Next Article in Journal
Expanding the Horizons of Pre-Transplant Renal Vascular Assessment Using Ex Vivo Perfusion
Previous Article in Journal
Pharmacological and Pathological Effects of Mulberry Leaf Extract on the Treatment of Type 1 Diabetes Mellitus Mice
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
CIMB
Volume 45
Issue 7
10.3390/cimb45070344
cimb-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Genome-Wide Identification, Evolution and Expression Profile Analysis of NAC Transcription Factor in Simmondsia chinensis

by
Fan Xia
1,
Xiaoyu Liang
1,
Lina Tan
1,
Wen Sun
1,
Xiaogang Dai
2 and
Hanwei Yan
1,*
1
Laboratory of Modern Biotechnology, School of Forestry and Landscape Architecture, Anhui Agricultural University, Hefei 230036, China
2
Key Laboratory of Tree Breeding & Germplasm Improvement, Southern Modern Forestry Collaborative Innovation Center, College of Forestry, Nanjing Forestry University, Nanjing 210037, China
*
Author to whom correspondence should be addressed.
Curr. Issues Mol. Biol. 2023, 45(7), 5422-5436; https://doi.org/10.3390/cimb45070344
Submission received: 10 May 2023 / Revised: 16 June 2023 / Accepted: 25 June 2023 / Published: 29 June 2023
(This article belongs to the Section Bioinformatics and Systems Biology)
Browse Figures
Review Reports Versions Notes

Abstract

:
NAC transcription factors (TFs) are one of the largest plant-specific gene families and play important roles in plant growth, development, and the biotic and abiotic stress response. Although the sequencing of Jojoba (Simmondsia chinensis) has been completed, the genome-wide identification and analysis of its NAC TFs has not been reported. In this study, a total of 57 genes were identified in Jojoba, which were divided into eight groups based on phylogenetic analysis. The genes clustered in the same groups have a similar gene structure and motif distribution. Based on the analysis of cis-elements in NAC TFs, nine cis-acting elements were identified in the promoter region that involved in light response, hormonal response, and stress response. Synteny analysis showed a greater collinearity between Jojoba and V. vinifera than Arabidopsis thaliana. The 24 genes in the Jojoba NAC TFs are derived from fragment replication, which may be the main source of NAC amplification. Gene expression analysis identified seven genes that were highly expressed in seeds. The differential expression analysis of NAC TFs in cotyledon and embryonic axis tissues showed that the expression of 10 genes was up-regulated and 1 gene was down-regulated. This study provides more information on the classification, gene structure, conserved motif, and evolution of NAC TFs in Jojoba, facilitating further exploration of their specific functional analysis in Jojoba seed development.

1. Introduction

Transcription factors (TFs) are a class of proteins that specifically interact with cis-acting elements in the gene promoter region of eukaryotes [1]. NAC TFs are one of the largest families of TFs widely present in plant species [2], which are named according to the NAM (no apical meristem) found in Petunia hybrida [3], the ATAF1/2, and CUC2 (cup-shaped cotyledon) found in Arabidopsis thaliana [4]. The N-terminal contains a conserved NAC domain consisting of about 150 amino acids, and the C-terminal is a highly transcriptional regulatory region that is a common feature of NAC proteins [5].
Currently, the genome-wide identification of NAC TFs in some plants has been completed, for example, 117 NAC genes in Arabidopsis thaliana [6], 163 genes in Populus trichocarpa [7], 125 NAC genes in Phyllostachys edulis [8], 269 genes in Glycine max [9], and 83 genes in Sesamum indicum [10]. Meanwhile, a variety of regulatory functions of NAC in plant physiology have also been revealed, including drought response [11], cold response [12], salt stress [13], lateral root development [14], leaf senescence [15], embryo development [16], and the biosynthesis of secondary metabolites [17]. OsNAC2 was overexpressed in Oryza sativa to promote root growth by regulating auxin and cytokinin [18]. The overexpression of ANAC019, ANAC055, and ANAC072 in Arabidopsis transgenic plants improves tolerance to drought [19]. In Arabidopsis thaliana, overexpressed ANAC087 accelerates the process of leaf senescence [20]. Additionally, NAC TFs play a vital role in the development of plant seeds. VvNAC26 in Vitis vinifera regulates seed development by influencing ABA and ethylene hormone synthesis pathways [21]. OsNAC20 and OsNAC26 have essential functions in the formation and storage of starch and protein in rice seeds [22]. Similarly, TaNAC19 in wheat (Triticum aestivum L.) also plays a key role in the cumulative mechanism of seed storage protein (SSP), a protein that determines the quality of its grains [23]. TaNAC019 enables the expression of the SSP accumulation mechanism by directly activating high molecular weight glutenin and indirectly regulating the expression of TaSPA, an ortholog of maize Opaque2.
Jojoba (Simmondsia chinensis) is a woody plant native to southern North America and is now widely cultivated around the world. Jojoba has a high economic value, and the liquid wax ester extracted from its seeds as a raw material has positive application prospects in cosmetics, medicine, food, and other industries [24]. Jojoba genome sequencing was published in 2020 [25]. So far, the systematic analysis of the NAC gene family in Jojoba has not been reported. Therefore, the comprehensive analysis and expression patterns of NAC TFs could lay a theoretical basis for the regulatory mechanism of wax ester production in jojoba seeds.
In this study, 57 NAC genes in Jojoba were identified based on the completed sequencing of genome data. We further analyzed their characteristics, including multiple sequence alignment, gene structure, and promoter analysis. Information on the phylogenetic relationship, Ka/Ks ratio, and collinearity was obtained for evolutionary analysis. Importantly, the expression data on different stages of seeds was exploited using RNA-seq. These results may provide a basis for further validation of the relevant function of the NAC gene during the development of Jojoba seeds.

