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Article

Comparative Analysis of Transcriptomes to Identify Genes during Bud Dormancy of Pyrus pyrifolia ‘Huanghua’

by
Huiquan Wang
1,
Chunying Liu
1,
Qinghua Ye
1,
Yunyu Shen
1,
Shaohua Wu
2 and
Lizhong Lin
1,*
1
College of Horticulture and Forest, Fujian Vocational College of Agriculture, Fuzhou 350303, China
2
College of Horticulture, Fujian Agriculture and Forest University, Fuzhou 350000, China
*
Author to whom correspondence should be addressed.
Horticulturae 2024, 10(6), 619; https://doi.org/10.3390/horticulturae10060619
Submission received: 18 April 2024 / Revised: 26 May 2024 / Accepted: 3 June 2024 / Published: 10 June 2024
(This article belongs to the Section Genetics, Genomics, Breeding, and Biotechnology (G2B2))
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Abstract

:
The study of pear dormancy mechanisms is currently a major research area in pear production and has high economic significance for agricultural production. We selected the southern sand pear cultivar Pyrus pyrifolia ‘Huanghua’ as the test material to study the pear dormancy process through microscopic observation of pear flower buds. The endodormancy period is abbreviated as D_bud. Similarly, the endodormancy release initiation period and the ecodormancy period are referred to as DB_bud and G_bud, respectively. Meanwhile, RNA sequencing was used to obtain the gene expression profile of Pyrus pyrifolia ‘Huanghua’ flower buds. The RNA sequencing results indicated that there were 224 differentially expressed genes (DEGs) in endodormancy (D) vs. endodormancy release initiation period (DB), while 975 were identified between endodormancy and ecodormancy (G). Finally, a total of 868 DEGs were found in the DB vs. G comparison. The expression levels of the genes Pbr009498.1 (LAX1-1), Pbr012348.1 (LAX1-2), Pbr021158.1 (GH35), and Pbr031621.1 (LAX2) encoding IAA were significantly higher during the DB_bud than during the D_bud. The expression level of Pbr025864.2 (IAA13) during the D_bud was significantly higher than the DB_bud and G_bud. The Pbr041942.1 (GID1B) gene also showed a significant increase during ecodormancy. Taken together, these results suggest that these genes, annotated as LAX1, GH35, LAX2, IAA13, and GID1C, are involved in endodormancy maintenance and in the transition from endodormancy to ecodormancy in Pyrus pyrifolia ‘Huanghua’.

