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Molecular identification and characterization of a serine carboxypeptidase-like gene associated with abiotic stress in tea plant, Camellia sinensis (L.)

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Abstract

Tea (Camellia sinensis L.) contains secondary metabolites including polyphenolic proanthocyanidins (PAs) and their precursors. The SCPL (serine carboxypeptidase-like) proteins are a group of acyltransferase enzymes that modify plant natural products. We isolated CsSCPL, which encodes a SCPL protein, from oolong tea. Sequence alignment analyses showed that CsSCPL is a serine carboxypeptidase with high homology to other SCPLs, including those in persimmon, grape, woodland strawberry, and sweet orange. Quantitative RT-PCR analyses revealed that the highest transcript levels of CsSCPL were in young leaves of tea seedlings and buds of mature plants. CsSCPL transcription increased in response to heat but decreased in response to cold, high salinity, and drought. The degree of epigallocatechin galloylation increased after heat treatment and the degree of epicatechin galloylation decreased after cold treatment. In field-grown tea plants, the highest transcript levels of CsSCPL were in summer. Together, these results show that CsSCPL transcripts accumulate in one-tip-two-leaf tissues of oolong tea plants during the hottest parts of the growing season, and in response to abiotic stress. The degree of catechin galloylation was positively correlated with CsSCPL transcript levels after heat or cold treatments. Our results will be useful for further research on the functions of SCPLs in plants.

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References

  • Astill C, Birch MR, Dacombe C, Humphrey PG, Martin PT (2001) Factors affecting the caffeine and polyphenol contents of black and green tea infusions. J Agric Food Chem 49(11):5340–5347

    Article  CAS  PubMed  Google Scholar 

  • Bizjak J, Weber N, Mikulic-Petkovsek M, Alam Z, Thill J, Stich K, Halbwirth H, Veberic R (2013) Polyphenol gene expression and changes in anthocyanins and polyphenols in the skin of ‘Braeburn’ apples after the autumn application of prohexadione-calcium. Plant Growth Regul 71(3):225–233

    Article  CAS  Google Scholar 

  • Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140(4):1384–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buer CS, Muday GK, Djordjevic MA (2007) Flavonoids are differentially taken up and transported long distances in Arabidopsis. Plant Physiol 145(2):478–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen GH, Yang CY, Lee SJ, Wu CC, Tzen JTC (2014) Catechin content and the degree of its galloylation in oolong tea were inversely correlated with cultivation altitude. J Food Drug Anal 22:303–309

    Article  Google Scholar 

  • Das A, Das S, Mondal TK (2012) Identification of Differentially expressed gene profiles in young roots of tea [Camellia sinensis (L.) O. Kuntze] subjected to drought stress using suppression subtractive hybridization. Plant Mol Biol Rep 30(5):1088–1101

    Article  CAS  Google Scholar 

  • Debeaujon I, Leon-Kloosterziel KM, Koornneef M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 122(2):403–414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng WW, Fei Y, Wang S, Wan XC, Zhang ZZ, Hu XY (2013) Effect of shade treatment on theanine biosynthesis in Camellia sinensis seedlings. Plant Growth Regul 71(3):295–299

    Article  CAS  Google Scholar 

  • Eungwanichayapant PD, Popluechai S (2009) Accumulation of catechins in tea in relation to accumulation of mRNA from genes involved in catechin biosynthesis. Plant Physiol Biochem 47(2):94–97

    Article  CAS  PubMed  Google Scholar 

  • Feng Y, Xue Q (2006) The serine carboxypeptidase like gene family of rice (Oryza sativa L. ssp. japonica). Funct Integr Genomics 6(1):14–24

    Article  CAS  PubMed  Google Scholar 

  • Fraser CM, Rider LW, Chapple C (2005) An expression and bioinformatics analysis of the Arabidopsis serine carboxypeptidase-like gene family. Plant Physiol 138(2):1136–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita A, Soma N, Goto-Yamamoto N, Shindo H, Kakuta T, Koizumi T, Hashizume K (2005) Anthocyanidin reductase gene expression and accumulation of flavan-3-ols in grape berry. Am J Enol Viticult 56(4):336–342

    CAS  Google Scholar 

  • Hayashi N, Chen R, Hiraoka M, Ujihara T, Ikezaki H (2010) Beta-cyclodextrin/surface plasmon resonance detection system for sensing bitter-astringent taste intensity of green tea catechins. J Agric Food Chem 58(14):8351–8356

    Article  CAS  PubMed  Google Scholar 

  • Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125(2):683–700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikegami A, Eguchi S, Kitajima A, Inoue K, Yonemori K (2007) Identification of genes involved in proanthocyanidin biosynthesis of persimmon (Diospyros kaki) fruit. Plant Sci 172(5):1037–1047

