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Article

Genome-Wide Analysis and Expression Profiling of YUCCA Gene Family in Developmental and Environmental Stress Conditions in Tea Plant (Camellia sinensis)

by
Liping Zhang
1,†,
Shan Jin
2,†,
Peixian Bai
1,
Shibei Ge
1,
Peng Yan
1,
Zhengzhen Li
1,
Lan Zhang
1,
Wenyan Han
1,
Jianming Zeng
1,* and
Xin Li
1,*
1
Key Laboratory of Tea Quality and Safety Control, Ministry of Agriculture and Rural Affairs, Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou 310008, China
2
Key Laboratory of Tea Science in Universities of Fujian Province, College of Horticulture, Fujian Agriculture and Forestry University, Fuzhou 350002, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2023, 14(11), 2185; https://doi.org/10.3390/f14112185
Submission received: 24 August 2023 / Revised: 15 October 2023 / Accepted: 23 October 2023 / Published: 2 November 2023
(This article belongs to the Special Issue Strategies for Tree Improvement under Stress Conditions — 2nd Edition)
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Abstract

:
The tea plant is a perennial leaf-used economical crop and cultivated all over the world. Indole-3-acetic acid (IAA) plays key roles in plant development and environmental stress. YUCCA (YUC) flavin monooxygenases are the rate-limiting enzymes of the TAA/YUC pathway, which is the most important IAA biosynthetic pathway in plants. The YUC gene family in tea plants has not been systematically studied so far. A total of 17 CsYUC members were identified from a tea plant genome database and phylogenetically classified into three subfamilies. Phylogenetic analysis showed that the CsYUC gene family is evolutionarily conserved. The physical and chemical properties, gene structures, and conserved domains were analyzed. The expression profiles of CsYUCs were analyzed on the basis of open available RNA-seq data, as well as by RNA-seq and qRT-PCR assays. Combined with previous studies, it can be concluded that YUC10 may play key roles in seed development. The results also showed that CsYUC2.1 may play important roles in the coordinated regulation of the growth of leaf buds and flower buds induced by pruning. Low temperature markedly induced the expression of CsYUC2.2, -11.8, and -11.9. Furthermore, CsYUC genes that might play key roles in the specific development stages and involve enhancing the resistance to drought and NaCl stress were screened, respectively. This study could provide a research basis for deeply studying the gene functions of the CsYUC family in the tea plant.

1. Introduction

Auxin is a kind of endogenous plant hormone that affects every process of plant development and environmental stress [1,2,3]. The auxin pathway depends on its gradient within tissues and cells [4], and auxin synthesis occurs at both local and distant sites [3]. IAA is the richest and most predominant auxin in plants [5,6,7]. In plants, the central IAA biosynthetic pathway is the indole-3-pyruvic acid (IPyA) pathway (i.e., TAA/YUC pathway), which is essential for almost all the major developmental processes in plants [7,8,9]. YUCCA (YUC) enzymes catalyze the rate-limiting second step in the TAA/YUC pathway, which converts IPyA into IAA, and belong to a class of flavin-containing monooxygenases (FMOs) [1,9,10,11].
In higher plants, the YUC genes are widespread and characterized [1,5]. A wealth of studies have suggested that the functions of YUC family genes are conserved among various plants [4,12,13]. To date, 11, 14, 22, 14, 12, 20, 8, and 13 YUC genes have been identified in Arabidopsis [4], rice [1], soybeans [1], maize [13], Populus [14], apples [3], Solanum tuberosum [15], and I. indigotica [16], respectively. YUC genes play key regulatory roles in multiple developmental processes, as well as environmental stresses [5,14]. For example, OsYUC1, -3, -6, and -7 played regulatory roles in the development of the shoot, root, and panicle of rice [1]. The specific repression of FvYUC6 expression by RNA interference significantly inhibited the vegetative growth of woodland strawberries [17]. On the other hand, YUC-mediated IAA biosynthesis in many tissues enhances the resistance of plants to high-temperature stress [3,4,7]. Under low temperature and salinity stress, CsYUC10b transcripts were remarkably upregulated in cucumbers [5].
The tea plant (Camellia sinensis) is a perennial crop and grows widely all over the world, and it is seriously affected by various environmental stress conditions, including high salinity, drought, temperature stress, etc. [18]. IAA metabolism regulates the development of tea plants and is essential for its adapting to environmental stresses [2,4]. For example, the transcriptional levels of CsYUC1 decreased gradually during the developmental processes of tea leaves [2]. However, studies on CsYUC genes in tea plants are limited and genome-wide studies of CsYUC genes have never been performed thus far.
In the current study, we identified 17 CsYUC genes in the genome database of the tea cultivar (cv.) Longjing 43 (LJ43). The phylogenetic relationships, as well as conserved motifs and domains of the CsYUC genes, were systematically analyzed. Moreover, based on the Short-Read Archive (SRA) database in the NCBI and through RNA-seq and qRT-PCR assays, the expression profiles of these CsYUCs in different tissues, during several development processes and in response to environmental stresses of tea plants, were explored. The results suggested that CsYUC genes have different expression patterns in different processes. Furthermore, some CsYUC genes that play important regulatory roles in tea plants were preliminarily screened. This study indicated the potential functions of CsYUC genes in regulating development and enhancing the stress resistance of tea plants. The results could provide a theoretical basis for further investigating the functions of CsYUC genes in the tea plant.

2. Materials and Methods

2.1. Identification of Tea CsYUC Genes

Using the amino acid sequences of Arabidopsis AtYUC as queries (Table S1), a local BLASTP was executed to search the YUC proteins in the genome database of tea cv. LJ43 [19]. A total of 17 CsYUC genes were retrieved. For the obtained CsYUC numbers that contained abnormal protein sequences, the homologous genes in other plant species and tea varieties were searched, respectively, through blasting the NCBI (https://www.ncbi.nlm.nih.gov/, accessed on 5 September 2022), UniProt database (https://www.uniprot.org/, accessed on 5 September 2022), and the database of multiple tea varieties (http://www.teaplant.top/teagvd) accessed on 5 September 2022.
For the homologous genes obtained from the above three databases, multiple sequence alignment was carried out to correct or eliminate the CsYUC numbers that contained abnormal sequences. Next, the CsYUC sequences were submitted to the NCBI CD search program (https://www.ncbi.nlm.nih.gov/Structure/cdd/wrpsb.cgi, accessed on 5 September 2022) to obtain the conserved domains in the candidate proteins, and visualization was carried out using TBtools software of the lastest version then [20]. The obtained putative CsYUC sequences were submitted to the Pfam database, the Conserved Domain Database, and SMART database to confirm the presence of domain signatures.

