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Article

The Auxin/Indole-3-Acetic Acid (Aux/IAA) Gene Family Analysis of Four Rosaceae Genomes and Expression Patterns of PmIAAs in Prunus mume

by
Nuoxuan Liu
1,
Li Li
1,
Xiling Chen
1,
Yanlong Zhang
1 and
Tengxun Zhang
1,2,*
1
College of Landscape Architecture and Arts, Northwest A & F University, Yangling 712100, China
2
Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, Beijing Forestry University, Beijing 100083, China
*
Author to whom correspondence should be addressed.
Horticulturae 2022, 8(10), 899; https://doi.org/10.3390/horticulturae8100899
Submission received: 7 August 2022 / Revised: 10 September 2022 / Accepted: 27 September 2022 / Published: 30 September 2022
(This article belongs to the Section Genetics, Genomics, Breeding, and Biotechnology (G2B2))
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Abstract

:
Auxin is an important phytohormone through plant growth and development. Aux/IAA protein, as a core component in the auxin signaling pathway, plays a vital role in various biological processes such as flower development and floral volatile metabolism in many plants. However, there were a few studies on the Aux/IAA gene family in Prunus plants in Rosaceae and expression patterns of PmIAAs in P. mume. Here, we identified a total of 108 RoIAA gene family members in four typical Rosaceae plants, which included 22 PmIAAs from P. mume, 22 PpIAAs from Prunus persica, 31 PdIAAs from Prunus dulcis and 33 PaIAAs from Prunus armeniaca. Subsequently, the results of the phylogenetic analysis of Aux/IAAs showed that they were categorized into ten groups, and gene structures and motifs were conservative in each group, suggesting that RoIAAs in Rosaceae species had a strong relationship. However, the physical distributions of RoIAAs on chromosomes of every species showed completely uneven. Gene duplications suggested that seven pairs of PmIAAs, eleven pairs of PpIAAs, eleven pairs of PdIAAs, and three pairs of PaIAAs suffered from tandem and segmental duplications. Moreover, the results of the synteny analysis indicated that RoIAAs in four Rosaceae species might come from one ancestor. To explore the roles of PmIAAs in P. mume, expression patterns in five tissues and at four flowering development stages were performed. The results showed that PmIAAs variously expressed in five tissues and five genes (PmIAA2, −9, −10, −12, and −15) might affect flower development and the synthesis of floral compounds in P. mume. This study provided valuable information for further elucidating the regulatory function of PmIAAs in metabolism processes in P. mume.

1. Introduction

The hormone auxin plays an essential role in a blend of development processes in plants, such as flower and fruit development, wood formation, seed development, and vascular tissue formation [1,2,3,4]. Auxin also regulates various cellular processes and responses, such as cell division, expansion, and differentiation [5,6]. Aux/IAA protein is one of the core components in the auxin signaling pathway involved in early auxin response, which can contribute to balancing the level of auxin. When auxin concentration was high, the degradation of Aux/IAA genes was activated via an SCFTIR1 ubiquitin–ligase complex to release ARFs from inhibitions. On the other hand, Aux/IAA would inhibit the normal function of ARFs via domains III and IV to bind with ARFs when the level of auxin was low [7]. Typical Aux/IAA protein was known as short-lived nuclear proteins and obtained four highly conserved domains, called domains I–IV [8,9]. Domain I, the smallest and least conserved domain [10], was located at the N-terminal of the sequence and characterized by the leucine repeat motif with the amino acid sequence ‘LxLxLx’ that was important for repressing the function of the auxin response factor (ARF) protein [11]. Located in the middle region, domain II contained a conservative sequence ‘GWPPV’, which bound with the ubiquitin–proteasome protein (TIR1) to promote the rapid degradation of the Aux/IAA protein [12]. Domains III and IV at C-terminal interacted with ARF to induce or repress the transcription of auxin-responsive genes [13].
Auxin signaling might be related to floral scent metabolism. In RNA interference-based (RNAi) plants for a benzoyl-CoA:benzyl alcohol/phenylethanol benzoyltransferase (BPBT) gene, flower and seed morphology increased along with a decrease in the amount of floral volatiles [14]. In addition, some research on Aux/IAA genes involved in the secondary metabolite biosynthesis has been reported, which included color formation and floral scent biosynthesis. For instance, MdIAA26 in apples positively regulated the accumulation of anthocyanin [15]. In the flower of Hedychium coronarium, HcIAA2 was a negative regulator of the key volatile compounds, whereas HcIAA4 could alter the volatile emission amounts [16]. When the expression of SlIAA15 was downregulated, the monoterpene content in the trichome of tomatoes was reduced [17]. To sum up, Aux/IAA genes might play important roles in the floral scent formation, and their functions are diverse in different species.
Prunus mume, a species of the Rosaceae family, is well-known as an ornamental woody plant blooming in winter or early spring and widely cultivated in the southern regions of China [18]. Due to the unique flowering time of P. mume, it can be an essential horticultural plant. Distinguishing P. mume from other species in Prunus, such as Prunus persica and Prunus armeniaca, its flowers emit pleasant and recognizable scents, mainly consisting of phenylpropanoids/benzenoids such as benzyl acetate, cinnamyl acetate, eugenol, and so on [18,19,20]. Given that most interspecific hybrids in P. mume lost their fragrance during breeding [21], the work to breed new cultivars of P. mume with floral aroma is needed. However, the molecular mechanism of floral volatile compound synthesis in P. mume is still unclear. Although many Aux/IAA gene families have been identified in flowering plants, such as Arabidopsis thaliana [10], Malus domestica [22], Populus trichocarpa [23], blueberries [24], H. coronarium [16], and so on, little information was found in the genome-wide analysis of the Aux/IAA gene family in Prunus plants in Rosaceae.
In this study, the Aux/IAA gene family in four Rosaceae species containing P. mume, P. persica, P. dulcis, and P. armeniaca were identified. In addition, we performed a comprehensive bioinformatics analysis of their gene structure, conserved motifs, chromosomal location, phylogenetic tree, synteny analysis, and cis-acting elements in promoters. Furthermore, the expression patterns of Aux/IAAs of P. mume in different tissues and at different flowering stages were carried out to be conducive for future studies on illustrating their roles in metabolism processes during flower development. Our results attempted to lay a foundation and give clues to the functions of Aux/IAA genes in Rosaceae especially in P. mume.