1. Introduction

Pear (Rosaceae: Pomoideae: Pyrus) produces delicious and nutritious fruits, making it the third most economically important temperate fruit variety after grapes and apples [1,2,3]. Pears are widely planted around the world. By 2020, the total area of pear cultivation in China reached 940,700 hectares, with a yield of 16.078 million tons. The annual cold storage capacity of pear fruits exceeds 5 million tons [4]. China is one of the three origin centers of pear cultivation in the world, with abundant pear germplasm resources and the largest cultivation area and yield in the world [5]. The pear varieties commonly cultivated in China include white pear, autumn pear, sand pear, Xinjiang pear, Western pear, and interspecific hybrid types. Huanghua pear (Pyrus pyrifolia Nakai cv. Huanghua) is an important subtropical fruit in China, widely cultivated in southern China [6].
The dormancy of buds in temperate deciduous fruit trees is an adaptive mechanism that enables them to survive under adverse winter conditions [7]. The three stages of dormancy are paradormancy, endodormancy, and ecodormancy [8]. Endodormancy is caused by the endogenous signals of plant dormancy and providing suitable environmental conditions for plant growth [9]. Paradormancy is caused by endogenous factors (such as the apical dominance phenomenon), and its growth inhibition state can be relieved by removing the influence of endogenous signals. Ecodormancy is induced by environmental factors, providing suitable environmental conditions for plant growth during the ecological dormancy period, which can restore normal growth [10]. In autumn, buds enter endophytic dormancy after the falling leaves and growth stop. At this stage, even under favorable environmental conditions, buds cannot grow. After a sufficiently low temperature, known as the cooling requirement (CR), internal dormancy will be interrupted, and the required temperature and duration of the CR depend on the species and variety [11]. However, if the CR is not met, such as during periods of climate change or global warming, internal dormancy will not be interrupted, and new organ growth will not occur in spring [12]. With increasing global climate warming, the average global temperature has risen by 0.74 °C in the past century, and it is expected to continue to rise in the future [13]. A survey shows that the annual average temperature in Fujian Province is gradually increasing every year, and the phenomenon of “warm winter” is frequent, which has a great impact on the agricultural and forestry production in Fujian Province [14]. Deciduous fruit trees, such as pears, have the biological characteristics of winter bud dormancy. Once they enter internal dormancy, insufficient cold demand will lead to obstacles in bud growth and development, affecting fruit yield and quality, and bringing huge challenges to the production and cultivation of fruit trees [15]. Research has found that many fruit trees growing in warm regions may experience problems such as delayed autumn phenology, uneven leaf expansion and flowering, and long flowering periods if there is insufficient cold accumulation in winter, which is not conducive to the sustainable production of fruit trees [16]. Nishitani et al. [17] performed a cDNA microarray to analyze the differences in internal and ecological dormancy of ‘Xingshui’ pear leaf buds and identified over 1000 differentially expressed genes, most of which are related to chloroplast, plastid function, electron transfer, and energy metabolism. Wu et al. [1] conducted whole genome sequencing of pears, providing strong support for the study of pear dormancy release. More research on bud dormancy both domestically and internationally is focused on the woody plant poplar, while research on dormancy of deciduous fruit trees mainly focuses on tree species such as grapes [18], peaches [19], sweet cherries [20], and apples [21], while research on pear trees is relatively scarce.
The release and dormancy of plants are controlled by multiple genes as well as environmental and internal factors [22]. The breaking of plant dormancy requires the coordination and interaction of multiple hormones. Abscisic acid (ABA) is a positive regulatory factor that induces plant dormancy and a negative regulatory factor for plant germination [23,24,25]. In many species, endogenous ABA is involved in inducing and maintaining plant dormancy [26]. Gibberellins (GAs) can release dormancy, promote germination, and antagonize ABA [27]. Dormancy release is also associated with declining sensitivity to indole-3-acetic acid (IAA) in wheat, enhancing IAA signaling or biosynthesis in Arabidopsis, and influencing IAA homeostasis in rice [28]. To date, several transcriptome studies have been conducted to reveal the molecular mechanisms of pear dormancy release. The construction of regulatory networks for regulating dormancy still needs further improvement. Since 2012, significant breakthroughs have been made in the molecular mechanisms of pear dormancy, mainly focusing on carbohydrates, dehydrating elements, and transcription factors such as DAM, but the mechanism of pear dormancy is still unclear. Therefore, studying and elucidating the physiological and molecular regulatory mechanisms of winter dormancy in pear flower buds in southern China not only has important biological significance for species survival and reproduction but also has important economic significance in agricultural production and cultivation. In this study, the lateral flower buds of the Pyrus pyrifolia ‘Huanghua’ were selected to analyze the dormancy process of sand pear at the morphological, physiological, and molecular levels. It explores the dormancy mode and mechanism of Pyrus pyrifolia ‘Huanghua’, aiming to provide a theoretical basis for the study of the dormancy mechanism of southern sand pear cultivars. In addition, differentially expressed genes were analyzed using RNA sequencing, and the function of hormone metabolism-related genes in the dormancy process was analyzed at the molecular level, laying the foundation for future research.

2. Materials and Methods

2.1. Plant Materials

Pyrus pyrifolia ‘Huanghua’ were planted in Jianning County, Fujian Province, China (26°50′28″ N, 116°48′09″ E, altitude 317 m). The pear trees were 10 years old and considered to be in the reproductive phase, with no chemical treatment or pruning during the sampling process. The flower buds of Pyrus pyrifolia ‘Huanghua’ were collected every 10 days from 17 December 2012 to 18 February 2013 and from 5 December 2013 to 27 February 2014. We selected 1-year-old branches that are healthy with no pests or diseases, which were wrapped in damp cloth. Then, we selected plump lateral flower buds to remove external scales and fuzz and fix the flower buds for paraffin sectioning at 4 °C using FAA fixative. Annual branches around the crown were collected for water insertion experiments. The endodormancy period is abbreviated as D_bud. Similarly, the endodormancy release initiation period and the ecodormancy period are referred to as DB_bud and G_bud, respectively.

