Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature

Zhu, Xujun; Liao, Jieren; **a, **ngli; **ong, Fei; Li, Yue; Shen, Jiazhi; Wen, Bo; Ma, Yuanchun; Wang, Yuhua; Fang, Wan**

doi:10.1186/s12870-019-1646-9

Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature

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Published: 30 January 2019

Volume 19, article number 43, (2019)
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Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature

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Abstract

Background

Internal γ-Aminobutyric Acid (GABA) interacting with stress response substances may be involved in the regulation of differentially abundant proteins (DAPs) associated with optimum temperature and cold stress in tea plants (Camellia sinensis (L.) O. Kuntze).

Results

Tea plants supplied with or without 5.0 mM GABA were subjected to optimum or cold temperatures in this study. The increased GABA level induced by exogenous GABA altered levels of stress response substances – such as glutamate, polyamines and anthocyanins – in association with improved cold tolerance. Isobaric tags for relative and absolute quantification (iTRAQ) – based DAPs were found for protein metabolism and nucleotide metabolism, energy, amino acid transport and metabolism other biological processes, inorganic ion transport and metabolism, lipid metabolism, carbohydrate transport and metabolism, biosynthesis of secondary metabolites, antioxidant and stress defense.

Conclusions

The iTRAQ analysis could explain the GABA-induced physiological effects associated with cold tolerance in tea plants. Analysis of functional protein–protein networks further showed that alteration of endogenous GABA and stress response substances induced interactions among photosynthesis, amino acid biosynthesis, and carbon and nitrogen metabolism, and the corresponding differences could contribute to improved cold tolerance of tea plants.

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Background

Tea is one of the most popular non-alcoholic beverages all over the world, and tea plants (Camellia sinensis (L.) O. Kuntze) are one of the most vital commercial crops in many countries such as China, India, Sri Lanka and Kenya [1]. As an evergreen woody plant, tea is grown from tropical to subtropical areas. Tea plants continuously suffer from a wide variety of environmental stresses, including low temperature, which affects growth, survival and geographical distribution [2]. Cold stress can easily disturb photosynthesis process which is the most important process required for plant production [3, 4]. Intensive studies have explored the molecular, cellular and physiological events that regulate the growth of tea plants and differentiation under cold stress [5,6,7]. For genetic engineering and plant breeding, it is vital to understand the mechanism for regulating tea plants’ growth under cold stress. Extensive molecular and genetic studies have greatly contributed to help us understand how plants survive and grow at low temperature. Various genes and metabolic pathways have been identified that function in enhancing cold tolerance. Well-known stress tolerance mechanisms including damage to membranes, GABA accumulation and its signaling pathways leading to osmotic adjustment, and other mechanisms associated with various secondary messengers, GABA also leads to transcriptional and post-transcriptional regulation [5, 7, 8]. Numerous genes encoding transcription factors and other metabolites related to cold stress have been reported and used for genetic engineering of plants with enhanced cold tolerance [9, 10]. Genome-wide analysis through transcriptomics and proteomics has been employed to illuminate events of some molecular types in environmental stress reaction, and the tea tree genome was sequenced very recently [Full size image

GO and COG analyses of DAPs in response to exogenous GABA at normal and low temperature

The proteins corresponding to the identified peptides in tea plants exposed toT2/T1, T4/T1 and T4/T3 were annotated using Blast2GO according to the cell component, biological and molecular function. According to the molecular functions, the DAPs for T2/T1, T4/T1 and T4 /T3 were classified into nine functional categories. For T2/T1, the main functional categories were protein metabolism and nucleotide metabolism (25.3%), energy (30.9%), amino acid transport and metabolism and other biological processes (11.2%), carbohydrate transport and metabolism (7.9%) and antioxidant and stress defense (15.7%) (Fig. 4a). The identified DAPs were mainly predicted to localize in chloroplast part, plastid part, chloroplast, plastid and thylakoid (Fig. 4b). For T4/T1, the main functional categories were protein metabolism and nucleotide metabolism (30.9%), energy (24.5%), amino acid transport and metabolism and other biological processes (11.8%), carbohydrate transport and metabolism (11.3%) and antioxidant and stress defense (15.2%) (Fig. 4c). The DAPs identified were mainly predicted to localize in chloroplast part, plastid part, chloroplast and thylakoid (Fig. 4d). For T4/T3, the main functional categories were protein metabolism and nucleotide metabolism (31.5%), energy (24.0%), amino acid transport and metabolism and other biological processes (10.8%), carbohydrate transport and metabolism (9.9%) and antioxidant and stress defense (15.0%) (Fig. 4e). The identified DAPs were mainly predicted to localize in chloroplast, plastid, chloroplast part and plastid part (Fig. 4f).

