Multi-Omics Research Accelerates the Clarification of the Formation Mechanism and the Influence of Leaf Color Variation in Tea (Camellia sinensis) Plants
by
,
Yan-Gen Fan
1,†,
Ting-Ting Zhao
1,†,
Qin-Zeng **ang
1,
**ao-Yang Han
1,
Shu-Sen Yang
2,
Li-**a Zhang
1,* and
Li-Jun Ren
1,* 1
College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an 271018, China
2
Yipinming Tea Planting Farmers Specialized Cooperative, Longnan 746400, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Plants 2024, 13(3), 426; https://doi.org/10.3390/plants13030426
Submission received: 26 December 2023
/
Revised: 24 January 2024
/
Accepted: 29 January 2024
/
Published: 31 January 2024
(This article belongs to the Special Issue Recent Advances in Horticultural Plant Genomics)
Abstract
:Tea is a popular beverage with characteristic functional and flavor qualities, known to be rich in bioactive metabolites such as tea polyphenols and theanine. Recently, tea varieties with variations in leaf color have been widely used in agriculture production due to their potential advantages in terms of tea quality. Numerous studies have used genome, transcriptome, metabolome, proteome, and lipidome methods to uncover the causes of leaf color variations and investigate their impacts on the accumulation of crucial bioactive metabolites in tea plants. Through a comprehensive review of various omics investigations, we note that decreased expression levels of critical genes in the biosynthesis of chlorophyll and carotenoids, activated chlorophyll degradation, and an impaired photosynthetic chain function are related to the chlorina phenotype in tea plants. For purple-leaf tea, increased expression levels of late biosynthetic genes in the flavonoid synthesis pathway and anthocyanin transport genes are the major and common causes of purple coloration. We have also summarized the influence of leaf color variation on amino acid, polyphenol, and lipid contents and put forward possible causes of these metabolic changes. Finally, this review further proposes the research demands in this field in the future.
1. Introduction
The tea plant (Camellia sinensis) is a widespread crop with high economic and health potential. Tea plant buds and leaves can be processed into popular non-alcoholic beverages [1]. The primary reasons for tea’s popularity are its heightened metabolites and rich flavors. Among these metabolites, catechins are an expansive class of polyphenols making up 12–24% of the dry weight of young tea leaves, imparting an astringent flavor [2]. Regarding human health, catechins have characteristic antioxidative, anti-inflammatory, and other important biological activities [3]. Theanine (γ-glutamylethylamide), a non-proteinogenic amino acid, is specifically synthesized in tea plants. Generally, theanine is the predominant free amino acid in tea leaves and makes up 1–2% of its dry weight [2]. Theanine has conventional health benefits, including antioxidation and neuroprotection [4]. When drinking tea, theanine is the main flavorful substance related to its sweetness and umami, which can neutralize the astringent flavors of polyphenols and the bitter taste resulting from caffeine [2]. Additionally, tea contains other important functional metabolites, including chlorophylls, carotenoids, lipids, and anthocyanins [5]. The content and ratio of these compounds contribute significantly to the economic and nutritional value of tea plants.
Typically, green-leaf tea varieties are most commonly planted and used to make tea. Recently, increasing numbers of tea mutants with variable leaf colors, including albinism, etiolation, and purple hues, have been used in tea production due to their characterized accumulation of certain bioactive substances and increased economic value [6]. As albinistic or etiolated leaves often lead to a limited photosynthetic capacity and an impaired plant survivability, chlorina tea varieties should adopt special survival strategies. In agricultural practices, certain tea cultivars with periodic chlorina behavior are widely utilized because of their good balance between quality and environmental adaptability [6,7,8,9,10]. For periodic chlorina tea varieties, an albinistic or etiolated phenotype is induced according to specific developmental stages or ecological conditions. For instance, chlorina leaves are observed in Anjibaicha (Alternative names: Baiye No1, White leaf No.1, and Anji white 1) and Huabai 1 under low temperatures [11,12], and high-density light is required for the etiolated phenotype in other varieties such as Huang**ya [9,13,14]. When these environmental factors are not satisfied, these varieties will exhibit green leaves to enhance their environmental adaptability [14,15]. In other periodic chlorina tea varieties, leaf re-greening is not modulated by ecological factors but by foliar age [16]. Aside from periodic chlorina cultivars, some varieties with variegated leaves have also been chosen for tea cultivation. In variegated-leaf varieties, a percentage of green tissue is retained on the chlorina leaves, also offering the tea plants an acceptable environmental adaptability [6,17,18]. Alongside changes in leaf color, there are drastic and complex influences on the accumulation of various important functional components in chlorina tea [6,8,9].
Tea varieties possessing purple leaves represent another emerging popular tea type [19]. Compared to traditional green-leaf cultivars, purple-leaf tea is rich in purple-colored bioactive anthocyanins [20,21,22]. Anthocyanins are polyphenols and possess powerful antioxidative and anti-inflammatory capacities [23]. The high-level accumulation of anthocyanins in purple tea hinders the accumulation of other metabolites, predominantly flavonoids [19]. Clearly, enhanced anthocyanin accumulation will greatly alter the flavor of the tea, not just its appearance [19].
As a crop with its leaves acting as the primary economically valuable components, variations in tea leaf color often lead to positive changes in nutritional value and flavor quality. Exploring the metabolites that are associated with leaf color formation and quality changes has theoretical value and important practical value. Therefore, tea is an ideal model plant for investigating the relationship between leaf color and metabolism regulation. Due to the lack of effective gene identification and functional confirmation tools, the cloning of mutated genes for tea leaf color variations is relatively undefined. Fortunately, due to the recent rapid progress of multi-omics technology and its extensive application to tea studies, several high-quality genomes of tea plants have been documented and used to guide physiological and molecular analysis of various important traits [1,24,25,26,27]. To date, over 70 articles have reported the utilization of genome, transcriptome, metabolome, proteome, and lipidome approaches alone or in combination to uncover the color variations in tea. This review will summarize these recent advances and propose challenges for further research.
