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Article

Genome-Wide Identification and Expression Analysis of the NF-Y Transcription Factor Family in Prunus armeniaca

by
Jiangting Wu
1,
Yanguang He
2,
Lin Wang
1,3,4,
Han Zhao
1,3,4,
Nan Jiang
1,3,4,
Tana Wuyun
1,3,4 and
Huimin Liu
1,3,4,*
1
State Key Laboratory of Tree Genetics and Breeding, Research Institute of Non-Timber Forestry, Chinese Academy of Forestry, Zhengzhou 450003, China
2
College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China
3
Key Laboratory of Non-Timber Forest Germplasm Enhancement and Utilization of National Forestry and Grassland Administration, Zhengzhou 450003, China
4
Kernel-Apricot Engineering and Technology Research Center of National Forestry and Grassland Administration, Zhengzhou 450003, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(11), 1986; https://doi.org/10.3390/f15111986
Submission received: 2 October 2024 / Revised: 5 November 2024 / Accepted: 8 November 2024 / Published: 10 November 2024
(This article belongs to the Section Genetics and Molecular Biology)
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Abstract

:
The nuclear factor Y (NF-Y) gene family plays important roles in regulating many of the biological processes of plants, including oil accumulation. The apricot (Prunus armeniaca) is one of the most commercially traded plants, and apricot kernel oil has a high nutritional value owing to its richness in fatty acids and bioactive compounds. However, the systematic characterization of the PaNF-Y family in the apricot and the underlying regulatory mechanisms involved in oil biosynthesis remain unclear. In this study, a total of 28 PaNF-Y members from the apricot genome were identified and divided into three subfamilies (6 PaNF-YAs, 15 PaNF-YBs, and 7 PaNF-YCs) based on phylogenetic analysis results. The types and distributions of the gene structures and conserved motifs were similar in the clustered PaNF-Ys of the same subfamily. Gene duplication analysis results revealed that segmental duplication events were important for the expansion of the PaNF-Y family. Importantly, transcriptome data analysis results showed that most genes of the PaNF-YA subfamily and PaNF-YB4 of the PaNF-YB subfamily were specifically expressed in the apricot kernel. Furthermore, highly positive correlations were observed between apricot oil content and the transcript levels of PaNF-YA2, PaNF-YA6, and PaNF-YB4. In conclusion, our results provide insights into the molecular mechanisms of the key PaNF-Y genes regulating apricot oil biosynthesis.

1. Introduction

The nuclear factor Y (NF-Y) transcription factor family is widely found in eukaryotes and consists of three subunits: NF-YA, NF-YB, and NF-YC [1]. The core region of the NF-YA subunit comprises 53 amino acids, containing two conserved α-helix domains (A1 and A2) [2]. The A1 α-helix domain in the N-terminal functions by interacting with NF-YB and NF-YC subunits; in comparison, the A2 α-helix domain in the C-terminal is involved in the recognition and binding of the CCAAT element of targeted genes [3]. The NF-YB and NF-YC subunits possess a conserved histone fold domain (HFD), which promotes chromatin accessibility to NF-YA and interaction with other proteins [4,5]. The NF-YB and NF-YC subunits can form a heterodimer through their HFDs in the cytoplasm; once this process is complete, the NF-YB-YC heterodimer transfers to the nucleus and forms an active heterotrimeric complex with NF-YA [6]. In animals and yeast, each subunit of NF-Y is encoded by only one gene [7]. However, plants typically possess multiple NF-Y genes encoding each subunit, which results in broad functional diversity of NF-Y genes in plants [7]. Thus far, NF-Y families have been identified in many plant species including Arabidopsis thaliana [8], Triticum aestivum [9], Solanum lycopersicum [10], Ricinus communis [11], Glycine max [12], and Prunus persica [13].
NF-Ys are crucial transcription factors involved in regulating many of the physiological processes in plants, such as stress responses, flowering time, and seed development. In Arabidopsis, overexpression of AtNF-YA1 improves sensitivity to salinity [14]. The transcript level of OsNF-YA7 is induced by drought treatment and its overexpression enhances drought resistance in Oryza sativa [15]. In Glycine max, GmNF-YC14-overexpressing A. thaliana plants showed enhanced drought and salt tolerance [16]. Multiple AtNF-Y subunits have been reported to be involved in the regulation of flowering time. For example, AtNF-YB2 and AtNF-YB3 accelerate plant flowering by directly binding to the promoter of FLOWERING LOCUS T (FT), which is the key floral activator in the flowering time pathway [17]. In contrast, some AtNF-Ys, such as AtNF-YA1 and AtNF-YB1, delay plants flowering by suppressing the expression of FT [18,19]. LEAFY COTYLEDON 1 (AtLEC1 or AtNF-YB9) has been verified as a vital regulator involved in oil biosynthesis during seed development in A. thaliana [20]. Overexpression of AtLEC1 enhances oil contents, and the expression levels of genes involved in fatty acid metabolism were markedly upregulated in the AtLEC1-overexpressing lines compared to those in the WT plants [21]. AtLEC1-LIKE (L1L) and BnL1L of Brassica napus, which are homologs of AtLEC1, exhibit similar functions in the regulation of oil accumulation [21,22]. Therefore, NF-Y members play important roles in various plant biological processes, including oil biosynthesis.
The apricot (Prunus armeniaca) is one of the most economically valuable crops and is widely grown in Asia, Europe, and the Americas [23]. The fruit of the apricot is delicious and nutritious for humans, and its by-product, the kernel, also has high nutritional value. Apricot kernels contain large amounts of oil, comparable to oil from common oilseed crops such as sunflower and soybean [24]. The oil extracted from apricot kernels has been found to be rich in fatty acids comprising oleic acid, linoleic acid, and palmitic acid and contain various biologically active substances including sitosterol, tocopherols, provitamin A, tocopherols, and β-carotene, which have a wide range of applications in the food, cosmetic, and pharmaceutical industries [25,26,27]. In recent years, global demand for vegetable oils has been growing rapidly. Thus, it is necessary to illustrate molecular mechanisms that govern the process of oil accumulation in the apricot, which could be beneficial in meeting the increasing demand for vegetable oil. Some NF-Ys have been reported to regulate oil biosynthesis in herbaceous plants. However, to date, limited information is available on the molecular mechanisms by which PaNF-Ys regulate oil biosynthesis in the apricot.
In this study, the PaNF-Y family of the apricot was systematically characterized at a genome-wide level. A total of 28 PaNF-Y members were identified and further grouped into three subfamilies (6 NF-YA members, 15 NF-YB members, and 7 NF-YC members) in the apricot genome based on phylogenetic analysis. Subsequently, their protein properties, gene structures, conserved motifs, chromosomal distributions, duplication events, collinearity relationships, and cis-acting elements were analyzed using bioinformatic approaches. To explore the expression patterns of the PaNF-Y family in various tissues, apricot transcriptome data were used to analyze the expression levels of PaNF-Y genes in the flower, flower bud, leaf, kernel (K1–K5), and flesh (F1–F8) of five and eight different developmental stages. Through correlation analysis, highly positive correlations were observed between the apricot oil content and expression levels of PaNF-YA2, PaNF-YA6, and PaNF-YB4. This study lays a foundation for further investigations into the molecular mechanism of PaNF-Y genes in regulating apricot oil biosynthesis.