Combined analysis of proteins involved in amino acid transport and contents

To investigate a possible amino acid transport model for proteins involved in exogenous GABA and temperature, we visualized the expression patterns of amino acid transport-related proteins in response to T2/T1, T3/T1, T4/T3, T4/T1 and T4/T2. There were 36 proteins identified as related to amino acid transport (Fig. 5), some of which had important roles in production of stress response substances and metabolic pathways. Previous study indicated that sk1 (Q9SJ05) was strongly expressed attenuated jasmonate (JA), which forerunner OPDA could stop JA-mediated pistil elimination that protecting a machine-made of sk1 [32]. The significance of ASA1(P32068) in JA-induced auxin synthesis was reported and revealed acharacter for JA attenuated auxin transport in roots and local auxin distribution in fine-tuning root meristems [33]. Liepman [34] concluded that Arabidopsis AGT1 (Q9S7E9) was a peroxisomal photorespiratory enzyme that catalyzed transamination reactions with multiple substrates. Phosphotriglyceride kinase (PGK) transforms 1,3- two phosphate glyceride into 3- phosphate glycolic acid, and participates in the trans reaction of glycolysis and Calvin Benson cycle (CBC) during glycolysis, and the double mutants of PGK3 (Q9SAJ4) and phosphoric acid transporter (PGK3.2-TPT3) exhibited a strong growth phenotype, but feasible [35].

A cut off value of a 1.5-fold-change was employed to strictly assessment a protein as being responsive to T2/T1 compared with T4/T3. The results indicated that amino acid transport in treatments with exogenous GABA under optimum and low temperatures had different expression patterns in tea plants. Comparing treatments T3/T1 with T4/T1, the proteins Glycine-rich RNA-binding protein 2 (Q9SVM8), 3-phosphoshikimate 1-carboxyvinyltransferase (P05466), Enolase 1 (Q9C9C4) and Fructose-bisphosphate aldolase 3 (Q9ZU52) had the same expression patterns; and proteins Aldolase superfamily protein (F4IC59), Leucine aminopeptidase 2 (Q944P7), Thiol protease aleurain-like (Q8RWQ9), Reactive Intermediate Deaminase A (Q94JQ4), Proteasome subunit alpha type-2-B (Q8L4A7) showed no significant differences, but had lower expression in T4 than T3. No proteins showed great differences between treatments T4/T1 and T3/T1; and most of the amino acid transport proteins showed the opposite trend in treatments T4/T1 compared with T3/T1. These results indicated that exogenous GABA under cold stress could redirect amino acid transport toward stress response substances that could relieve stress from low temperature in tea plants. All of the amino acid transport proteins had opposite expression patterns between treatments T3/T1 and T4/T3, which indicated that there were different mechanisms relieving low-temperature stress with or without exogenous GABA at the protein level.

The amino acid contents were measured in the four treatments at 0, 4 and 7 days (Additional file 7: Table S7). Surprisingly, most amino acid contents in tea leaves with exogenous GABA at optimum temperature declined by day 7; However, those at low temperature increased immediately. These results also indicated that amino acid metabolism with exogenous GABA at optimum and low temperatures had completely different expression models. Serine and valine contents in tea leaves in the low compared to optimum temperature treatments declined at day 7 but the other amino acid contents rose. The results implied that application of exogenous GABA raised the amino acid contents and so strengthened plant resistance to low temperature. A previous study summarized GABA accumulates rapidly in stress tissue and might supply a key link for event chain that perceives physiological response from environmental pressure. [15] These results indicate that exogenous GABA may lead to transport of amino acids to take part in metabolic pathways to adapt to low temperature.