2. Multi-Omics Approaches Further Our Understanding of Leaf Color Variation in Tea
2.1. Physiological Mechanisms of Albinism or Etiolation in Tea
Chlorophylls and carotenoids are the two primary pigment types in plant leaves. The biosynthesis and degradation of chlorophylls and carotenoids are complex processes with multiple steps, and chloroplast development is a delicate process. Therefore, from a genetic point of view, the mutations causing chlorina phenotypes in the leaves are very rich [28].
As in all albinistic and etiolated tea mutants, varying degrees of reduced chlorophyll a, chlorophyll b, and total chlorophyll content are the most direct factors causing the leaf color to become lighter (Table 1) [12,16,29,30,31,32,33,34]. The ratio of chlorophyll a/b is down-regulated in Anjibaicha [10,35], Huang**ya [32,36,37], and Yanlingyinbiancha [18] but up-regulated in Baijiguan [38], **-by-sequencing, Zhang et al. constructed a genetic map of the full-sibling population of Baijiguan and Long**g43 and successfully identified the major effect QTL linked to the total chlorophyll contents [38]. Using bulked segregant analysis sequencing (BSA-Seq)-assisted genetic map**, a nonsynonymous mutation in the magnesium chelatase I subunit encoding the gene CsChlI blocks the conversion of protoporphyrin IX (Proto IX) into MgP IX throughout chlorophyll synthesis, impacting leaf coloring [38]. In many annual plants, similar non-synonymous mutations are reported to be responsible for the reduced function of ChlI and chlorophyll accumulation [58,59,60,61]. A common feature of these mutants and Baijiguan is that the degree of leaf yellowing is gene-dosage-dependent [58,59,60].
In another study, a pan-genome analysis of 22 tea accessions revealed various genomic deletions in the glutamyl-tRNA synthetase (GluRS/EARS) gene of both Anjibaicha and Huang**ya [24]. GluRS/EARS catalyzes the formation of L-Glu-tRNA, which is considered the first step of chlorophyll biosynthesis in higher plants [62]. The truncated GluRS/EARS protein may limit chlorophyll synthesis and contribute to the formation of the chlorina phenotype in these two varieties. Additionally, structural variations (SVs) have been identified in another three chlorophyll synthesis genes (chlorophyllide a oxygenase, CAO; geranylgeraniol reductase, CHLP; glutamyl-tRNA reductase, GluTR) and one (magnesium chelatase D subunit, ChlD) chlorophyll synthesis gene in Huang**ya and Anjibaicha, respectively. These findings suggest the presence of multiple blocked genetic sites in the chlorophyll synthesis pathways of Anjibaicha and Huang**ya [24]. Additionally, the genomic region of the chlorophyll-degradation-related gene chlorophyll b reductase (NOL) has a 1-base-pair deletion in Anjibaicha, suggesting that the chlorophyll degradation may also have changed [24,63,64]. Comparative genomic analysis identified a genomic variation in the CYP97A3 gene causing a 20-amino-acid alteration that may affect its ability to catalyze zeaxanthin synthesis of lutein [24,65]. However, the true functions of the aforementioned candidate genes identified using either genetic map** or pan-genome analysis remain unclear in vivo.
Given the difficulty of identifying mutated genes at the genomic level, much of the research in this field uses metabolomes, proteomes, and transcriptomes to indirectly investigate the molecular mechanisms underlying leaf chlorosis in tea. A joint assessment of proteomes and metabolomes revealed one potential blocked site of chlorophyll synthesis in etiolated leaves of Huang**ya: from protochlorophyllide (Pchlide) into chlorophyllide a (Chlide a). The significantly lowered protein abundance of protochlorophyllide oxidoreductase (POR) in the etiolated leaves was considered to be responsible for the excessive accumulation of the substrate (MgP IX) in the previous step [9]. While the metabolic flow from coproporphyrinogen III (Coprogen III) to Proto IX aligns with the trend of the excessive accumulation of substrates and a reduced product content, the abundance of protein (coproporphyrinogen III oxidase, COPX/HEMF) mediating this catalytic reaction does not change in etiolated leaves [9]. The alterations in the content of Coprogen III and Proto IX are more likely influenced by other metabolic events. In addition, a dramatically lower level of CAO may further decrease the content of chlorophyll b (Figure 1) [9]. Pheophorbide a oxygenase (PAO/ACD1)-mediated chlorophyll breakdown is essential for the loss of green pigments in plant leaves [66]. Overactivated PAO/ACD1 in Huang**ya may enhance the chlorina phenotype. In the etiolated leaves of Huang**ya, proteome analysis demonstrates that the function of the photosynthetic chain is greatly damaged [9,36]. Fan et al. reported that most protein members of Photosystem I (PSI), PSII, and plastid quinone pool (PQ) are significantly down-regulated in yellowish leaves [9]. In another study, differentially expressed protein (DEP) analysis also indicates an impaired photosynthetic chain, but the DEPs identified are less repetitive and reduced in number [36].
Proteome, acetyl-proteome, and succinyl-proteome analysis in Anjibaicha uncovered an enrichment of differentially expressed or modified proteins in the photosynthetic pathway during the whitening and re-greening processes of Anjibaicha, suggesting that the destruction and reconstruction of the photosynthetic chain function is closely associated with the change in leaf color [8,46,67]. In support of this, transcriptomic analysis also identified enriched down-regulated differentially expressed genes (DEGs) in the photosynthetic chain and chlorophyll metabolism, respectively, including eight and six genes [35]. Among them, the antenna protein LHCA4 exhibits a consistently lower abundance in etiolated leaves at the transcriptional, protein, and protein modification levels [8,35,46].