2.2. Determination of Flower Bud Break Percentage and Respiration Intensity

In 2013 and 2014, the branches of Pyrus pyrifolia ‘Huanghua’ were collected for the water immersion experiment. We collected 15 branches each time and cut off both ends of the branches, leaving a length of 30–40 cm and 5–10 cm of bud-free parts at the base of the branches. At the same time, the branches were divided into three groups, with five branches in each group, and were inserted into a flask containing distilled water (with a depth of about 2 cm). The flask was placed in the intelligent artificial climate box, with a temperature of 25 ± 2 °C/(18 ± 2) °C day/night, 16 h/8 h of light (light/dark), and a relative humidity of about 70%. After 21 consecutive days of cultivation, the break percentage of pear flower buds was analyzed. Then, we used the GXH-3051C plant photosynthesis analyzer (Shanghai Shuangxu Electronics Co., Ltd, Shanghai, China) to measure the respiratory intensity of pear flower buds. We weighed about 10 g of pear flower buds each time, recorded the CO2 concentration during the measurement process, measured the temperature and airflow intensity, and the following formula was used to calculate the respiration intensity of pear flower buds:
Q ( mgCO 2   ×   kg − 1   ×   h − 1 ) = F × 60 × C 22.4   ×   44 w   ×   10 − 6   ×   273 273 + T

2.3. RNA Extraction and Library Preparation for RNA Sequencing

The extraction of total RNA from the flower buds of Pyrus pyrifolia ‘Huanghua’ was carried out using the Trizol method. Using flower buds from 7 January 2013 (endodormancy period), 22 January 2013 (endodormancy release initiation period), and 4 February 2014 (ecodormancy period) as experimental materials for RNA sequencing. During RNA extraction, an equal amount of flower buds was taken from each of the three repeated tubes for mixed extraction. The Agilent Bioanalyzer 2100 system (Agilent Technologies, Santa Clara, CA, USA) was utilized to detect the quality and integrity of RNA in the test sample.
Enrichment of mRNA was performed using Oligo (dT) magnetic beads according to the manufacturer’s instructions (Magen, Guangzhou, China). The mRNA was then divided into fragments by fragmentation buffer. A cDNA strand was synthesized using the mRNA template with six-base random hexamers, and then a two-strand cDNA was synthesized by adding buffer, dNTPs, and DNA polymerase I. AMPure XP beads were then used to purify double-stranded cDNA. The purified double-stranded cDNA was then end-repaired and added to tail A, and sequencing joints were connected. Finally, PCR enrichment was performed to obtain the final cDNA library. The constructed cDNA library was sequenced using Illumina HiSeqTM2000 (Novogen, Beijing, China). Using the pear (Pyrus × bretschneideri) genome as the reference genome (https://ftp.ncbi.nlm.nih.gov/genomes/all/GCF/019/419/815/GCF_019419815.1_Pyrus_bretschneideri_v1/, accessed on 30 July 2021). TopHat v2.0.9 was used as the alignment tool.

2.4. Differential Expression Gene Analysis

Differential expression analysis was performed using the DESeq R package (1.10.1). DESeq provided statistical routines for determining differential expression in gene expression data using a model based on the negative binomial distribution. The p-values were adjusted using the Benjamini and Hochberg approach for controlling the false discovery rate. Genes with an adjusted p-value < 0.05 found by DESeq were assigned as differentially expressed.

2.5. GO and KEGG Enrichment Analysis of Differentially Expressed Genes

Gene Ontology (GO) enrichment analysis of DEGs was implemented by the GOseq R package, in which gene length bias was corrected. GO terms with a corrected p-value less than 0.05 were considered significantly enriched by differentially expressed genes. KEGG is a database resource for understanding the high-level functions and utilities of the biological system, such as the cell, organism, and ecosystem (http://www.genome.jp/kegg/, (accessed on 1 May 2024). KOBAS software version 3.0 was used to test the statistical enrichment of differential expression genes in KEGG pathways.

2.6. Real-Time Fluorescence Quantitative PCR

qRT-PCR-specific primers were obtained by using Primer Premier 5. According to Takara Fluorescence Quantitative PCR Kit (TakaRa SYBR® PrimeScript™ RT reagent Kit Dalian, China), the total reaction volume was 20 µL, including 1 µL of diluted cDNA, 0.4 µL of upstream and downstream primers, 10 µL of SYBR® Premix Ex TagTM, and 8.2 µL of RNase-free ddH2O. Light Cycles® 480 (Roche, Munich, Germany) was used, and the reaction program was set according to the SYBR Premium Ex TaqTM manual. Each round of reaction was set with a negative control, and the experiment was repeated 3 times. Data analysis was performed using the 2−ΔΔCt method. PpActin (JN684184) was used as an internal standard gene.