2.2. Multiple Sequence Alignment and Phylogenetic Analysis

The full-length amino acid sequences of 17 CsYUCs and 11 AtYUCs were used to study the phylogenetic relationships among them. Multiple sequence alignments of tea CsYUCs with the Arabidopsis orthologs were performed by MUSCLE in MEGA 7.0. The alignment and manual adjustments were carried out. A phylogenetic tree was constructed with the 1000 bootstrapped maximum likelihood (ML) method [21].

2.3. Gene Structure and Conserved Motifs Analysis of CsYUC Numbers

For studying the structure and conservation of the CsYUC genes, the exon–intron structures were analyzed using the TBtools program. The conserved motifs were identified using the MEME online tool. Next, the conserved motifs and domains were visualized using TBtools [20].

2.4. Physical and Chemical Properties Analysis of CsYUCs

The predicting methods of the physicochemical properties of the CsYUC proteins were described in our previous report [22].

2.5. Analysis of Cis-Acting Elements in the Promoter Regions of CsYUC Genes

The 2000 bp upstream of the initiation codons of the CsYUC numbers were analyzed. The possible cis-acting elements, which are responsible for developmental and environmental stress regulations of CsYUC gene expression, were identified using the PlantCARE database, and the identified cis-acting elements were classified and visualized using TBtools [20].

2.6. Open Available RNA-Seq Data Analysis

To study the expression patterns of CsYUCs during multiple development processes and under environmental stresses, the raw data were downloaded from the NCBI SRA database. The methods of the filtration of low-quality raw sequences and the standardization of the transcripts per kilobase million (TPM) were described in our previous report [22]. The downloaded data were remapped back onto the genome of LJ43 when needed. The expression levels of CsYUCs were plotted on a log2 scale. Heat maps were established based on their TPM values using TBtools software.

2.7. RNA-Seq and qRT-PCR Detection

For the pruning experiment, the materials and methods were described in our previous report [22]. In early July, uniform and healthy tea twigs of cv. LJ43 were sampled from the tea garden, and the ends of the twigs were submerged in distilled water. Subsequently, the twigs were used for 3 kinds of stress treatments.
For the drought treatment, the ends of the twigs were immersed in 12.5% PEG for 24 h.
For the low-temperature treatment, the twigs were put under 4 °C for 3 h and were put under room temperature for 3 h subsequently to recovering.
For the NaCl treatment, the ends of the tea twigs were immersed in 250 mM NaCl solution for 24 h.
For the above experiments, the first and second leaves from the top of the branch were sampled for RNA extraction. Total RNA extraction, reverse transcription, and the qRT-PCR assay were performed according to our previous study [22].

2.8. Statistical Analysis

The analysis methods of the qRT-PCR data were described in our previous report [22].

3. Results and Discussion

3.1. Identification and Bioinformatics Analysis of the CsYUC Gene Family in Tea Plants

To identify CsYUC family members in tea plants, a BlastP search of the genome database of LJ43 was conducted using the annotated amino acid sequences of Arabidopsis AtYUC proteins in the TAIR as queries. The E-value was set to 1 × 10−5 (the sequences of the AtYUCs and CsYUCs are shown in Table S1). A total of 17 unique CsYUC members with confirmed conserved domains were identified after manual filtering and merging. The CsYUCs were named based on the phylogenetic relationships with the Arabidopsis homologs. To be specific, they were named from CsYUC1 to CsYUC11 (CsYUC1 (one copy), CsYUC2 (three copies), CsYUC6 (one copy), CsYUC7 (one copy), CsYUC8 (one copy), CsYUC10 (one copy), and CsYUC11 (nine copies)) (Figure 1 and Table 1). Based on the genome data, the genetic mapping of CsYUC genes on the chromosomes was investigated. The 17 CsYUC genes were located on eight chromosomes, with CsYUC11.8 and -11.9 located on Chr02; CsYUC11.4 located on Chr03; CsYUC2.2, -2.3, -11.1, -11.2, -11.3, and -11.7 located on Chr06; CsYUC7 located on Chr09; CsYUC8 and -10 located on Chr11; CsYUC1, -6, and -11.6 located on Chr12; CsYUC2.1 located on Chr14; and CsYUC11.5 located on Chr15 (Figure S1 and Table S2). It should be noted that CsYUC11.8 and -11.9 (located on Chr02), CsYUC11.1 and -11.2 (located on Chr06), and CsYUC2.2 and -2.3 (located on Chr06) were very close to each other, and whether they might have similar biologic functions needs to be confirmed.
Detailed information on the identified CsYUCs is listed in Table 1. The CDS lengths of the CsYUCs ranged from 885 (CsYUC11.4) to 2685 bp (CsYUC11.5), encoding peptides ranging from 295 to 894 amino acids. The expected MS ranged from 33.36 to 102.27 kDa. The pI ranged from 5.79 to 9.1. Among them, one was neutral, eight were acidic, and eight were basic in nature.
The grand average of hydropathy (GRAVY) of the CsYUCs varied from −0.345 to −0.027, indicating that they are hydrophilic in nature [23]. There were 5 CsYUCs, including CsYUC2.1, -2.3, -10, -11.5, and -11.8, which instability index were below 40, indicating that they were relatively stable, whereas the instability index of the other 12 CsYUCs exceeded 40 (41.15–50.07). The aliphatic index of the globular proteins might be regarded as a positive factor in the increase of their thermal stability. Here, the aliphatic index of the 17 CsYUCs was from 77.32 to 92.37 (Table S2). The analysis of the subcellular localization of the proteins could help to understand their variable functions. The prediction results showed that CsYUC1 and -11.1 might be localized in the nucleus; CsYUC2.1, -2.2, -6, -7, -11.2, -11.3, and -11.5 might be localized in the cytosol; CsYUC2.3, -11.4, and -11.6 might be localized in the chloroplast; CsYUC8 might be localized in the plasma membrane; and CsYUC10, -11.7, -11.8, and -11.9 might be localized in the endoplasmic reticulum. The prediction results showed that none of the CsYUCs had signal peptides.

3.2. Multiple Sequence Alignment and Phylogenetic Analysis of the CsYUC Gene Family

To reveal the evolutionary relationships of the CsYUC gene family, multiple sequence alignment of the 17 CsYUCs and their homologs in Arabidopsis was performed (Figure S2), and a phylogenetic tree was constructed. The results suggested that the CsYUC genes were grouped into three clades according to their phylogenetic relationships with Arabidopsis YUC proteins. Similar to those in rice and strawberries, the first clade is the biggest and consists of 8 CsYUCs and 11 AtYUCs (Clade I) [5]. The second clade is made exclusively of 4 CsYUCs (II), while there are 5 CsYUCs in the third clade (III). Homologs of Arabidopsis YUC3, -4, -5, and -9 were not found in the tea plant (Figure 1). YUC11 was expanded in the tea plant, which contained nine CsYUC11 members. This is similar to that in apples and white pears, which contain six and seven YUC11 members, respectively [3].

