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Article

Genome-Wide Identification and Expression Profiling of the NCED Gene Family in Cold Stress Response of Prunus mume Siebold & Zucc

by
Ke Chen
1,2,3,
Xue Li
1,2,3,
Xiaoyu Guo
1,2,3,
Lichen Yang
1,2,3,
Like Qiu
1,2,3,
Weichao Liu
1,2,3,
Jia Wang
1,2,3 and
Tangchun Zheng
1,2,3,*
1
Beijing Key Laboratory of Ornamental Plants Germplasm Innovation and Molecular Breeding, National Engineering Research Center for Floriculture, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, China
2
Beijing Laboratory of Urban and Rural Ecological Environment, Engineering Research Center of Landscape Environment of Ministry of Education, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, China
3
Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants of Ministry of Education, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, China
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(7), 839; https://doi.org/10.3390/horticulturae9070839
Submission received: 25 June 2023 / Revised: 20 July 2023 / Accepted: 21 July 2023 / Published: 23 July 2023
(This article belongs to the Special Issue Recent Scientific Developments in Breeding and Genetics of Ornamental and Beverage Plants)
Browse Figures
Versions Notes

Abstract

:
The 9-cis-epoxy carotenoid dioxygenase (NCED) is an enzyme that is crucial in abscisic acid (ABA) biosynthesis, and its role is vital in plant development and abiotic stress. However, the function of the NCED family in Rosaceae plant species remains unclear. Through genome-wide screening, we identified 10, 10, 11, 12 and 13 NCED genes in Prunus mume, Prunus apricot, Prunus salicina, Prunus persica, and Rosa chinensis, respectively. Phylogenetic analysis showed that these NCED genes were divided into six groups. Gene structure analysis showed that the number and size of introns were relatively constant in each subfamily, while the motif composition differed significantly among them. Collinearity analysis revealed a high homology of NCEDs in the Prunus genus. Promoter cis-acting element analysis showed that eight PmNCEDs contained abscisic acid-responsive elements (ABRE). Furthermore, expression profile analysis based on qRT-PCR revealed that PmNCED3, PmNCED8 and PmNCED9 were up-regulated in response to low temperature stress, suggesting their significant role in the plant’s response to cold stress. These findings provide insights into the structure and evolution of PmNCEDs and lay the foundation for further studies regarding their function during cold stress.

1. Introduction

Japanese apricot (Prunus mume Sieb. et Zucc.) is a perennial woody tree of the Prunus genus in the family Rosaceae, with attractive, colourful flowers in early spring that have important ornamental and economic value and are loved by people [1]. P. mume is widely planted in Asia and is mainly distributed in the south of China [2]. However, due to its limited tolerance to low temperatures, P. mume cannot be widely cultivated in all regions, severely limiting its economic and ornamental value [3]. Therefore, breeding for cold tolerant varieties is an important direction for P. mume breeding. It is very important to explore the cold-resistant genes and understand the expression patterns of candidate genes under low temperature stress for the breeding of new cold-resistant varieties of P. mume.
Under abiotic stress conditions such as low temperature, freezing damage, drought, salt and alkali, plants can adapt to or resist these stresses through self-regulation [4]. Abscisic acid (ABA) is a very important endogenous plant hormone that not only plays an important role in regulating plant growth and development, but also increases ABA content in response to various environmental stresses such as drought, high salinity and cold, which can improve plant stress resistance under environmental stresses [5,6]. Studies have shown that the content of ABA in plants increases with the decrease in ambient temperature, while the content of ABA decreases with the increase in ambient temperature [7,8]. The concentration of ABA in the buds and roots of Acer saggharum, which was domesticated in winter, increased by about 10 times [9]. The ABA content of Carpobrotus edulis increased under cold stress [10]. Exogenous application of ABA could improve the frost resistance of Vitis vinifera [11]. Therefore, regulating the expression level of key ABA biosynthesis genes is crucial for enhancing plant stress resistance. ABA can be synthesized in plants through two pathways: the indirect pathway (C15 pathway) and the direct pathway (carotenoid pathway). The indirect pathway is the primary route for ABA synthesis in higher plant tissues [12].
9-cisepoxy-carotenoid dioxygenase (NCED) is a rate-limiting enzyme that is important in the synthesis and regulation of ABA through indirect pathways. It can induce the increase of endogenous ABA content and improve plant stress resistance under stress conditions [5,13,14,15]. The gene encoding NCED was initially isolated from ABA deficient mutants in maize [15,16] and subsequently identified in other plant species such as A. thaliana [15], Solanum lycopersicum [16], Glycine max [17], V. vinifera [18] and Malus pumila [19]. In A. thaliana, the NCED gene belongs to a multi-gene family with nine members. When induced by drought stress, AtNCED3 can control endogenous ABA levels in plants, and overexpression of AtNCED3 can reduce leaf transpiration rate and drought tolerance of A. thaliana [20]. Ectopic expression of OsNCED5 and OsNCED3 in A. thaliana, not only can enhance tolerance to drought stress and delay seed dormancy time, but also change the morphology of plants and leaves [21]. CstNCED gene can be induced by low temperature, drought, sorbitol, salt and exogenous ABA treatment [22]. Under salinity, low temperature and drought stress, NCED was closely related to endogenous ABA content in Crocus sativus [22]. Under the influence of drought, low temperature and high temperature, the expression of MpNCED2 in M. pumila was significantly up-regulated, while the expression level of MpNCED1 was affected by low temperature and high temperature, but not by drought [23]. In Vigna unguiculata, salt stress specifically induced VuNCED1 expression, while cold (4 °C) or heat (40 °C) stress did not induce VuNCED1 expression [24]. Cold stress and the application of exogenous ABA induced CkNCED1 expression and ABA accumulation in Caragana korshinskii [25]. Furthermore, transgenic plants that overexpress the NCED genes can accumulate a lot of ABA and have stronger resistance to abiotic stress [20,26,27].
Cold injury is an important factor affecting the growth and distribution of P. mume, and the NCED gene family plays an important role in enhancing plant stress resistance, but the function of the NCED gene family in cold resistance of P. mume is still unclear. Here, 56 NCEDs family members were identified from 5 Rosaceae species and analyzed for their physicochemical properties, evolutionary relationships, structural characteristics, collinearity and expression pattern of PmNCEDs under different low temperature stress. These results contribute to a further understanding of the phylogenetic relationship of the NCED family in Roseaceae and the response mechanism of P. mume under low temperature stress.