In most other albinistic or etiolated varieties, the evidence at the protein or transcriptome level supports one or more of the processes of chlorophyll metabolism, the photosynthetic chain, and carotenoid synthesis being impacted in chlorosis leaves (Table 1). Understandably, blocked biosynthesis of chlorophyll and carotenoids and activated chlorophyll degradation contribute to the lightened color of the leaves [68,69]. While not all genes in the biosynthetic pathways of chlorophyll and carotenoids are uniformly down-regulated (Table 1), the reduced expression of crucial upstream genes may explain the decreased accumulation of total chlorophyll or carotenoids in Anjibaicha (POR and PBGD/HMBS/HEMC) [35] and the albinistic branches of Huangshan (CHLP and POR) [48], Huang**shuixian (DXS and GGPPS) [16], and Zhonghuang 3 (GluTR/HEMA, GSA-AM/HEML, UROD/HEME, HEMF/CPOX, and CHLP) [14].
In plants, the biosynthesis and degradation of chlorophyll are highly coordinated with the structural and functional integrity of the photosynthetic chain [28]. The LHC proteins associated with the antenna complex are responsible for light harvesting and Chl a/b binding [70]. Incompletely assembled photosystems will hinder the localization of antenna proteins to the thylakoids and will cause reduced contents of LHC-bound chlorophyll [71]. As free chlorophyll is photosensitive, the absence of LHCB1 and LHCB2 can lead to reduced chlorophyll accumulation [72,73]. In various chlorina tea varieties, the functional modules (antenna complex [8,9,13,29,30,40,41,48,52,53], photosystems [8,9,12,17,48,53], quinone pools [36], cytochrome b6/f complexes [9,40], and ATPase complexes [8,9,48,53]) of the photosynthetic chain have been differentially impaired (Table 1). The reduction in antenna protein abundance and the photooxidative stress triggered by photosynthetic electron transfer defects may be common factors leading to or exacerbating leaf chlorosis in these tea variations [74].
Reduced chlorophyll content will disrupt photosynthetic chain stability. Light-induced thylakoid biogenesis is a prerequisite for the assembly of the photosynthetic chain, which is highly coordinated with the reduction of Pchlide into chlorophyllide (Chlide) in the penultimate step of chlorophyll biosynthesis [73]. In addition, the protein stability of the LHCII members is modulated by chlorophyll [64]. In Arabidopsis cao1 mutant chloroplasts, down-regulated chlorophyll b promotes the proteolysis metabolism of the LHCII proteins [75]. Therefore, it is still difficult to distinguish whether a reduced chlorophyll content or an impaired photosynthetic chain is more likely to cause leaf chlorosis in tea according to the available omics results.
Multi-omics technologies have identified potential transcriptional factors involved in regulating the chlorophyll metabolism in chlorina tea plants [16,39,50,51]. Both transcriptome and translatome analyses reveal that ELONGATED HYPOCOTYL 5 (HY5) (Figure 1), a bZIP-type transcription factor (TF) involved in photomorphogenesis, is up-regulated in ** and comparative genomics have been effective in identifying mutated genes in tea plants. Therefore, more efforts should focus on dissecting the genetic basis of leaf color variation and cloning mutated genes. (4) The influence of ecological or developmental factors on the metabolic flow allocation and the foundational molecular mechanisms should be explored. Through the above efforts, we will truly comprehend the mechanism of tea leaf color formation, explore its characteristic qualities more efficiently and accurately, and enhance the breeding utilization efficiency of these specific germplasms.
Author Contributions
L.-J.R. and L.-X.Z. conceived the present work; L.-J.R., Y.-G.F. and T.-T.Z. drafted the manuscript; Q.-Z.X., X.-Y.H. and S.-S.Y. retrieved the relevant literature; L.-X.Z. revised the manuscript. All authors have read and agreed to the published version of the manuscript.
Funding
This work was financially supported by the Lugan Technology Collaboration Special Project of the Science and Technology Planning Project of Gansu Province, China (Grant No. 22CX8NK246) and the Special Funds of Taishan Scholar Project of Shandong Province, China (Grant No. tsqnz20231202).
Data Availability Statement
All the data are contained within the article.
Conflicts of Interest
The authors declare no conflicts of interest.
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Figure 1.
Proteins and genes involved in chlorophyll synthesis pathway. Next to the arrow, the word above represents the protein name, and the corresponding gene name is below. GluRS, glutamyl-tRNA synthetase; GluTR, glutamyl-tRNA reductase; GSA-AM, glutamate-1-semialdehyde 2,1-aminomutase; PBGS, porphobilinogen synthase; HMBS, hydroxymethylbilane synthase; UROS, uroporphyrinogen-III synthase; UROD, uroporphyrinogen decarboxylase; CPOX, coproporphyrinogen III oxidase; PPOX, protoporphyrinogen III oxidase; MgCh, magnesium chelatase; MgPMT, magnesium-protoporphyrin O-methyltransferase; MgPEC, magnesium-protoporphyrin IX monomethyl ester (oxidative) cyclase; DVR, divinyl chlorophyllide a 8-vinyl-reductase; POR, protochlorophyllide reductase; NOL, chlorophyll(ide) b reductase; CAO, chlorophyllide a oxygenase; ChlG, chlorophyll/bacteriochlorophyll a synthase; CLH, chlorophyllase; HCAR, hydroxymethyl chlorophyll a reductase; SGR, magnesium dechelatase; PAO/ACD1, pheophorbide a oxygenase; ACD2, red chlorophyll catabolite reductase; PPD, pheophorbidase.
Figure 1.