3.3. Gene Structure and Conserved Domain Analysis of CsYUC Genes

Structural diversity in gene families implies the possibility of their functional diversification. The exon–intron structure among the genes in the same group, especially homologs, was relatively conservative [1,14]. In order to illustrate the structural diversity of the CsYUC family, an exon–intron organization was visualized from the coding sequences of the CsYUC genes. The results showed that, in branch I, CsYUC7 and -8 both have three exons, respectively. CsYUC1, -2.1, -2.2, -2.3, and -6 all have four exons, respectively. CsYUC10 has five exons. Furthermore, the lengths of the first three introns of CsYUC10 are much longer than those of the other seven CsYUC genes in branch I. In branch II, CsYUC11.1 has four exons, and CsYUC11.2 and -11.3 both have five exons, respectively, whereas CsYUC11.4 has three exons. In branch III, the exon numbers of the five CsYUC genes are all significantly higher than those of the CsYUCs in the other two branches. To be special, CsYUC11.5 has 14 exons, and CsYUC11.6, -11.8, and -11.9 all have 7 exons, while CsYUC11.7 has 15 exons. Furthermore, the lengths of the seventh and ninth introns of CsYUC11.5 and the sixth intron of CsYUC11.7, as well as the fifth intron of CsYUC11.9, are much longer than the other introns of the CsYUCs in branch III (Figure 2A).
The conserved motifs in the 17 CsYUCs were analyzed with the MEME program (http://meme.nbcr.net/, accessed on 5 September 2022). A total of 10 distinct motifs were found. In branch I, CsYUC proteins share common motif profiles. To be specific, except for CsYUC2.3 and -10, the other six CsYUCs all contain nine conserved motifs, and their locations in the six protein sequences are nearly identical. However, CsYUC2.3 and -10 contain seven and eight motifs, respectively. Compared to the other six CsYUCs, which all contain nine conserved motifs, CsYUC2.3 lacks motifs 2 and 8, while CsYUC10 lacks motif 7. In branch II, the four CsYUCs all contain four conserved motifs, respectively. They all contain motifs 1, 8, and 9, and the motifs in CsYUC11.2 and -11.3 are exactly the same. In branch III, the five CsYUCs all have the same kinds of motifs, namely motifs 1, 5, 6, 8, and 9. In CsYUC11.5 and -11.7, the number of motifs 1, 5, 6, and 9 are all two, while their numbers in the other three proteins are all only one (Figure 3A). The above results suggest that the closely related proteins share common motif profiles in terms of the number and type of the motifs. Motif 9 is unique to branches II and III, suggesting functional conservation among the CsYUC proteins within the same branch. This is consistent with previous reports, which have suggested that the motifs that are specific to each branch may contribute to group-specific functions [14,16].
The conserved domain of the identified CsYUC proteins was analyzed using TBtools. From Figure 3B, we can see that all of the CsYUCs contain the conserved flavin-binding monooxygenase (FMO) domain, including one FMO-like domain, two FAD-binding domains (FAD_binding_2 and FAD_3), and two NAD-binding domains (NAD_binding_8 and _9). There are 11 CsYUC proteins that contain the NAD_binding_8 domain, including CsYUC2.1, -2.2, -6, -11.1, -11.2, -11.4, -11.5, -11.6, -11.7, -11.8, and -11.9. Previous reports have suggested that the FMO domain can bind FAD and NADPH, and these are its most prominent characteristics [8]. Thus, the FMO domain, acting as the FAD- and NADPH-binding sites, is essential for YUC enzymatic activities [3]. Here, except for CsYUC11.8, the sequences of the other 15 CsYUCs all possessed a common conserved FMO-like domain located near the C-terminus.

3.4. The Cis-Acting Elements of CsYUC Genes

The cis-acting elements could regulate gene expression by controlling the efficiency of its promoters; thus, identification of the cis-acting elements can contribute to the studies of gene function [22]. Here, the results suggested that the light-responsive cis-elements were prominent in all elements and common to all CsYUC genes. In plants, they may modulate endogenous auxin accumulation under different light conditions. The second are hormone-responsive elements, including abscisic acid (ABA)-, salicylic acid (SA)-, auxin-, methyl jasmonate (MeJA)-, and gibberellin-responsive elements. For example, ABA-responsive elements were present on the promoters of CsYUC1, -2.2, -2.3, -6, -7, -8, -10, and -11.5. On CsYUC promoters, there were two kinds of environmental stress-responsive elements, including low-temperature and drought. ABA- and MeJA-responsive elements were found only in members of subfamilies I and III, while low-temperature elements were found only in members of subfamilies I and II (Figure 2B and Table S3).

3.5. Expression Profiles of the CsYUC Family Numbers in Tea Plants

IAA is mainly synthesized through the TAA/YUC pathway, in which the YUC enzyme is a rate-limiting enzyme [24]. Considering that gene expression patterns generally contribute to biological functions, the analysis of RNA-seq data in the SRA database, as well as RNA-seq and qRT-PCR assays, was conducted to investigate CsYUC expression profiles in multiple tissues and different developmental processes, as well as under several environmental stress conditions.
In the heat maps here, simultaneous usage of the color and circle size could show the gene expression levels more clearly; however, it could not distinguish the expression level of zero and the undetected expression. Thus, another type of heat map containing the expression values was drawn and put in the Supplementary Materials. The combined analysis of the two types of heat maps could illustrate the expression levels of CsYUC genes more clearly [20].

3.5.1. CsYUC Gene Expression Analysis during the Development Processes of Tea Plants

Local auxin biosynthesis plays important roles in the major developmental processes of plants [4,14,16]. RNA-seq datasets were downloaded from the SRA database for studying CsYUC expression in different tissues and during several development processes: (1) the expression of CsYUC genes in different tissues and during leaf development and senescence (accession number of raw RNA-seq data: SRP034436) [12], and (2) CsYUC transcription during the process of flower development. The flowers of cv. Ruixue at three stages were harvested on the same day (SRR5487527 to SRR5487532) [25].