2. Materials and Methods

2.1. Identification and Physicochemical Properties of NCEDs Gene Family

The genome data of P. mume, P. apricot, P. salicina, P. persica, R. chinensis and A. thaliana were downloaded from EnsemblPlants (https://plants.ensembl.org, accessed on 10 December 2022) [28]. The NCED protein sequences for A. thaliana were downloaded from UniProt (https://www.uniprot.org/, accessed on 10 December 2022). In TB tools [29], the NCED family members of five Rosaceae species were searched by BLAST GUI Wrapper Two Sequences Files (E = 10−5). Subsequently, NCBI CD-Search (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi, accessed on 3 January 2023) and Pfam (https://pfam.xfam.org, accessed on 3 January 2023) were used to further analyze and identify the conserved domains of NCED proteins in five Rosaceae species. Finally, after removing the redundant, incomplete domain and incorrect sequences, the remaining sequences can be regarded as NCED members of five Rosaceae species. The protein molecular weight (MW), and theoretical isoelectric point (pI) and subcellular location of five Rosaceae species NCEDs were predicted using ExPASY (http://web.expasy.org/protparam/, accessed on 20 January 2023) and WoLF PSORT (https://wolfpsort.hgc.jp/, accessed on 20 January 2023), respectively.

2.2. Phylogenetic Analysis

Phylogenetic analysis was conducted on the amino acid sequences of A. thaliana, P. mume, P. apricot, P. salicina, P. persica and R. chinensis NCED proteins. Protein sequences from six species were first compared using ClustalX [30], followed by the construction of a great likelihood tree using IQ-tree [31]. Finally, ChiPlot (https://www.chiplot.online/, accessed on 12 February 2023) was used to beautify the phylogenetic tree.

2.3. Chromosomal Localization and Collinear Analysis

The Multiple Collinearity Scan Toolkit (MCScanX) was utilized with default parameters in TB tools to analyze gene tandems [32]. Using MCScanX, collinearity of NCEDs in P. mume, P. salicina, P. apricot, and A. thaliana was analyzed and visualized in TB tools [29]. Additionally, TB tools were used to extract the location and length information of NCED genes on the chromosomes of five Rosaceae species and map their distribution on chromosomes.

2.4. Gene Structure and Protein Conserved Motif Analysis

To further understand the evolutionary relationships among the NCED genes of the five Rosaceae species, we used the online website MEME (https://meme-suite.org/meme/doc/meme.html, accessed on 24 February 2023) [33] to analyze the conserved motifs of five Rosaceae species NCED proteins and set the number of motifs to 10. Multiple sequence alignment of the full-length sequence of NCED proteins from the five Rosaceae species was performed using Muscle, and the results were trimmed using trimAI, followed by an automatic screening of amino acid substitution models using IQ-tree [31]. Finally, tree-structure-motif mapping was performed by TBtools [29].

2.5. Cis-Acting Regulating Element Analysis

The upstream 2-kb sequence of the initiation codon of P. mume NCEDs gene was extracted as the promoter region and submitted to the PlantCARE online website (https://bioinformatics.psb.ugent.be/webtools/plantcare/html/, accessed on 25 February 2023) for analysis (Tables S1 and S2), and then screened and visualized by TBtools [30].