Interaction network analysis of response to exogenous GABA at low temperature

Proteins do not perform their functions in cells as single entities, but act in a network. [36] There were 47 proteins identified in this interaction network (Fig. 6, Additional file 8: Table S8, S9 & S10). These proteins were classified functionally into carbon fixation in photosynthetic organisms (13 proteins), glyoxylate and dicarboxylate metabolism (11), biosynthesis of amino acids (17), pentose phosphate pathway (8), flavonoid biosynthesis (4), glutathione metabolism (6), TCA cycle (5), ascorbate and aldarate metabolism (4) and purine metabolism (2). These may be critical components in the response to low temperature between with and without exogenous GABA in the tea plants. For example, purple-leaf tea plants are anthocyanin-rich cultivars that are valuable materials for manufacturing teas with unique colors or flavors; and metabolites in the flavonoid biosynthetic pathway remain at high levels in purple leaves [37]. Flavonol synthase can be silenced or overexpressed to shunt the flavonoid biosynthetic pathway toward anthocyanin production without adverse effects on plant growth and development [38]. ACO (1-aminocyclopropane-1-carboxylate oxidase) isoforms might be necessary for plants to synthesis ethylene under various abiotic environment [39].

Discussion

Physiological and proteomic mechanisms with different temperatures and exogenous GABA through GABA shunt

Plants have evolved complex mechanisms to deal with low temperature. When plants sense low temperature, a series of protective mechanisms are triggered – including decreasing malondialdehyde (MDA) content, which is considered to be an indicator of plant oxidative stress; synthesizing cryoprotectant molecules and low-molecular-weight nitrogenous compounds; and improving the scavenging activity of reactive oxygen species (ROS) [40,41,42]. In addition, chlorophyll fluorescence imaging can be employed to evaluate cold tolerance in numerous plants. [43] These alterations help plants keep a metabolic balance of substance and energy in cold environments. Under low temperature, tea plants adopted a ‘survival mode’ as shown by higher free proline content, decreased MDA content, regulating the antioxidant activity and reduced photosynthesis, resulting in growth arrest (Additional file 9: Figure S1 and Additional file 10: Figure S2). GABA can be quickly accumulated and is involved in adapting to low-temperature stress [44, 45]. However, in our study, the endogenous GABA content decreased when plants were exposed to low temperature. We speculate that endogenous GABA degraded to promote synthesis of other stress response substances and feedback to the TCA cycle at low temperature, which showed that other amino acid contents and the DAPs in the TCA cycle were up-regulated at low compared to optimum temperature.

The GABA metabolism in tea plants could regulate the GABA precursor glutamate and PAs contents to relieve anoxia stress in our previous study [67,68,69], which is also important in primary carbon and nitrogen metabolism [70]. Increased GABA promoted the alanine substance accumulation, which entered the proline metabolism and TCA cycle. All amino acid contents except for glycine were increased by elevated GABA at low temperature, which suggested that GABA increased the carbon and nitrogen metabolism. However, the proteins related to the GABA shunt showed no significant changes, but the GABA precursors and the enzyme activity of GABA metabolism clearly changed.