2. Materials and Methods

2.1. Identification of Aux/IAA Genes in Four Rosaceae Species

The whole protein and genomic sequences of P. mume were obtained from the website of the P. mume genome project (http://prunusmumegenome.bjfu.edu.cn/, accessed on 2 November 2021). The genome datasets of the other species in Rosaceae, including P. persica, P. armeniaca, and P. dulcis, were downloaded from the Genome Database for Rosaceae (GDR, https://www.rosaceae.org, accessed on 13 November 2021) and Ensembl Plants (https://plants.ensembl.org/, accessed on 15 November 2021). Moreover, a hidden Markov model (HMM) file of Aux/IAA (PF02309) was obtained from Pfam (http://pfam.xfam.org/, accessed on 1 November 2021), and then it was employed as a query to search against the Aux/IAA amino acid sequences of Rosaceae by HMMER3.0 software (http://hmmer.org/, accessed on 20 November 2021) with a cutoff value of 10−5. The Aux/IAAs of Rosaceae species were confirmed by the NCBI Conserved Domain Search Service (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi, accessed on 29 November 2021). The online tool Expasy (https://web.expasy.org/protparam/, accessed on 9 February 2022) was applied to compute the amino acid length (aa), molecular weight (MW), and theoretical isoelectric point (pI) of all predicted Aux/IAAs.

2.2. Phylogenetic Analysis

All amino acid sequences of IAAs were downloaded to construct the phylogenetic tree. The AtIAAs of A. thaliana were obtained from TAIR (https://www.arabidopsis.org/, accessed on 3 November 2021). Sequences of other IAAs were downloaded from the National Center for Biotechnology Information (NCBI) database. Multiple sequence alignment of RoIAAs and other plants was performed by Clustal X [25]. Subsequently, a phylogenetic tree was established using MEGA7.0 software [26] by a neighbor joining (NJ) method with 1000 bootstrap replicates. The online tool iTOL (https://itol.embl.de/, accessed on 7 April 2022) was used to visualize the phylogenetic tree.

2.3. Exon–Intron Structural and Conserved Motif Analysis

The online program Gene Structure Display Server (GSDS: http://gsds.cbi.pku.edu.cn/, accessed on 7 April 2022) was applied to investigate the structure of the exons and introns in the RoIAA genes of four Rosaceae plants. The conserved motifs were analyzed and visualized by MEME tool (https://meme-suite.org/meme/, accessed on 7 April 2022) with the parameters given as follows: the maximum number of motifs and optimum motif width were set to 10 and 6–50, respectively. The distribution of conserved motifs and gene structure in the RoIAAs of Rosaceae was visualized using TBtools software [27]. Multiple sequence alignment of PmIAA proteins was conducted by DNAMAN software (Lynnon Biosoft, Quebec, Canada, accessed on 9 May 2022). Moreover, conserved domains were marked.

2.4. Chromosomal Distribution, Synteny Analysis, and Gene Duplication

The detailed information of the physical distributions and collinearities of the Aux/IAAs in Rosaceae was retrieved from the database and then was mapped in TBtools software. Then, a Dual Systeny Plot for MCscan in TBtools was employed to analyze the syntenic relationships of Aux/IAAs between P. mume and P. dulcis, P. persica, and P. armeniaca. The mutation rates of Ka (nonsynonymous) versus Ks (synonymous) were calculated by a Ka_Ks calculator [28]. The divergence time (T) of Aux/IAA segmental duplication pairs was calculated with the equation T = Ks/2r. The ‘r’ was taken to be 1.5 × 10−8 synonymous substitutions per site per year for dicotyledonous plants [29].

2.5. Gene Expression Analysis

The expression patterns of PmIAAs in different tissues and at different flowering development stages of P. mume were analyzed using the transcriptome data, of which five tissues (flowering, fruit, leaf, root, and stem) were obtained from the NCBI Sequence Reading Archive (SRA) with the accession number of SRP014885. The advanced heatmap was drawn using OmicStudio tool with the Euclidean clustering method (https://www.omicstudio.cn/tool/4, accessed on 24 June 2022) in rows according to the fragments per kilobase of transcript per million fragments mapped (FPKM) values of Aux/IAAs.

2.6. Analysis of Cis-Acting Elements in Promoters

Upstream promoter sequences (2000 bp) were extracted from the genome of P. mume, and cis-acting regulatory elements were predicted by the online PlantCare database (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 2 July 2022). The location of every cis-acting element was visualized by TBtools software with BioSequence Structure Illustrator tool.

3. Results

3.1. Genome-Wide Identification of Aux/IAA Genes in Rosaceae

A total of 108 members were identified in four Rosaceae plant genomes, among which 22 were in P. mume, 22 in P. persica, 31 in P. dulcis, and 33 in P. armeniaca (Table 1). The number of the Aux/IAAs in P. persica was equivalent to that in P. mume. We named them PmIAA1-22, PpIAA1-22, PdIAA1-24, and PaIAA1-16(a–f). The characteristics of Aux/IAA genes include physical location, ORF (open reading frame) length, amino acid length, molecular weight (kDa), isoelectric points (PI), and exon numbers, which are listed in Table 1. The amino acid length of RoIAAs widely varied from 111 (PmIAA22) to 501 aa (PdIAA7). The molecular weight (MW) of RoIAA protein was between 12.87 (PmIAA22) and 56.07 kDa (PdIAA7), with an average of 30.28 kDa. The isoelectric point (pI) of the RoIAAs ranged from 4.89 (PpIAA19) to 9.51 (PaIAA4), with an average of 7.35.

3.2. Phylogenetic Analysis of RoIAAs

To examine the evolutionary relationship of Aux/IAA family members, the Aux/IAAs in A. thaliana and other plants whose function had been characterized in several plants were downloaded as well. Based on the putative protein sequences, a phylogenetic tree was constructed by MEGA 7, in which all Aux/IAA family members mainly fell into ten groups named A–J (Figure 1). The Aux/IAAs from P. mume, P. persica, P. dulcis, and P. armeniaca were distinctly distributed in almost every group, suggesting that they might be derived from the same ancestor. Canonical RoIAAs were generally located in the A–E groups. Other noncanonical PmIAAs were clustered with noncanonical AtIAAs such as PmIAA6 and PmIAA11 that lacked domains II and IV.

