig. 5.

    Predicted protein–protein interaction networks of Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) proteins. Different genes are shown in different colors, and the lines illustrate the way in which they interacted.

  • Fig. 6.

    Relative expression levels of auxin response factor (ARF) genes in flower, leaves, root, and stem tissues of Arabian jasmine (Jasminum sambac). The color scale on the right represents the log2 expression values, with blue and red indicating low and high levels of transcript abundance. Gene names are listed on the right side. Expression-based hierarchical clustering of genes is shown.

  • Fig. 7.

    Expression of 10 Arabian jasmine (Jasminum sambac) auxin response factor (JsARF) genes after 0, 1, 6, and 12 h under indoleacetic acid (IAA) treatment. Asterisks indicate statistically significant differences as determined using an analysis of variance (*P < 0.05, **P < 0.01, ***P < 0.001, ****P < 0.0001).

 

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