Expression Profiles of CsYUCs in Different Tissues

The expression of YUC in plant tissues suggested its involvement in the development of specific tissues [1,3]. Here, the RNA-seq data from SRA database were analyzed for the tissue specific expression of CsYUC genes in five tissues, including root, stem, mature leaf, flower, and seed.
The results showed that the expression profiles of CsYUCs varied widely in the five tissues. CsYUC10 and -11.6 both had the highest transcript level in the flower and seed. CsYUC11.1 and -11.2 both had higher transcript levels in the stem and seed. CsYUC1 and -11.5 both had the highest expression in the seed and the lowest expression in the flower. CsYUC11.3 and -11.7 both had the highest expression in the seed and the lowest expression in the stem. CsYUC11.8 and -11.9 both had the highest expression in the root, followed by that in the seed, as compared to that in other tissues. CsYUC2.1 had the highest and lowest expression in the flower and root, respectively, and CsYUC8 had the highest and lowest expression in the stem and mature leaf, respectively. CsYUC6 expression in the root and seed was relatively higher than that in the other three tissues (Figure 4A and Figure S3A). To summarize, the above results suggested that CsYUC2.1, -10, -11.4, and -11.6 were highly expressed in the flower. Eleven CsYUC genes, including CsYUC-1, -6, -10, -11.1, -11.2, -11.3, -11.5, -11.6, -11.7, -11.8, and -11.9, were highly expressed in the seed. CsYUC-8, -11.1, and -11.2 were highly expressed in the stem. CsYUC-6, -11.8, and -11.9 were highly expressed in the root. CsYUC11.4 was highly expressed in the mature leaf.
Xia et al. [24] reported that AtYUC2 promoter activity was observed in mature leaves of Arabidopsis. Here, compared to the other CsYUC numbers, CsYUC-2.1, -2.3, -6, -10, -11.4, and -11.6 had higher expression levels in mature tea leaves. Yang et al. [1] reported that, in wheat, TaYUC1A, -2, -7D, -8B, -2A, -2B, and -2D were highly expressed in roots. Here, CsYUC6, -11.8, and -11.9 were highly expressed in the roots of tea plants. There were 11 CsYUC genes, including CsYUC-1, -6, -10, -11.1, -11.2, -11.3, -11.5, -11.6, -11.7, -11.8, and -11.9, which were highly expressed in seeds. Consistent with this, Yang et al. [1] reported that TaYUC10.3 was specifically expressed in young seeds of transgenic wheat. Zheng et al. [26] reported that a YUC10 homolog was preferentially expressed in Arabidopsis seeds. Thus, it can be concluded that YUC10 may play key roles in the seed development of many plants. In addition, the results showed that CsYUC2.1, -10, -11.4, and -11.6 were highly expressed in the flowers. Xia et al. [24] reported that AtYUC6 promoter activity was mainly in the stamens and pollen of Arabidopsis. Yang et al. [1] reported that AtYUC1, -2, -4, and -6 were mainly expressed in the inflorescence apex and flowers. In addition, CsYUC8, -11.1, and -11.2 were highly expressed in the stem, indicating their importance in stem development.
In summary, the results here showed that CsYUC2.3 was only expressed in the mature leaf and flower, CsYUC11.4 was predominantly expressed in the mature leaf, flower, and seed, while CsYUC7 was only expressed in the root. The FLOOZY (FZY) gene, an ortholog of Arabidopsis YUC1, was expressed in young leaves and developing flowers in petunias [3]. Here, CsYUC1 was only expressed in the stem, flower, and seed. In apples, MdYUC2b, -11b, and -11d may be mainly responsible for auxin synthesis in flower organs [3]. Here, the expression levels of CsYUC10 and -11.6 in the flower and seed were significantly higher than that in the other three vegetative tissues.

The Regulatory Roles of CsYUC Genes in Tea Leaf Development

We analyzed CsYUC expression in tea leaves from our development stages using two sets of RNA-seq data from the SRA database. The results showed that CsYUC10 expression showed a trend of decreasing first and then increasing, whereas CsYUC11.6 expression showed an increasing trend. CsYUC1, -2.1, and -11.5 were highly expressed in the first and second leaves, while CsYUC8 was highly expressed in the first leaves. The transcription of CsYUC7 and -11.9 both showed an increasing trend in the first two stages, while they both were zero in the last two stages. CsYUC11.3 and -11.4 were both highly expressed in the mature leaves, followed by that in the old leaves (Figure 4B and Figure S3B). The above results showed that CsYUC1, -2.1, -7, -8, -11.5, and -11.9 all play key regulatory roles in the early stage of leaf development, while CsYUC11.3 and -11.4 may play key roles in the process of tea leaf maturation and senescence.
The analysis of other RNA-seq data showed that, compared to the other stages, CsYUC2.2 expression was the highest in the third and mature leaves, and CsYUC2.3 expression was the highest in the mature leaves. In the last four stages, CsYUC1 expression showed a trend of decreasing first and then increasing, and the highest expression was observed in the second leaves. With leaf development, the expression of CsYUC2.1, -7, -8, and -11.9 all showed a trend of gradually decreasing (Figure 4C and Figure S3C). The above results suggest that CsYUC1, -2.1 -7, -8, and -11.9 play key roles in the early stage of tea leaf development, while CsYUC2.2 and -2.3 play key regulatory roles in the process of tea leaf maturation and senescence.
In summary, the above two sets of RNA-seq data showed that CsYUC1, -2.1, -7, -8, -11.5, and -11.9 play key roles in the early stage of tea leaf development, while CsYUC2.2, -2.3, -11.3, and -11.4 play key roles in the process of tea leaf maturation and senescence. It is noteworthy that two sets of RNA-seq data both suggested that CsYUC1, -2.1, -7, -8, and -11.9 play key roles in the early stage of leaf development. Consistent with our results, Wang et al. [2] reported that CsYUC1 transcription gradually decreased during tea leaf growth and ripening. Yang et al. [1] reported that OsYUC1 overexpression inhibited leaf growth. Xia et al. [24] reported AtYUC2 promoter activity was observed in young leaf primordia and mature leaves of Arabidopsis. Here, CsYUC2.1 played key roles in the early stage of leaf development, and CsYUC2.2 and -2.3 played a key regulatory role in the process of leaf maturation and senescence. Additionally, numerous studies have shown that delayed leaf senescence was observed in a dominant activation Arabidopsis mutant yuc6-1D and the 35S:YUC6 transgenic plants of tobacco and Arabidopsis [3,16,27]. However, CsYUC6 expression showed no obvious changes during leaf development here.