2. Materials and Methods

2.1. Identification of the NF-Y Gene Family in P. armeniaca

To identify the members of the NF-Y family in P. armeniaca, the amino acid sequences of AtNF-Ys from A. thaliana (https://www.Arabidopsis.org/, accessed on 1 September 2024) were downloaded, and BLASTp searches with default parameter settings were performed in the genome of P. armeniaca (Sungold, http://apricotgpd.com/, accessed on 1 September 2024) using homologous AtNF-Y protein sequences by TBtools 2.119 [28]. Thereafter, the obtained PaNF-Y sequences were further examined using HMMER (https://www.ebi.ac.uk/Tools/hmmer/, accessed on 1 September 2024) and PFAM (http://pfam.xfam.org/, accessed on 1 September 2024) to verify the completeness of NF-Y proteins. The chromosomal location, length of amino acids, molecular weight, theoretical isoelectric point (pI), instability index, aliphatic index, and grand average of hydropathicity (GRAVY) of PaNF-Ys were predicted using ExPASy (https://web.expasy.org/protparam/, accessed on 1 September 2024). The subcellular localization of each PaNF-Y protein was predicted using WoLF PSORT II (https://www.genscript.com/wolf-psort.html?src=leftbar, accessed on 29 October 2024).

2.2. Phylogenetic, Gene Structure, and Conserved Motif Analyses

The phylogenetic tree was constructed with 28 PaNF-Y proteins and 36 AtNF-Y proteins using MEGA 11 via the maximum likelihood method with 1000 bootstrap replicates [29]. Thereafter, the constructed phylogenetic tree was visualized using Evolview (https://www.evolgenius.info/evolview/, accessed on 5 September 2024). The gene structures of PaNF-Ys were analyzed using TBtools 2.119 [28]. The conserved motifs of PaNF-Ys were predicted using MEME (https://meme-suite.org/meme/, accessed on 5 September 2024), and the maximum number of the motifs was set to 10. The obtained results were then visualized using TBtools (version 2.119) [28].

2.3. Chromosomal Distribution and Synteny Analysis

The chromosomal locations of the PaNF-Y family were displayed via TBtools 2.119 based on the gff file of the P. armeniaca genome [28]. The gene duplication events of PaNF-Ys and the collinearity relationship of NF-Y gene pairs between the genome of P. armeniaca and that of A. thaliana were analyzed using the Multiple Collinearity Scan Toolkit (MCScanX) [30]. The nonsynonymous (Ka), and synonymous (Ks) and Ka/Ks ratios of the NF-Y homologous gene pairs were calculated using TBtools (version 2.119 ) [28].