2. Materials and Methods

2.1. ScNAC TF Database Searches

We downloaded the Jojoba genomic data from the Beijing Institute of Genomics (BIG) data center (http://bigd.big.ac.cn/gwh, accessed on 26 November 2022) by using accession no. GWHAASQ00000000, and applied it to the NAC TFs identification process [25]. Subsequently, 96 Arabidopsis NAC protein sequences were downloaded from Arabidopsis Information Resource site (https://www.arabidopsis.org/browse/genefamily/index.jsp, accessed on 26 November 2022). Then the genes in Jojoba genomic data with homologous sequences to the Arabidopsis NAC members were identified using local BLASTP [26] (E value cutoff of 1 × 10−5), and these genes were considered as candidates for the Jojoba NAC TFs. Pfam is a collection of multiple alignments and profile hidden Markov models of protein domain families [27]. To verify that all candidate genes belonged to the NAC family, a hidden Markov model of Pfam was used to check whether they had a specific NAM domain (PF02365). The protein sequences of all NAC candidate members were submitted to the Pfam website and their domains were identified by an hmmscan search, HMMER (http://www.ebi.ac.uk/Tools/hmmer/search/hmmscan, accessed on 26 November 2022), with all parameters as default. The redundant sequences and sequences without a NAM domain were removed from the dataset. The identified NAC genes were renamed based on their location on the Jojoba chromosome. Information about the NAC family of Jojoba genes, including coding sequence (CDS), isoelectric point (PI), and molecular weight (MW) information, was obtained by the Expasy—ProtParam tool. Maplnspect (http://www.plantbreeding.wur.nl/uk/software_mapinspect.html, accessed on 26 November 2022) was used to draw the chromosomal location of the ScNAC genes.

2.2. Phylogenetic Analysis

Multiple sequence alignments between the amino acids of the NAC family were performed by MEGA7.0 (version 7.0.21) software (http://www.megasoftware.net/, accessed on 3 December 2022), which is set as the default parameter. A phylogenetic tree was constructed using the neighbor-joining with 1000 bootstrap replicates on MEGA 7.0 [28]. BLASTP [26] (E value cutoff of 1 × 10−5) was used to perform similarity searching for ScNACs and NAC members in Arabidopsis thaliana. Based on the phylogenetic analysis of the NAC members in Jojoba and Arabidopsis thaliana as well as sequence similarity, homologs of each ScNAC in Arabidopsis thaliana were identified (Table S1).

2.3. Analysis of Exon/Intron Structure, Conserved Motifs, and Promoter Element

The exon/intron gene structure of each ScNAC was visualized based on the Gene Structure Display Server (http://gsds.cbi.pku.edu.cn, accessed on 10 December 2022) [29], with all parameters as default. Additionally, the amino acid sequences of this family were submitted to the online MEME motif search tool, using a maximum pattern number of 20 and default parameters [30]. The cis-acting elements in promoter were identified by PlantCARE (http://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 3 December 2022) [31], which are located in the 2000-bp region upstream of each gene transcription start site. The cis-acting elements involved in the same response process were given the same named label. Visualization was conducted through TBtools’ Simple Biosequence Viewer, with all parameters as default.

2.4. Syntenic Analysis and Ka/Ks Ratios

The whole genomes of Arabidopsis thaliana (TAIR 10) and Vitis vinifera (IGGP_12x) were downloaded from TAIR [32] and the Ensemble genome [33] database, respectively. The duplication of the NAC gene was identified based on MCScanX [34] (http://chibba.pgml.uga.edu/mcscan2/, accessed on 3 December 2022). First, the Jojoba protein sequences were aligned to each other and the protein sequences from Arabidopsis and grape using BLASTP, with an E-value cutoff of 1 × 10−10. Then, under the MCScanX default parameter settings, we identified the synteny regions. Finally, the results were visualized using Circos [35].
Gene pairs were identified with BLASTN. The synonymous substitution rate (Ks), non-synonymous substitution rate (Ka) and Ka/Ks ratio between the homologous gene pairs were obtained by KaKs_Calculator2.0 [36]. The calculation of the divergence time of the NAC gene pair is based on the formula T = Ks/2λ × 10−6 Mya (λ = 7.0 × 10−9).

2.5. Expression Analysis of ScNAC in Different Tissues and Stages of Developing Seed

The gene expression data of ScNAC in different tissues and developmental stages of Jojoba seed were obtained based on published RNA-seq data in Jojoba [25]. The RNA-seq data can be obtained from the NCBI GEO database (accession no. GSE130603) In this experiment, seeds were divided into three developmental stages based on their average weight, early (0.2 g), middle (0.45 g), and late (0.7 g), and the average weight of seeds used for tissue-specific RNA-seq experiments was 0.45 g. Each tissue contained five biological replicates, each consisting of three seeds. The expression data from different tissues and the developmental stages of seeds were visualized by pheatmap (CRAN—Package pheatmap (hppt://cran.r-project.org/web/packages/pheatmap/index.html), accessed on 12 March 2023).

2.6. Differential Expression Analysis of ScNAC in Different Tissues of Developing Seed

Based on the same RNA-seq data as above, the differential expression data of the cotyledon and embryonic axis tissues were obtained [25]. The average seed weight of these tissues was 0.45 g, which was in the mid- to mid-late stage of oil accumulation. The differential expression of ScNAC genes in the cotyledon and embryonic axis tissues was analyzed using DESeq2 with default settings [37]. The difference significance was calculated using more stringent q value than p value, in that they also account for the false discovery rate rather than the false-positive rate [38]. The genes with an absolute log2FC (log of fold change) value less than 1 were filtered. A volcano plot was created using the Jojoba differential expression genes in the cotyledons and embryonic axis, and the ScNAC genes with an absolute log2FC value greater than 2 were annotated on the volcano plot. The volcano plot was obtained by using TBtools’ Volcano Plot with default parameters.

3. Results

3.1. Identification of NAC TFs in Jojoba

A total of 57 genes were identified, all of which contained a NAM domain (PF02365) specific to a family of NAC TFs. According to their location on the chromosome, they were named ScNAC1 to ScNAC57. The coding sequence (CDS) of the NAC TFs ranged from 814 bp (ScNAC22) to 13877 bp (ScNAC15) in length. Their molecular weights (MWs) ranged from 8.75 kDa (ScNAC22) to 75.33 kDa (ScNAC40), with an average of 39.22 kDa. The isoelectric point (PI) varied from 4.34 (ScNAC22) to 9.84 (ScNAC10), and the average was 6.88. Of these, 29 members had isoelectric points less than 7 and 28 had isoelectric points greater than 7, suggesting that they may function under different physiological conditions [39]. In addition, Jojoba has fewer NAC members than Vitis vinifera (74 members) [40] and Arabidopsis thaliana (117 members) [6], which may be due to the fact that it does not undergo additional genome duplications in addition to the whole-genome triplication shared among all eudicots [25].