Proteins and genes involved in chlorophyll synthesis pathway. Next to the arrow, the word above represents the protein name, and the corresponding gene name is below. GluRS, glutamyl-tRNA synthetase; GluTR, glutamyl-tRNA reductase; GSA-AM, glutamate-1-semialdehyde 2,1-aminomutase; PBGS, porphobilinogen synthase; HMBS, hydroxymethylbilane synthase; UROS, uroporphyrinogen-III synthase; UROD, uroporphyrinogen decarboxylase; CPOX, coproporphyrinogen III oxidase; PPOX, protoporphyrinogen III oxidase; MgCh, magnesium chelatase; MgPMT, magnesium-protoporphyrin O-methyltransferase; MgPEC, magnesium-protoporphyrin IX monomethyl ester (oxidative) cyclase; DVR, divinyl chlorophyllide a 8-vinyl-reductase; POR, protochlorophyllide reductase; NOL, chlorophyll(ide) b reductase; CAO, chlorophyllide a oxygenase; ChlG, chlorophyll/bacteriochlorophyll a synthase; CLH, chlorophyllase; HCAR, hydroxymethyl chlorophyll a reductase; SGR, magnesium dechelatase; PAO/ACD1, pheophorbide a oxygenase; ACD2, red chlorophyll catabolite reductase; PPD, pheophorbidase.
Figure 2.
The synthesis process of flavonoids and anthocyanins. The yellow textboxes represent the flavonols, the pale green textboxes represent the catechins, and the purple textboxes represent the decorated anthocyanins. PAL, phenylalanine ammonia lyase; C4H, cinnamate-4-hydroxylase; 4CL, 4-coumarate: CoA ligase; CHS chalcone synthase; CHI chalcone isomerase; F3H, flavanone 3-hydroxylase; F3′H, flavonol 3′-hydroxylase; F3′5′H, flavonol 3′5′-hydroxylase; FLS, flavonol synthase; DFR, dihydroflavonol 4-reductase; LAR, leucoanthocyanidin reductase; ANS/LDOX, leucoanthocyanidin dioxygenase; ANR, anthocyanin reductase; UGT, UDP-glucose: flavonol-3-O-glycosyltransferase.
Figure 2.
The synthesis process of flavonoids and anthocyanins. The yellow textboxes represent the flavonols, the pale green textboxes represent the catechins, and the purple textboxes represent the decorated anthocyanins. PAL, phenylalanine ammonia lyase; C4H, cinnamate-4-hydroxylase; 4CL, 4-coumarate: CoA ligase; CHS chalcone synthase; CHI chalcone isomerase; F3H, flavanone 3-hydroxylase; F3′H, flavonol 3′-hydroxylase; F3′5′H, flavonol 3′5′-hydroxylase; FLS, flavonol synthase; DFR, dihydroflavonol 4-reductase; LAR, leucoanthocyanidin reductase; ANS/LDOX, leucoanthocyanidin dioxygenase; ANR, anthocyanin reductase; UGT, UDP-glucose: flavonol-3-O-glycosyltransferase.
Figure 3.
Red/green frameless arrows represent a promoting/inhibitory effect, while red/green framed arrows represent an increase/decrease in substances. Substances surrounded with a dashed outline are in a free state. Compared to green varieties, chlorotic varieties are hindered in chlorophyll synthesis and degradation under strong light or low-temperature conditions, resulting in imbalanced carbon (C) and nitrogen (N) metabolism and reduced flavonoid content in the chlorotic leaves. Excess free nitrogen promotes the accumulation of free amino acids in chlorotic leaves. On the other hand, the loss of chloroplast structure and degradation of photosynthetic-chain-related proteins further increase the content of free amino acids in chlorotic leaves. In addition, the synthesis of fatty acids has also increased in chlorotic varieties. In purple varieties, low temperature or strong light enhances the expression of flavonoid-pathway-related genes, promoting the synthesis of more anthocyanins.
Figure 3.
Red/green frameless arrows represent a promoting/inhibitory effect, while red/green framed arrows represent an increase/decrease in substances. Substances surrounded with a dashed outline are in a free state. Compared to green varieties, chlorotic varieties are hindered in chlorophyll synthesis and degradation under strong light or low-temperature conditions, resulting in imbalanced carbon (C) and nitrogen (N) metabolism and reduced flavonoid content in the chlorotic leaves. Excess free nitrogen promotes the accumulation of free amino acids in chlorotic leaves. On the other hand, the loss of chloroplast structure and degradation of photosynthetic-chain-related proteins further increase the content of free amino acids in chlorotic leaves. In addition, the synthesis of fatty acids has also increased in chlorotic varieties. In purple varieties, low temperature or strong light enhances the expression of flavonoid-pathway-related genes, promoting the synthesis of more anthocyanins.
Table 1.
A summary of multi-omics-generated molecular evidence related to leaf color variations in tea.
Table 1.
A summary of multi-omics-generated molecular evidence related to leaf color variations in tea.