Glyoxylate cycle was firstly discovered in microorganisms, which provided substrates for biosynthetic processes and respiration [71]. In addition to lipids, glyoxylate cycle is another carbon source necessary for growth after germination [72]. Most of the proteins involved in the glyoxylate cycle were down-regulated in response to low temperature with exogenous GABA compared to the control. Furthermore, the exogenous GABA could relieve the cold damage to photosystem II, which was crucial in carbon metabolic [73]. There are many signaling molecules, such as nitrate, ammonium, sugar, amino acids and organic acids, also contain interactions between carbon and nitrogen metabolism [74]. Nitrogen uptake and metabolism is contributed by carbon metabolism since it requires carbon skeletons, reducing power, ATP, reductants and co-transporters. [73, 75,76,77]. Their control may be closely linked and coordinated at the level of gene expression [78]. However, only aminomethyl transferase and fructose-bisphosphate aldolases (FBAs) were up-regulated in the TCA cycle, glyoxylate and dicarboxylate metabolism, and carbon fixation in photosynthetic organisms in treatment T4 compared to T3. Fructose 1,6-bisphosphate aldolases, which are important in the Calvin-Benson cycle (CBC), were dramatically altered when tomato seedlings suffer from heat/cold stresses [79]. This might imply that exogenous GABA application could improve photosynthesis to regulate low-temperature response through FBA expression and enzyme activity.

The above evidence suggests that, as a signal molecule, GABA regulates the glyoxylate cycle, the TCA cycle and carbon fixation in photosynthetic organ metabolism in a complex manner, especially in the carbon and nitrogen cycle. It will be interesting to establish how tea plants respond to low temperature via different mechanisms and how the signal molecule GABA influences the operating mechanisms. Several genes in the TCA cycle, glyoxylate cycle and carbon fixation in photosynthetic organisms had their relative expression determined by RT-qPCR (Fig. 9b) and the expression mode of genes was similar to the response of related DAPs.

Oxidative pentose phosphate pathway and purine metabolism and exogenous GABA at low temperature

The energy and metabolic intermediates in the biosynthesis are mainly derived from the pentose oxidation pathway. However, further details are needed on how the pathway and its effects on other processes in plants. Nitrate is the major source of nitrogen that plants need, and the location of nitrate assimilation significantly affect the plant energy budget [73]. This implies that exogenous GABA application could affect the energy budget in tea plants. Only FBA in the oxidative pentose phosphate pathway was up-regulated in treatment T4 compared to T3 here. Lu et al. [80] reported that all FBA genes in Arabidopsis thaliana, except AtFBA6, were up-regulated in response to cold stress. The carbon skeleton of the amino acid synthesis pathway arises from different sectors of the respiratory pathway. Some root in the oxidative pentose phosphate pathway (or, in the light, the CBC) and glycolysis (Ery4P and PEP for the synthesis of aromatic amino acids), some stem from the final product of glycolysis (pyruvate for alanine) and other organic acids from the TCA cycle [73]. For treatment T4 compared to T3, FBA was not only in glycolysis cycle but also in CBC, FBA2 and FBA3 genes were up-regulated, but the DAPs in the TCA cycle were down-regulated. Testing how the application of exogenous GABA in tea plants affects the respiration pathway of amino acid biosynthesis through reverse genetic pathway under low temperature, is further needed.

Purine nucleotides are produced by two distinct routes in plants: de novo and salvage pathways. The de novo synthesis employs 5-phosphoribosyl-1-pyrophosphate, aspartate, glycine, glutamine, HCO³⁻ and 10-formyltetrahydrofolateas for building blocks, which could be found in all plants, such as tea-leaves; however, the salvage pathways are more diverse and less well understood [81, 82]. Tea plants engender special nitrogen compounds including theanine and caffeine and their effects on human health have been studied in detail [83]. In order to against herbivores and pathogens, young shoots will accumulate caffeine and leaves may be treated as a chemical defense of young soft tissue [84]. All the DAPs in purine metabolism, except ureidoglycolate amidohydrolase, were up-regulated (Fig. 10a).

Thus, the evidence suggests that exogenous GABA application either directly or indirectly stimulated flux into amino acid and caffeine biosynthesis and regulated the plant energy budget. This affected the resistance to cold in tea plants and the quality of tea flavor through the oxidative pentose phosphate pathway and purine metabolism. Key genes in the oxidative pentose phosphate pathway and purine metabolism were selected for RT-qPCR, which showed that expression mode of genes were similar to that of related DAPs (Fig. 10b). Above all, the effects of exogenous GABA at low temperature on physiological index and DAPs in metabolism pathways, were summarized on Fig. 11.