3.2. Phylogenetic Analysis of NAC TFs

In order to investigate the phylogenetic relationships of ScNAC TFs, a phylogenetic tree was constructed by neighbor-joining (NJ) using 57 proteins from Jojoba and members of the NAC family of Arabidopsis thaliana (Table S1). As shown in Figure 1, NAC TFs were divided into two major groups, A and B, based on a previous study about the classification of NAC domains in Oryza sativa and Arabidopsis thaliana [6]. Groups A and B had five and eight subgroups, respectively. There was only one ScNAC gene in group A and 56 ScNAC genes in group B. The maximum number of ScNACs in the subgroup is nine (B4, B6, B8) and the minimum number is one (A4) (Figure 1).
Moreover, previous studies of NAC TFs suggested that genes clustered together in the evolutionary tree may have similar functions [41]. Notably, regulatory genes related to seed dormancy and germination emerged in B5 subgroup, such as ANAC060 (AT3G44290.1), ANAC040 (AT2G273000.1), and ANAC089 (AT5G22290.1) [42]. The members in the B5 subgroup may have a relevant function during seed development (Table S3).

3.3. Gene Structure and Motif Composition Analysis

To explore the evolutionary relationships among ScNACs, a phylogenetic tree was constructed using 57 protein sequences from Jojoba. Based on the phylogenetic analysis of NAC members in Jojoba and Arabidopsis (Figure 1), we divided the NAC members in Jojoba into groups I~VIII. From group I to VIII, its members are 7, 9, 7, 9, 4, 9, 7, 5, respectively. In total, 20 conserved motifs were predicted through the MEME program to explore the structural diversity and similarity of NAC TFs in Jojoba. Most NAC members contained five motifs (motif 3, motif 4, motif 1, motif 2, and motif 5), which are components of the highly conserved N-terminus of NAC. It is noteworthy that certain motifs occur in certain groups, such as motif 11 in group VI and motif 7 in group VII (Figure 2). This may indicate that these particular motifs have specific functions.
At the same time, we compared the exon/intron structure in Jojoba. The number of introns varied from 1 to 5. Most ScNAC genes contained two introns. Six genes contained one intron, thirteen genes contained three introns, three genes contained four introns, and three genes contained four introns (Figure 2).

3.4. Analysis of Cis-Elements in NAC TFs

Cis-acting elements are specific DNA sequences that have transcriptional regulatory functions in the same DNA molecule. In order to further understand the regulatory mechanism of NAC transcription family in the growth and development of Jojoba seeds, we extracted upstream 2000 bp sequences of 57 ScNAC genes from transcription start sites, and identified nine cis-acting elements using PlantCARE (Table S2). The ScNAC promoter contains a number of hormone-associated cis-acting elements, including gibberellin responsiveness, the MeJA-responsiveness, abscisic acid responsiveness, salicylic acid responsiveness, and auxin responsiveness (Figure 3). Some promoters contained stress-related elements, defense and stress responsiveness in 20 genes, low-temperature responsiveness in 25 genes, and wound-responsive elements in 4 genes. In addition, light responsiveness is present in all genes. These results suggest that NAC genes in Jojoba function and expression are regulated by the cis-elements involved in plant growth and development and stress.

3.5. Syntenic and Evolutionary Patterns of NAC TFs

Gene replication events exist widely in all species and provide the necessary materials for species evolution [43]. To further investigate the evolution of NAC TFs in Jojoba, we explored genome duplication events by syntenic analysis. In total, 12 gene pairs appeared to originate from segmental duplication, and 24 (42%) ScNACs were duplicated due to whole-genome duplication (WGD) (Figure 4). Previous studies have suggested that Jojoba diverged from V. vinifera about 100 million years ago [25]. We performed collinearity analysis between Jojoba and two representative plants: Arabidopsis and grape. The Jojoba NAC genes had 31 and 41 homologous pairs with Arabidopsis and grape, respectively (Figure 5).
To estimate the rate of evolution and selection pressure in Jojoba, we calculated the nonsynonymous substitution rate (Ka), synonymous substitution rate (Ks), and Ka/Ks for 10 pairs of homologous ScNAC. The Ks value of ScNAC ranged from 0.8458 to 2.8582, and the divergence time was 60.4–204.2 MAY. The Ka/Ks values of gene pairs in ScNAC were all less than 1.0, indicating that these genes may have undergone purifying selection during evolution.