| Tea Varieties | Omics Approaches | Potential Molecular Mechanisms | References |
|---|---|---|---|
| Anjibaicha (Alternative names: Baiye No1, White leaf No.1, and Anji white 1) | Succinyl-proteome | Photosynthetic chain: The succinylation levels of PsbS and light-harvesting complex LHCA4 are down-regulated; the succinylation level of LHCB4 is up-regulated. | [46] |
| Proteome and acetyl-proteome | Photosynthetic chain: lower abundance of LHCB1, LHCB2, LHCB3, LHCB4, LHCB5, LHCB7, LHCA1, LHCA2, LHCA3, LHCA4, PsbC, PsbD, PsbO, PsbP, PsbQ, PsbR, PsbS, Psb27, PsaE, PsaG, PsaL, PsaN, PetA, PetC, PetE, PetF, PetH, ATPA, ATPB, ATPD, ATPE, ATPG; a lower acetylation level of LHCA1. | [8] | |
| Pangenome | Chlorophyll synthesis: The GluRS/EARS gene in Anjibaicha showed a loss of anti-codon recognition domains; SVs were revealed in ChlD. Chlorophyll degradation: 1 bp deletion is revealed in NOL/NYC1. | [24] | |
| Whole-transcriptome | Chlorophyll synthesis: down-regulated expression of POR (two alleles), CLH1, PBGD/HMBS/HEMC; up-regulated expression of COX15. Photosynthetic chain: down-regulated expression of CAB7, CAB21, LHCA4, CAB40 (three alleles), CAB13, LHCB5, PetA (two alleles), PsbA (TEA_001460), PsaB, PsbP1, ATPA, PsaH, ATPI, PetB, Psb28; up-regulated expression of PsbA (TEA_001460). | [35] | |
| Huang**ya | Proteome | Chlorophyll synthesis: higher abundance of GluRS/EARS, MgCh/ChlH, and HMBS; lower abundance of POR. Photosynthetic chain: lower abundance of Photosystem Q(B) protein. | [36] |
| Metabolome and proteome | Chlorophyll synthesis: higher abundance of GluRS/EARS and UROD/HEME; lower abundance of POR and CAO. Chlorophyll degradation: higher abundance of PAO/ACD1 Photosynthetic chain: lower abundance of LHCA1, LHCA3, LHCB1, LHCB2, LHCB3, LHCB4, LHCB5, LHCB6, PsaD, PsaF, PsaL, PsaN, PsbA, PsbD, PsbE, PsbO, PsbP, PsbQ; higher abundance of PsbS, FNR, ATPB. Carotenoid synthesis: lower abundance of ZEP; higher abundance of PSY. | [9] | |
| Pangenome | Chlorophyll synthesis: The GluRS/EARS gene in Huang**ya showed a loss of anti-codon recognition domains, which may inhibit chlorophyll synthesis; SVs were detected in CAO, CHLP, and GluTR. Carotenoid synthesis: mutated amino acids in CYP97A3HJY and elevated expression of the CYP97A3HJY allele. | [24] | |
| Transcriptome | Carotenoid synthesis: down-regulated expression of PSY, PDS, ZDS, LCYE, LCYB, CHY, ZEP, and VDE. | [47] | |
| Baijiguan | BSR-seq | Photosynthetic chain: co-down-regulated expression of LHCA3, three LHCB1 alleles (TEA001863, TEA001868, TEA030368), two LHCB3 alleles (TEA017256, TEA021966), and LHCB4 in bulked groups and parents. | [29] |
| Genome: Genoty** by sequencing and BSA-seq | Chlorophyll synthesis: a non-synonymous polymorphism (G1199A) in the magnesium chelatase I subunit (CsChlI). | [38] | |
| HY1 | Proteome | Photosynthetic chain: lower abundance of LHCA3, LHCA4, LHCB1, LHCB2, LHCB6, PsbC, PsBO, PsbS, PsaB, PsaC, PsaD, PsaF, PetA, PetH. | [17] |
| HY2 | Proteome | Photosynthetic chain: lower abundance of LHCB2, PsbA, PsbD, PsbC, PsbB, PsbQ, PsaA, PsaB, PsaD, PsaH, PetB, PetA, beta F-type ATPase. | [17] |
| HY | Transcriptome | Chlorophyll degradation: the activation of SGR and CLH. | [43] |
| **angfeihuangye | Transcriptome, translatome, and metabolome | Chlorophyll synthesis: up-regulation of HY5 in EL inhibited the expression of GluTR/HEMA and POR. | [39] |
| Huabai 1 | Transcriptome | Photosynthetic chain: down-regulated expression of light-harvesting complex II (LHCII) chlorophyll-a/b-binding protein. Chlorophyll degradation: up-regulated expression of SGR. | [12] |
| Albinistic branch of Huangshan | Transcriptome | Chlorophyll synthesis: down-regulated expression of four CHLP alleles (TEA027589, TEA019124, BGI_novel_G007262, TEA016514) and one POR allele (TEA014780); up-regulated expression of one CHLP allele (TEA009538), one POR allele (TEA027994), and one CLH allele (TEA027808). Photosynthetic chain: down-regulated expression of three LHCB1 alleles (TEA019232, TEA030366, TEA030368), PsbC, five PsbB alleles (TEA028468, TEA011113, TEA032780, TEA018797, BGI_novel_G013475), PsbP, Psb28, PsaA, five ATPD alleles (TEA030038, TEA004696, TEA002611, BGI_novel_G006800, BGI_novel_004911), two ATPA alleles (TEA019276, BGI_novel_G009498), ATPE. | [48] |
| Huang**ju | Transcriptome | Chlorophyll synthesis: up-regulated expression of POR. Photosynthetic chain: down-regulated expression of LHCA2, LHCA4, LHCB1, LHCB2, LHCB6. | [13] |
| Yanlingyinbiancha | Transcriptome | Chlorophyll synthesis: down-regulated expression of UROS/HEMD, PPOX, ChlH/GUN5, MgPEC/CRD1, DVR/PCB2, and CAO. Chlorophyll degradation: down-regulated expression of NOL/NYC1, HCAR, CLH1, and ACD2. Photosynthetic chain: fifty-five DEGs involved in photosynthetic complexes were found to be down-regulated. Carotenoid synthesis: down-regulated expression of Z-ISO, ZDS, ZEP, LUT2, NCED4. | [18] |