The Roles of CsYUC Genes in Tea Flower Development

Auxin plays important roles in floral organ development [3]. For example, the phenotypic analysis of an Arabidopsis yucca1/2/4/6 quadruple-mutant and a cucumber yuc1 yuc4 mutant showed that YUC1, -2, -4, and -6 were important in flower development [1,5]. FvYUC6 overexpression delayed flowering in woodland strawberries [3,17]. YUC11 has specific roles in flower development [3], and GmYUC5 plays important roles in the flower development of Arabidopsis [14]. The expression of the SPI1 gene, a homolog of AtYUC1, is essential for maize inflorescence development [28].
Here, the expression patterns of the CsYUCs were analyzed in the process of flower development using RNA-seq data in the SRA database. The results suggested that CsYUC2.1 expression decreased from S1 to S2. From S2 to S3, CsYUC1 expression elevated, whereas CsYUC11.3 expression decreased. During the three stages, the expression of CsYUC11.8 and -2.3 both showed a tendency to decrease and then increase, and they both showed the highest expression at the S1 stage. During the three stages, the expression of CsYUC2.2, -6, and -11.9 all gradually decreased, whereas CsYUC8 expression gradually increased (Figure 5A and Figure S4A).
In summary, CsYUC2.1, -2.2, -6, and -11.9 played roles in the early stages, and CsYUC1 and -11.3 played roles in the later stages, whereas CsYUC2.3, -8, and -11.8 played key roles in the three stages of flower development. Consistent with our results, Xia et al. [24] reported that AtYUC1 was expressed in the floral organs at the later stages of Arabidopsis flower development.

The Regulatory Roles of CsYUCs in the Lateral Bud Development of Tea Plants Induced by Pruning

Previous reports have suggested that locally synthesized auxin could promote bud outgrowth [27,28]. In late July, the typical lateral bud of tea plants contains a leaf bud (LB) in the middle and two flower buds (FBs) on both sides. Our previous study suggested that, compared to the control, pruning broke the dormancy and promoted the growth of LBs, whereas it depressed the growth of FBs simultaneously [22]. Here, RNA-seq analysis was carried out for CsYUC expression in FBs and LBs at 3 d after pruning. The results showed that, in FBs, compared to the control, except for CsYUC2.3 and -8, which expression was undetected, the expression of the other fourteen CsYUCs all significantly decreased. In LBs, compared to the control, the expression of CsYUC2.1 and -11.5 both significantly increased, whereas the expression of the other twelve CsYUCs, including CsYUC-1, -6, -7, -8, -10, -11.1, -11.2, -11.3, -11.6, -11.7, -11.8, and -11.9, all significantly decreased (Figure 5B and Figure S4B).
The transcription of the CsYUCs was also detected through qRT-PCR. The results showed that, after pruning, in FBs, the expression of CsYUC1 and -2.1 both significantly decreased at 7 and 14 d, respectively. At 7 d, the expression of CsYUC2.2, -2.3, and -11.7 decreased 85.7, 91.0, and 82.7%, respectively. The expression of CsYUC7, -11.2, and -11.9 all significantly decreased at the three time points. The expression of CsYUC11.1, -11.3, -11.5, and -11.8 all significantly decreased at 3 d and 7 d. The expression of CsYUC8 and -11.4 decreased at 3 d and 7 d, whereas they increased 159.5 and 41.4%, respectively, at 14 d. At 3 d, CsYUC11.6 expression increased 95.3% (Figure 6). In LBs, the expression of 10 CsYUCs, including CsYUC1, -2.2, -10, -11.1, -11.2, -11.3, -11.5, -11.6, -11.7, and -11.9, all significantly decreased at 3 and 7 d. The expression of six CsYUC genes, including CsYUC2.1, -2.3, -7, -8, -11.4, and -11.8, all significantly decreased at 3 and 7 d, whereas they increased 424.6, 146.4, 210.1, 143.9, 83.5, and 294.0%, respectively, at 14 d. CsYUC6 expression decreased 65.9% and increased 204.2% at 7 and 14 d, respectively (Figure 7).
In summary, the above results of RNA-seq suggested that, at 3 d after pruning, the decreased expression of the vast majority of CsYUC genes may inhibit the growth of FBs through decreasing the endogenous IAA content. Meanwhile, the increased expression of CsYUC11.5 and -2.1 may promote the growth of LBs. The results of the qRT-PCR suggested that, 14 d after pruning, the decreased expression of most of the CsYUC genes might inhibit the growth of FBs. Meanwhile, the increased expression of seven CsYUC genes, including CsYUC2.1, -2.3, -6, -7, -8, -11.4, and -11.8, at 14 d might promote the growth of LBs. Consistent with our results, previous studies have also reported that YUC genes play key regulatory roles in the development of plant lateral buds. For example, the maize sparse inflorescence1 (ZmSPI1) gene is a homolog of the AtYUC1 gene. The maize spi1 mutant has defects in lateral organs initiation during both vegetative and inflorescence development [13,28]. Similarly, Song et al. [3] reported that a YUC-like gene mutant sparse inflorescence of maize showed defects in the formation of branches, spikelets, florets, and floral organs.

3.5.2. The Expression of CsYUC Numbers under Several Environmental Stress Conditions

Environmental stresses cause severe damage to plants and negatively impact their growth and development [7]. Previous studies have shown that plant YUC genes play potential regulatory roles in stress responses [5,14,16]. For example, in Isatis indigotica, the IiYUC6-1 gene was sensitive to NaCl, PEG, and cold treatments. C. sativus CsYUC10b was sensitive to low temperature and salt stress. GmYUC5 and -8 were sensitive to drought, temperature, and salt stress [16]. TaYUC1A, -2B, -3A, -6A, -10.1, -8B, and -10.2 were involved in drought and heat stress in wheat [1]. Tea plants are very sensitive to environmental stress. Here, to investigate how CsYUC genes are regulated by environmental factors in tea plants, systematic analyses of the expression of CsYUC genes were carried out exposed to different stress conditions.