3.6. Expression Profiles of ScNAC Based on RNA-Seq

To further investigate the function of ScNACs during the development of Jojoba seeds, we analyzed ScNACs expression in different tissues (i) and stages (ii) of developing seeds based on published gene expression data. The liquid wax esters (WEs) and triacylglycerols (TAGs) are the two major lipid storage substances in Jojoba seeds. Based on a previous study [25], WE and TAG were differentially enriched in seed tissues, WE mainly existed in cotyledons, and TAG mainly existed in the embryonic axis. We also analyzed the differential expression of ScNACs gene in the cotyledon and embryonic axis tissues (iii) based on RNA-seq data.
(i) NAC gene family expression was analyzed in different seed tissues using published RNA-seq data (Figure 6). Among them, 46 genes were expressed in all tissues of the seed, 8 genes were expressed in some tissues, and 3 genes were not found to be expressed in the seed. Of the 46 genes that were all expressed in seed tissues, each gene was expressed at different levels in different seed tissues. The members from groups V and VI were expressed in all tissues, whereas the members from group VII were not expressed or expressed at very low levels in seeds. All members in V contained the cis-acting elements involved in light responsiveness. In addition, the intron/exon structures located in the V group are roughly the same in number and distribution. All members in V contained the cis-acting elements involved in the MeJA-responsiveness. This may indicate similar functions of ScNAC members in the same group during seed development. It is worth noting that the expression of three genes (ScNAC34, ScNAC37, ScNAC14) in the embryonic axis was much higher than that of other genes. The number and publication of exons/introns of these three genes were similar. Among them, the homologs of ScNAC34 and ScNAC37 in Arabidopsis belong to the same subfamily. They all had cis-acting elements involved in light response. This may indicate that these three genes (ScNAC34, ScNAC37, ScNAC14) play a critical role in Jojoba seed development. Similarly, ClNAC68, which is highly expressed in watermelon flesh, affects seed development cumulatively by controlling sugar and IAA [44]. OsNAC129 is highly expressed in rice seeds and plays an important role in seed development [45].
(ii) NAC gene family expression was analyzed at different developmental stages using published RNA-seq data (Figure 7). Most ScNACs were expressed at different stages of seed development, but the level of gene expression is different. In total, 51 genes were expressed at all developmental stages (early, middle, late), of which 27 genes showed increased expression levels and 7 genes exhibited reduced expression levels in each developmental stage compared to the control group (mature dry seeds). In addition, 19 genes showed decreased expression levels with seed development. The expression levels of seven genes increased with seed development. Particularly, four of these genes (ScNAC54, ScNAC28, ScNAC43, ScNAC36) have high expression levels and an increasing trend at different stages of seed development. Members from group IV, most of which showed a downward trend, may indicate that they have a similar negative role in seed development. However, some members from subfamilies V and VI have distinct expression profiles, suggesting that structurally similar NAC genes have different functions. In conclusion, a positive or negative correlation between NAC gene expression and seed development may indicate that the ScNAC is involved in regulating the growth and development of Jojoba seeds, although the methods of regulation are complex and diverse.
(iii) To further understand the function of NAC genes in Jojoba seed development, we analyzed the differential expression of NAC genes in the cotyledon and embryonic axis tissues using RNA-seq data (Figure 8). According to the published RNA-seq data mentioned above, we obtained differentially expressed genes in the seed cotyledon and embryonic axis tissues. All differentially expressed Jojoba genes were shown in the volcano plot, and ScNAC genes were labeled among them (absolute value of log2FC greater than 2). A total of 11 ScNACs genes showed significant differential gene expression. Among these genes, three genes (ScNAC34, ScNAC37, ScNAC39) were highly expressed in both the cotyledon and embryonic axis tissues. Ten of these genes (ScNAC49, ScNAC32, ScNAC37, ScNAC34, ScNAC13, ScNAC14, ScNAC11, ScNAC9, ScNAC24, ScNAC57) were significantly down-regulated in cotyledons (log2FC < −2), and only one gene (ScNAC10) was significantly up-regulated (log2FC > 2). ScNACs were significantly more expressed in the embryonic axis than in the cotyledon, which may indicate ScNACs play an important regulatory role in the development of the embryonic axis.

4. Discussion

Simmondsia chinensis is an oil crop of important economic value in medicine and industry [24]. However, studies on its transcription factors have not been reported. The NAC gene family, as one of the widespread transcription families in plants, plays an important role in plant growth and development as well as in biological and abiotic stress. At present, the completion of the sequencing of the Jojoba genome makes it possible to explore the characteristics and functions of its important gene families. In this study, we identified 57 members of the NAC family from Jojoba. Based on previous studies between Oryza sativa and Arabidopsis thaliana, we divided the Jojoba and Arabidopsis sequences into 13 groups. The results showed that the distribution of the NAC gene family was not uniform among different subgroups. Subgroups A1, A2, A3, and A5 contained only NAC members from Arabidopsis, while the NAC members from Jojoba in B2 and B3 are more than Arabidopsis. This may be because Jojoba and Arabidopsis evolved in different environments, with the different differentiation of NAC gene families leading to inconsistent numbers of members in different subgroups.
The analysis of gene structure showed that there were differences in gene structure in the same group, such as the number of introns in V ranging from 1 to 4. This may be due to the insertion or splicing of gene fragments during evolution [46]. However, a similar gene structure and conserved motif distribution in the same group indicate that the members of the same group have similar functions. Cis-acting elements in promoters play an important role in regulating gene expression. In this study, we identified nine cis-acting elements that are involved in light response, hormonal response, and stress response. It has been reported that ABA plays a role in the regulation of seed development. ABA induced the expression of DELAY OF GERMINATION 1-LIKE 4 (DOGL4), which is a key factor mediating the increase of seed storage, including lipids, protein, and polysaccharides [47]. In addition, the ABA response plays a dominant role in the regulation of strawberry fruit ripening [48]. There are 42 cis-acting elements associated with the ABA response in ScNACs. In Arabidopsis thaliana, auxin response factor 2 works with SEEDSTICK (STK) and GODITA (GOA) to regulate the seed growth by promoting cell expansion in the seed coat [49]. In addition, 30 ScNAC genes have auxin response elements. The NAC family in Jojoba may play an important role in seed development.
Gene duplication is of great importance to species evolution, and the common modes of gene duplication in plant gene families are segmental and a tandem duplication [50]. Jojoba contained 57 NAC genes, 17 and 60 fewer than V. vinifera (74) [39] and Arabidopsis (117) [6], and 0.35, 0.46, and 0.56 times more than Populus trichocarpa (163) [7], Phyllostachys edulis (125) [8], and Theobroma cacao (102) [51], respectively. The number of NAC genes was significantly lower in Jojoba compared to other species, consistent with previous reports of WGD in Jojoba [25]. Therefore, we performed synteny analyses of NAC within and across species. The Jojoba NAC TFs have 24 genes derived from segmental duplication and only one from tandem duplication, and segmental duplication is the main source of amplification of the Jojoba NAC TFs. The synteny analysis of the Jojoba genome and the two other sequenced plant genomes showed that the collinearity between Jojoba and V. vinifera was more significant than that between Jojoba and Arabidopsis. This may be due to the additional crucifer genome duplication experienced by Arabidopsis compared to Jojoba and grape.
In order to explore the important role of the NAC family in developing Jojoba seeds, we analyzed the expression of ScNACs in different tissues and stages of developing seeds. The four genes (ScNAC54, ScNAC28, ScNAC43, ScNAC36) were highly expressed at different stages of seed development, and expression increased gradually with seed development. In Arabidopsis Thaliana, NAC103 positively regulates the ABA response during seed germination [52]. The NAC gene GmNAC42-1 in soybean (Glycine max L. Merr) is an important positive regulator of glyceollin biosynthesis [53]. This may indicate that these genes play a key positive role in the regulation of seed growth and development. Differential gene expression showed that ScNAC expression was significantly up-regulated in the embryonic axis. As the region of TAG enrichment, ScNACs may directly or indirectly participate in the regulation of TAG synthesis. Similarly, in oil palm (Elaeis guineensis Jacq.), NAC TFs are indirectly involved in fatty acid synthesis and lipid metabolism [54]. The combination of NAC transcription factor (HvNAM1) and RNA binding protein (HvGR-RBP1) extended grain fill duration, grain size, and protein concentration [55]. However, more genetic evidence is required to further understand the specific function of the NAC TFs during Jojoba seed development.