| Yanling Huayecha | Transcriptome | Chlorophyll synthesis: down-regulated expression of PPOX. Photosynthetic chain: down-regulated expression of LHCB6 and FdC2. Thylakoid membrane structure: down-regulated expression of SCY1. | [40] |
| Menghai Huangye | Transcriptome | Chlorophyll synthesis: four genes related to chlorophyll synthesis (HEME2 and POR). Photosynthetic chain: ten genes related to photosynthesis (LHCA and LHCB) are down-regulated. | [41] |
| Zhonghuang 3 | Transcriptome | Chlorophyll metabolism: down-regulated expression of GluTR/HEMA3 and CLH4. | [49] |
| Zhonghuang 3 | Transcriptome | Chlorophyll synthesis: down-regulated expression of GluTR/HEMA, GSA-AM/HEML, UROD/HEME, HEMF/CPOX, DVR (CSS0009780), and CHLP; up-regulated expression of PBGS/HEMB, DVR (CSS0011936), and CLH. Chlorophyll degradation: down-regulated expression of NOL/NYC1 (CSS0031926) and SGR (CSS0030812); up-regulated expression of NOL/NYC1 (CSS0015127), SGR (CSS0050352), and SGRL (CSS0004139 and CSS0036450). Carotenoid synthesis: up-regulated expression of Z-ISO, CRTISO (CSS0027469, CSS0033902, and CSS0044870), NCED1, NCED2; down-regulated expression of LCYB and NXS. | [14] |
| Zhonghuang 2 | Transcriptome | Transcripts encoding enzymes such as those functioning in early enzymatic steps, from the formation of glutamate 1-semialdehyde to protoporphyrin IX, showed lower levels. Critical enzymes for converting Mg-protoporphyrin IX into chlorophyll were also inhibited. | [42] |
| Koganemidori | Transcriptome | Chlorophyll synthesis: down-regulated expression of POR, CAO, and ChlG. Chlorophyll degradation: up-regulated expression of CLH. Transcriptional regulation: two homologs of GLK were significantly down-regulated. | [50] |
| Huang**shuixian | Transcriptome and metabolome | Chlorophyll degradation: down-regulated expression of SGR. Carotenoid synthesis: the expression of DXS and GGPPS was significantly down-regulated. Transcriptional regulation: PIFs related to chlorophyll biosynthesis were significantly suppressed. | [16] |
| Huangyu | Transcriptome and metabolome | Chlorophyll synthesis: down-regulated expression of UROD/HEME, MgCh/ChlH, and CAO. Chlorophyll degradation: up-regulated expression of CLH. Photosynthetic chain: down-regulated expression of three LHCII genes (CSS0013089, CSS0017825, and CSS0039893) | [30] |
| Huangkui | Transcriptome | Transcriptional regulation: the transcriptional expression of CsRVE1 increased during seasonal greening and was tightly correlated with increases in the expression of genes involved in light harvesting (LHCB) and chlorophyll biosynthesis (MgCh/ChlH, GluTR/HEMA1, and CAO). | [51] |
| Fuhuang 1 | Transcriptome | Chlorophyll synthesis: down-regulated expression of CAO. Chlorophyll degradation: down-regulated expression of NOL/NYC1 and SGR. Photosynthetic chain: down-regulated expression of LHCA2, LHCA4, LHCB1, LHCB3. Carotenoid synthesis: down-regulated expression of LCYE, ZEP, NCED; up-regulated expression of PSY, PDS, VDE. | [52] |
| Fuhuang 2 | Transcriptome | Chlorophyll synthesis: down-regulated expression of GluTR/HEMA. Chlorophyll degradation: down-regulated expression of CLH. Photosynthetic chain: down-regulated expression of PsbB, PetC, ATPF1B, LCHBs, LCHAs. Carotenoid synthesis: down-regulated expression of NCED. | [53] |
Table 2.
A summary of anthocyanin composition in purple leaves of tea.
| Tea Varieties | Sampling Location | Measurement Technique | Anthocyanin Composition | References |
|---|---|---|---|---|
| Zijuan | Tea garden of South China Agricultural University, Guangzhou, China | HPLC | Major anthocyanin compositions: cyanidin-3-O-galactoside and delphinidin-3-O-galactoside. | [77] |
| Tea garden of the Institute of Tea Science, Yunnan Province Academy of Agricultural Sciences (Menghai, China) | Non-targeted metabolomics approach: UHPLC– Orbitrap–MS/MS | Cyanidin 3-diglucoside 5-glucoside, cyanidin 3-O-(6-O-p-coumaroyl) glucoside, cyanidin 3-sambubioside, cyanidin 3-(6″-acetylglucoside)-5-glucoside, delphinidin 3-(6-p-coumaroyl) galactoside, delphinidin-3-O-arabinoside, pelargonidin 3-sophoroside 5-glucoside, pelargonidin 3-coumarylglucoside-5-acetylglucoside, pelargonidin 3-rhamnoside 5-glucoside; compared with Yunkang, the contents of cyanidin 3-diglucoside 5-glucoside and pelargonidin 3-sophoroside 5-glucoside are most increased in Zijuan. | [86] | |
| Pu’er City Institute of Tea Science, Yunnan Province | UPLC–ESI–MS/MS metabolomic analysis | Specific metabolites: petunidin 3-O-glucoside, peonidin 3-O-glucoside chloride, peonidin 3-O-glucoside, peonidin O-hexoside, malvidin 3-O-glucoside (oenin), petunidin 3,5-O-diglucoside. Marker metabolites: cyanidin 3-O-galactoside, cyanidin 3-O-glucoside (Kuromanin), delphinidin 3-O-glucoside (Mirtillin), pelargonidin 3-O-glucoside | [87] | |
| Changsha, Hunan, China | UPLC–ESI–MS/MS metabolomic analysis | Major anthocyanin compositions: cyanidin-3-ogalactoside, delphinidin-3-O-galactoside, and petunidin-3-O-galactoside | [88] | |