2.4. Identification of Cis-Acting Elements

The 2 kb upstream sequence of PaNF-Ys was obtained from the genome of P. armeniaca; thereafter, the cis-acting elements of these sequences were identified using PlantCARE (https://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 5 September 2024).

2.5. Expression Analysis Using RNA-Seq Data and Verification via RT-qPCR

To explore the expression profiles of PaNF-Y genes in various tissues, including the kernel, fruit, flower, flower bud, and leaf, apricot RNA-seq data were searched from the Genome Sequence Archive (PRJCA001987). Thereafter, the data were quantified using the fragments per kilobase of exon per million mapped (FPKM) algorithm [31]. The heatmaps of PaNF-Ys expression levels were generated using TBtools (version 2.119) [28].
RT-qPCR experiments were performed to verify the expression levels of PaNF-Ys from RNA-seq data. The apricots were cultivated at the Yuanyang Long-Term Experimental Base of the Research Institute of Non-Timber Forestry (Yuanyang County, Henan Province, China). The apricot kernels were harvested at 50, 60, 70, 80, and 90 days after flowering (DAF) and then stored at −80 °C. Total RNA extraction and RT-qPCR were performed using the method described by Liu et al. [32]. Expression levels were calculated using the 2−ΔCT method [33] with the apricot Ubiquitin (UBQ) gene as an internal control. The utilized primers are listed in Table S1.

2.6. Oil Content Detection

The oil contents of apricot kernels collected at 50, 60, 70, 80, and 90 DAF were examined according to the method described by Deng et al. [34]. Briefly, the apricot kernels were ground into fine powder with a universal grinder (XM-2500, Xuman, Zhejiang, China) and screened using a 60-mesh sieve. Thereafter, the lipids were extracted from the apricot kernel powders with 1:20 (v/v) petroleum ether (b.p. 30–60 °C) as the solvent in a Soxhlet apparatus for 8 h. The resulting lipids were transferred into a rotary vacuum evaporator to remove the remaining solvent, and dried with a stream of nitrogen to obtain the apricot kernel oil. The yield of the oil was calculated as a percentage of dry weight as follows: oil content (%) = (initial weight of lyophilized kernel powder (g) − final weight of defatted powder (g)) × 100/initial weight of lyophilized kernel powder (g).

3. Results

3.1. Identification of NF-Y Family Members in P. armeniaca

There are 10 NF-YA, 13 NF-YB, and 13 NF-YC members in the A. thaliana genome [8]. To identify the NF-Y family in the apricot, AtNF-Y protein sequences were used to blast against the genome of P. armeniaca. A total of 28 PaNF-Y members were identified and named based on the subfamilies and chromosomal distributions (Table S2). The protein lengths of PaNF-Y members ranged from 156 to 351 aa, and the corresponding molecular weights ranged from 17.53 to 38.11 kDa (Table S2). Their predicted isoelectric points ranged from 4.38 to 9.70, their instability indices ranged from 33.00 to 85.92, their aliphatic indices ranged from 43.99 to 77.63, and their GRAVY ranged from −1.30 to −0.22 (Table S2). The subcellular localization analysis results showed that all PaNF-Y family proteins were located in the nucleus (Table S2).

3.2. Phylogenetic Analysis of the PNF-Y Family

To further explore the evolutionary relationships of PaNF-Ys, a phylogenetic tree was constructed using the NF-Y proteins from P. armeniaca and A. thaliana (Figure 1, Table S3). The phylogenetic analysis results showed that these NF-Y members were divided into three subfamilies, namely, NF-YA, NF-YB, and NF-YC, which were consistent with the classification results of PaNF-Ys (Table S2). NF-YB was the largest subfamily with 15 PaNF-YB members; in comparison, the NF-YA and NF-YC subfamilies contained 6 and 7 members, respectively (Figure 1). Based on the phylogenetic tree, two pairs of NF-YA orthologues (PaNF-YA3/AtNF-YA7 and PaNF-YA4/AtNF-YA9), seven pairs of NF-YB orthologues (PaNF-YB8/AtNF-YB7, PaNF-YB2/AtNF-YB1, PaNF-YB13/AtNF-YB10, PaNF-YB14/AtNF-YB4, PaNF-YB4/AtNF-YB9, PaNF-YB7/AtNF-YB6, and PaNF-YB11/AtNF-YB10), and three pairs of NF-YC orthologues (PaNF-YC3/AtNF-YC11, PaNF-YC6/AtNF-YC10, and PaNF-YC2/AtNF-YC13) were identified between P. armeniaca and A. thaliana, suggesting the possibility of similar biological functions between the various pairs of NF-Y orthologues (Figure 1).