5. Conclusions

In this study, we performed the first genome-wide identification and analysis of the NAC TFs in Jojoba. We identified a total of 57 ScNACs belonging to eight different groups. Moreover, the structural and conserved motif analysis of NAC TFs indicated that they may be involved in light response, hormonal response, and stress response. Evolutionary analyses support that Jojoba experienced only one whole-genome triplication shared among all eudicots. Based on RNA-seq data, the specificity of ScNAC expression in seeds at different developmental stages and tissues was revealed. The seven genes (ScNAC54, ScNAC28, ScNAC43, ScNAC36, ScNAC34, ScNAC37, ScNAC39) may be closely related to seed development, and, of them, three genes (ScNAC34, ScNAC37, ScNAC39) may play a key role in the embryonic axis of developing seeds. In conclusion, this study has obtained more information on NAC TFs in Jojoba and laid the foundation for further studies on the specific functions of ScNACs in Jojoba seeds.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/cimb45070344/s1.

Author Contributions

Conceptualization, F.X. and H.Y.; formal analysis, F.X. and L.T.; methodology, X.L. and W.S.; writing—original draft, F.X.; funding acquisition, X.D. and H.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research and the APC were funded by the Science and Technology Project of Anhui Province (Grant No. 2022j11020010) and Outstanding Young Talents in Colleges and Universities of Anhui Province (Grant No. gxyqZD2022020).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All the data relevant to the study are included in the article or uploaded as Supplementary Materials.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Romani, F.; Moreno, J.E. Molecular mechanisms involved in functional macroevolution of plant transcription factors. New Phytol. 2021, 230, 1345–1353. [Google Scholar] [CrossRef]
  2. Olsen, A.N.; Ernst, H.A.; Leggio, L.L.; Skriver, K. NAC transcription factors: Structurally distinct, functionally diverse. Trends Plant Sci. 2005, 10, 79–87. [Google Scholar] [CrossRef]
  3. Souer, E.; van Houwelingen, A.; Kloos, D.; Mol, J.; Koes, R. The no apical meristem gene of Petunia is required for pattern formation in embryos and flowers and is expressed at meristem and primordia boundaries. Cell 1996, 85, 159–170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Aida, M.; Ishida, T.; Fukaki, H.; Fujisawa, H.; Tasaka, M. Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 1997, 9, 841–857. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Welner, D.H.; Deeba, F.; Leggio, L.L.; Skriver, K. NAC transcription factors: From structure to function in stress-associated networks. In Plant Transcription Factors; Academic Press: Cambridge, MA, USA, 2016; pp. 199–212. [Google Scholar]
  6. Ooka, H.; Satoh, K.; Doi, K.; Nagata, T.; Otomo, Y.; Murakami, K.; Matsubara, K.; Osato, N.; Kawai, J.; Carninci, P.; et al. Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res. Int. J. Rapid Publ. Rep. Genes Genomes 2003, 10, 239–247. [Google Scholar] [CrossRef]
  7. Hu, R.; Qi, G.; Kong, Y.; Kong, D.; Gao, Q.; Zhou, G. Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol. 2010, 10, 145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Shan, X.; Yang, K.; Xu, X.; Zhu, C.; Gao, Z. Genome-Wide Investigation of the NAC Gene Family and Its Potential Association with the Secondary Cell Wall in Moso Bamboo. Biomolecules 2019, 9, 609. [Google Scholar] [CrossRef] [Green Version]
  9. Singh, S.; Koyama, H.; Bhati, K.K.; Alok, A. The biotechnological importance of the plant-specific NAC transcription factor family in crop improvement. J. Plant Res. 2021, 134, 475–495. [Google Scholar] [CrossRef]
  10. Zhang, Y.; Li, D.; Wang, Y.; Zhou, R.; Wang, L.; Zhang, Y.; Yu, J.; Gong, H.; You, J.; Zhang, X. Genome-wide identification and comprehensive analysis of the NAC transcription factor family in Sesamum indicum. PLoS ONE 2018, 13, e0199262. [Google Scholar] [CrossRef] [Green Version]
  11. Thirumalaikumar, V.P.; Devkar, V.; Mehterov, N.; Ali, S.; Ozgur, R.; Turkan, I.; Mueller-Roeber, B.; Balazadeh, S. NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnol. J. 2018, 16, 354–366. [Google Scholar] [CrossRef] [Green Version]
  12. Hussey, S.G.; Saïdi, M.N.; Hefer, C.A.; Myburg, A.A.; Grima-Pettenati, J. Structural, evolutionary and functional analysis of the NAC domain protein family in Eucalyptus. New Phytol. 2015, 206, 1337–1350. [Google Scholar] [CrossRef] [Green Version]
  13. Alshareef, N.O.; Wang, J.Y.; Ali, S.; Al-Babili, S.; Tester, M.; Schmöckel, S.M. Overexpression of the NAC transcription factor JUNGBRUNNEN1 (JUB1) increases salinity tolerance in tomato. Plant Physiol. Biochem. 2019, 140, 113–121. [Google Scholar] [CrossRef]
  14. Huysmans, M.; Buono, R.A.; Skorzinski, N.; Radio, M.C.; De Winter, F.; Parizot, B.; Mertens, J.; Karimi, M.; Fendrych, M.; Nowack, M.K. NAC Transcription Factors ANAC087 and ANAC046 Control Distinct Aspects of Programmed Cell Death in the Arabidopsis Columella and Lateral Root Cap. Plant Cell 2018, 30, 2197–2213. [Google Scholar] [CrossRef] [Green Version]
  15. Fraga, O.T.; de Melo, B.P.; Quadros, I.P.S.; Reis PA, B.; Fontes, E.P.B. Senescence-Associated Glycine max (Gm)NAC Genes: Integration of Natural and Stress-Induced Leaf Senescence. Int. J. Mol. Sci. 2021, 22, 8287. [Google Scholar] [CrossRef] [PubMed]
  16. Dalman, K.; Wind, J.J.; Nemesio-Gorriz, M.; Hammerbacher, A.; Lundén, K.; Ezcurra, I.; Elfstrand, M. Overexpression of PaNAC03, a stress induced NAC gene family transcription factor in Norway spruce leads to reduced flavonol biosynthesis and aberrant embryo development. BMC Plant Biol. 2017, 17, 6. [Google Scholar] [CrossRef] [Green Version]