Conclusions

GABA effectively improved tea plant tolerance at low temperature and regulated various physio-biochemical processes at optimum condition, as reflected by higher SPAD value, chlorophyll fluorescence transients and membrane stability, as well as antioxidant activity regulation. The iTRAQ-based protein profiling offered a global road to show metabolic processes related to plant tolerance which was regulated by endogenous GABA at low temperature. Not only the transformation of endogenous GABA is further demonstrated in functional protein networks, but also is revealed in metabolism pathways, such as flavonoid metabolism, amino acid metabolism, AsA/glutathione cycle, TCA cycle, glyoxylate cycle, carbon fixation in photosynthetic organisms, oxidative pentose phosphate pathway and purine metabolism cause an interaction among plant cell components like chloroplasts, plastids and thylakoids. How GABA works as a signaling molecule involving in tea plants resistance regulation under cold stress, may be an interesting topic in the future work.

Abbreviations

ABA:: Abscisic acid
ACO:: 1-Amino cyclopropane carboxylic acid oxidase
AGT1 :: Alanine-glyoxylate transaminase
AlaAT:: Alanine aminotransferase
ALDH1 :: Aldehyde dehydrogenase
APX:: AsA peroxidase
ASA1:: anthranilate synthase alpha subunit 1
BAN:: NAD(P)-binding Rossmann-fold superfamily protein
CAT:: Catalase
CBC:: Calvin-Benson cycle
CHI1 :: Shalcone flavanone isomerase 1
CHS :: Chalcone synthase
CM2 :: Chorismate mutase 2
CYFBP :: Fructose-1,6-bisphosphatase
DAO:: Diamine oxidase
DAPs:: Differentially abundant proteins
F3H :: Flavanone 3-hydroxylase
FBA:: Fructose-1,6-bisphosphate aldolase
FBA2 :: Fructose-bisphosphate aldolase 2
FLS1 :: Flavonol synthase 1
GABA:: Gamma-aminobutyric acid
GABAT:: Gamma aminobutyrate transaminase
GAD:: Glutamate decarboxylase
GAPB:: Glyceraldehyde-3-phosphate dehydrogenase B subunit
GDH3 :: Glutamate dehydrogenase 3
GGAT2 :: Glutamate--glyoxylate aminotransferase 2-like
GLDP2 :: Glycine decarboxylase P-protein 2
GLN1–4 :: Glutamine synthetase 1–4
GLO1 :: Glyoxalase
GME:: GDP-mannose-3′, 5′-diisomerase
GPX7 :: Glutathione peroxidase 7
GS:: Glutamine synthetase
GSTF10 :: Glutathione S-transferase PHI 10
GSTF9 :: Glutathione S-transferase PHI 9
H₂O₂ :: Hydrogen peroxide
iTRAQ:: Isobaric tags for relative and absolute quantification
LAP2 :: Cytosol aminopeptidase family protein
LGALDH :: L-galactose dehydrogenase
MDA:: Malondialdehyde
MDAR5 :: Monodehydroascorbate reductase 5, chlorplastic-like
MDH:: Malate dehydrogenase
METK4 :: S-adenosylmethionine synthetase 4
NADP-ME4 :: NADP-malic enzyme 4
PAO:: Polyamine oxidase
PAs:: Polyamines
PDH-E1 :: Pyruvate dehydrogenase E1
PEP:: Phosphoenolpyruvate
PGK:: Phosphotriglyceride kinase
PGK3 :: Phosphoglycerate kinase precursor
PGK3.2-TPT3:: phosphoric acid transporter
PMDH1 :: Peroxisomal NAD-malate dehydrogenase 1
POD:: Peroxidase
Put:: Putrescine
RBCL :: Ribulose-1,5-bisphosphate carboxylase/oxygenase large subunit
RBCS-2B :: Ribulose bisphosphate carboxylase small chain 2B
ROS:: Reactive oxygen species
RPE :: Ribulose-5-phosphate-3-epimerase
SDH:: Succinate dehydrogenase
SDH1–1 :: succinate dehydrogenase 1–1
SK1 :: Shikimate kinase 1
SOD:: Superoxide dismutase
Spd:: Spermidine
Spm:: Spermine
TCA cycle:: Tricarboxylic acid cycle
TKL-2 :: Transketolase 2