3.3. Gene Structure and Conserved Motif of the PNF-Y Family

To investigate the sequence structure and conservation of PaNF-Y members, the exon/intron structure and conserved motif composition of PaNF-Ys were analyzed (Figure 2A–C). Most members of the PaNF-YA subfamily contained five exons (Figure 2B). Our results showed that 8 out of 15 PaNF-YB subfamily members possessed only one exon whereas the number of exons of the rest PaNF-YB members varied between two and six (Figure 2B). Similarly, the majority of PaNF-YC members were found to contain one exon. A total of 10 motifs were identified in the amino acid sequences of the PaNF-Y family (Figure 2C, Table S4). Most members of the PaNF-YB and PaNF-YC subfamilies contained motifs 1 and 7, while most members of the PaNF-YA and PaNF-YB subfamilies contained motif 2 (Figure 2C). Motif 3 was found only in the PaNF-YB subfamily (Figure 2C). Motifs 4 and 5 existed only in the PaNF-YC subfamily (Figure 2C). Motif 6 was found in the PaNF-YA and PaNF-YC subfamilies, whereas motif 9 was found only in the PaNF-YA subfamily (Figure 2C). Motif 8 was found in a pair of PaNF-YC paralogues (PaNF-YC1/ PaNF-YC7) (Figure 2C). Motif 10 was found only in PaNF-YC2 (Figure 2C).

3.4. Chromosomal Distribution and Synteny Analysis of the PaNF-Y Family

The chromosomal locations of the PaNF-Y family were visualized (Figure 3). The results showed that the PaNF-Y genes were unevenly distributed on the eight chromosomes of P. armeniaca (Figure 3). The number of PaNF-Y genes on chromosome 4 was the largest with eight such genes, followed by seven on chromosome 6 (Figure 3). Three genes were found on each of chromosomes 1 and 2. In comparison, chromosomes 3, 5, and 7 each contained two genes, and chromosome 8 contained one gene (Figure 3).
To explore the duplication events of the PaNF-Y family in P. armeniaca, we analyzed the segmental and tandem duplication events among the PaNF-Ys using MCScanX (Figure 4A, Table S5). Six pairs of segmental duplication events were found on seven chromosomes of P. armeniaca, with one pair (PaNF-YA2 and PaNF-YA6) in the PaNF-YA subfamily, four pairs (PaNF-YB1 and PaNF-YB14, PaNF-YB1 and PaNF-YB15, PaNF-YB2 and PaNF-YB13, and PaNF-YB3 and PaNF-YB4) in the PaNF-YB subfamily, and one pair (PaNF-YB1 and PaNF-YB7) in the PaNF-YC subfamily (Figure 4A). In contrast, only a pair of tandem duplication events (PaNF-YB11 and PaNF-YB12) was detected in the PaNF-Y family (Table S5).
To further investigate the interspecific collinearity relationships of the NF-Y family, the syntenies of NF-Y genes between the genome of P. armeniaca and that of A. thaliana were analyzed (Figure 4B, Table S6). The results showed that 11 PaNF-Y genes were collinear with 18 AtNF-Y genes, and the number of collinear gene pairs was 19 between the apricot and Arabidopsis (Figure 4B, Table S6).
To better understand the driving forces behind the evolution of the PaNF-Y family, the Ka, Ks, and Ka/Ks ratio of NF-Y homologous gene pairs were calculated (Table S7). The results showed that all pairs of NF-Y homologous genes had a Ka/Ks ratio of less than 1 (Table S7), indicating purifying selective pressure during NF-Y family evolution and conserved functions of these NF-Y homologous genes.

3.5. Cis-Acting Elements Analysis of the PaNF-Y Family

To explore the potential function of the PaNF-Y family, we identified the putative cis-acting elements in the promoter sequences of PaNF-Y genes (Figure 5). The results indicated that the PaNF-Y promoter regions contained multiple types of cis-elements involved in growth and development, and respond to phytohormone, light, and stress (Figure 5). Among them, the stress-responsive elements were the most numerous cis-elements in the NFY gene family, in which MYB, MYC, STRE, and ARE elements accounted for the highest proportion (Figure 5). Box 4 and G-box elements of light-responsive elements were widely displayed in most PaNF-Y genes (Figure 5). Additionally, the abscisic acid–response element (ABRE) accounted for the largest proportion of phytohormone-responsive elements in the NFY gene family (Figure 5).