2.6. Expression Pattern Analysis

The tissues of flower buds, fruits, roots, stems and leaves from P. mume were collected and sequenced by Illumina HiSeq2000 [34]. Buds of the cultivar ‘Zao Lve’ of P. mume overwintered in the open ground in Beijing were used as test material at four different periods: EDI (Endodorman I, November), EDII (Endodorman II, December), EDIII (Endodorman III, January) and NF (Natural flush, February), respectively [35]. Stem samples of the cultivar ‘Songchun’ were collected from three places (Beijing [39°54′ N, 116°28′ E], Chifeng [42°17′ N, 118°58′ E], Gongzhuling [43°42′ N, 124°47′ E]) in autumn (October 2012), winter (January 2013) and spring (March 2013) [36]. Subsequently, the original data of RNA-seq obtained (Tables S3–S5) were analyzed and the gene expression heat map was drawn using TBtools [29].
To investigate the expression pattern of the cultivated variety ‘Zao Lve’ of P. mume in diverse cold stress situations, the grafted annual ‘Zao Lve’ was chosen as the test material. This material was collected from the greenhouse of Beijing Forestry University. It was treated at 4 °C for various durations (0, 1, 3, 5, 7, 9, 11 d) and at different temperatures (4, 0, −4, −8 °C) for 6 h. The control material was also maintained at 24 °C. The annual shoots of five plants under different treatment conditions were mixed for RNA-seq, and there were biological repeats at the same time. They were frozen in liquid nitrogen and then stored at −80 °C for subsequent use. Total RNA was extracted using the RNA extraction kit (TIANGEN, Beijing, China) and reverse transcribed into cDNA as per the cDNA synthesis kit (Tiangen, Beijing, China). qRT-PCR primers were used and listed in Table S6. qRT-PCR was performed using the PikoReal real-time PCR system (Thermo Fisher Scientific, Waltham, MA, USA). We selected PmPP2A as the housekeeping gene [37]. To ensure accuracy, we conducted three biological replicates and three technical replicates, and calculated gene expression using 2−ΔΔCT [38].

3. Results

3.1. Genome-Wide Identification of NCEDs Gene Family in Five Rosaceae Species

In total, 56 NCED genes were characterized by Blastp comparison and conserved domain analysis of five Rosaceae species. There were 10, 10, 11, 12 and 13 NCED genes in P. mume, P. apricot, P. salicina, P. persica and R. chinensis, respectively. They were named successively according to their position distribution on chromosomes (Table 1). The NCEDs gene of five Rosaceae species encoded 75–1496 aa, among which the longest was PmNCED1 (1496 aa) and the shortest was PsNCED5 (75 aa). The molecular weight (MW) of the NCEDs was 8.36–168.43 kDa. The predicted pI ranged from 4.71 to 7.93, and most of the pI were less than 7, indicating they were mostly weakly acidic. Subcellular localization prediction of NCEDs in five Rosaceae species showed that 55.3% of 56 NCED genes were located in chloroplasts, which was congruous with the functional location of NCED genes in ABA biosynthesis pathway, while other genes were located in the nucleus, cytoplasm and mitochondria (Table 1).

3.2. Phylogenetic Analysis of NCEDs Gene Family

The NCED phylogenetic tree of A. thaliana, P. mume, P. apricot, P. salicina, P. persica and R. chinensis was constructed using the full-length amino acid sequences (Figure 1). Based on the topological structure analysis of the evolutionary tree, six NCED gene species were divided into six subfamilies: Group I~Group VI. Among them, PmNCED6, PmNCED7 and PmNCED8 of P. mume formed Group I with AtNCED2, AtNCED3, AtNCED5, AtNCED6 and AtNCED9 directly related to ABA synthesis in A. thaliana. PmNCED4, PmNCED5 and AtCCD4 constitute Group II; PmNCED9 and AtCCD1 constitute Group III. PmNCED1 and PmNCED2 constitute Group IV. PmNCED3 and AtCCD8 constitute Group V. PmNCED10 and AtCCD7 constitute Group VI. Analysis of the affinities between the PmNCEDs and other species of NCEDs showed that most of the PmNCEDs belonged to the same branch as the PaNCEDs, indicating that the PmNCEDs were close in kinship to the PaNCEDs.

3.3. Chromosomal Localization of NCEDs Gene Family in Five Rosaceae Species

The chromosome map showed that NCED genes were mostly unequally spread on the chromosomes of five Rosaceae plants (Figure 2). PmNCEDs and PaNCEDs were each distributed on chromosomes 2, 3 and 5 (Figure 2A,B), and chromosome 2 contained the highest number of NCED genes (6 PmNCEDs and 7 PaNCEDs), and we found that PmNCED1 and PmNCED2 of the P. mume NCED genes were adjacent to each other on chromosome 2 and were tandem repeats. PsNCEDs and PpNCEDs were each distributed on chromosomes 1, 2 and 4 (Figure 2C,D), with the largest number of NCED genes on chromosome 1 (8 PsNCEDs and 7 PpNCEDs) and PsNCED9 alone on chromosome 2 (Figure 2C). RcNCEDs were randomly located on chromosomes 1, 4, 5, 6 and 7 (Figure 2E), with chromosome 1 containing a higher number of NCED genes (5).