3.3. Gene Structure and Motif Analysis of RoIAAs

To further illustrate the structural similarity and difference of RoIAAs, the exon and intron distributions and conserved motifs were analyzed and visualized on the basis of the phylogenetic tree of RoIAAs. As shown in Figure 2a, RoIAAs obtained different numbers of exons, widely ranging from 2 to 10. In addition, most RoIAAs obtained 5 exons. Moreover, the distribution and number of exons show similarities in accordance with the phylogenetic alignment of RoIAAs. For example, PmIAA14, PpIAA13, and PdIAA23 shared a similar number of exons, although the length of each exon and intron was divergent.
To further understand the characteristic regions of RoIAAs, the online program MEME was employed to analyze the motif distribution of 108 RoIAAs with 10 individual motifs identified (Figure 2b). The number and length of conserved motifs were various and changed from 1 to 10 and 15 to 50, respectively. RoIAAs that were in the same group shared a quite high degree of similarity in the distribution and number of motifs. For example, PmIAA9, PaIAA3, PdIAA2, and PpIAA7 closely clustered, and they all had six motifs namely motif 1, motif 2, motif 3, motif 4, motif 6, and motif 9. PmIAA14, PdIAA22, and PpIAA13 in group E contained five motifs, namely motifs 1–4 and motif 6. Out of the 108 RoIAA proteins, 75 were detected to obtain motifs 1–4, which were related to the four typical conserved domains (domains I–IV) of the Aux/IAA family (Figure S1). Meanwhile, some of the nontypical RoIAAs in groups I and J would have one or two of these four motifs; for example, only motif 1 was in PmIAA22 and motif 3 in PmIAA21, and motifs 2 and 3 were found in PdIAA19, PpIAA17, and PaIAA7. Motif 2 existed in 106 RoIAAs, except for PmIAA21 and PmIAA22.

3.4. Chromosomal Location Analyses

Based on the genome datasets of P. mume, P. persica, P. dulcis, and P. armeniaca, the chromosomal location of 108 RoIAAs was mapped (Figure 3), showing that the distributions of RoIAAs in chromosomes were uneven, and RoIAAs were not on each chromosome of these four Rosaceae plants. For example, the largest number of PmIAAs was distributed on Pm2, followed by Pm4, which had five PmIAAs. Pm3, Pm5, and Pm7 missed the PmIAA gene. PpIAAs were only located on chromosomes G1, G3, G6, G7, and G8, and chromosome G1 obtained the largest number of PpIAAs in P. persica, followed by chromosome G3. In P. dulcis, PdIAAs were situated in chromosomes Pd01, Pd03, Pd06, Pd07, and Pd08. PaIAAs were settled on chromosomes LG1, LG2, LG4, LG6, and LG8 in P. armeniaca. Most RoIAAs were distributed on the chromosomes except for PmIAA22, which was on Pm0, PdIAA23 and PdIAA24 were on Pd00, and PaIAA16 was on LG0. The chromosomes Pm1, Pm6, and Pm8 shared a similar number of PmIAAs; the chromosomes Pp6, Pp7, and Pp8 obtained a similar number of PpIAAs; the chromosomes Pd03 and Pd06 had a similar number of PdIAAs; and the chromosomes LG4 and LG8 possessed a similar number of PaIAAs. The uneven distribution of RoIAAs on chromosomes suggested the diversification of the RoIAA gene family.

3.5. Synteny Analyses

Duplication events played vital roles in gene family expansion [30]. In order to further detect the homology and paralog of the RoIAA genes in Rosaceae, duplicated gene pairs among 108 RoIAAs were performed. Three pairs of PmIAAs mapping on Pm1, Pm2, and Pm4; two pairs of PpIAAs mapping on G1 and G6; one pair of PdIAAs mapping on Pd01; and one pair of PaIAAs mapping on LG2 were considered as tandem duplication (Figure 3). As shown in Figure 4, there were four pairs of PmIAAs, nine pairs of PpIAAs, ten pairs of PdIAAs, and two pairs of PaIAAs, which were described as segmental duplication. It was worth noticing that the events of duplication were similar in these four Rosaceae plants, which might indicate that these four Rosaceae had a stable evolutionary relationship.
To further explore the evolutionary mechanism of the Aux/IAA gene family, three of the comparative synteny maps of P. mume were constructed and associated with the other three Rosaceae species, namely P. persica, P. dulcis, and P. armeniaca (Figure 5). A total of 35 pairs were found in P. mume and P. persica, 30 orthologous pairs of collinearity were identified between P. mume and P. dulcis, and 27 gene pairs were in P. mume and P. armeniaca (Table S2). Interestingly, we found that one PmIAA sometimes could correspond to several genes in these syntenic orthologous gene pairs (particularly PmIAA2 and PmIAA17), suggesting that these genes might play significant roles in the Aux/IAA gene family evolution. In addition, almost every collinear gene pair of PmIAA was found in P. persica (Figure 5A). However, no collinear gene pair of PmIAA14 and PmIAA8 was detected in P. dulcis and P. armeniaca, respectively (Figure 5B,C). These findings suggested that the Aux/IAA gene families of P. mume, P. dulcis, P. persica, and P. armeniaca might come from a common ancestor and have undergone a similar evolutionary period.
The selection pressure of gene duplications was calculated by using the mutation rates of Ka (nonsynonymous) versus Ks (synonymous). As shown in Table 2, all the Ka/Ks values of duplicated RoIAA pairs were under 1.0 and ranged from 0.097 to 0.344, indicating a strong purifying selection during RoIAAs expansion. The divergence time of the duplicated pairs of RoIAAs ranged from 44.48 to 108.54 million years (Mya).

3.6. Sequence Analysis of PmIAAs in P. mume

To further discover the potential function of PmIAAs, multiple sequence alignment was carried out. The results indicated that all PmIAAs presented 22.19% similarity (Figure 6). Although the similarity was low, most PmIAAs contained the four conserved domains in Aux/IAA. Highly conserved domain I (LxLxLx) was absent in six out of twenty-two PmIAAs. Domain II was also weakly conservative in six PmIAAs. Only PmIAA21 lost domain IV.