3.6. Tissue-Specific Expression Patterns of the PaNF-Y Family

To explore the expression profiles of the PaNF-Y family in various tissues, the apricot transcriptome data were used to analyze the expression levels of PaNF-Y genes in the flower, flower bud, leaf, kernel (K1–K5), and flesh (F1–F8) of five and eight different developmental stages (Figure 6A). Excluding PaNF-YA3, the transcript levels of the PaNF-YA subfamily genes were highest in the kernel compared to those in the other tissues (Figure 6A). In the PaNF-YB subfamily, 7 out of 15 PaNF-YB genes (PaNF-YB14, PaNF-YB15, PaNF-YB2, PaNF-YB6, PaNF-YB12, PaNF-YB7, and PaNF-YB10) were mainly expressed in the multiple developmental stages of the flesh, whereas PaNF-YB13 and PaNF-YB4 exhibited higher expression and abundance in the multiple developmental stages of the kernel (Figure 6A). Additionally, PaNF-YB1 and PaNF-YB8 were expressed at high levels in the flower and flower buds. PaNF-YB5 was specifically expressed in the flower bud, whereas PaNF-YB3 showed the highest expression in the leaf (Figure 6A). In the PaNF-YC subfamily, PaNF-YC3 showed the highest expression in the late developmental stage of the kernel (Figure 6A). PaNF-YC2, PaNF-YC1, and PaNF-YC4 were mainly expressed in the flesh, whereas PaNF-YC6, PaNF-YC7, and PaNF-YC5 showed high expression in the flower, flower bud, and leaf (Figure 6A). To further verify the transcript levels of PaNF-Ys obtained from RNA-seq analysis, we selected some genes (PaNF-YA1, PaNF-YA4, PaNF-YA6, PaNF-YA5, PaNF-YA2, PaNF-YB13, and PaNF-YB4) for RT-qPCR analysis to check their expression levels in the different developmental stages of the kernel (Figure 6B–H). The results of our RT-qPCR analysis were consistent with those from the RNA-seq analysis.
To obtain greater insight into the function of PaNF-Y members in the regulation of oil biosynthesis, we performed the correlation analysis between the kernel oil contents and expression levels of PaNF-Ys based on the FPKM values. The results showed that most genes of the PaNF-YA subfamily were positively correlated with oil accumulation, especially PaNF-YA2 and PaNF-YA6 with high Pearson correlation coefficients (>0.9) (Table S8). Similar results were found in PaNF-YB4 of the PaNF-YB subfamily. Notably, these three PaNF-Y genes showed specifically high expressions in the apricot kernel. These results indicated that PaNF-YA2, PaNF-YA6, and PaNF-YB4 probably play important roles in the oil biosynthesis of apricot.