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Acknowledgements

The authors would like to thank the reviewers for their valuable comments and suggestions to improve the quality of the manuscript.

Funding

This research was supported by The Fundamental Research Funds for the Central Universities (KYZ201842; KYZ201841), The National Natural Science Foundation of China (31870680), The Earmarked Fund for China Agriculture Research System (CARS-19), The earmarked fund for Jiangsu Agricultural Industry Technology System (JATS[2018]280), and Jiangsu Agriculture Science and Technology Innovation Fund (CX(17)2018). The Funding bodies had no influence over the experimental design, data analysis or interpretation, or manuscript writing.

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The data sets are included within the article and its Additional files.

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Xujun Zhu and Jieren Liao contributed equally to this work.

Authors and Affiliations

College of Horticulture, Nan**g Agricultural University, No.1 Weigang, Nan**g, Jiangsu Province, 210095, People’s Republic of China
Xujun Zhu, Jieren Liao, ** Fang
Wuxi NextCODE Genomics, 288 Fute Zhong Road, Shanghai, 200131, People’s Republic of China
Yue Li

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Xujun Zhu
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Jieren Liao
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**ngli **a
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Fei **ong
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Yue Li
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Jiazhi Shen
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Bo Wen
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Yuanchun Ma
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Yuhua Wang
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Wan** Fang
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Contributions

XZ JL WF designed and conducted the experiments, JL XX YL FX JS BW YM YW analyzed the data, JL XZ drafted the manuscript, WF supervised the project. All authors have read and approved the final version of this manuscript.

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Correspondence to Wan** Fang.

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Additional files

Additional file 1:

Table S1: Nucleotide sequences of primers specific to flavonoid biosynthesis, amino acid metabolism and AsA/glutathione cycle, TCA cycle, glyoxylate cycle and carbon fixation in photosynthetic organisms and oxidative pentose phosphate pathway and purine metabolism related genes used for qRT-PCR. (XLSX 10 kb)

Additional file 2:

Table S2: Functional classifications of identified proteins significantly expressed in leaves of tea plants exposed to the treatments T2/T1 for 7 days (25 °C and 25 °C + GABA for T1 and T2 respectively). Each value represents the average of three biological replicates. The average is significant at a p < 0.01 level. A t-test value < 0.05 is considered to be significant between treatment T2 and T1. (XLSX 41 kb)

Additional file 3:

Table S3: Functional classifications of identified proteins significantly expressed in leaves of tea plants exposed to the treatments T4/T3 for 7 days (4 °C and 4 °C + GABA for T3 and T4, respectively). Each value represents the average of three biological replicates. The average is significant at a p < 0.01 level. A t-test value < 0.05 is considered to be significant between treatment T4 and T3. (XLSX 47 kb)

Additional file 4:

Table S4: Functional classifications of identified proteins significantly expressed in leaves of tea plants exposed to the treatments T4/T1 for 7 days (25 °C and 4 °C + GABA for T1 and T4, respectively). Each value represents the average of three biological replicates. The average is significant at a p < 0.01 level. At-test value < 0.05 is considered to be significant between treatment T4 and T1. (XLSX 40 kb)

Additional file 5:

Table S5: Functional classifications of identified proteins significantly expressed in leaves of tea plants exposed to the treatments T3/T1 for 7 days (25 °C and 4 °C for T1 and T3, respectively). Each value represents the average of three biological replicates. The average is significant at a p < 0.01 level. A t-test value < 0.05 is considered to be significant between treatment T3 and T1. (XLSX 32 kb)