2.7. Statistical Analysis

Data were input into SPSS 18.0 software to compare the differences according to Duncan’s multiple range test. A means separation was performed using the least significant difference test at p = 0.05.

3. Results

3.1. Physiological Indexes of Pyrus pyrifolia ‘Huanghua’ during Dormancy

As shown in Figure 1A, significant changes in temperature were observed during the nine sampling periods. The temperature showed an upward trend during the early stage of flower bud dormancy but decreased on 31 December 2013, and dropped to 6 °C on 8 January 2014. Subsequently, the temperature began to rise, but on 27 January 2014, a ‘late spring cold’ occurred, causing a sudden drop and reaching 2 °C on 19 February. Then, a study was conducted on the dormant state of flower buds of ‘Huanghua pear’ in 2013/2014 using in vitro branch culture. In Figure 1B, the break percentage of the flower buds of ‘Huanghuali’ was 0 on 5 December 2013, indicating that the flower buds were completely in the internal dormancy stage at this time. On 17 December and 25 December 2013, the break percentage reached 38.89% and 33.97%, indicating that the flower buds were in a transitional stage from endodormancy to ecodormancy. On 31 December 2013, the break percentage reached 88.55%, indicating that the flower buds had released their internal dormancy. In Figure 1C, the respiration rate of ‘Huanghua pear’ flower buds decreased sharply between 25 December and 8 January, which indicated that it is in the endodormancy period, and as dormancy progresses, the respiration rate of flower buds remains at a low level and shows a downward trend. From 8 January to 15 January, the respiratory rate rapidly increased and then sharply decreased, but on 21 January, the respiratory rate was higher than on 8 January. From 21 January to 27 January, the breathing rate tended to be stable. From 27 January to 27 February, the breathing rate began to show an upward trend again. On 8 January, it was the starting point for the release of dormancy, and the enhancement of life activities required energy consumption. Therefore, the respiratory rate began to increase on 8 January, and by 15 January, the flower bud dormancy was released, so the respiratory intensity also reached its maximum value. Subsequently, it entered ecodormancy, and the respiratory rate had little change. As the temperature rises and life activities increase, the respiratory intensity increases.

3.2. Histomorphological Analysis of Pear Buds during the Dormancy Process in 2012/2013 Year

The morphological features of the dormancy process of Pyrus pyrifolia ‘Huanghua’ flower buds in 2012/2013 were observed using microscopic techniques. In Figure 2, the flower buds in period A (17 December 2012) were still in the stage of morphological differentiation, and the stamen primordia can be found. During period B (26 December 2012), the stamen primordia were still visible, while the pistil primordia gradually elongated and grew. At stage C (7 January 2013), the stamen primordia differentiated and the spore primordia tissue became obvious. During period D (16 January 2013), the stamens were still in the state of sporogenous tissue, while there was no obvious growth or healing shape observed in the pericardial envelope. At stage E (22 January 2013), an upward and inward growth of the carpel was observed. In period F (28 January 2013), the volume of the stamen primordia has increased, and butterfly-shaped four/two chambered anthers have appeared. Sporous tissue is clearly visible, and the vascular bundle of the anther septum is slightly visible. It showed that the stamens are still in the sporulation stage and further differentiated, while the carpels of the pistils have healed to form the ovary and the ovule primordia have appeared in period G. The stamens have differentiated into pollen sacs, and the pollen mother cells begin meiosis to form diploids and tetrads, with scattered pollen grains appearing in stage H (18 February 2013). At this time, the carpels of the pistil have healed and formed a central placenta, indicating that each ovary contains two ovules.

3.3. Differentially Expressed Gene Analysis in Pyrus pyrifolia ‘Huanghua’

To understand the differences in gene expression during dormancy, it is necessary to identify DEGs between different stages. As shown in Figure 3A, the RPKM distribution of all genes was used to compare the gene expression levels in different groups. Among them, the raw reads of DB_bud, D_bud, and G_bud were 15,649,422, 17,329,672, and 15,162,263, respectively. Clean reads were 15,500,247, 17,151,297, and 15,162,263, accounting for 99.05%, 98.97%, and 99.02% of the total read segment data, respectively (Supplementary Table S1). Furthermore, the results indicated that there were 224 DEGs in D_bud vs. DB_bud, with 112 upregulated and 11 downregulated. Furthermore, a total of 975 DEGs were identified in D_bud vs. G_bud, of which 672 were upregulated and 303 were downregulated. A total of 868 DEGs were found in DB_bud vs. G_bud, of which 590 were upregulated and 278 were downregulated. Furthermore, the accumulation pattern of DEGs among different stages was visualized through a heatmap hierarchical cluster analysis (Figure 3B). Through the Venn plot (Figure 3C), it was found that there were 28 common differentially expressed genes among the three stages.