4. Discussion

NF-Y transcription factors are widely found in plants, with them playing crucial roles in regulating growth and response to biotic and abiotic stresses [35,36,37]. In this study, a total of 28 PaNF-Y genes were identified in the genome of P. armeniaca. The number of PaNF-Y members in the apricot was lower than that in Arabidopsis (36 members) [8], rice (34 members) [38], tomato (49 members) [10], and Populus (52 members) [39]. The presence of fewer PaNF-Y members is probably linked to the smaller size of the apricot genome. Protein properties including molecular weights, isoelectric points, and aliphatic index vary widely among PaNF-Y members, implying the diverse functions of the NF-Y family.
The phylogenetic tree showed that the PaNF-Y members grouped into three subfamilies (PaNF-YA, PaNF-YB, and PaNF-YC) based on the classification of AtNF-Ys [8]. The members of the PaNF-YA, PaNF-YB, and PaNF-YC subfamilies accounted for 21%, 54%, and 25%, respectively. However, in Arabidopsis thaliana, the AtNF-YA, AtNF-YB, and AtNF-YC subfamilies represented 28%, 36%, and 36%, respectively [8]. These results suggest that members of the PaNF-YB subfamily may undergo more gene duplications during the process of evolution. According to our phylogenetic analysis results, 12 pairs of NF-Y orthologues were found between P. armeniaca and A. thaliana, implying the similar biological functions of the NF-Y orthologues.
The genetic structure, as a type of evolutionary relic, bears the imprint of the evolution of the gene family. The exon/intron structure analysis showed that the number of exons varied among the PaNF-Y family, with most NF-YA subfamily members containing five exons while some NF-YBs and NF-YCs consisted of only one exon. Our results are in line with those obtained for Populus × canescens [40], Prunus persica [13], and Petunia hybrida [41], suggesting the relative conservation of PaNF-Ys in plants. Moreover, we analyzed the conserved motifs of the PaNF-Y family. The types and distributions of the motifs were similar in the clustered PaNF-Ys of the same subfamily, whereas they varied considerably across the different subfamilies. For instance, motif 9 and motif 3 exist only in the NF-YA and NF-YB subfamily, respectively. However, motifs 4, 5, 8, and 10 were only found in the NF-YC subfamily. These results indicate that the PaNF-Y members of different subfamilies may have different functions.
The main factors driving gene family expansion are tandem and segmental duplications during the process of evolution, which contribute to the generation of new genes and functional differentiation in plants [42,43]. The results of the duplication event analysis showed that six segmental duplication pairs were identified in the PaNF-Y family, whereas only one tandem duplication pair was detected, indicating that segmental duplication events were important for the expansion of PaNF-Y members. Moreover, the most duplication events were found in the PaNF-YB subfamily, which can explain the largest proportion of PaNF-YB members in the PaNF-Y family. We also analyzed the collinearity of NF-Y genes between the apricot and Arabidopsis, and 19 pairs of collinear genes were identified. Among them, four pairs were single syntenic pairs, suggesting that these genes were probably derived from the last common ancestor of the apricot and Arabidopsis. In addition, 13 pairs were single PaNF-Y genes corresponding to multiple AtNF-Ys; in comparison, only two pairs were single AtNF-Y genes corresponding to multiple PaNF-Ys, which indicated that the ancestor gene expanded fewer times in the apricot than in Arabidopsis. We found that the Ka/Ks ratios of NF-Y homologous gene pairs between the genome of P. armeniaca and A. thaliana were much smaller than 1, indicating that these genes have undergone purifying selection pressure and are probably conserved in function during evolution. However, some NF-Y genes in the two species were not found to show any collinear relationships. This may be due to the multiple rounds of chromosomal rearrangement and fusions during the evolution of the apricot and Arabidopsis, which severely affect the identification of chromosome synthesis [44].
The cis-acting elements in the upstream regions of promoters play vital roles in gene expression and regulatory mechanisms. A variety of elements involved in growth and development, and in response to phytohormone, light, and stress were detected in the promoter sequences of the PaNF-Y family. Among them, ABRE, MYB, MYC, and STRE elements were abundant in the PaNF-Y promoters. ABRE, an ABA-responsive element, has been reported to be involved in the regulation of drought and high-salinity stresses [45,46]. MYB and MYC elements are associated with the ABA-mediated response to abiotic stresses such as drought and salt [47,48]. Previous studies have shown that STRE is a key element in response to heat and drought stresses [49,50,51]. In A. thaliana, AtNF-YA5-overexpressing lines exhibit more resistance to drought stress compared to wild-type plants [52]. Overexpression of AtNF-YA3, 7, and 10 makes plants more sensitive to ABA and less affected by drought treatment [53]. Overexpression of AtNF-YB2 and AtNF-YB3 enhances drought and heat stress tolerance [54]. The authors of a recent study have reported that GmNF-YC14 can form a heterotrimer with GmNF-YA16 and GmNF-YB2 to activate the ABA signaling pathway to enhance drought tolerance in soybean [16]. Interestingly, our findings showed that most PaNF-Y family members contained multiple ABA- and stress-responsive elements, suggesting their potential functions in enhancing the resistance of the apricot. To more deeply investigate the functions of the PaNF-Y family involved in regulating the stress resistance of the apricot, it is important to apply stress treatments such as drought and salt to the apricot and further analyze the expression profiles of PaNF-Ys to screen key PaNF-Y genes in response to abiotic stress in future studies.
The expression patterns of genes are usually closely associated with their biological functions. In our analyses, the PaNF-YA subfamily members were more highly expressed in the different developmental stages of the kernel than those in other tissues. Increasing evidence indicates that NF-YAs such as AtNF-YA1, 5, 6, and 9 of Arabidopsis, OsNF-YA8 of rice, and ZmNF-YA13 of maize play important roles in regulating seed development [55,56,57]. These findings may explain the high expression levels of PaNF-YAs in apricot kernels. In rice, OsNF-YC2 and OsNF-YC4 regulate the photoperiodic flowering response by interacting with OsNF-YB8, OsNF-YB10, and OsNF-YB11 proteins [58]. In Arabidopsis, AtNF-YC3, AtNF-YC4, and AtNF-YC9 can form complexes with a key regulator of flowering time CONSTANS (CO) and activate the expression of FT to promote flowering [59]. Intriguingly, our results showed that PaNF-YC7 clustered closely with AtNF-YC3/9, and PaNF-YC5 shared close homology with AtNF-YC4. PaNF-YC7 and PaNF-YC5 were highly expressed in the flower and flower buds. Therefore, we speculate that these two PaNF-YC members may have similar functions in regulating apricot flowering.
The oil extracted from the apricot kernel contains beneficial fatty acids and bioactive compounds, making it highly nutritious for humans [60]. Therefore, it is of great importance to understand the regulatory mechanism of oil biosynthesis in apricot. Some NF-Ys have been reported to be key regulators in the transcriptional regulation of seed oil accumulation. In Elaeis guineensis, overexpression of EgNF-YA3 in A. thaliana resulted in a significant increase in oil content [61]. GmNFYA was found to be the key driver based on the gene co-expression networks in Glycine max. Further analyses have revealed that GmNFYA-overexpressing A. thaliana plants promote oil accumulation, and the expression of GmNFYA has been found to be highly correlated with oil content [62]. In this present study, most PaNF-YA members were specifically expressed in the kernel; in particular, PaNF-YA2 and PaNF-YA6 showed highly positive correlations with apricot oil content. Moreover, in A. thaliana, AtLEC1 (also referred to as AtNF-YB9) upregulates the expression of more than 50% of the fatty acid synthetic genes, resulting in seed oil accumulation [21,63]. Similar to AtLEC1, BnLEC1-overexpressing Brassica napus and ZmLEC1-overexpressing Zea mays increase oil production during seed development [22,64]. Consistent with these results, in this study, PaNF-YB4 was identified as an apricot homolog of AtLEC1. The transcript levels of PaNF-YB4 were particularly high in the kernel and strongly correlated with apricot oil content. Taken together, it is speculated that PaNF-YA2, PaNF-YA6, and PaNF-YB4 are potential vital drivers in regulating oil biosynthesis of P. armeniaca.