The Expression of CsYUC Numbers under Temperature Stresses

Three RNA-seq datasets of temperature stresses in tea plants were downloaded for analyzing CsYUC gene expression: (1) the expression of CsYUC genes under chilling and freezing stress conditions. The third leaf of two-year-old cv. LJ43 was harvested (accession number: SRP051838) [29]; (2) the expression of CsYUC genes under cold stresses (SRP116862) [30]; and (3) the transcription of CsYUC genes under high- and low-temperature stresses (SRP116862) [31].
  • The Roles of CsYUC Genes in Response to High Temperature
Here, the RNA-seq data in the SRA database showed that, compared to the control, moderately high temperatures (MH) significantly inhibited the expression of CsYUC-2.2, -2.3, and -11.5, while severe high temperatures (SH) significantly inhibited the expression of CsYUC2.1, -11.5, and -11.9 (Figure 8A and Figure S5A). In summary, it can be seen that, under MH and SH, both the tea plants could not enhance their resistance through inducing the transcription of CsYUCs. Consistent with the above results, high temperatures repressed the expression of YUC2 and -6 in barley and Arabidopsis [3,32]. On the other hand, previous studies have reported that plants can activate the transcription of some YUC genes to resist heat injury [3,4,5]. For example, high temperatures specifically induced the transcription of YUC8 and -9 in Arabidopsis and cucumbers [4,7,16]. Under heat stress, the expression of TaYUC6A and -10.1 was upregulated, whereas that of TaYUC10.2 and -10.3 was downregulated [1]. High temperatures induced the expression of MdYUC4a, -6a, -8a, and -10a while downregulating the expression of MdYUC2b and -6b in apples [3].
Overall, the above results showed that low temperatures, including ML and SL, inhibited the expression of a vast majority of CsYUC genes, whereas they significantly induced the transcription of CsYUC2.2, -11.8, and -11.9, and LT and recovering combined treatments significantly induced CsYUC11.3 expression. Yan et al. [5] reported that, in cucumbers, low temperatures dramatically induced CsYUC10b expression, whereas the expression of CsYUC4 decreased.
2.
The Regulatory Roles of CsYUC Genes in Response to Low Temperature
Here, the expression profiles of CsYUC genes were analyzed based on three sets of RNA-seq data from the SRA database, as well as the qRT-PCR assay. The first RNA-seq data showed that, compared to the control, moderately low temperatures (ML) significantly inhibited the expression of CsYUC2.1, -2.2, and -2.3, while severe low temperatures (SL) significantly inhibited the expression of CsYUC2.1, -11.5, and -11.9 (Figure 8A and Figure S5A). Other RNA-seq data showed that, compared to the control, 4 °C or −5 °C treatments for 4 and 8 h all significantly inhibited the transcription of eight CsYUC genes, including CsYUC6, -10, -11.1, -11.2, -11.3, -11.5, -11.6, and -11.7 (Figure 8B and Figure S5B). The third RNA-seq data showed that, firstly, in mature leaves (MLs), compared to the control (20 °C), 4 °C significantly inhibited CsYUC11.4 expression. Both 4 °C and 0 °C significantly inhibited the transcription of eleven CsYUC genes, including CsYUC2.1, -6, -8, -10, -11.1, -11.2, -11.3, -11.5, -11.6, -11.7, and -11.8, while 0 °C significantly inhibited the transcription of CsYUC11.9 expression. Secondly, in young leaves (YLs), compared to the control, 4 °C significantly inhibited CsYUC7 transcription. Both 4 °C and 0 °C significantly inhibited the transcription of 15 CsYUC genes, including CsYUC1, -2.1, -2.3, -6, -8, -10, -11.1, -11.2, -11.3, -11.4, -11.5, -11.6, -11.7, -11.8, and -11.9 (Figure 8C and Figure S5C). Here, the expression levels of the CsYUC numbers were also detected through qRT-PCR. The results showed that, after low-temperature (LT) treatment, the expression of CsYUC2.1 and -11.5 decreased 56.5 and 51.0%, respectively, whereas the transcript levels of CsYUC2.2, -11.8, and -11.9 increased 309.2, 37.3, and 27.4%, respectively. After LT and recovering combined treatment, CsYUC11.3 expression increased 85.5%, whereas the transcript levels of CsYUC1, -2.1, -6, -7, -11.1, -11.4, -11.5, and -11.7 decreased 38.4, 38.7, 27.5, 40.5, 29.1, 55.2, 41.8, and 36.4%, respectively (Figure S7).

The Roles of CsYUC Genes in Response to Drought Stress

In recent decades, drought has been one of the most frequent environmental stresses in the context of global climate change [4]. YUC-mediated IAA biosynthesis involves in the positive regulation of drought stress resistance [7,33,34]. For example, TaYUC2D, -3B, and -9D might be upregulated under drought stress in wheat [1]. Here, an RNA-seq dataset was downloaded to analyze CsYUC expression under drought stress and recovery (accession number: PRJNA297732) [30]. The RNA-seq data showed that, compared to the control, drought significantly inhibited the transcription of CsYUC2.3, -6, -7, and -11.8, and drought and rewatering co-treatment significantly inhibited the expression of CsYUC2.2, -2.3, -6, -7, and -11.8 (Figure 9A and Figure S6A). On the other hand, the qRT-PCR results showed that, compared to the control, PEG treatment inhibited the transcription of CsYUC1, -2.1, -2.3, -10, and -11.5 by 62.9, 25.7, 59.8, 56.1, and 43.9%, respectively, whereas it induced the transcription of CsYUC6, -7, -8, -11.3, -11.4, -11.6, -11.7, -11.8, and -11.9 by 133.5, 109.5, 148.7, 440.9, 125.1, 60.6, 276.6, 109.8, and 53.7%, respectively (Figure S8).
Based on the above results, it can be speculated that the transcript of nine CsYUC genes, including CsYUC6, -7, -8, -11.3, -11.4, -11.6, -11.7, -11.8, and -11.9, may be involved in the positive regulation of the drought stress resistance of tea plants. Drought induced AtYUC7 expression in Arabidopsis roots [4,6], and AtYUC7 overexpression enhanced drought resistance in tomato and Arabidopsis [7,14]. AtYUC6 overexpression led to enhanced drought tolerance in Arabidopsis, potato, and tomato plants [7,15,35]. The activation-tagged mutant yuc-1D in Arabidopsis showed enhanced resistance to drought stress [4,5,36], whereas the yuc1yuc2yuc6 triple-mutant and rice YUC mutant Oscow1 both had decreased drought tolerance [4]. After drought stress, the expression of TaYUC2D, -3B, -6A, and -9D was upregulated [1]. On the other hand, there have also been many studies that reported YUC genes involved in the negative regulation of drought stress resistance. For example, Blakeslee et al. [7] reported that the decreased expression of YUCs in roots caused increased drought tolerance in rice. After drought stress for 1 h, the expression of TaYUC2A and -2B was downregulated [1].