3.4. KEGG Functional Enrichment Analysis of Differentially Expressed Genes in Pyrus pyrifolia ‘Huanghua’

We further analyzed the functional involvement of the DEGs in different pathways by mapping them to the KEGG database. In Figure 4, the results showed that ‘Plant hormone signal transduction’ and ‘Protein processing in endoplasmic reticulum’ pathways were significantly enriched in DB_bud vs. D_bud. Meanwhile, the biosynthesis of secondary metabolites, plant hormone signal transduction, and flavonoid biosynthesis pathways were highly enriched in the G_bud vs. D_bud comparison. The biosynthesis of secondary metabolites, carotenoid biosynthesis, and galactose metabolism pathways were dominant in the G_bud vs. DB_bud comparison. Based on the KEGG database, the ‘Plant hormone signal transduction’ pathway was further mapped to analyze the hormone signaling pathway differential genes (Figure 5).

3.5. Expression Analysis of Differential Genes Related to Plant Hormone Metabolism in Pyrus pyrifolia ‘Huanghua’

By analyzing the plant hormone signaling pathways during the dormancy process of Pyrus pyrifolia ‘Huanghua’ flower buds, DEGs related to hormone metabolism were identified. In Figure 6, the expression levels of the genes Pbr009498.1 (LAX1), Pbr012348.1 (LAX1), Pbr021158.1 (GH35), and Pbr031621.1 (LAX2) encoding IAA were significantly higher in the endodormancy release initiation period (DB_bud) than the endodormancy period (D_bud). The expression level of Pbr025864.2 (IAA13) in the endodormancy period (D_bud) was significantly higher than the endodormancy release initiation (DB_bud) and the ecodormancy period (G_bud). The Pbr041942.1 (GID1B) gene also showed a significant increase during ecodormancy (G_bud), indicating that the expression of the GID1B gene is related to environmental conditions and promotes the progress of ecological dormancy. According to the RPKM values, there was a significant difference in the expression of genes PP2C24 (Pbr003841.1, Pbr018965.1) and PP2C08 (Pbr013576.1, Pbr022745.1) between the endodormancy initiation release and the endodormancy release period. These results indicated that the expression of the PP2C08 and PP2C24 genes encoding protein phosphatase has a significant impact on endodormancy release.

3.6. Expression Analysis of DEG in Pyrus pyrifolia ‘Huanghua’ by Real-Time PCR

In Figure 7 and Figure 8, a total of 8 DEGs, including MYBG, HSP21, P2C08, TIP21, APX1, DHN2, GASA4, and CCD31, were analyzed using real-time PCR. The results showed that the qPCR data and RNA seq data of 8 DEGs showed similar trends of change. Among the 8 DEGs, the expression levels of APX1 and CCD31 were significantly higher in the DB_bud than in the D_bud and G_bud. The expression levels of GASA4 and TIP21 were significantly higher in the G_bud than in the D_bud and DB_bud.