3.7. Expression Profiles of PmIAAs in Different Tissues and at Different Flowering Development Stages

Based on the RNA-seq data for the five tissues and four flowering stages of P. mume, the heatmap was drawn by the FPKM values of PmIAAs. The expression patterns of PmIAAs, such as PmIAA2, PmIAA3, PmIAA9, and PmIAA16, generally showed distinct differences in five tissues (Figure 7A), suggesting that PmIAAs played different roles in various tissues. Five genes (PmIAA7, PmIAA11, PmIAA20, PmIAA21, and PmIAA22) were expressed mostly lower in five tissues. Only PmIAA3 was highly expressed in five tissues, and the expression level in fruit was slightly higher than that in others. The expression levels of six PmIAA genes (PmIAA1, PmIAA4, PmIAA14, PmIAA16, PmIAA17, and PmIAA19) in the stem were the highest, which indicated that they might participate in the metabolism in the stem. There were also four genes (PmIAA2, PmIAA9, PmIAA10, and PmIAA15) that were expressed higher in flowers than in other tissues, in which the expression of PmIAA9 was the highest. The results speculated that these genes might be involved in the physical and biological processes that occurred in flowers.
Generally, floral scent was mainly emitted from the flower in P. mume [31]. To screen the potential PmIAAs involved in floral scent biosynthesis, the expression patterns of PmIAAs at four flowering stages were analyzed (Figure 7B). Moreover, the expression of PmIAA2, PmIAA15, and PmIAA16 increased from the budding stage to full-blooming stage when reaching their peak and then decreased during wilting. The expression level of four genes, namely PmIAA3, PmIAA9, PmIAA10, and PmIAA12, was raised from the budding stage to wilting stage. As the flowering developed, the expression of these genes presented dynamic changes.

3.8. Promoter Analysis of Cis-Acting Elements of PmIAAs

The cis-acting elements of promoters played essential roles in regulating the expression of PmIAAs especially in the plant environment, hormone response, and stress response. Nineteen cis-acting elements were detected by the PlantCARE database as shown in Figure 8. The largest number of cis-acting elements was associated with the light response, mainly including Box 4, I-box, Box II, TCCC-motif, G-box, ATCT-motif, P-box, LAMP-element, and so on. There were also many hormone-responsive elements in promoters, such as the abscisic acid responsiveness element (ABRE), MeJA-responsiveness element (CGTCA-motif and TGACG-motif), auxin responsive element (TGA and AuxRE-core), and gibberellin responsive element (P-box, GARE-motif, and TATC-box), suggesting that the expression of PmIAAs might be affected by several hormones. In addition, stress-response elements, including defense and stress responsive element (TC-rich repeats), drought inducibility element (MBS), low-temperature responsive element (LTR), and wound responsive element (WUN-motif), were distributed in promoter regions, which indicated that the expression of PmIAAs might be induced by abiotic stress as well.

4. Discussion

Aux/IAA protein is a crucial component in the auxin signaling pathway. To date, biological functions of Aux/IAA proteins have been revealed during growth and development processes in many plants. However, there were a few studies on the comprehensive bioinformatic analysis of the Aux/IAA gene family in Prunus plants in Rosaceae and the expression patterns of PmIAA in P. mume. Aux/IAA gene family members have been identified in various plants, such as monocots including Oryza sativa (31), Hordeum vulgare (36), and Phyllostachys edulis (35); and dicotyledons, for example, Arabidopsis (29), radish (65), and Gossypium hirsutum (10) [10,30,32,33,34,35]. A total of 22 PmIAAs in P. mume were identified in this study. In addition, the Aux/IAA genes in the other three Rosaceae species were also obtained, including 31 PdIAAs for P. dulcis, 33 PaIAAs for P. armeniaca, and 22 PpIAAs for P. persica. The number of gene family members in P. persica was the same as that in P. mume. Each PmIAA except for PmIAA22 could exist one orthologous gene in P. persica (Figure 5A), suggesting that the Aux/IAA gene family in these two species might have a close evolutionary relationship, which has also been proved in the phylogenetic tree.
The canonical Aux/IAA proteins usually contain four highly conserved domains [9]. Nevertheless, some Aux/IAA proteins might lack one or more domains [36]. Domain I was considered as a repression domain that could inactivate the transcription of ARFs [11], which was absent in six PmIAAs, namely PmIAA5, PmIAA6, PmIAA7, PmIAA11, PmIAA12, and PmIAA22 (Figure 6), suggesting that these PmIAAs might lose the function of repressing the ARF function. Domain II played an important role in Aux/IAA protein instability [12]. PmIAA6, PmIAA7, PmIAA11, PmIAA12, PmIAA21, and PmIAA22, which were short of domain II, might not be degraded by the SCRTIR1 protein complex and have a longer half-life compared with the typical Aux/IAA protein [33]. Although three domains in typical Aux/IAAs were missed in PmIAA22, it still was considered as a member of the PmIAA gene family because of the lightly conserved domain IV. A similar phenomenon appeared in tomatoes as well in which SlIAA33 only contained a weakly conserved domain III [37]. These results further illustrated the functional diversities among members of the PmIAA gene family.
Gene duplication events can accelerate the rapid expansion of the evolution of gene families, including whole-genome duplication, tandem duplication, and segmental duplication [22,33]. In this study, three pairs of PmIAA genes had experienced tandem duplications, and four pairs of segmental duplications were identified (Table 2). Previous studies have shown that tandem duplication usually occurs on the same chromosome and segmental duplication on different chromosomes [38]. For example, four pairs of genes in apples, including MdAux/IAA14-19, MdAux/IAA38-32, MdAux/IAA36-16, and MdAux/IAA25-39, were considered as tandem duplicated pairs, and each pair was distributed on the same chromosome [22]. Meanwhile, PmIAA2 and PmIAA3 were on Pm1, whereas PmIAA1 and PmIAA4 were located on Pm1 and Pm2, respectively (Figure 3A). The Ka/Ks values of all the pairs of gene duplication were calculated and they were less than 1, indicating that PmIAA paralogous pairs had suffered from purifying the selection. The results indicated that Aux/IAA families were amplified by tandem and segmental duplication, which might play significant roles in gene function diversification.
Floral scent formation was a complex metabolic process characterized by changes in the floral volatiles from P. mume [39]. The emission of floral volatiles had a spatial–temporal rhythm, which was regulated by the related genes in many plants such as Lilium, Freesia x hybrida, and roses [40,41,42]. Previous studies have shown a strong relationship between Aux/IAA genes and floral scent formation, such as in H. coronarium and tomatoes [16,17]. In addition, several Aux/IAA gene functions on the floral scent formation have been reported. The expression level of HcIAA4 that played a positive role in the volatile compound contents of H. coronarium peaked at the blooming period and then declined during senescence [16]. PmIAA12 was close to HcIAA4 (Figure 1) and mainly expressed in flowers and leaves, indicating that PmIAA12 might be also one potential gene regulating floral scent metabolism in P. mume. Although the expression of PmIAA16 was similar with the emission of benzyl acetate and cinnamyl acetate, PmIAA16 expressed the highest in the stem and clustered together with HcIAA2, a negative gene of floral volatiles in H. coronarium. Thus, the potential function of PmIAA16 awaits future research.
In addition, PmIAA2, PmIAA9, PmIAA10, and PmIAA15 expressed the highest in flowers (Figure 7A), suggesting that they might be involved in secondary metabolism in flowers. The expression trends of PmIAA2 and PmIAA15 at different flowering development stages were consistent with the emissions of benzyl acetate and cinnamyl acetate [31,43], speculating that they might play important roles in the synthesis of these two compounds. Furthermore, in the phylogenetic tree, PmIAA15 clustered together with SlIAA15 (Figure 1), which was involved in the volatile monoterpene synthesis in tomatoes [17], and PmIAA2 was close to EgrIAA4 that functioned on the wood formation in Eucalyptus [3], speculating that PmIAA2 and PmIAA15 might participate in the secondary metabolism such as floral scent and color formation. Although PmIAA9 and PmIAA10 were clustered together with AtIAA17 and AtIAA3, respectively, which affected the root hair growth [44], PmIAA9 and PmIAA10 significantly expressed the highest in flowers, indicating that they might play roles in the metabolism in flowers. PmIAA9 and PmIAA10 might participate in the synthesis of cinnamyl alcohol and eugenol [31,43], since the expression patterns of the two genes were in accordance with the contents of the two volatile compounds (Figure 7B). The results might investigate the potential biological functions of PmIAAs, and further study should be needed to prove them.