Additional file 6:

Table S6: Functional classifications of identified proteins significantly expressed in leaves of tea plants exposed to the treatments T4/T2 for 7 days (25 °C + GABA and 4 °C + GABA for T2 and T4, respectively). Each value represents the average of three biological replicates. The average is significant at a p < 0.01 level. At-test value < 0.05 is considered to be significant between treatment T4 and T2. (XLSX 27 kb)

Additional file 7:

Table S7: The contents of amino acids composition in tea plant leaves in the treatments T1, T2, T3, T4 at day 0, 4, 7 (25 °C, 25 °C + GABA, 4 °C and 4 °C + GABA for T1, T2, T3 and T4, respectively). All experiments were performed in triplicate. Data represent the mean value ± standard deviation. Means with different letters are significantly different fromeach other (p ≤ 0.05). Asp, Aspartic acid; Ser, Serine; Glu, Glutamate; Gly, Glycine; Ala, Alanine; Cys, Cysteine; Val, Valine; Met, Methionine; Ile, Isoleucine; Leu, Leucine; Tyr, Tyrosine; Phe, Phenylalanine; GABA, Gama-aminobutyric acid; Lys, Lysine; His, Histidine; Trp, Tryptophane; Arg, arginine. (DOCX 15 kb)

Additional file 8:

Table S8, S9 & S10: Sequences of all unique peptides matched to each identified proteins. (ZIP 1383 kb)

Additional file 9:

Figure S1: Changes in free proline content and MDA activity during the four treatments (25 °C, 25 °C + GABA, 4 °C and 4 °C + GABA for T1, T2, T3 and T4, respectively). All experiments were performed in triplicate. Data represent the mean value ± standard deviation. Means with different letters are significantly different from each other (p ≤ 0.05). MDA, malonaldehyde. (PDF 153 kb)

Additional file 10:

Figure S2: Changes in antioxidant enzyme activity during the four treatments (25 °C, 25 °C + GABA, 4 °C and 4 °C + GABA for T1, T2, T3 and T4, respectively). Data represent the mean value ± standard deviation. Means with different letters are significantly different from each other (p ≤ 0.05). CAT, catalase; SOD, superoxide dismutase; POD, peroxidase. (PDF 167 kb)

Additional file 11:

Figure S3: Changes in DAO, PAO, GAD and GABA-T activity. Data represent the mean value ± standard deviation. Means with different letters are significantly different from each other (p ≤ 0.05). DAO, diamine oxidase; PAO, polyamine oxidase; GAD, glutamate decarboxylase; GABA-T, GABA transaminase. (PDF 170 kb)

Additional file 12:

Figure S4: Changes in polyamines contents during the four treatments (25 °C, 25 °C + GABA, 4 °C and 4 °C + GABA for T1, T2, T3 and T4, respectively). Data represent the mean value ± standard deviation. Means with different letters are significantly different from each other (p ≤ 0.05). Put, putrescine; Spd, spermidine; Spm, spermine. (PDF 158 kb)

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Zhu, X., Liao, J., **a, X. et al. Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature. BMC Plant Biol 19, 43 (2019). https://doi.org/10.1186/s12870-019-1646-9

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Received: 02 August 2018
Accepted: 11 January 2019
Published: 30 January 2019
DOI: https://doi.org/10.1186/s12870-019-1646-9

Physiological and iTRAQ-based proteomic analyses reveal the function of exogenous γ-aminobutyric acid (GABA) in improving tea plant (Camellia sinensis L.) tolerance at cold temperature

Abstract

Background

Results

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Background

GO and COG analyses of DAPs in response to exogenous GABA at normal and low temperature

Combined analysis of proteins involved in amino acid transport and contents

Interaction network analysis of response to exogenous GABA at low temperature

Discussion

Physiological and proteomic mechanisms with different temperatures and exogenous GABA through GABA shunt

Oxidative pentose phosphate pathway and purine metabolism and exogenous GABA at low temperature

Conclusions

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