5. Conclusions

In this study, we identified 28 putative PaNF-Y members, which were categorized into three subfamilies (6 PaNF-YAs, 15 PaNF-YBs, and 7 PaNF-YCs) according to our phylogenetic analysis results. The types and distributions of gene structures and conserved motifs were similar in the clustered PaNF-Ys, which further supported the results regarding phylogenetic relationships. Six segmental duplication events and one tandem duplication event were found in the apricot genome, demonstrating that segmental duplication was the main model of the PaNF-Y family expansion. The results of expression pattern analysis showed that most genes of the PaNF-YA subfamily and PaNF-YB4 of the PaNF-YB subfamily were prominently expressed in the multiple developmental stages of the kernel. Notably, the expression levels of PaNF-YA2, PaNF-YA6, and PaNF-YB4 showed highly positive correlations with apricot oil content. Our research provides a systematic and high-quality chromosomal-based characterization of the PaNF-Y family, facilitating further investigation into the molecular mechanisms of the key PaNF-Y genes in regulating apricot oil biosynthesis.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15111986/s1. Table S1: Primer sequences used in this study. Table S2: Characteristics of apricot PaNF-Y family. Table S3: Accession numbers of NF-Y genes presented in Figure 1. Table S4: The conserved motifs of the PaNF-Y proteins in Figure 2. Table S5: Duplication events of PaNF-Y genes. Table S6: Synteny NF-Y gene pairs between apricot and Arabidopsis. Table S7: Ka/Ks ratios of NF-Y homologous gene pairs between the genome of P. armeniaca and A. thaliana. Table S8: Correlation analysis between the expression level of PaNF-Y genes and oil content.

Author Contributions

Conceptualization, H.L.; methodology, Y.H.; software, J.W. and N.J.; validation, Y.H.; formal analysis, L.W. and H.Z.; investigation, H.L.; resources, H.L.; writing—original draft preparation, J.W.; writing—review and editing, T.W. and H.L.; visualization, J.W.; project administration, T.W. and H.L.; funding acquisition, H.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the central non-profit research institution of the Chinese Academy of Forestry, grant number CAFYBB2021MA008, and National Natural Science Foundation of China, grant number 32101562.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors have no conflicts of interest to declare.