3.4. Gene Structure and Conserved Motifs Analysis of NCED in Five Rosaceae Species

The structure and function of genes are closely related, which can reflect their evolutionary relationship. In order to further understand the phylogenic relationships between the NCED genes in five species of Rosaceae, the gene structures of intron/exon were compared according to their distribution patterns (Figure 3B). The results suggested that the NCED genes in Group I had no intron and only one exon. In Group II, except for RcNCED7 and PmNCED5, only one exon had no intron, and other NCED genes contained 1–2 introns. The number of introns in Group IV was the most abundant, and the number of introns in PmNCED1 was the highest, with a total of 22 introns. Therefore, with some exceptions, the number and size of introns in five Rosaceae species were relatively conservative in each subfamily, thus consolidating the taxonomy obtained in the phylogenetic tree (Figure 3A). However, intron-exon organization differs between subfamilies, suggesting that intra recombination such as insertion/deletion contributes to the amplification of the NCED family in five Rosaceae species besides their functional differentiation.
MEME was used to detect conserved motifs to further analyze the differences among NCED genes, where 10 conserved motifs were identified (Figure 3C). Of these, motifs 1, 2, 3, 5, 6, 7 and 10 are conserved in most NCEDs, which indicates that these motifs may be the reason for their common function. For example, Group I contains 10 conserved motifs except for RcNCED8 and RcNCED13; Group VI does not contain motif 4 and motif 8; Group V does not contain motif 9; and Group IV is more diverse. These data indicate that, in general, NCED isoforms with similar genetic structure also have similar motif composition and domain location, and belong to the same clade.

3.5. Collinear Analysis of NCEDs in Prunus Species and A. thaliana

Collinearity analysis was performed for four species: P. mume, P. apricot, P. salicina and A. thaliana (Figure 4). The number of collinear gene pairs of P. mume, P. apricot, P. salicina and A. thaliana were 6, 6 and 2, respectively, indicating that the homology of NCED family genes was high in Prunus. No corresponding homologous genes were found for PmNCED2, PmNCED5, PmNCED6 and PmNCED9 genes, suggesting that some genes were lost during the evolution of the NCED gene family of P. mume, or the NCED gene family of P. mume was expanded. PmNCED10 was present in collinear gene pairs of P. mume, P. apricot, P. salicina and A. thaliana, suggesting that PmNCED10 may be common in monocotyledonous and dicotyledonous plants, forming before species differentiation and having a longer evolutionary time.

3.6. Analysis of Cis-Elements in the Promoters of PmNCEDs

The upstream 2-kb sequence of the initiation codon of the PmNCEDs was used for cis-element analysis (Figure 5). Except for PmNCED9, the promoter region of PmNCEDs generally had light responsive elements (Figure 5A,B), such as G-box, GT1-motif, Box 4, MRE, CTt-motif, etc. Six PmNCEDs (PmNCED1, PmNCED2, PmNCED3, PmNCED4, PmNCED5, and PmNCED10) each contained a low-temperature response (LTR) element. PmNCED2, PmNCED4 and PmNCED7 also contain drought responsive component MBS. The promoter region of PmNCEDs was also enriched with several cis-acting elements associated with phytohormone response (Figure 5A,B), such as the TCA-element associated with salicylic acid responsive; the P-box associated with gibberellin-responsive; the MeJA-responsive element G-box and CGTCA-motif. In addition, PmNCEDs contain an abscisic acid responsive element (ABRE), which accounts for 16.59% of all elements, except for PmNCED7 and PmNCED9, of which the PmNCED6 gene contains 12 elements (Figure 5A,C).