The Regulatory Roles of CsYUC Genes in Response to NaCl Stress

In this study, the qRT-PCR results showed that, compared to the control, NaCl treatment inhibited the expression of CsYUC1, -2.1, -2.2, -2.3, -10, and -11.5 by 58.6, 32.1, 49,6, 40.5, 51.8, and 56.2%, respectively, whereas it significantly induced the expression of CsYUC7, -11.3, -11.4, -11.6, -11.7, -11.8, and -11.9 by 70.6, 504.8, 117.0, 83.7, 317.7, 60.6, and 61.3%, respectively (Figure S8). An RNA-seq dataset was downloaded to analyze CsYUC expression under salt stresses (accession number: SRP107589) [37]. The RNA-seq data showed that, compared to the control, salt treatment significantly inhibited the expression of CsYUC2.1, -2.2, -2.3, -6, and 11.5 while significantly inducing the expression of CsYUC11.9 and -1 (Figure 9B and Figure S6B).
In summary, there are eight CsYUC genes, including CsYUC1, -7, -11.3, -11.4, -11.6, -11.7, -11.8, and -11.9, which may be involved in the positive regulation of NaCl stress resistance of tea plants. Consistent with our results, Wang et al. [14] found that 12 GmYUC genes were all hyperresponsive toward salt treatment. In particular, the results of the qRT-PCR and RNA-seq data both showed that NaCl stress induced the transcription of CsYUC11.9, suggesting that CsYUC11.9 may play key roles in the positive regulation of NaCl stress resistance. Yan et al. [5] reported that, in cucumbers, CsYUC10b transcripts were dramatically upregulated, but the expression of CsYUC10a and -11 were repressed, under salinity stress.
The results revealed that, consistent with previous reports, most of the tested CsYUC genes responded differentially to the same kind of environmental stress and even antagonized each other to maintain the proper endogenous auxin level. Some CsYUC genes were upregulated under one or more stresses, suggesting that they may play important roles in response to these environmental stresses.

4. Conclusions

In this study, 17 CsYUC family genes were identified from the tea plant genome of cv. LJ43. Based on phylogenetic analysis, they were divided into three subfamilies. All of the CsYUCs showed conserved motif structures among the members of every type.
The results of the gene expression analysis showed that CsYUC2.1 and -11.4 in the flower, CsYUC8 in the stem, CsYUC11.8 and -11.9 in the root, and CsYUC11.4 in the mature leaf were highly expressed, respectively. Combined with previous studies, it can be concluded that the YUC10 gene may play key roles in the seed development of many plants. CsYUC genes that play key regulatory roles in the specific stages of leaf and flower development were screened, respectively. CsYUC2.1 may play the most important roles in the coordinated regulation of the growth of leaf buds and flower buds induced by pruning. Low temperatures significantly induced the transcription of CsYUC2.2, -11.8, and -11.9 in tea leaves. There were nine and eight CsYUC genes that might positively regulate the resistance of tea plants to drought and NaCl stress, respectively.
This study suggested the wide involvement of CsYUC genes in development and stress resistance and thus indicated their potential functions in tea plants. The results provided a foundation for the future function research of CsYUC genes and will allow us to develop powerful tools for the regulation of auxin levels to improve certain agronomic traits and stress resistance in tea plants.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/f14112185/s1: Figure S1: LJ43 CsYUC genes locations; Figure S2: The multiple sequence alignments of CsYUC sequences with Arabidopsis AtYUCs; Figure S7: Expression profiles of CsYUC genes in tea plants in response to low temperatures (LT) and recovering detected by qRT-PCR; Figure S8: Expression profiles of CsYUC genes in tea plants in response to PEG and NaCl treatments detected by qRT-PCR. Table S1: Amino acid sequences of YUCs in tea plants and Arabidopsis; Table S2: Chromosome localization and other physical and chemical properties of CsYUC proteins; Table S3: Cis-elements of the 17 CsYUC promoters. Note: Figure S3, Figure S4, Figure S5, and Figure S6 are another form of heat maps of Figure 4, Figure 5, Figure 8, and Figure 9, respectively.

Author Contributions

L.Z. (Liping Zhang), X.L. and J.Z.: Conceptualization; P.B. and S.G.: methodology; Z.L.: software; S.G. and Z.L.: validation; L.Z. (Lan Zhang): formal analysis; L.Z. (Liping Zhang) and W.H.: investigation and project administration; S.J. and P.B.: resources and data curation; L.Z. (Liping Zhang) and S.J.: writing—original draft preparation; J.Z. and X.L.: writing—review and editing; P.Y.: visualization and supervision; and X.L.: funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Zhejiang Province Public Welfare Technology Application Research Project (LGN21C020005) and the Innovation Project of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2015-TRICAAS).