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Figure 1. Phylogenetic analysis of the NF-Y gene family in P. armeniaca (Pa) and A. thaliana (At). The red and blue dots represent the genes from the genome of P. armeniaca and A. thaliana, respectively. Orange, purple, and green branches represent NF-YAs, NF-YBs, and NF-YCs, respectively. The accession numbers of NF-Y genes are listed in Table S3.
Figure 1. Phylogenetic analysis of the NF-Y gene family in P. armeniaca (Pa) and A. thaliana (At). The red and blue dots represent the genes from the genome of P. armeniaca and A. thaliana, respectively. Orange, purple, and green branches represent NF-YAs, NF-YBs, and NF-YCs, respectively. The accession numbers of NF-Y genes are listed in Table S3.
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Figure 2. Schematic diagram of the gene structure and conserved motifs of the PaNF-Y gene family in P. armeniaca. (A) The phylogenetic tree of PaNF-Y proteins based on amino acid sequences. Orange, purple, and green branches represent PaNF-YAs, PaNF-YBs, and PaNF-YCs, respectively. (B) The exon/intron structure of the PaNF-Y genes. UTRs, exons, and introns are shown in blue boxes, yellow boxes, and gray lines, respectively. (C) The conserved motifs of PaNF-Y proteins were identified using MEME. Different colored boxes represent the different motifs of proteins. The scales at the bottom in panels (B,C) indicate the sequence lengths. The conserved motifs are listed in Table S4.
Figure 2. Schematic diagram of the gene structure and conserved motifs of the PaNF-Y gene family in P. armeniaca. (A) The phylogenetic tree of PaNF-Y proteins based on amino acid sequences. Orange, purple, and green branches represent PaNF-YAs, PaNF-YBs, and PaNF-YCs, respectively. (B) The exon/intron structure of the PaNF-Y genes. UTRs, exons, and introns are shown in blue boxes, yellow boxes, and gray lines, respectively. (C) The conserved motifs of PaNF-Y proteins were identified using MEME. Different colored boxes represent the different motifs of proteins. The scales at the bottom in panels (B,C) indicate the sequence lengths. The conserved motifs are listed in Table S4.
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Figure 3. Chromosomal locations of PaNF-Y genes on eight apricot chromosomes. The different colors represent gene density on the chromosomes, with red representing high gene density and blue representing low gene density. The scale on the left represents the lengths of the P. armeniaca chromosomes.
Figure 3. Chromosomal locations of PaNF-Y genes on eight apricot chromosomes. The different colors represent gene density on the chromosomes, with red representing high gene density and blue representing low gene density. The scale on the left represents the lengths of the P. armeniaca chromosomes.
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Figure 4. Synteny analysis of PaNF-Y genes. (A) Synteny analysis of PaNF-Y genes in P. armeniaca. The lines and heatmaps along the rectangles represent gene density on the chromosomes. The gray lines indicate synteny blocks in the apricot genome, while the red lines between chromosomes delineate segmental duplicated gene pairs. (B) Synteny analysis of PaNF-Y genes between the genome of P. armeniaca and that of A. thaliana. The gray lines represent the collinear blocks between the apricot and Arabidopsis. The syntenic NF-Y gene pairs are shown to be connected by the red lines.
Figure 4. Synteny analysis of PaNF-Y genes. (A) Synteny analysis of PaNF-Y genes in P. armeniaca. The lines and heatmaps along the rectangles represent gene density on the chromosomes. The gray lines indicate synteny blocks in the apricot genome, while the red lines between chromosomes delineate segmental duplicated gene pairs. (B) Synteny analysis of PaNF-Y genes between the genome of P. armeniaca and that of A. thaliana. The gray lines represent the collinear blocks between the apricot and Arabidopsis. The syntenic NF-Y gene pairs are shown to be connected by the red lines.
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Figure 5. Cis-elements of PaNF-Y genes in the genome of P. armeniaca. PaNF-Y genes are listed on the Y axis; orange, purple, and green represent different clades of the PaNF-Y family. The regulatory elements on the promoter regions of PaNF-Y genes are listed on the X axis. The different intensity colors and figures of the grids indicate the number of elements.
Figure 5. Cis-elements of PaNF-Y genes in the genome of P. armeniaca. PaNF-Y genes are listed on the Y axis; orange, purple, and green represent different clades of the PaNF-Y family. The regulatory elements on the promoter regions of PaNF-Y genes are listed on the X axis. The different intensity colors and figures of the grids indicate the number of elements.
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Figure 6. Expression patterns of the PaNF-Y gene family in different tissues of P. armeniaca. (A) Heatmaps showing the gene expression profiles of PaNF-Ys in the kernel, fruit, flower, flower bud, and leaf. The heatmaps were generated in the R package based on normalized FPKM values. Blue, white, and red represent low, medium, and high expression, respectively. K1–K5: kernels from different developmental stages. F1–F8: flesh from different stages. FL: flower. FB: flower bud. (B–H) Reverse transcription–quantitative polymerase chain reaction analysis of the selected PaNF-Y genes in the different developmental stages of apricot kernels. The bars in each panel indicate the means ± SE (n = 3). Different letters on the bars indicate significant differences between the groups.
Figure 6. Expression patterns of the PaNF-Y gene family in different tissues of P. armeniaca. (A) Heatmaps showing the gene expression profiles of PaNF-Ys in the kernel, fruit, flower, flower bud, and leaf. The heatmaps were generated in the R package based on normalized FPKM values. Blue, white, and red represent low, medium, and high expression, respectively. K1–K5: kernels from different developmental stages. F1–F8: flesh from different stages. FL: flower. FB: flower bud. (B–H) Reverse transcription–quantitative polymerase chain reaction analysis of the selected PaNF-Y genes in the different developmental stages of apricot kernels. The bars in each panel indicate the means ± SE (n = 3). Different letters on the bars indicate significant differences between the groups.
Forests 15 01986 g006
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MDPI and ACS Style

Wu, J.; He, Y.; Wang, L.; Zhao, H.; Jiang, N.; Wuyun, T.; Liu, H. Genome-Wide Identification and Expression Analysis of the NF-Y Transcription Factor Family in Prunus armeniaca. Forests 2024, 15, 1986. https://doi.org/10.3390/f15111986

AMA Style

Wu J, He Y, Wang L, Zhao H, Jiang N, Wuyun T, Liu H. Genome-Wide Identification and Expression Analysis of the NF-Y Transcription Factor Family in Prunus armeniaca. Forests. 2024; 15(11):1986. https://doi.org/10.3390/f15111986

Chicago/Turabian Style

Wu, Jiangting, Yanguang He, Lin Wang, Han Zhao, Nan Jiang, Tana Wuyun, and Huimin Liu. 2024. "Genome-Wide Identification and Expression Analysis of the NF-Y Transcription Factor Family in Prunus armeniaca" Forests 15, no. 11: 1986. https://doi.org/10.3390/f15111986

APA Style

Wu, J., He, Y., Wang, L., Zhao, H., Jiang, N., Wuyun, T., & Liu, H. (2024). Genome-Wide Identification and Expression Analysis of the NF-Y Transcription Factor Family in Prunus armeniaca. Forests, 15(11), 1986. https://doi.org/10.3390/f15111986

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