3.7. Expression Pattern of PmNCEDs

Expression patterns of PmNCEDs were analyzed based on transcriptome data sets to further explore the function of PmNCEDs (Figure 6). PmNCEDs were expressed differently in the buds, leaves, roots and stems of P. mume (Figure 6A). The expression level of most PmNCEDs in different tissues was low, such as PmNCED5 and PmNCED10 were almost not expressed. PmNCED7 was slightly expressed in buds, leaves, roots and stems, but hardly expressed in fruits. The expression level of PmNCED8 in each tissue was higher than that of other genes. PmNCED4 and PmNCED9 were highly expressed in buds, while PmNCED4 was almost not expressed in fruits and leaves, and the expression of PmNCED9 in all tissues was high. Expression of PmNCEDs in buds of ‘Zao lve’ cultivated species at three endodermal developmental stages differs considerably under low temperature conditions (Figure 6B). In general, the expression levels of PmNCED2, PmNCED5, and PmNCED6 were low, while there were no significant changes observed in the expression of PmNCED9. On the other hand, the expression levels of PmNCED1 and PmNCED3 were comparatively lower, but showed a mild up-regulation during the NF stage from EDIII to bud dormancy release. The expression level of PmNCED7 showed a downward trend from EDI to NF. The expression level of PmNCED8 was similar in the EDI stage and the EDIII stage, but down-regulated in the EDII stage and NF stage. However, the expression level of PmNCED4 was a gradually cumulative one and reached the peak in the NF stage of bud dormancy release. The expression level in the stem of ‘Songchun’ was also different in Beijing, Chifeng and Gongzhuling in different seasons (Figure 6C). Among them, PmNCED1, PmNCED2, PmNCED5 and PmNCED10 were almost not expressed. PmNCED3 was slightly expressed in autumn and winter in Beijing and Chifeng, but there was no obvious change trend from autumn to winter. The expression of PmNCED4 was high in spring, but low in autumn and winter, and showed a downward trend from autumn to winter. PmNCED8 was highly expressed in autumn and winter, but decreased from winter to spring. PmNCED9 was highly expressed in the three regions in different seasons, but there was no obvious change trend. As the average winter temperature in three regions decreased, the expression of PmNCED7 and PmNCED8 showed an increase, and there was a noticeable change in the trend of PmNCED7, while the change of the two genes from autumn to winter was not obvious.
Obtaining the expression levels of PmNCEDs through qRT-PCR was done to investigate their role in dealing with cold stress under various treatments (Figure 7). Under chilling treatment at 4 °C (Figure 7A), the expressions of PmNCED4 and PmNCED7 slightly changed with the extension of chilling treatment time, but showed a downward trend overall. The expression levels of PmNCED3 and PmNCED6 were low on the whole but increased sharply on the 9th day. Although the expression levels of PmNCED8 and PmNCED9 fluctuated in a small range, the expression levels of the two genes remained high with the extension of cold treatment time. As the processing temperature gradually reduced (Figure 7B), the expression of PmNCED6 and PmNCED7 showed an overall downward trend. When the cool treating temperature decreased, there were some small fluctuations in PmNCED4 expression, but there was no obvious regularity, with a slight upward trend overall. Compared to the expression of PmNCED4, the expression of PmNCED8 fluctuated greatly, and peaked at −4 °C with the increase of chilling stress degree, and then decreased at −8 °C. At 0 °C, the expression level of PmNCED3 reached its peak, then decreased at −4 °C, but slightly increased at −8 °C, overall higher than the control group. The expression level of PmNCED9 increased gradually and peaked at −8 °C, although the range of change was small.

4. Discussion

As a typical abiotic stress factor, low temperature has a significant influence on plant development and crop yield [39]. Under the influence of climate change, severe weather such as cold and freezing often occurs in China (especially in the southern region). Cold and low temperature damage causes certain damage to the somatic structure of fruit trees and ornamental plants, causing disorder of material metabolism and even death, causing serious economic losses to the production of the fruit industry in China, thus restricting the healthy and sustainable development of the fruit industry [40]. Low temperature is also one of the most principal factors restricting the growth and distribution of Prunus genus. The main ornamental organ of P. mume is the flower, the low temperature in early spring may affect the normal growth and development of flowers and reduce the ornamental effect of flowers. Therefore, it is of great significance to explore the response and tolerance mechanism of P. mume to low temperature stress to improve its cold tolerance. ABA is a significant signaling molecule in plants under stress, and NCED is a key rate-limiting enzyme in ABA synthesis. In most species, the NCED family is a small gene family, which has been confirmed in plants such as A. thaliana [15], S. lycopersicum [16], G. max [17], V. vinifera [18] and M. pumila [19].
In this research, we identified 56 NCEDs in total from five Rosaceae species, with P. mume and P. apricot identifying the same number of NCED family members. R. chinensis had the highest number of NCED genes (13), while P. persica and P. salicina had the next highest number of NCED family members, with 12 and 11 NCED genes, respectively. In contrast, only nine, five and five members of the NCED family were found in A. thaliana, Oryza sativa and Zea mays [41], respectively. This indicates a relatively consistent evolutionary relationship among the five Rosaceae species and shows the extension of the NCED gene family in the evolution of the Prunus genus. Gene replication events occur frequently in biological evolution, but only one pair of tandem replication events was found in the PmNCEDs (Figure 2A). The collinearity results manifested that the number of collinearity gene pairs of P. apricot, P. salicina and A. thaliana was 6, 6, and 2, respectively, indicating that P. mume had a close homology relationship with the NCED of P. apricot and P. salicina, but a distant homology relationship with the NCED of A. thaliana. In addition, no corresponding homologous genes were found for PmNCED2, PmNCED5, PmNCED6 and PmNCED9, suggesting that the NCED gene family of P. mume may have expanded.
Through the analysis of cis-elements, it was found that the promoter region of PmNCEDs contains a wide range of cis-elements involved in light response and phytohormone induction. Among them, ABRE related to abscisic acid responsive accounted for 16.59% of all components, TGACG-motif and CGTCA-motif related to MEJA- responsive accounted for 16.6%. At the same time, some genes also contain elements related to low temperature response, which is consistent with the existing studies on the involvement of NCED in the process of plant resistance. For example, transcriptional factor NGATHA1 of A. thaliana activates AtNCED3 to induce ABA biosynthesis through dehydration stress [42]. However, there is a positive feedback adjustment of ABA in the biosynthesis of ABA in plants under dehydration stress, and ABA induced AtNCED3 expression requires the distal ABA response element ABRE [43].
Thus far, numerous studies have investigated how NCED genes react to environmental stresses such as drought, high temperatures, and excessive salt. In Vigna unguiculata, salt stress specifically induced VuNCED1 expression, while cold (4 °C) or heat (40 °C) stress did not induce VuNCED1 expression [24]. Cold stress and the application of exogenous ABA induced CkNCED1 expression and ABA accumulation in C. korshinskii [25]. Under salinity, low temperature and drought stress, NCED was closely related to endogenous ABA content in C. sativus [22]. Under the influence of drought, low temperature and high temperature, the expression of MpNCED2 in M. pumila was significantly up-regulated, while the expression of MpNCED1 was affected by low temperature and high temperature, but not by drought [23]. Dehydration, salt stress, low temperature stress and drought stress can induce SgNCED1 transcription and ABA accumulation [44]. In our study, under low temperature stress, only PmNCED8 reacted strongly, and the expression of PmNCED9 showed an upward trend under cold stress, but its expression level changed little, while the expression of PmNCED3 changed significantly, and its expression level changed unsteadily during long-term cold treatment (Figure 7). These results indicate that PmNCED3, PmNCED8 and PmNCED9 have different responses to low temperature stress.
By checking cis-elements of the PmNCEDs, it was found that only PmNCED3 contained cold stress response elements, while PmNCED8 and PmNCED9 had no cold stress response elements (Figure 4). In addition, PmNCED3 contains elements related to both abscisic acid response and MeJA-response, while PmNCED8 contains elements related to MeJA-response. ABA and MeJA, as signaling molecules in response to abiotic stress, can participate in controlling the expression of resistance genes in plants, and exogenous hormones can enhance plant cold tolerance [45,46]. The promoter region of MpNCED1 and MpNCED2 contains regulatory elements such as ABRE, ARE and TCA-element, in addition, MpNCED2 also contains CGTCA-motif and TGACG-motif relevant to MeJA-response [23]. Therefore, the response of PmNCED3 and PmNCED8 to low temperature stress may be due to the presence of elements related to abscisic acid response and MeJA-response.