| Dechang Fabrication Base of Shucheng County in Anhui Province, China | LC−TOF–MS | Cyanidin-3-O-galactoside, Cyanidin 3-O-(6-O-p-coumaroyl) galactoside, Delphinidin 3-O-(6-O-p-coumaroyl) galactoside, Delphinidin-3-O-galactoside. | [89] | |
| Zijuan Ziyan and Chuanzi (ZZ) | Muchuan County, Sichuan Province, China | Targeted UPLC– ESI–MS/MS analysis | A total of 22 anthocyanins with a content ≥1 μg/g (DW) were detected in Chuanzi, Ziyan, and/or Zijuan and these included 6 cyanidins, 7 delphinidins, 5 pelargonidins, 2 peonidins, and 2 petunidins. In addition, 23 anthocyanins with a concentration of <1 μg/g were also detected. | [82] |
| Ziyan | Planted in plastic pots | HPLC | Delphinidin, cyanidin, and pelargonidin. | [90] |
| Hongyecha, Zijuan, 9803, Hongyafoshou | Changsha, Hunan, China | UPLC–DAD–QTOF–MS | Cyanidin-(E)-p-coumaroylgalactoside, cyanidin-3-O-galactoside, delphinidin-3-O-galactoside, delphinidin-(Z)-p-coumaroylgalactoside, delphinidin-(E)-p-coumaroylgalactoside, pelargonidin-O-hexose, and pelargonidin-O-dihexose. | [91] |
| **mingzao | Tea plantation of Wuqu in Fuan City, Fujian Province, China | Widely targeted metabolomics: UPLC–ESI–MS/MS | Cyanidin 3-O-glucoside, cyanidin 3-O-galactoside, cyanidin 3-rutinoside, cyanidin chloride, delphinidin 3-O-glucoside, peonidin 3-O-glucoside chloride (most affected). | [83] |
| Zikui | South Campus of Guizhou University, Huaxi District, Guiyang City, Guizhou Province, China | ESI–QTRAP–MS/MS | Cyanidin 3-O-galactoside, cyanidin 3-O-glucosid, petunidin 3-O-glucoside. | [84] |
| Long**g43 | Tea Research Institute, Chinese Academy of Agricultural Sciences, Hangzhou, China | LC–MS/MS | Delphinidin-hexose-coumaroyl showed the greatest increase. | [80] |
| TRFK 306 | Tea Research Institute (TRI), Kericho County, Kenya | HPLC | Malvidin 3-glucoside, peonidin 3-glucoside, pelargonidin 3,5-O-diglucoside, cyanidin 3-O-glucoside, cyanidin 3-O-galactoside, cyanidin 3-O-rutinoside. | [81] |
| 9 tea cultivars possessing purple leaves | Wuxi Institute of Tea Varieties in Wuxi City, Jiangsu Province, China | Widely targeted metabolomics: UPLC–ESI–MS/ MS | Thirty-three anthocyanins were identified, and delphinidin 3-O-galactoside and cyanidin 3-O-galactoside were found to be the most abundant in PTLs. | [85] |
| Unknown | Experimental tea farm (IHBT-269) of CSIR—Institute of Himalayan Bioresource Technology, HP, India | UHPLC | 3-O-alpha-l-arabinopyranosylproantho cyanidin A5′ and 3,3′-Di-O-galloylprocyanidin B. | [92] |
Table 3.
A summary of multi-omics-generated molecular evidence related to purple leaves in tea.
| Tea Varieties | Omics Approaches | Potential Molecular Mechanisms | References |
|---|---|---|---|
| Zijuan | Transcriptome | Transcriptional regulation: Activation of the R2R3-MYB transcription factor (TF) anthocyanin1 (CsAN1) and the bHLH TF CsGL3; CsAN1 interacts with bHLH TFs (CsGL3 and CsEGL3) and recruits a WD-repeat protein CsTTG1 to form the MYB-bHLH-WDR (MBW) complex that regulates anthocyanin accumulation. Late biosynthetic genes (LBGs): activation of CsF3′H, CsF3′5′H, CsDFR1, CsDFR2, CsANS1/LDOX1, CsANS2/LDOX2, and CsANS3/LDOX3. Metabolic substrate competition: activation of CsLAR1, CsLAR2, and CsLAR3, which encode enzymes for catechin biosynthesis, was highly expressed in red foliage. | [77] |
| Transcriptome, proteome | Phenylpropanoid metabolism: significantly increased expression of three PALs (CSA016076, 022024, 022025); significantly decreased expression of 4CL (CSA001434). Early biosynthesis genes (EBGs): significantly increased expression of CHS (CSA029775); significantly decreased expression of CHI (CSA008261). LBGs: significantly increased expression of two DFRs (CSA003949, XLOC_010242), one ANS/LDOX (CSA011508), six UGT75L12/13 (CSA005544, 005545, 010001, 036671, 036672, 029026), and two UGT94P1 (CSA007394, 008750); significantly decreased expression of F3′5′H (CSA031792), ANS/LDOX (CSA035767), two UGT75L12s (CSA008693, 028873), and two UGT94P1s (CSA005965, 026000). Metabolic substrate competition: significantly increased expression of two LARs (CSA014943, XLOC_016774). | [87] | |
| Transcriptome | Phenylpropanoid metabolism: activation of C4H. LBGs: activation of ANS/LDOX, UGT. Chlorophyll degradation: activation of CLH1. | [97] | |
| Full-length transcriptome | Alternative splicing (AS) events identified in transcriptional regulation (MYB113-1), phenylpropanoid metabolism (C4H1, PAL2), LBGs (UDP75L122), and metabolic substrate competition (FLS1). | [98] | |
| Proteome | EBGs: increased abundance of CHS and CHI. LBGs: increased abundance of DFR, ANS/LDOX, and UGT. Anthocyanin transportation: increased abundance of ABC transporter B8. | [20] | |