  17. Kumar, R.; Das, S.; Mishra, M.; Choudhury, D.R.; Sharma, K.; Kumari, A.; Singh, R. Emerging roles of NAC transcription factor in medicinal plants: Progress and prospects. 3 Biotech 2021, 11, 425. [Google Scholar] [CrossRef] [PubMed]
  18. Mao, C.; He, J.; Liu, L.; Deng, Q.; Yao, X.; Liu, C.; Qiao, Y.; Li, P.; Ming, F. OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol. J. 2020, 18, 429–442. [Google Scholar] [CrossRef] [Green Version]
  19. Tran, L.S.; Nakashima, K.; Sakuma, Y.; Simpson, S.D.; Fujita, Y.; Maruyama, K.; Fujita, M.; Seki, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell. 2004, 16, 2481–2498. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  20. Vargas-Hernández, B.Y.; Núñez-Muñoz, L.; Calderón-Pérez, B.; Xoconostle-Cázares, B.; Ruiz-Medrano, R. The NAC Transcription Factor ANAC087 Induces Aerial Rosette Development and Leaf Senescence in Arabidopsis. Front. Plant Sci. 2022, 13, 818107. [Google Scholar] [CrossRef]
  21. Zhang, S.; Dong, R.; Wang, Y.; Li, X.; Ji, M.; Wang, X. NAC domain gene VvNAC26 interacts with VvMADS9 and influences seed and fruit development. Plant Physiol. Biochem. 2021, 164, 63–72. [Google Scholar] [CrossRef]
  22. Wang, J.; Chen, Z.; Zhang, Q.; Meng, S.; Wei, C. The NAC Transcription Factors OsNAC20 and OsNAC26 Regulate Starch and Storage Protein Synthesis. Plant Physiol. 2020, 184, 1775–1791. [Google Scholar] [CrossRef]
  23. Gao, Y.; An, K.; Guo, W.; Chen, Y.; Zhang, R.; Zhang, X.; Chang, S.; Rossi, V.; Jin, F.; Cao, X.; et al. The endosperm-specific transcription factor TaNAC019 regulates glutenin and starch accumulation and its elite allele improves wheat grain quality. Plant Cell. 2021, 33, 603–622. [Google Scholar] [CrossRef]
  24. Al-Obaidi, J.R.; Halabi, M.F.; AlKhalifah, N.S.; Asanar, S.; Al-Soqeer, A.A.; Attia, M.F. A review on plant importance, biotechnological aspects, and cultivation challenges of jojoba plant. Biol. Res. 2017, 50, 25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Sturtevant, D.; Lu, S.; Zhou, Z.W.; Shen, Y.; Wang, S.; Song, J.M.; Zhong, J.; Burks, D.J.; Yang, Z.Q.; Yang, Q.Y.; et al. The genome of jojoba (Simmondsia chinensis): A taxonomically isolated species that directs wax ester accumulation in its seeds. Sci. Adv. 2020, 6, eaay3240. [Google Scholar] [CrossRef] [Green Version]
  26. Altschul, S.F.; Madden, T.L.; Schäffer, A.A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997, 25, 3389–3402. [Google Scholar] [CrossRef] [Green Version]
  27. Mistry, J.; Chuguransky, S.; Williams, L.; Qureshi, M.; Salazar, G.A.; Sonnhammer, E.L.L.; Tosatto, S.C.E.; Paladin, L.; Raj, S.; Richardson, L.J.; et al. Pfam: The protein families database in 2021. Nucleic Acids Res. 2021, 49, D412–D419. [Google Scholar] [CrossRef]
  28. Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef] [Green Version]
  29. Hu, B.; Jin, J.; Guo, A.Y.; Zhang, H.; Luo, J.; Gao, G. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics 2015, 31, 1296–1297. [Google Scholar] [CrossRef] [Green Version]
  30. Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res. 2009, 37, W202–W208. [Google Scholar] [CrossRef] [PubMed]
  31. Lescot, M.; Déhais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van de Peer, Y.; Rouzé, P.; Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002, 30, 325–327. [Google Scholar] [CrossRef] [PubMed]
  32. Lamesch, P.; Berardini, T.Z.; Li, D.; Swarbreck, D.; Wilks, C.; Sasidharan, R.; Muller, R.; Dreher, K.; Alexander, D.L.; Garcia-Hernandez, M.; et al. The Arabidopsis Information Resource (TAIR): Improved gene annotation and new tools. Nucleic Acids Res. 2012, 40, D1202–D1210. [Google Scholar] [CrossRef]
  33. Jaillon, O.; Aury, J.M.; Noel, B.; Policriti, A.; Clepet, C.; Casagrande, A.; Choisne, N.; Aubourg, S.; Vitulo, N.; Jubin, C.; et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007, 449, 463–467. [Google Scholar]
  34. Wang, Y.; Tang, H.; Debarry, J.D.; Tan, X.; Li, J.; Wang, X.; Lee, T.H.; Jin, H.; Marler, B.; Guo, H.; et al. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012, 40, e49. [Google Scholar] [CrossRef] [Green Version]
  35. Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: An information aesthetic for comparative genomics. Genome Res. 2009, 19, 1639–1645. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Wang, D.; Zhang, Y.; Zhang, Z.; Zhu, J.; Yu, J. KaKs_Calculator 2.0: A toolkit incorporating gamma-series methods and sliding window strategies. Genom. Proteom. Bioinform. 2010, 8, 77–80. [Google Scholar] [CrossRef] [Green Version]
  37. Love, M.I.; Huber, W.; Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014, 15, 550. [Google Scholar] [CrossRef] [Green Version]
  38. Storey, J.D.; Tibshirani, R. Statistical significance for genomewide studies. Proc. Natl. Acad. Sci. USA 2003, 100, 9440–9445. [Google Scholar] [CrossRef] [Green Version]
  39. He, F.; Zhang, L.; Zhao, G.; Kang, J.; Long, R.; Li, M.; Yang, Q.; Chen, L. Genome-Wide Identification and Expression Analysis of the NAC Gene Family in Alfalfa Revealed Its Potential Roles in Response to Multiple Abiotic Stresses. Int. J. Mol. Sci. 2022, 23, 10015. [Google Scholar] [CrossRef] [PubMed]
  40. Wang, N.; Zheng, Y.; Xin, H.; Fang, L.; Li, S. Comprehensive analysis of NAC domain transcription factor gene family in Vitis vinifera. Plant Cell Rep. 2013, 32, 61–75. [Google Scholar] [CrossRef] [PubMed]
  41. Ahmad, M.; Yan, X.; Li, J.; Yang, Q.; Jamil, W.; Teng, Y.; Bai, S. Genome wide identification and predicted functional analyses of NAC transcription factors in Asian pears. BMC Plant Biol. 2018, 18, 214. [Google Scholar] [CrossRef] [Green Version]