5. Conclusions

A total of 56 NCED genes were identified in 5 species of Rosaceae through genome-wide screening and were divided into 6 subfamilies according to phylogenetic analysis. The analysis of motif and gene structure further proved the accuracy of classification. Evolutionary analysis showed that the homology of NCEDs genes in P. mume, P. apricot and P. salicina was high. qRT-PCR analysis showed that PmNCED3, PmNCED8 and PmNCED9 may be related to cold stress response. These results increased our understanding of the gene structure and the evolution of the NCED gene family in five Rosaceae specie, and lay a foundation for further study on the function of PmNCEDs under low temperature stress.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae9070839/s1, Table S1: The promoter sequence of PmNCEDs; Table S2: Cis-acting element on the promoter of PmNCEDs; Table S3: Expression profiles of PmNCEDs in different tissues; Table S4: Expression profiles of PmNCEDs during the process of flower bud dormancy release; Table S5: Expression profiles of PmNCEDs in different regions and seasons; Table S6: The primers of qRT-PCR used in this study.

Author Contributions

Conceptualization, T.Z.; Data curation, X.L., X.G., L.Y., L.Q. and W.L.; Funding acquisition, T.Z.; Investigation, K.C., X.L. and X.G.; Methodology, K.C. and W.L.; Project administration, T.Z.; Resources, J.W.; Software, K.C., X.L., L.Y., L.Q. and W.L.; Supervision, J.W.; Writing—original draft, K.C.; Writing—review & editing, T.Z. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by the Fundamental Research Funds for the Central Universities (No. QNTD202306) and Beijing High-Precision Discipline Project, Discipline of Ecological Environment of Urban and Rural Human Settlements and the Special Fund for Beijing Common Construction Project.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