5. Conclusions

Although the Aux/IAA gene family has been reported in many plants, in the Prunus plants in Rosaceae, it was little known. A study on the genome-wide identification of four typical Rosaceae genomes, namely P. mume, P. persica, P. dulcis, and P. armeniaca, and expression analyses of the Aux/IAA gene family in P. mume needs to be performed. Moreover, the expression patterns of PmIAA2, PmIAA9, PmIAA10, PmIAA12, and PmIAA15 were consistent with flower development and floral volatiles emitting in P. mume. The results attempted to create a foundation and clarify the potential functions of Aux/IAA genes in metabolism processes during flower development in P. mume.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae8100899/s1, Table S1: Gene_id numbers of Aux/IAAs were used in phylogenetic tree; Table S2: Orthologous pairs between PmIAA and IAAs from other three Rosaceae species. Figure S1: Motifs 1–4 of Aux/IAA proteins were investigated by MEME.

Author Contributions

Conceptualization, N.L. and T.Z.; methodology, N.L.; software, N.L.; validation, L.L., Y.Z. and T.Z.; formal analysis, Y.Z.; investigation, L.L. and X.C.; resources, T.Z.; data curation, T.Z.; writing—original draft preparation, N.L.; writing—review and editing, T.Z.; supervision, T.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Fundamental Research Funds for the Central Universities, grant number: BFUKF202209; and Chinese Universities Scientific Fund, grant number: 2452021098.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. Phylogenetic tree of Aux/IAA family members from P. mume, P. persica, P. dulcis, P. armeniaca, A. thaliana, and other species. The tree was constructed on the basis of sequence alignment of amino acid sequences using neighbor-joining method with 1000 bootstrap replications. Different colors indicate ten different subgroups, and red dots highlight PmIAAs. All referred Aux/IAA genes are listed in Table S1.
Figure 1. Phylogenetic tree of Aux/IAA family members from P. mume, P. persica, P. dulcis, P. armeniaca, A. thaliana, and other species. The tree was constructed on the basis of sequence alignment of amino acid sequences using neighbor-joining method with 1000 bootstrap replications. Different colors indicate ten different subgroups, and red dots highlight PmIAAs. All referred Aux/IAA genes are listed in Table S1.
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Figure 2. Gene structure and motif compositions of RoIAAs from Rosaceae based on phylogenetic tree. In phylogenetic tree, groups A–J are in the same color box. (a) Exons and introns structure of RoIAAs. The yellow rectangle shows exon, the green rectangle exhibits nontranslate area, and the black line represents intron. Length of exons could be inferred by the scale at the bottom. (b) Conserved motifs in RoIAAs. Each motif is shown by one color box. Details of motifs 1–4 are referred to Supplementary Figure S1.
Figure 2. Gene structure and motif compositions of RoIAAs from Rosaceae based on phylogenetic tree. In phylogenetic tree, groups A–J are in the same color box. (a) Exons and introns structure of RoIAAs. The yellow rectangle shows exon, the green rectangle exhibits nontranslate area, and the black line represents intron. Length of exons could be inferred by the scale at the bottom. (b) Conserved motifs in RoIAAs. Each motif is shown by one color box. Details of motifs 1–4 are referred to Supplementary Figure S1.
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Figure 3. Chromosomal location of RoIAA genes. (A–D) Chromosomal distribution of PmIAAs (purple), PpIAAs (pink), PdIAAs (blue), and PaIAAs (green), respectively. Pm, G, Pd, and LG represent the number of chromosomes in P. mume, P. persica, P. dulcis, and P. armeniaca, respectively. Pm0, Pd00, and LG0 represent unassigned chromosomes. Pm0 is scaffold205 in the genome of P. mume. Pd00 is pdulcis26_s0670 in the genome of P. dulcis. LG0 is tig00008361 in the genome of P. armeniaca. Red line represents tandem duplication of RoIAAs. Length of chromosomes could be inferred by the left scale.
Figure 3. Chromosomal location of RoIAA genes. (A–D) Chromosomal distribution of PmIAAs (purple), PpIAAs (pink), PdIAAs (blue), and PaIAAs (green), respectively. Pm, G, Pd, and LG represent the number of chromosomes in P. mume, P. persica, P. dulcis, and P. armeniaca, respectively. Pm0, Pd00, and LG0 represent unassigned chromosomes. Pm0 is scaffold205 in the genome of P. mume. Pd00 is pdulcis26_s0670 in the genome of P. dulcis. LG0 is tig00008361 in the genome of P. armeniaca. Red line represents tandem duplication of RoIAAs. Length of chromosomes could be inferred by the left scale.