Data Availability Statement

The research data are available upon request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phylogenetic relationships of CsYUCs, together with their Arabidopsis counterparts, respectively. Trees were constructed using the ML method by the MEGA (version 7.0) program. CsYUCs were divided into three groups, indicated by different colored dots.
Figure 1. Phylogenetic relationships of CsYUCs, together with their Arabidopsis counterparts, respectively. Trees were constructed using the ML method by the MEGA (version 7.0) program. CsYUCs were divided into three groups, indicated by different colored dots.
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Figure 2. Gene structure and cis-element analysis of CsYUCs. Exons and introns are represented by green boxes and black lines (A). PlantCARE was used to identify the putative cis-acting element distribution in the 2000 bp promoter sequences of the 17 CsYUC genes. The phylogenetic tree and the cis-elements were combined into one map using the TBtools program (B).
Figure 2. Gene structure and cis-element analysis of CsYUCs. Exons and introns are represented by green boxes and black lines (A). PlantCARE was used to identify the putative cis-acting element distribution in the 2000 bp promoter sequences of the 17 CsYUC genes. The phylogenetic tree and the cis-elements were combined into one map using the TBtools program (B).
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Figure 3. Conserved motifs and conserved domain analysis of CsYUCs. Conserved motifs analysis of CsYUCs (A). Conserved domain analysis of CsYUCs. The relative position of each domain within each protein are shown in color (B). CsYUCs were divided into three groups, indicated by different numbers I, II, and III.
Figure 3. Conserved motifs and conserved domain analysis of CsYUCs. Conserved motifs analysis of CsYUCs (A). Conserved domain analysis of CsYUCs. The relative position of each domain within each protein are shown in color (B). CsYUCs were divided into three groups, indicated by different numbers I, II, and III.
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Figure 4. Expression profiles of CsYUC genes in different tissues of tea plants based on a set of RNA-seq data downloaded from the SRA database (A). The expression profiles of CsYUCs during the process of leaf development and senescence based on two sets of RNA-seq data in the SRA database (B,C). The scale of the color and circle is shown at the right, and higher expression levels are shown in red.
Figure 4. Expression profiles of CsYUC genes in different tissues of tea plants based on a set of RNA-seq data downloaded from the SRA database (A). The expression profiles of CsYUCs during the process of leaf development and senescence based on two sets of RNA-seq data in the SRA database (B,C). The scale of the color and circle is shown at the right, and higher expression levels are shown in red.
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Figure 5. Expression profiles of CsYUC genes during different development processes of tea plants. The expression profiles of CsYUCs during the process of flower development based on a set of RNA-seq data in the SRA database (A). Expression profiles of CsYUCs in the flower buds (FBs) and leaf buds (LBs) induced by pruning based on the transcriptome assay (B).
Figure 5. Expression profiles of CsYUC genes during different development processes of tea plants. The expression profiles of CsYUCs during the process of flower development based on a set of RNA-seq data in the SRA database (A). Expression profiles of CsYUCs in the flower buds (FBs) and leaf buds (LBs) induced by pruning based on the transcriptome assay (B).
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Figure 6. The expression profiles of CsYUC gene numbers in the flower buds at different time points after pruning, detected by qRT-PCR. (A–Q) showed the expression profiles of different CsYUC gene numbers, respectively. In each figure, asterisks show marked difference in the expression levels of CsYUC gene between control and pruning (* p < 0.05, ** p < 0.01; Student’s t-test).
Figure 6. The expression profiles of CsYUC gene numbers in the flower buds at different time points after pruning, detected by qRT-PCR. (A–Q) showed the expression profiles of different CsYUC gene numbers, respectively. In each figure, asterisks show marked difference in the expression levels of CsYUC gene between control and pruning (* p < 0.05, ** p < 0.01; Student’s t-test).
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Figure 7. The expression profiles of CsYUCs in the leaf buds at different time points after pruning, detected by qRT-PCR. (A–Q) showed the expression profiles of different CsYUC gene numbers, respectively. In each figure, asterisks show marked difference in the expression levels of CsYUC gene between control and pruning (* p < 0.05, ** p < 0.01; Student’s t-test).
Figure 7. The expression profiles of CsYUCs in the leaf buds at different time points after pruning, detected by qRT-PCR. (A–Q) showed the expression profiles of different CsYUC gene numbers, respectively. In each figure, asterisks show marked difference in the expression levels of CsYUC gene between control and pruning (* p < 0.05, ** p < 0.01; Student’s t-test).
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Figure 8. Expression profiles of CsYUC genes in tea plants in response to temperature stresses based on three sets of RNA-seq data in the SRA database. Transcriptional levels of CsYUC genes under high- and low-temperature stresses (A). Expression profiles of CsYUC genes in tea plants in response to low-temperature stresses based on two sets of RNA-seq data in the SRA database (B,C).
Figure 8. Expression profiles of CsYUC genes in tea plants in response to temperature stresses based on three sets of RNA-seq data in the SRA database. Transcriptional levels of CsYUC genes under high- and low-temperature stresses (A). Expression profiles of CsYUC genes in tea plants in response to low-temperature stresses based on two sets of RNA-seq data in the SRA database (B,C).
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Figure 9. Expression profiles of CsYUC genes in tea plants in response to drought and salt stresses based on two sets of RNA-seq data in the SRA database. Transcriptional levels of CsYUC genes under drought stress and rewatering (A). Transcriptional levels of CsYUC genes under salt stress (B).
Figure 9. Expression profiles of CsYUC genes in tea plants in response to drought and salt stresses based on two sets of RNA-seq data in the SRA database. Transcriptional levels of CsYUC genes under drought stress and rewatering (A). Transcriptional levels of CsYUC genes under salt stress (B).
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Table 1. The genomic information of the CsYUC gene family and their physical and chemical properties in the tea plant cv. LJ43.
Table 1. The genomic information of the CsYUC gene family and their physical and chemical properties in the tea plant cv. LJ43.
GeneCDS Length (bp)Protein
NameLocus IDLength (aa)pIMS (kDa)
CsYUC1GWHPACFB00632312514168.9446.80
CsYUC2.1GWHPACFB00950813144378.6848.96
CsYUC2.2GWHPACFB02050212784258.7447.68
CsYUC2.3GWHPACFB02050310623538.0239.32
CsYUC6GWHPACFB00629112664218.8546.65
CsYUC7GWHPACFB02607412694229.1046.85
CsYUC8GWHPACFB00511013444478.4449.89
CsYUC10GWHPACFB00535413534508.7750.53
CsYUC11.1GWHPACFB02032910203396.3138.66
CsYUC11.2GWHPACFB02032715605196.3459.35
CsYUC11.3GWHPACFB01921815875286.5160.09
CsYUC11.4GWHPACFB0130418852957.0733.36
CsYUC11.5GWHPACFB01011726858945.98102.27
CsYUC11.6GWHPACFB00590414164715.7952.86
CsYUC11.7GWHPACFB01987925808596.3498.91
CsYUC11.8GWHPACFB01146112034006.0245.61
CsYUC11.9GWHPACFB01146213024336.0749.31
Abbreviation: MS = molecular mass and pI = isoelectric point.
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MDPI and ACS Style

Zhang, L.; Jin, S.; Bai, P.; Ge, S.; Yan, P.; Li, Z.; Zhang, L.; Han, W.; Zeng, J.; Li, X. Genome-Wide Analysis and Expression Profiling of YUCCA Gene Family in Developmental and Environmental Stress Conditions in Tea Plant (Camellia sinensis). Forests 2023, 14, 2185. https://doi.org/10.3390/f14112185

AMA Style

Zhang L, Jin S, Bai P, Ge S, Yan P, Li Z, Zhang L, Han W, Zeng J, Li X. Genome-Wide Analysis and Expression Profiling of YUCCA Gene Family in Developmental and Environmental Stress Conditions in Tea Plant (Camellia sinensis). Forests. 2023; 14(11):2185. https://doi.org/10.3390/f14112185

Chicago/Turabian Style

Zhang, Liping, Shan Jin, Peixian Bai, Shibei Ge, Peng Yan, Zhengzhen Li, Lan Zhang, Wenyan Han, Jianming Zeng, and Xin Li. 2023. "Genome-Wide Analysis and Expression Profiling of YUCCA Gene Family in Developmental and Environmental Stress Conditions in Tea Plant (Camellia sinensis)" Forests 14, no. 11: 2185. https://doi.org/10.3390/f14112185

APA Style

Zhang, L., Jin, S., Bai, P., Ge, S., Yan, P., Li, Z., Zhang, L., Han, W., Zeng, J., & Li, X. (2023). Genome-Wide Analysis and Expression Profiling of YUCCA Gene Family in Developmental and Environmental Stress Conditions in Tea Plant (Camellia sinensis). Forests, 14(11), 2185. https://doi.org/10.3390/f14112185

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