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Figure 1. The ML Phylogenetic tree of NCEDs family in 5 Rosaceae species and A. thaliana. Roman numerals indicate subgroups. At: A. thaliana; Pm: P. mume; Rc: R. chinensis; Ps: P. salicina; Pp: P. persica; Pa: P. apricot.
Figure 1. The ML Phylogenetic tree of NCEDs family in 5 Rosaceae species and A. thaliana. Roman numerals indicate subgroups. At: A. thaliana; Pm: P. mume; Rc: R. chinensis; Ps: P. salicina; Pp: P. persica; Pa: P. apricot.
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Figure 2. Chromosomal location of NCED genes in five Rosaceae species. (A–E). Chromosome distribution of NCED genes in P. mum, P. apricot, P. salicina, P. persica, and R. chinensis. Chromosome numbers are displayed on the left side of the bar, and the NCED genes are marked on the right side of the chromosomes. Scale on the left represents the chromosome length and is expressed in megabytes (Mb). Pm: P. mume; Pa: P. apricot; Ps: P. salicina; Pp: P. persica; Rc: R. chinensis.
Figure 2. Chromosomal location of NCED genes in five Rosaceae species. (A–E). Chromosome distribution of NCED genes in P. mum, P. apricot, P. salicina, P. persica, and R. chinensis. Chromosome numbers are displayed on the left side of the bar, and the NCED genes are marked on the right side of the chromosomes. Scale on the left represents the chromosome length and is expressed in megabytes (Mb). Pm: P. mume; Pa: P. apricot; Ps: P. salicina; Pp: P. persica; Rc: R. chinensis.
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Figure 3. Gene structure and conserved motifs analysis of NCED gene family in five Rosaceae species. (A). Phylogenetic trees of NCED proteins from five Rosaceae species. I~VI represent 6 groups; (B). Exon-intron structure of NCED genes. The black lines represent introns; (C). The conserved motifs of NCED genes in five Rosaceae species. Conservative motifs are represented by different colored boxes. The black lines represent non-conserved sequences.
Figure 3. Gene structure and conserved motifs analysis of NCED gene family in five Rosaceae species. (A). Phylogenetic trees of NCED proteins from five Rosaceae species. I~VI represent 6 groups; (B). Exon-intron structure of NCED genes. The black lines represent introns; (C). The conserved motifs of NCED genes in five Rosaceae species. Conservative motifs are represented by different colored boxes. The black lines represent non-conserved sequences.
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Figure 4. Collinear analysis of NCED genes in three Prunus species and A. thaliana. Gray lines in the background represent collinear relationships throughout the genome, and the blue lines mainly represent the collinear NCED gene pairs.
Figure 4. Collinear analysis of NCED genes in three Prunus species and A. thaliana. Gray lines in the background represent collinear relationships throughout the genome, and the blue lines mainly represent the collinear NCED gene pairs.
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Figure 5. Cis-element analysis of PmNCEDs promoter. (A). Cis-elements in 2-kb sequence upstream of PmNCEDs. Different cis-elements are represented by round rectangles of different colors; (B). The number of PmNCEDs in each class of cis-elements. Cis-elements are divided into hormone, light and stress response classes; (C). Proportion of cis-elements involved in hormonal, light and stress responses in the PmNCEDs promoter (%).
Figure 5. Cis-element analysis of PmNCEDs promoter. (A). Cis-elements in 2-kb sequence upstream of PmNCEDs. Different cis-elements are represented by round rectangles of different colors; (B). The number of PmNCEDs in each class of cis-elements. Cis-elements are divided into hormone, light and stress response classes; (C). Proportion of cis-elements involved in hormonal, light and stress responses in the PmNCEDs promoter (%).
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Figure 6. Expression pattern of the PmNCEDs. (A). The heatmap of the expression of PmNCEDs in different tissues; (B). The heat map of the expression of PmNCEDs in buds of P. mume ‘Zao lve’ at three stages of endo dormancy under low temperature conditions; (C). The heatmap of the expression of PmNCEDs in the stems of ‘Songchun’ from different regions and seasons.
Figure 6. Expression pattern of the PmNCEDs. (A). The heatmap of the expression of PmNCEDs in different tissues; (B). The heat map of the expression of PmNCEDs in buds of P. mume ‘Zao lve’ at three stages of endo dormancy under low temperature conditions; (C). The heatmap of the expression of PmNCEDs in the stems of ‘Songchun’ from different regions and seasons.