  42. Song, S.; Willems LA, J.; Jiao, A.; Zhao, T.; Eric Schranz, M.; Bentsink, L. The membrane associated NAC transcription factors ANAC060 and ANAC040 are functionally redundant in the inhibition of seed dormancy in Arabidopsis thaliana. J. Exp. Bot. 2022, 73, 5514–5528. [Google Scholar] [CrossRef]
  43. Lynch, M.; Conery, J.S. The evolutionary fate and consequences of duplicate genes. Science 2000, 290, 1151–1155. [Google Scholar] [CrossRef] [Green Version]
  44. Wang, J.; Wang, Y.; Zhang, J.; Ren, Y.; Li, M.; Tian, S.; Yu, Y.; Zuo, Y.; Gong, G.; Zhang, H.; et al. The NAC transcription factor ClNAC68 positively regulates sugar content and seed development in watermelon by repressing ClINV and ClGH3.6. Hortic. Res. 2021, 8, 214. [Google Scholar] [CrossRef] [PubMed]
  45. Jin, S.K.; Zhang, M.Q.; Leng, Y.J.; Xu, L.N.; Jia, S.W.; Wang, S.L.; Song, T.; Wang, R.A.; Yang, Q.Q.; Tao, T.; et al. OsNAC129 Regulates Seed Development and Plant Growth and Participates in the Brassinosteroid Signaling Pathway. Front. Plant Sci. 2022, 13, 905148. [Google Scholar] [CrossRef]
  46. Staiger, D.; Brown, J.W. Alternative splicing at the intersection of biological timing, development, and stress responses. Plant Cell 2013, 25, 3640–3656. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  47. Sall, K.; Dekkers BJ, W.; Nonogaki, M.; Katsuragawa, Y.; Koyari, R.; Hendrix, D.; Willems LA, J.; Bentsink, L.; Nonogaki, H. DELAY OF GERMINATION 1-LIKE 4 acts as an inducer of seed reserve accumulation. Plant J. Cell Mol. Biol. 2019, 100, 7–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Guo, J.; Wang, S.; Yu, X.; Dong, R.; Li, Y.; Mei, X.; Shen, Y. Polyamines Regulate Strawberry Fruit Ripening by Abscisic Acid, Auxin, and Ethylene. Plant Physiol. 2018, 177, 339–351. [Google Scholar] [CrossRef] [Green Version]
  49. Paolo, D.; Orozco-Arroyo, G.; Rotasperti, L.; Masiero, S.; Colombo, L.; de Folter, S.; Ambrose, B.A.; Caporali, E.; Ezquer, I.; Mizzotti, C. Genetic Interaction of SEEDSTICK, GORDITA and AUXIN RESPONSE FACTOR 2 during Seed Development. Genes 2021, 12, 1189. [Google Scholar] [CrossRef]
  50. Cannon, S.B.; Mitra, A.; Baumgarten, A.; Young, N.D.; May, G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004, 4, 10. [Google Scholar] [CrossRef] [Green Version]
  51. Shen, S.; Zhang, Q.; Shi, Y.; Sun, Z.; Zhang, Q.; Hou, S.; Wu, R.; Jiang, L.; Zhao, X.; Guo, Y. Genome-Wide Analysis of the NAC Domain Transcription Factor Gene Family in Theobroma cacao. Genes 2019, 11, 35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Sun, L.; Liu, L.P.; Wang, Y.Z.; Yang, L.; Wang, M.J.; Liu, J.X. NAC103, a NAC family transcription factor, regulates ABA response during seed germination and seedling growth in Arabidopsis. Planta 2020, 252, 95. [Google Scholar] [CrossRef] [PubMed]
  53. Jahan, M.A.; Harris, B.; Lowery, M.; Coburn, K.; Infante, A.M.; Percifield, R.J.; Ammer, A.G.; Kovinich, N. The NAC family transcription factor GmNAC42-1 regulates biosynthesis of the anticancer and neuroprotective glyceollins in soybean. BMC Genom. 2019, 20, 149. [Google Scholar] [CrossRef] [PubMed]
  54. Zheng, Y.; Chen, C.; Liang, Y.; Sun, R.; Gao, L.; Liu, T.; Li, D. Genome-wide association analysis of the lipid and fatty acid metabolism regulatory network in the mesocarp of oil palm (Elaeis guineensis Jacq.) based on small noncoding RNA sequencing. Tree Physiol. 2019, 39, 356–371. [Google Scholar] [CrossRef] [PubMed]
  55. Alptekin, B.; Mangel, D.; Pauli, D.; Blake, T.; Lachowiec, J.; Hoogland, T.; Fischer, A.; Sherman, J. Combined effects of a glycine-rich RNA-binding protein and a NAC transcription factor extend grain fill duration and improve malt barley agronomic performance. Theor. Appl. Genet./Theor. Angew. Genet. 2021, 134, 351–366. [Google Scholar] [CrossRef]
Cimb 45 00344 g001 550
Figure 1. Phylogenetic tree of NAC TFs in Simmondsia chinensis and Arabidopsis thaliana. The tree was built by the neighbor-joining (NJ) in MEGA7. Different subgroups A1~A5, B1~B8, are shown in different colors. Simmondsia chinensis and Arabidopsis thaliana are shown in brown and green, respectively.
Figure 1. Phylogenetic tree of NAC TFs in Simmondsia chinensis and Arabidopsis thaliana. The tree was built by the neighbor-joining (NJ) in MEGA7. Different subgroups A1~A5, B1~B8, are shown in different colors. Simmondsia chinensis and Arabidopsis thaliana are shown in brown and green, respectively.
Cimb 45 00344 g001
Cimb 45 00344 g002 550
Figure 2. Phylogenetic relationships, conserved motifs, and gene structure of ScNAC genes. (A) Phylogenetic tree of Jojoba protein sequences constructed by neighbor-joining (NJ) in MEGA7, with 1000 bootstrap replicates. NAC members in Jojoba were classified into groups I to VIII based on the results of Arabidopsis subgroup classification, with different groups represented by different colors. (B) Distribution of the conserved motif predicted by MEME in the NAC protein sequence. The sequence of motif 1 to motif 20 was shown in the upper right corner. (C) NAC gene structure, yellow for exons, gray lines for introns, green for untranslated regions (UTR).
Figure 2. Phylogenetic relationships, conserved motifs, and gene structure of ScNAC genes. (A) Phylogenetic tree of Jojoba protein sequences constructed by neighbor-joining (NJ) in MEGA7, with 1000 bootstrap replicates. NAC members in Jojoba were classified into groups I to VIII based on the results of Arabidopsis subgroup classification, with different groups represented by different colors. (B) Distribution of the conserved motif predicted by MEME in the NAC protein sequence. The sequence of motif 1 to motif 20 was shown in the upper right corner. (C) NAC gene structure, yellow for exons, gray lines for introns, green for untranslated regions (UTR).