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Figure 4. Segmental duplications of RoIAAs in P. mume, P. persica, P. dulcis, and P. armeniaca. Each scale of circle indicates a chromosome or fragment obtained RoIAAs. Gray lines indicate collinear relationships among the synteny blocks in a whole genome, and red lines highlight segmental duplication gene pairs of RoIAAs. (A–D) Segmental duplications of PmIAAs (purple), PpIAAs (pink), PdIAAs (blue), and PaIAAs (green), respectively. Gene names are emphasized at the outside of chromosomal boxes.
Figure 4. Segmental duplications of RoIAAs in P. mume, P. persica, P. dulcis, and P. armeniaca. Each scale of circle indicates a chromosome or fragment obtained RoIAAs. Gray lines indicate collinear relationships among the synteny blocks in a whole genome, and red lines highlight segmental duplication gene pairs of RoIAAs. (A–D) Segmental duplications of PmIAAs (purple), PpIAAs (pink), PdIAAs (blue), and PaIAAs (green), respectively. Gene names are emphasized at the outside of chromosomal boxes.
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Figure 5. Synteny analyses of Aux/IAA genes. (A) Synteny analyses in P. mume and P. persica (Pp). (B) Synteny analyses in P. mume and P. dulcis (Pd). (C), Synteny analyses in P. mume and P. armeniaca (Pa). Red line means orthologous gene pair. Gray line indicates collinear blocks within P. mume and other Rosaceae plant genomes. Red line implies orthologous gene pair. Chromosomal names with prefixes ‘Pm’, ‘G’, ‘Pd’, and ‘LG’ indicate P. mume, P. persica, P. dulcis, and P. armeniaca, respectively.
Figure 5. Synteny analyses of Aux/IAA genes. (A) Synteny analyses in P. mume and P. persica (Pp). (B) Synteny analyses in P. mume and P. dulcis (Pd). (C), Synteny analyses in P. mume and P. armeniaca (Pa). Red line means orthologous gene pair. Gray line indicates collinear blocks within P. mume and other Rosaceae plant genomes. Red line implies orthologous gene pair. Chromosomal names with prefixes ‘Pm’, ‘G’, ‘Pd’, and ‘LG’ indicate P. mume, P. persica, P. dulcis, and P. armeniaca, respectively.
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Figure 6. Multiple sequence alignment of PmIAAs. Conserved domains I–IV are marked by thick black lines. More than 75% similarity of amino acids are shaded in red, and ranged from 50% to 75% amino acids are shaded in blue. Location information of domains is inferred by right numbers.
Figure 6. Multiple sequence alignment of PmIAAs. Conserved domains I–IV are marked by thick black lines. More than 75% similarity of amino acids are shaded in red, and ranged from 50% to 75% amino acids are shaded in blue. Location information of domains is inferred by right numbers.
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Figure 7. Heatmaps of PmIAAs expression. (A,B) Expression patterns of PmIAAs in five tissues and at different flowering development stages. BS: budding stage; IFS: initial flowering stage; FS: flowering stage; and WS: wilting stage. FPKM values are log10-transformed. Blue represents low expression, and red represents high expression.
Figure 7. Heatmaps of PmIAAs expression. (A,B) Expression patterns of PmIAAs in five tissues and at different flowering development stages. BS: budding stage; IFS: initial flowering stage; FS: flowering stage; and WS: wilting stage. FPKM values are log10-transformed. Blue represents low expression, and red represents high expression.
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Figure 8. Cis-acting elements distribution in promoters of PmIAAs. The 2000 bp promoter sequences of PmIAA genes were used to analyze specific responsive cis-acting elements. Different colors indicated nineteen different cis-acting elements.
Figure 8. Cis-acting elements distribution in promoters of PmIAAs. The 2000 bp promoter sequences of PmIAA genes were used to analyze specific responsive cis-acting elements. Different colors indicated nineteen different cis-acting elements.
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Table
Table 1. Characteristics of Aux/IAA family members in four Rosaceae plants genome.
Table 1. Characteristics of Aux/IAA family members in four Rosaceae plants genome.
Locus NameGene IDChr. 1Start
(bp)		End
(bp)		ORF Length
(bp)		Protein Length
(aa)		MW
(kDa)		pINum_Exons
PmIAA1Pm002286Pm118,410,49018,413,935113737840.826.975
PmIAA2Pm003529Pm125,485,47925,486,33459419722.278.103
PmIAA3Pm003530Pm125,493,71525,495,24777125628.216.765
PmIAA4Pm004328Pm24,075,8564,078,825129943246.766.685