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Figure 7. qRT-PCR analysis of PmNCEDs under low temperature treatment. (A). The expression level of PmNCEDs under 4 °C treatment for 0, 1, 3, 5, 7, 9,11 d; (B). The expression level of PmNCEDs under 4 °C, 0 °C, −4 °C, and −8 °C treatment for 6 h. The samples at 24 °C were used as the inner group control.
Figure 7. qRT-PCR analysis of PmNCEDs under low temperature treatment. (A). The expression level of PmNCEDs under 4 °C treatment for 0, 1, 3, 5, 7, 9,11 d; (B). The expression level of PmNCEDs under 4 °C, 0 °C, −4 °C, and −8 °C treatment for 6 h. The samples at 24 °C were used as the inner group control.
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Table
Table 1. Basic information and physicochemical properties of NCED genes in five Rosaceae species.
Table 1. Basic information and physicochemical properties of NCED genes in five Rosaceae species.
SpeciesGene NameGene IDChromosome LocalizationLength (aa)MW (kDa)pIPrediction of Subcellular
Localization
Prunus mumePmNCED1Pm005147Chr21496168.435.83Nucleus
PmNCED2Pm005148Chr254060.335.32Chloroplast
PmNCED3Pm005153Chr256362.256.53Mitochondrion
PmNCED4Pm006647Chr258664.736.21Peroxisome
PmNCED5Pm006977Chr28910.135.54Cell wall
PmNCED6Pm008988Chr260066.447.92Chloroplast
PmNCED7Pm010425Chr361768.186.43Chloroplast
PmNCED8Pm011164Chr362269.016.39Chloroplast
PmNCED9Pm016267Chr546352.586.45Peroxisome
PmNCED10Pm017769Chr563470.475.63Chloroplast
Prunus apricotPaNCED1PARG03953m01Chr260066.437.92Chloroplast
PaNCED2PARG06146m02Chr258664.696.21Peroxisome
PaNCED3PARG06146m01Chr260466.526.48Peroxisome
PaNCED4PARG07910m01Chr256562.476.20Mitochondrion
PaNCED5PARG07915m02Chr252058.215.76Cytoplasm
PaNCED6PARG07915m01Chr226730.145.44Nucleus
PaNCED7PARG07916m01Chr21073120.205.61Chloroplast
PaNCED8PARG11107m01Chr362769.576.63Chloroplast
PaNCED9PARG11892m01Chr361768.126.43Chloroplast
PaNCED10PARG17947m01Chr561568.355.69Chloroplast
Prunus salicinaPsNCED1evm.model.LG01.539Chr159765.776.21Peroxisome
PsNCED2evm.model.LG01.2322Chr156562.556.36Chloroplast
PsNCED3evm.model.LG01.2327Chr117619.635.63Nucleus
PsNCED4evm.model.LG01.2328Chr122325.156.22Nucleus
PsNCED5evm.model.LG01.2329Chr1758.364.71Cytoplasm
PsNCED6evm.model.LG01.2330Chr161769.095.75Chloroplast
PsNCED7evm.model.LG01.2331Chr158665.925.55Cytoplasm
PsNCED8evm.model.LG01.4261Chr160566.827.93Chloroplast
PsNCED9evm.model.LG02.1859Chr261568.395.76Chloroplast
PsNCED10evm.model.LG04.787Chr461467.726.36Chloroplast
PsNCED11evm.model.LG04.1420Chr462769.647.34Chloroplast
Prunus persicaPpNCED1transcript:ONI26993Chr160566.957.24Chloroplast
PpNCED2transcript:ONI30522Chr160866.816.29Peroxisome
PpNCED3transcript:ONI30523Chr142747.306.23Peroxisome
PpNCED4transcript:ONI33831Chr156562.506.33Chloroplast
PpNCED5transcript:ONI33839Chr156863.625.18Nucleus
PpNCED6transcript:ONI33840Chr161768.965.64Chloroplast
PpNCED7transcript:ONI33841Chr155562.496.01Cytoplasm
PpNCED8transcript:ONI20423Chr243049.126.09Cytoplasm
PpNCED9transcript:ONI20422Chr254761.835.97Peroxisome
PpNCED10transcript:ONI22509Chr261568.705.77Chloroplast
PpNCED11transcript:ONI11006Chr461768.166.43Chloroplast
PpNCED12transcript:ONI12196Chr463270.356.63Chloroplast
Rosa chinensisRcNCED1transcript:PRQ54664Chr149456.046.56Peroxisome
RcNCED2transcript:PRQ54676Chr163171.207.70Peroxisome
RcNCED3transcript:PRQ56952Chr163171.576.98Chloroplast
RcNCED4transcript:PRQ57420Chr162469.896.27Chloroplast
RcNCED5transcript:PRQ57426Chr162268.976.45Chloroplast
RcNCED6transcript:PRQ36937Chr461367.296.81Chloroplast
RcNCED7transcript:PRQ41175Chr458463.725.70Chloroplast
RcNCED8transcript:PRQ29478Chr568875.956.74Chloroplast
RcNCED9transcript:PRQ30744Chr561267.617.25Chloroplast
RcNCED10transcript:PRQ27514Chr633037.344.71Chloroplast
RcNCED11transcript:PRQ27515Chr656363.055.34Cytoplasm
RcNCED12transcript:PRQ27522Chr656162.106.04Chloroplast
RcNCED13transcript:PRQ21333Chr730334.625.56Peroxisome
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Chen, K.; Li, X.; Guo, X.; Yang, L.; Qiu, L.; Liu, W.; Wang, J.; Zheng, T. Genome-Wide Identification and Expression Profiling of the NCED Gene Family in Cold Stress Response of Prunus mume Siebold & Zucc. Horticulturae 2023, 9, 839. https://doi.org/10.3390/horticulturae9070839

AMA Style

Chen K, Li X, Guo X, Yang L, Qiu L, Liu W, Wang J, Zheng T. Genome-Wide Identification and Expression Profiling of the NCED Gene Family in Cold Stress Response of Prunus mume Siebold & Zucc. Horticulturae. 2023; 9(7):839. https://doi.org/10.3390/horticulturae9070839

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Chen, Ke, Xue Li, Xiaoyu Guo, Lichen Yang, Like Qiu, Weichao Liu, Jia Wang, and Tangchun Zheng. 2023. "Genome-Wide Identification and Expression Profiling of the NCED Gene Family in Cold Stress Response of Prunus mume Siebold & Zucc" Horticulturae 9, no. 7: 839. https://doi.org/10.3390/horticulturae9070839

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