4. Discussion

The dormancy of temperate deciduous fruit trees is a strictly regulated survival strategy [29]. With global climate warming, the phenomenon of abnormal flowering of deciduous fruit trees due to insufficient cold demand is becoming increasingly apparent [30]. As an adaptive performance of deciduous fruit trees to resist external stress, dormancy has been increasingly studied in recent years [31,32]. The most important aspect of dormancy research is to determine the time for flower buds to enter and release internal dormancy, which is the basis for all subsequent studies [33,34]. At present, research on pear dormancy mainly focuses on the physiological stage of dormancy, and the internal molecular mechanism is still unclear, especially for the division of dormancy periods in the dormancy process, which has not formed clear standards. Therefore, we used Pyrus pyrifolia ‘Huanghua’ as the test material and divided the pear dormancy process through microscopic observation of pear flower buds. Furthermore, the respiratory rate and changes in endogenous hormones of pear flower buds during the dormancy process were explored. At the same time, RNA sequencing analysis was used to obtain the gene expression profile of Pyrus pyrifolia ‘Huanghua’ flower buds, exploring the molecular mechanism of pear flower bud dormancy.
Respiratory metabolism is the foundation of plant life activities [35]. Although the meristem tissue temporarily stops growing after pear flower buds enter dormancy, life activities still continue [36]. There is an inevitable connection between respiratory metabolism and the dormancy of pear flower buds. Through the study of respiratory metabolism during the dormancy process of Pyrus pyrifolia ‘Huanghua’ in 2013/2014, it was found that during the endodormancy stage, the respiratory rate gradually decreased with the progress of dormancy. At the critical point of releasing endodormancy, the respiratory intensity began to increase and reached its maximum value during the release of endodormancy, gradually decreasing. However, the lowest point after the decrease was higher than the respiratory intensity at the critical point of releasing dormancy. This indicates that once the endodormancy of the flower bud is released, the internal life activity of the pear flower bud is enhanced. Even when entering the ecological dormancy stage, the respiratory intensity will be higher than when the endodormancy is released. During the endodormancy stage, the intensity of respiratory metabolism shows an increasing and decreasing pattern, indicating that during ecodormancy, respiratory intensity is related to changes in external temperature. When flower buds begin to sprout, the metabolism of energy and substances in the plant increases, and respiratory intensity also begins to sharply increase.
In this study, a model for the dormancy process of flower buds of Pyrus pyrifolia ‘Huanghua’ was determined by analyzing the morphology of flower buds in different years, which can determine the period of dormancy and dormancy release. When the pear flower buds enter dormancy, they present a state where the carpels are wrapped in pairs, but they are not closed to form the ovary. The stamens differentiate to the sporulation stage, but the differentiation is not significant during the sporulation stage. This feature can serve as a marker for determining the dormancy of flower buds. Traditional theory suggests that dormancy is related to flower bud differentiation, and that phenomena such as irregular flowering in the following year were caused by incomplete flower bud differentiation [26]. However, in this study, the established model showed that dormancy is not related to flower bud differentiation, and the flowering situation in the following year is closely related to winter dormancy. Dormancy is the adaptive performance formed by plants to adapt to adverse external environments for a long time. A previous study suggested that dormancy is necessary for deciduous fruit trees, but the phenomenon of “secondary flowering” showed that dormancy is not necessary [37]. Therefore, this study suggests that deciduous fruit trees can still bloom without dormancy. However, if they encounter low-temperature damage after flowering, the flowers cannot develop normally. This further explains why the phenomenon of “secondary flowers” is more common only in the southern sand pear varieties, while it is not common in the northern white pear varieties.