PmIAA5Pm005182Pm29,685,2209,690,217138045951.867.5910
PmIAA6Pm007165Pm221,921,86621,922,83958519421.316.794
PmIAA7Pm008719Pm235,394,52335,395,27349816518.249.202
PmIAA8Pm009031Pm238,082,78338,084,82183127629.465.525
PmIAA9Pm009169Pm239,166,64439,168,40486728832.59.275
PmIAA10Pm009170Pm239,182,27039,183,11159119622.036.763
PmIAA11Pm012868Pm4174,190175,42163921223.355.584
PmIAA12Pm013416Pm43,933,3193,937,638147048954.989.346
PmIAA13Pm013483Pm44,405,0424,407,525104734837.898.366
PmIAA14Pm013596Pm45,254,0185,257,14757319021.196.743
PmIAA15Pm013597Pm45,264,6725,265,93861820522.737.564
PmIAA16Pm020225Pm61,861,9061,863,66476225328.036.235
PmIAA17Pm020227Pm61,871,0621,871,87358219321.705.963
PmIAA18Pm020501Pm63,334,9303,337,14294831532.856.845
PmIAA19Pm027361Pm814,851,15514,853,71498732834.906.364
PmIAA20Pm027456Pm815,328,17615,329,55377425728.828.695
PmIAA21Pm027585Pm815,994,14515,994,90150116618.668.002
PmIAA22Pm029117Pm0 21,482,4081,483,23733611112.876.573
PpIAA1Prupe.1G540700.1G144,179,62944,185,073119439743.43 6.685
PpIAA2Prupe.6G210500.1G621,881,52621,887,147113737840.87 6.565
PpIAA3Prupe.3G064200.1G34,585,1654,588,237103234337.24 7.565
PpIAA4Prupe.7G225600.1G719,999,62520,002,91896632134.05 6.845
PpIAA5Prupe.8G232200.1G820,644,58920,646,34176225327.88 6.765
PpIAA6Prupe.6G343800.1G629,582,92729,585,21876825527.91 5.864
PpIAA7Prupe.1G027600.1G11,933,8121,936,07274724827.50 8.615
PpIAA8Prupe.6G343700.1G629,575,24729,576,74559419722.38 7.493
PpIAA9Prupe.1G027500.1G11,919,2071,920,88159119622.03 6.223
PpIAA10Prupe.8G232400.1G820,653,62420,655,67258219321.71 5.963
PpIAA11Prupe.3G074900.1G35,490,3395,492,76473224327.04 8.925
PpIAA12Prupe.7G234800.1G720,438,45120,440,48976825528.41 8.225
PpIAA13Prupe.3G074800.1G35,480,7865,484,24557319021.30 7.613
PpIAA14Prupe.3G058600.1G34,137,3694,141,973108336039.74 8.965
PpIAA15Prupe.8G215400.1G819,778,00919,780,27794231332.63 6.845
PpIAA16Prupe.1G049200.1G13,457,6753,460,523124241344.22 8.955
PpIAA17Prupe.7G247500.1G721,022,92521,025,30069923226.49 94
PpIAA18Prupe.1G481700.1G140,205,55640,206,74472324027.03 9.34
PpIAA19Prupe.1G317000.1G130,532,26530,533,09058519422.35 4.894
PpIAA20Prupe.1G208300.1G122,238,29222,239,26558819521.24 6.494
PpIAA21Prupe.3G001800.1G3141,629143,33664221323.36 5.584
PpIAA22Prupe.1G085900.1G16,379,4766,380,77648916217.98 9.242
PdIAA1-aPrudul26A001240P1Pd011,947,3641,948,89959119622.06 6.223
PdIAA1-bPrudul26A001240P2Pd011,947,3641,948,89948916218.30 7.832
PdIAA2Prudul26A014193P1Pd011,970,5521,972,93774724827.52 8.615
PdIAA3-aPrudul26A024018P1Pd013,538,0433,540,78493631132.66 6.785
PdIAA3-bPrudul26A024018P2Pd013,538,0433,540,78493331032.57 6.785
PdIAA4Prudul26A003100P1Pd016,586,8916,587,63348916218.00 9.462
PdIAA5-aPrudul26A001943P1Pd0119,446,84819,448,31458519421.20 6.494
PdIAA5-bPrudul26A001943P2Pd0119,446,84819,448,31458819521.24 6.494
PdIAA6Prudul26A002782P1Pd0127,098,03027,098,87258519422.30 5.144
PdIAA7Prudul26A022660P1Pd0134,374,46834,377,847150650156.07 8.375
PdIAA8Prudul26A031526P1Pd0136,644,32836,645,68572324027.11 9.324
PdIAA9-aPrudul26A030270P1Pd0140,499,21640,505,180110136639.74 7.056
PdIAA9-bPrudul26A030270P2Pd0140,499,21640,505,180119439743.41 7.066
PdIAA10Prudul26A009797P1Pd03156,374157,58764221323.43 5.584
PdIAA11Prudul26A015075P1Pd034,069,2334,073,513109536440.20 8.585
PdIAA12Prudul26A031482P1Pd034,553,5624,556,627103234337.23 8.15
PdIAA13Prudul26A003871P1Pd035,473,5045,474,75661820522.69 7.564
PdIAA14Prudul26A019193P1Pd0620,456,94520,461,668113737840.89 6.565
PdIAA15Prudul26A024452P1Pd0628,374,77328,376,88759419722.20 63
PdIAA16-aPrudul26A031524P1Pd0628,383,48028,385,56557018920.69 6.172
PdIAA16-bPrudul26A031524P2Pd0628,383,48028,385,56576825527.98 5.625
PdIAA17Prudul26A009915P1Pd0718,894,19718,897,39296031933.89 6.365
PdIAA18Prudul26A010551P1Pd0719,357,24619,358,56976825528.43 7.595
PdIAA19Prudul26A007192P1Pd0719,959,79719,961,00869923226.42 8.484
PdIAA20-aPrudul26A028501P1Pd0817,537,26917,540,30894831532.75 6.845
PdIAA20-bPrudul26A028501P2Pd0817,537,26917,540,30869923223.48 6.732
PdIAA20-cPrudul26A028501P3Pd0817,537,26917,540,30894531432.66 6.845
PdIAA21Prudul26A032023P1Pd0818,504,48518,511,83376225327.89 6.855
PdIAA22Prudul26A030184P1Pd0818,518,89918,520,73457919221.62 6.623
PdIAA23Prudul26A032154P1Pd00 332,75336,16557319021.33 7.613
PdIAA24Prudul26A013580P1Pd00 343,97545,22761820522.69 7.565
PaIAA1-aPARG03096m01LG123,057,22023,059,32876825527.96 6.765
PaIAA1-bPARG03096m03LG123,057,41423,062,237110736840.35 8.476
PaIAA2PARG03559m01LG21,794,4611,796,00359119621.96 6.763
PaIAA3PARG03560m01LG21,808,3321,810,09574724827.53 8.835