Cimb 45 00344 g002
Cimb 45 00344 g003 550
Figure 3. Cis-acting elements identified in 2000 bp region upstream of the Jojoba ScNAC promoter. Different cis-acting elements are represented by different colors, and some cis-acting elements overlap. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors.
Figure 3. Cis-acting elements identified in 2000 bp region upstream of the Jojoba ScNAC promoter. Different cis-acting elements are represented by different colors, and some cis-acting elements overlap. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors.
Cimb 45 00344 g003
Cimb 45 00344 g004 550
Figure 4. The location and relationship of ScNACs on chromosomes. White squares indicate no NAC genes distributed in that chromosome. Gray lines indicate all synteny regions in the Jojoba. Red lines indicate segmental duplicates of NAC gene pairs.
Figure 4. The location and relationship of ScNACs on chromosomes. White squares indicate no NAC genes distributed in that chromosome. Gray lines indicate all synteny regions in the Jojoba. Red lines indicate segmental duplicates of NAC gene pairs.
Cimb 45 00344 g004
Cimb 45 00344 g005 550
Figure 5. Synteny analysis of S. chinensis between V. vinifera and A. thaliana, respectively. Gray lines indicate regions of collinearity between Jojoba and other plants. Red lines indicate syntenic NAC gene pairs. The chromosomes of S. chinensis, V. vinifera, and A. thaliana are shown in orange, green, and blue, respectively.
Figure 5. Synteny analysis of S. chinensis between V. vinifera and A. thaliana, respectively. Gray lines indicate regions of collinearity between Jojoba and other plants. Red lines indicate syntenic NAC gene pairs. The chromosomes of S. chinensis, V. vinifera, and A. thaliana are shown in orange, green, and blue, respectively.
Cimb 45 00344 g005
Cimb 45 00344 g006 550
Figure 6. Heatmap of ScNAC expression in different seed tissues. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors. Samples were obtained from cotyledons, embryonic axis, seed coats, and whole seeds. Expression values were shown on color blocks. The color scale on the right indicates log2 expression of the mean value of ScNAC gene expression, with red representing high and blue representing low.
Figure 6. Heatmap of ScNAC expression in different seed tissues. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors. Samples were obtained from cotyledons, embryonic axis, seed coats, and whole seeds. Expression values were shown on color blocks. The color scale on the right indicates log2 expression of the mean value of ScNAC gene expression, with red representing high and blue representing low.
Cimb 45 00344 g006
Cimb 45 00344 g007 550
Figure 7. Heatmap of ScNAC expression at different stages of developing seeds. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors. Samples were obtained from early developing seeds (Early Dev. Seed), middle developing seeds (Mid Dev. Seed), late developing seeds (Late Dev. Seed), and mature dry seeds (Dry Seed). Expression values were shown on color blocks. The color scale on the right indicates log2 expression of the mean value of ScNAC gene expression, with red representing high and blue representing low.
Figure 7. Heatmap of ScNAC expression at different stages of developing seeds. NAC members were divided into groups I~VIII according to the phylogenetic analysis and marked with different colors. Samples were obtained from early developing seeds (Early Dev. Seed), middle developing seeds (Mid Dev. Seed), late developing seeds (Late Dev. Seed), and mature dry seeds (Dry Seed). Expression values were shown on color blocks. The color scale on the right indicates log2 expression of the mean value of ScNAC gene expression, with red representing high and blue representing low.
Cimb 45 00344 g007
Cimb 45 00344 g008 550
Figure 8. Differential expression of Jojoba genes in the cotyledon and embryonic axis tissues. Volcano plots were built based on significantly adjusted p-values less than 0.05 and absolute log2FC (log of fold change) values greater than 1. Genes whose expression is up-regulated are marked in red and genes whose expression is down-regulated are marked in blue. The NAC family members with an absolute value of log2FC greater than 2 are annotated.
Figure 8. Differential expression of Jojoba genes in the cotyledon and embryonic axis tissues. Volcano plots were built based on significantly adjusted p-values less than 0.05 and absolute log2FC (log of fold change) values greater than 1. Genes whose expression is up-regulated are marked in red and genes whose expression is down-regulated are marked in blue. The NAC family members with an absolute value of log2FC greater than 2 are annotated.
Cimb 45 00344 g008
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Xia, F.; Liang, X.; Tan, L.; Sun, W.; Dai, X.; Yan, H. Genome-Wide Identification, Evolution and Expression Profile Analysis of NAC Transcription Factor in Simmondsia chinensis. Curr. Issues Mol. Biol. 2023, 45, 5422-5436. https://doi.org/10.3390/cimb45070344

AMA Style

Xia F, Liang X, Tan L, Sun W, Dai X, Yan H. Genome-Wide Identification, Evolution and Expression Profile Analysis of NAC Transcription Factor in Simmondsia chinensis. Current Issues in Molecular Biology. 2023; 45(7):5422-5436. https://doi.org/10.3390/cimb45070344

Chicago/Turabian Style

Xia, Fan, Xiaoyu Liang, Lina Tan, Wen Sun, Xiaogang Dai, and Hanwei Yan. 2023. "Genome-Wide Identification, Evolution and Expression Profile Analysis of NAC Transcription Factor in Simmondsia chinensis" Current Issues in Molecular Biology 45, no. 7: 5422-5436. https://doi.org/10.3390/cimb45070344

Article Metrics

Back to TopTop