| Transcriptome | Transcriptional regulation: Most of the members belonging to the MYB, WRKY, AP2, GRF, bZIP, and MYC groups had a higher expression in Zijuan. LBGs: significantly increased expression of F3′5′H (CSS0022212.1), ANS/LDOX (CSS0010687.1), 3GT (anthocyanidin 3-O-glucosyltransferase, CSS0024320.1), 3AT (cyanidin-3-O-glucoside 6″-O-acyltransferase, CSS0015285.1). Metabolic substrate competition: significantly decreased expression of LAR (CSS0009063.1). Anthocyanin degradation: polyphenol oxidase (PPO, CSS0002951.1), showed negative correlation with the three anthocyanins, especially delphinidin and delargonidin. | [89] | |
| Chuanzi (ZZ) | Transcriptome | Transcriptional regulation: significantly increased expression of the well-known MYB transcription factor CsAN1/CsMYB75 (CSS0030514). LBGs: significantly increased expression of CsANSs/LDOXs (CSS0010687, CSS0018498 and CSS0046216), CsUGT94P1 (CSS0011196), and the anthocyanin O-methyltransferase gene (CsAOMT, CSS0015915). Anthocyanin transportation: significantly increased expression of CsGSTF1 (CSS0022086) and three other GST candidate genes (CSS0031248, CSS0026690, and CSS0018634) tightly linked to CsGSTF1. Metabolic substrate competition: down-regulated expression of LARs (CSS0028235 and CSS0009063) and ANRs (CSS0005927, and CSS0033195). | [82] |
| Zijuan, **guanyin and **mingzao | Pangenome | Read depth of the LTR insertion region in the promoter of CsMYB114 among a set of representative purple-leaf cultivars (‘ZJ’, ‘JMZ’, and ‘JGY’) and tea cultivars with green leaves (‘FDDB’, ‘BHZ’, and ‘GH3H’) | [24] |
| Ziyan | Transcriptome | Transcriptional regulation: UV-A induces the expression of the regulatory gene TT8; UV-AB induces the expression of the regulatory genes EGL1 and TT2. LBGs: UV-A induces the expression of F3H, F3′5′H, DFR, and ANS/LDOX; UV-AB induces the expression of F3′5′H, DFR, ANS/LDOX, and UGT. Metabolic substrate competition: UV radiation repressed the expression levels of LAR, ANR, and FLS, resulting in reduced ANR activity and a metabolic flux shift towards anthocyanin biosynthesis. | [90] |
| Wuyiqizhong18 | cDNA-AFLP | EBGs: increased expression of CHS. LBGs: increased expression of AT (TDF #3341_2f) and UGT (TDF #2421_1d and TDF #2411_1f). | [79] |
| Proteome | EBGs: increased abundance of CHS and CHI. Metabolic substrate competition: increased abundance of FLS. | [99] | |
| **mingzao | Transcriptome | Phenylpropanoid metabolism: activation of PAL, C4H, and 4CL. LBGs: activation of DFR, ANS/LDOX, and UGT (TEA004632 and TEA004632) genes. | [83] |
| Long**g43 | Transcriptome | Transcriptional regulation: activation of MYB75. LBGs: activation of ANS/LDOX and 3-GT. Anthocyanin transportation: activation of genes involved in anthocyanin transportation (GST, glutathione S-transferase). | [96] |
| Transcriptome | Phenylpropanoid metabolism: activation of PAL and C4H by high temperature and/or light levels in summer. EBGs: activation of CHI and CHS by high temperature and/or light levels in summer. LBGs: activation of ANR, ANS/LDOX, and DFR by high temperature and/or light levels in summer. Metabolic substrate competition: activation of FLS and LAR by high temperature and/or light levels in summer. | [80] | |
| TRFK 306 | Transcriptome | Transcriptional regulation: transcripts encoding pathway regulators of the MYB–bHLH–WD40 (MBW) complex were repressed, possibly contributing to the suppression of late biosynthetic genes of the pathway during the dry season. Anthocyanin transportation: suppression of anthocyanin transport genes could be linked to reduced accumulation of anthocyanin in the vacuole during the dry season. | [81] |
| Zikui | Transcriptome | Transcriptional regulation: CsMYB90 showed strong correlations with petunidin 3-O-glucoside, cyanidin 3-O-galactoside, and cyanidin 3-O-glucosid. LBGs: activation of two F3′H genes and two ANS/LDOX genes. Anthocyanin degradation: three negatively correlated PPO (polyphenol oxidase) genes with anthocyanin accumulation. | [84] |
| Hongyecha, Zijuan, 9803, Hongyafoshou | Transcriptome | Phenylpropanoid metabolism: activation of 4CL. LBGs: activation of ANS/LDOX and UGT. | [88] |
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Fan, Y.-G.; Zhao, T.-T.; **ang, Q.-Z.; Han, X.-Y.; Yang, S.-S.; Zhang, L.-X.; Ren, L.-J. Multi-Omics Research Accelerates the Clarification of the Formation Mechanism and the Influence of Leaf Color Variation in Tea (Camellia sinensis) Plants. Plants 2024, 13, 426. https://doi.org/10.3390/plants13030426
AMA Style
Fan Y-G, Zhao T-T, **ang Q-Z, Han X-Y, Yang S-S, Zhang L-X, Ren L-J. Multi-Omics Research Accelerates the Clarification of the Formation Mechanism and the Influence of Leaf Color Variation in Tea (Camellia sinensis) Plants. Plants. 2024; 13(3):426. https://doi.org/10.3390/plants13030426
Chicago/Turabian StyleFan, Yan-Gen, Ting-Ting Zhao, Qin-Zeng **ang, **ao-Yang Han, Shu-Sen Yang, Li-**a Zhang, and Li-Jun Ren. 2024. "Multi-Omics Research Accelerates the Clarification of the Formation Mechanism and the Influence of Leaf Color Variation in Tea (Camellia sinensis) Plants" Plants 13, no. 3: 426. https://doi.org/10.3390/plants13030426
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