PaIAA4-aPARG04113m01LG26,111,2986,112,04950116618.24 9.512
PaIAA4-bPARG04113m02LG26,111,1036,112,27050116618.24 9.512
PaIAA5-aPARG04885m01LG212,147,32112,149,05158519421.27 6.544
PaIAA5-bPARG04885m02LG212,148,20912,149,05153117619.08 9.172
PaIAA5-cPARG04885m03LG212,147,87112,148,91163321023.07 5.574
PaIAA6-aPARG07885m01LG232,902,08932,903,56194831534.85 8.315
PaIAA6-bPARG07885m02LG232,902,08932,903,56191830533.73 8.365
PaIAA6-cPARG07885m05LG232,902,08932,907,032134744850.56 6.910
PaIAA7PARG08244m01LG235,263,47435,264,60470523426.49 9.334
PaIAA8-aPARG09013m01LG241,017,04041,022,781110136639.72 7.056
PaIAA8-bPARG09013m02LG241,017,04041,022,781110136639.72 7.056
PaIAA8-cPARG09013m03LG241,017,04041,019,77988229331.35 6.974
PaIAA8-dPARG09013m04LG241,017,04041,019,70392730833.24 6.973
PaIAA9PARG15463m01LG419,847,12319,848,82363621123.27 7.564
PaIAA10PARG15551m01LG420,614,15420,617,123103234337.36 7.565
PaIAA11PARG15664m01LG421,590,85621,594,273108035939.46 8.585
PaIAA12-aPARG20177m01LG62,032,1122,034,81376225327.91 6.765
PaIAA12-bPARG20177m02LG62,025,7212,035,609138045950.97 9.466
PaIAA13-aPARG20341m01LG63,001,5003,014,66591830532.00 7.616
PaIAA13-bPARG20341m02LG63,012,4003,014,66593931232.50 7.615
PaIAA14PARG27893m01LG819,566,83619,570,22496031933.85 6.765
PaIAA15-aPARG27974m01LG820,043,83320,045,62876825528.46 8.555
PaIAA15-bPARG27974m02LG820,043,83320,045,22481627130.46 9.014
PaIAA16-aPARG29743m01LG0 4289,408294,763113737840.79 6.625
PaIAA16-bPARG29743m02LG0289,408294,763113737840.79 6.625
PaIAA16-cPARG29743m03LG0289,408294,763113737840.79 6.625
PaIAA16-dPARG29743m04LG0290,432294,763113737840.79 6.625
PaIAA16-ePARG29743m05LG0289,408293,554123941244.68 6.334
PaIAA16-fPARG29743m06LG0290,834296,512117639142.38 5.665
1 Chr. is Chromosome. 2 Pm0 is scaffold205 in genome of P. mume. 3 Pd00 is pdulcis26_s0670 in genome of P. dulcis. 4 LG0 is tig00008361 in genome of P. armeniaca.
Table
Table 2. Pairwise comparison of Ka/Ks values of RoIAA genes in four Rosaceae species.
Table 2. Pairwise comparison of Ka/Ks values of RoIAA genes in four Rosaceae species.
Syntenic Gene
Pairs		Type of DuplicationKaKsKa/KsDivergence Time (Mya)
PmIAA1&PmIAA4Segmental0.223 1.843 0.121 61.44
PmIAA2&PmIAA16Segmental0.427 2.963 0.144 98.76
PmIAA5&PmIAA12Segmental0.625 2.202 0.284 73.40
PmIAA9&PmIAA18Segmental0.642 2.262 0.284 75.41
PmIAA2&PmIAA3Tandem0.393 3.138 0.125 104.60
PmIAA9&PmIAA10Tandem0.390 3.256 0.120 108.54
PmIAA14&PmIAA15Tandem0.441 2.850 0.155 95.00
PpIAA1&PpIAA2Segmental0.208 1.599 0.130 53.30
PpIAA3&PpIAA12Segmental0.587 2.383 0.246 79.42
PpIAA4&PpIAA13Segmental0.385 3.090 0.125 102.99
PpIAA5&PpIAA8Segmental0.400 3.069 0.130 102.30
PpIAA5&PpIAA9Segmental0.455 2.846 0.160 94.86
PpIAA8&PpIAA9Segmental0.259 1.784 0.145 59.47
PpIAA11&PpIAA12SegmentalNANANA
PpIAA15&PpIAA16Segmental0.290 1.955 0.149 65.17
PpIAA17&PpIAA18Segmental0.493 2.316 0.213 77.21
PpIAA6&PpIAA8Tandem0.376 3.166 0.119 105.54
PpIAA7&PpIAA9Tandem0.364 3.241 0.112 108.04
PdIAA1-a&PdIAA15Segmental0.255 1.782 0.143 59.41
PdIAA3-a&PdIAA20-aSegmental0.309 1.729 0.179 57.62
PdIAA7&PdIAA11Segmental0.450 1.714 0.262 57.12
PdIAA8&PdIAA19Segmental0.499 2.280 0.219 75.99
PdIAA9-b&PdIAA14Segmental0.205 1.573 0.130 52.44
PdIAA12&PdIAA17Segmental0.200 1.334 0.150 44.48
PdIAA12&PdIAA18Segmental0.535 2.585 0.207 86.17
PdIAA13&PdIAA17Segmental0.316 3.221 0.098 107.36
PdIAA13&PdIAA18Segmental0.370 2.013 0.184 67.09
PdIAA15&PdIAA21Segmental0.456 2.912 0.157 97.08
PdIAA1-a&PdIAA2Tandem0.348 3.206 0.109 106.85
PaIAA6-c&PaIAA11Segmental0.565 1.641 0.344 54.71
PaIAA8-a&PaIAA16-eSegmental0.211 2.161 0.097 72.03
PaIAA2&PaIAA3Tandem0.396 3.192 0.124 106.41
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Liu, N.; Li, L.; Chen, X.; Zhang, Y.; Zhang, T. The Auxin/Indole-3-Acetic Acid (Aux/IAA) Gene Family Analysis of Four Rosaceae Genomes and Expression Patterns of PmIAAs in Prunus mume. Horticulturae 2022, 8, 899. https://doi.org/10.3390/horticulturae8100899

AMA Style

Liu N, Li L, Chen X, Zhang Y, Zhang T. The Auxin/Indole-3-Acetic Acid (Aux/IAA) Gene Family Analysis of Four Rosaceae Genomes and Expression Patterns of PmIAAs in Prunus mume. Horticulturae. 2022; 8(10):899. https://doi.org/10.3390/horticulturae8100899

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Liu, Nuoxuan, Li Li, Xiling Chen, Yanlong Zhang, and Tengxun Zhang. 2022. "The Auxin/Indole-3-Acetic Acid (Aux/IAA) Gene Family Analysis of Four Rosaceae Genomes and Expression Patterns of PmIAAs in Prunus mume" Horticulturae 8, no. 10: 899. https://doi.org/10.3390/horticulturae8100899

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