In the present study, the results showed that ‘Plant hormone signal transduction’ and ‘Protein processing in endoplasmic reticulum’ pathways were significantly enriched in DB_bud vs. D_bud. Meanwhile, the biosynthesis of secondary metabolites, plant hormone signal transduction, and flavonoid biosynthesis pathways were highly enriched in the G_bud vs. D_bud comparison. The biosynthesis of secondary metabolites, carotenoid biosynthesis, and galactose metabolism pathways were dominant in the G_bud vs. DB_bud comparison. Based on the KEGG database, the ‘Plant hormone signal transduction’ pathway was further mapped to analyze the hormone signaling pathway differential genes. It was found that changes in endogenous hormones can regulate the dormancy process of Pyrus pyrifolia ‘Huanghua’ flower buds, and the main regulatory factors are GA3 and ABA. This study analyzed the signaling pathways of plant hormones and attempted to identify the molecular mechanisms by which endogenous hormones regulate the dormancy process of ‘Huanghua pear’ flower buds. This study found that the number of ABA, IAA, GA, and ZT-related genes was higher in the dormancy process of Pyrus pyrifolia ‘Huanghua’ flower buds. The expression of LAX1, GH35, LAX2, and GID1C genes promotes the release of endodormancy.
From Figure 7, it was found that the gene of TIP21 exhibits significant differences in expression across three stages, and TIP (vacuolar intrinsic protein) is a type of aquaporin (AQP) [38]. Currently, TIP genes have been studied in deciduous fruit trees, but research is still not in depth, only in grapes [39], peaches [40], and chestnuts [41]. It is believed that TIP genes regulate water transport within and between cells to regulate dormancy. At present, there are no reports on the regulation of dormancy by TIP in pears. However, TIP may have a regulatory effect on the dormancy process of Pyrus pyrifolia ‘Huanghua’ flower buds, but its regulatory mechanism needs further research. The APX1 gene is a gene encoding ascorbic acid peroxidase, and research on APX metabolism has been reported. Mazzitelli et al. [42] found that APX1 was upregulated during dormancy release in raspberries. Hussain et al. [43] found that the activity of the APX during the endodormancy stage shows a decreasing trend and gradually increases after the endodormancy release in pear buds of ‘Cuiguan’. In this study, it was also found that the expression level of the APX1 gene was upregulated during the critical period of dormancy release, indicating that the APX1 gene is involved in the release of dormancy in pear flower buds.
The expression of PP2C08 and PP2C24 genes related to ABA metabolism was significantly different, which can inhibit the release of endodormancy. The PP2C08 and PP2C24 genes have a more significant inhibitory effect on dormancy release. The expression of the IAA13 gene also inhibited the initiation of flower bud dormancy release [44]. Many studies have shown that although the content of IAA increases during dormancy release, it does not directly participate in the regulation of dormancy release, and IAA is not a necessary factor for bud dormancy release [45,46]. This conclusion has also been verified in this study, and the impact of IAA on pear flower bud dormancy release is relatively limited. In this study, differential gene analysis of IAA regulation revealed that the expression of LAX1 and LAX2 genes encoding auxin AUX1 transporter protein promoted the initiation of internal dormancy release, while the expression of the IAA13 gene encoding auxin responsive protein inhibited the initiation of flower bud dormancy release. Therefore, IAA has a regulatory effect on pear flower bud dormancy. GID1, as a receptor for gibberellin signaling transduction, plays an important role in the action of gibberellin and can regulate various physiological processes in plant growth and development, such as stem elongation, flower bud differentiation, and breaking dormancy [47,48,49]. In recent years, Falavigan et al. [50] found three genes related to GA signal transduction, GAST1, GRAS, and SCL, during the study of apple bud dormancy using transcriptome sequencing technology. The expression of the GID1C gene identified in this study promoted the initiation of dormancy release in pear flower buds, suggesting that the GA receptor protein gene is one of the key factors regulating gibberellin-induced dormancy release.

5. Conclusions

In this study, we established a pattern of pear dormancy through anatomical observation of the Pyrus pyrifolia ‘Huanghua’ flower bud morphology and identified the time periods for pear dormancy initiation and release. The respiratory intensity gradually decreased during the endodormancy stage and began to rise when the endodormancy was released. It reached its maximum when the endodormancy was released and decreased slightly after entering ecodormancy. Furthermore, the regulation of GA, ZT, IAA, and ABA metabolism-related genes is mainly involved in the dormancy process in the flower buds of Pyrus pyrifolia ‘Huanghua’. These results can be preliminarily determined as a fast and simple method for judging the dormancy process.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae10060619/s1, Table S1. The analysis of DEG sequencing data.

Author Contributions

Conceptualization, H.W. and L.L.; methodology, C.L.; formal analysis, Q.Y.; resources, Y.S.; data curation, S.W. and L.L.; writing—original draft preparation, H.W.; writing—review and editing, H.W. and L.L.; visualization, L.L.; supervision, L.L.; project administration, H.W. All authors have read and agreed to the published version of the manuscript.

Funding

Fujian Province science and technology plan guiding project (2021N0020); Special research fund for doctoral program of higher education institutions (20113515110011); Fujian Province science and technology plan key project (2012N005).

Data Availability Statement

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. Changes in temperature, break percentage, and respiratory rate during bud dormancy of Pyrus pyrifolia ‘Huanghua’ in 2013/2014. (A) Temperature; (B) break percentage; (C) respiratory rate. The letter (a, b, c, d) indicate the significant levels at 5% level, according to Duncan’s multiple range test.
Figure 1. Changes in temperature, break percentage, and respiratory rate during bud dormancy of Pyrus pyrifolia ‘Huanghua’ in 2013/2014. (A) Temperature; (B) break percentage; (C) respiratory rate. The letter (a, b, c, d) indicate the significant levels at 5% level, according to Duncan’s multiple range test.
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Figure 2. The pattern of the dormancy process and anatomical observation of the flower bud of Pyrus pyrifolia ‘Huanghua’ in 2012/2013. All sections were observed under a 10 × objective lens. GC: growth cone; CP: calyx primordia; SP: stamen primordia; CS: scaly bracts; PP: pistil primordia; R: flower receptacle; CT: calyx tube; C: carpel; PE: petal primordia; L: ovary; ST: sporous tissue; CO: drug partition; O: embryo; P: perianth; PG: pollen grains; FI: fiber layer. (A): The pattern of the dormancy process of Pyrus pyrifolia ‘Huanghua’. (B) The anatomical observation of the flower bud of Pyrus pyrifolia ‘Huanghua’. Ⓐ: 17 December 2012; Ⓑ: 26 December 2012; Ⓒ: 7 January 2013; Ⓓ: 16 January 2013; Ⓔ: 22 January 2013; Ⓕ: 28 January 2013; Ⓖ: 4 February 2013; Ⓗ: 18 February 2013.
Figure 2. The pattern of the dormancy process and anatomical observation of the flower bud of Pyrus pyrifolia ‘Huanghua’ in 2012/2013. All sections were observed under a 10 × objective lens. GC: growth cone; CP: calyx primordia; SP: stamen primordia; CS: scaly bracts; PP: pistil primordia; R: flower receptacle; CT: calyx tube; C: carpel; PE: petal primordia; L: ovary; ST: sporous tissue; CO: drug partition; O: embryo; P: perianth; PG: pollen grains; FI: fiber layer. (A): The pattern of the dormancy process of Pyrus pyrifolia ‘Huanghua’. (B) The anatomical observation of the flower bud of Pyrus pyrifolia ‘Huanghua’. Ⓐ: 17 December 2012; Ⓑ: 26 December 2012; Ⓒ: 7 January 2013; Ⓓ: 16 January 2013; Ⓔ: 22 January 2013; Ⓕ: 28 January 2013; Ⓖ: 4 February 2013; Ⓗ: 18 February 2013.
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Figure 3. The differentially expressed gene analysis in Pyrus pyrifolia ‘Huanghua’. (A) RPKM distribution; (B) The hierarchical clustering of DEGs. (C) Venn plot of differentially expressed genes among the three stages.
Figure 3. The differentially expressed gene analysis in Pyrus pyrifolia ‘Huanghua’. (A) RPKM distribution; (B) The hierarchical clustering of DEGs. (C) Venn plot of differentially expressed genes among the three stages.
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Figure 4. KEGG enrichment analysis of Pyrus pyrifolia ‘Huanghua’. (A) DB_bud vs. D_bud; (B) G_bud vs. D_bud; (C) G_bud vs. DB_bud.
Figure 4. KEGG enrichment analysis of Pyrus pyrifolia ‘Huanghua’. (A) DB_bud vs. D_bud; (B) G_bud vs. D_bud; (C) G_bud vs. DB_bud.
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Figure 5. The visualization of the ‘Plant hormone signal transduction’ pathway.
Figure 5. The visualization of the ‘Plant hormone signal transduction’ pathway.
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Figure 6. Analysis of differentially expressed genes in Pyrus pyrifolia ‘Huanghua’. (A) DEGs encoding IAA; (B) DEGs encoding GA; (C) DEGs encoding ABA; (D) DEGs encoding ZT.
Figure 6. Analysis of differentially expressed genes in Pyrus pyrifolia ‘Huanghua’. (A) DEGs encoding IAA; (B) DEGs encoding GA; (C) DEGs encoding ABA; (D) DEGs encoding ZT.
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Figure 7. The verification and analysis of DEGs by qPCR (MYBG, HSP21, P2C08, and TIP21).
Figure 7. The verification and analysis of DEGs by qPCR (MYBG, HSP21, P2C08, and TIP21).
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Figure 8. Verification and analysis of DEGs by qPCR (APX1, DHN2, GASA4, and CCD31).
Figure 8. Verification and analysis of DEGs by qPCR (APX1, DHN2, GASA4, and CCD31).
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Wang, H.; Liu, C.; Ye, Q.; Shen, Y.; Wu, S.; Lin, L. Comparative Analysis of Transcriptomes to Identify Genes during Bud Dormancy of Pyrus pyrifolia ‘Huanghua’. Horticulturae 2024, 10, 619. https://doi.org/10.3390/horticulturae10060619

AMA Style

Wang H, Liu C, Ye Q, Shen Y, Wu S, Lin L. Comparative Analysis of Transcriptomes to Identify Genes during Bud Dormancy of Pyrus pyrifolia ‘Huanghua’. Horticulturae. 2024; 10(6):619. https://doi.org/10.3390/horticulturae10060619

Chicago/Turabian Style

Wang, Huiquan, Chunying Liu, Qinghua Ye, Yunyu Shen, Shaohua Wu, and Lizhong Lin. 2024. "Comparative Analysis of Transcriptomes to Identify Genes during Bud Dormancy of Pyrus pyrifolia ‘Huanghua’" Horticulturae 10, no. 6: 619. https://doi.org/10.3390/horticulturae10060619

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