    Article  CAS  Google Scholar 

  • Jiang X, Liu Y, Li W, Zhao L, Meng F, Wang Y, Tan H, Yang H, Wei C, Wan X, Gao L, Xia T (2013) Tissue-specific, development-dependent phenolic compounds accumulation profile and gene expression pattern in tea plant [Camellia sinensis]. PLoS One 8(4):e62315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kondo S, Fiebig A, Okawa K, Ohara H, Kowitcharoen L, Nimitkeatkai H, Kittikorn M, Kim M (2011) Jasmonic acid, polyamine, and antioxidant levels in apple seedlings as affected by ultraviolet-C irradiation. Plant Growth Regul 64(1):83–89

    Article  CAS  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157(1):105–132

    Article  CAS  PubMed  Google Scholar 

  • Lehfeldt C, Shirley AM, Meyer K, Ruegger MO, Cusumano JC, Viitanen PV, Strack D, Chapple C (2000) Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 12(8):1295–1306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li AX, Steffens JC (2000) An acyltransferase catalyzing the formation of diacylglucose is a serine carboxypeptidase-like protein. Proc Natl Acad Sci USA 97(12):6902–6907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H, Wang X, Zhang H, Yang Y, Ge X, Song F (2008) A rice serine carboxypeptidase-like gene OsBISCPL1 is involved in regulation of defense responses against biotic and oxidative stress. Gene 420(1):57–65

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Gao L, Liu L, Yang Q, Lu Z, Nie Z, Wang Y, Xia T (2012) Purification and characterization of a novel galloyltransferase involved in catechin galloylation in the tea plant (Camellia sinensis). J Biol Chem 287(53):44406–44417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milkowski C, Strack D (2004) Serine carboxypeptidase-like acyltransferases. Phytochemistry 65(5):517–524

    Article  CAS  PubMed  Google Scholar 

  • Mugford ST, Milkowski C (2012) Serine carboxypeptidase-like acyltransferases from plants. Methods Enzymol 516:279–297

    Article  CAS  PubMed  Google Scholar 

  • Mugford ST, Osbourn A (2010) Evolution of serine carboxypeptidase-like acyltransferases in the monocots. Plant Signal Behav 5(2):193–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mugford ST, Qi X, Bakht S, Hill L, Wegel E, Hughes RK, Papadopoulou K, Melton R, Philo M, Sainsbury F, Lomonossoff GP, Roy AD, Goss RJ, Osbourn A (2009) A serine carboxypeptidase-like acyltransferase is required for synthesis of antimicrobial compounds and disease resistance in oats. Plant Cell 21(8):2473–2484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mujib A, Ilah A, Aslam J, Fatima S, Siddiqui ZH, Maqsood M (2012) Catharanthus roseus alkaloids: application of biotechnology for improving yield. Plant Growth Regul 68(2):111–127

    Article  CAS  Google Scholar 

  • Pang Y, Abeysinghe IS, He J, He X, Huhman D, Mewan KM, Sumner LW, Yun J, Dixon RA (2013) Functional characterization of proanthocyanidin pathway enzymes from tea and their application for metabolic engineering. Plant Physiol 161(3):1103–1116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JS, Kim JB, Hahn BS, Kim KH, Ha SH, Kim JB, Kim YH (2004) EST analysis of genes involved in secondary metabolism in Camellia sinensis (tea), using suppression subtractive hybridization. Plant Sci 166(4):953–961

    Article  CAS  Google Scholar 

  • Perva-Uzunalic A, Skerget M, Knez Z, Weinreich B, Otto F, Gruner S (2006) Extraction of active ingredients from green tea (Camellia sinensis): extraction efficiency of major catechins and caffeine. Food Chem 96(4):597–605

    Article  CAS  Google Scholar 

  • Petroni K, Tonelli C (2011) Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci 181(3):219–229

    Article  CAS  PubMed  Google Scholar 

  • Saeid ZD, Zahra A, Abdolhamid NS (2014) Investigation of synergistic action between coronatine and nitric oxide in alleviating arsenic-induced toxicity in sweet basil seedlings. Plant Growth Regul 74(2):119–130

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425

    CAS  PubMed  Google Scholar 

  • Shirley AM, McMichael CM, Chapple C (2001) The sng2 mutant of Arabidopsis is defective in the gene encoding the serine carboxypeptidase-like protein sinapoylglucose:choline sinapoyltransferase. Plant J 28(1):83–94

    Article  CAS  PubMed  Google Scholar 

  • Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O, Delcher AL, Jaiswal P, Mockaitis K, Liston A, Mane SP, Burns P, Davis TM, Slovin JP, Bassil N, Hellens RP, Evans C, Harkins T, Kodira C, Desany B, Crasta OR, Jensen RV, Allan AC, Michael TP, Setubal JC, Celton JM, Rees DJ, Williams KP, Holt SH, Ruiz Rojas JJ, Chatterjee M, Liu B, Silva H, Meisel L, Adato A, Filichkin SA, Troggio M, Viola R, Ashman TL, Wang H, Dharmawardhana P, Elser J, Raja R, Priest HD, Bryant DW Jr, Fox SE, Givan SA, Wilhelm LJ, Naithani S, Christoffels A, Salama DY, Carter J, Lopez Girona E, Zdepski A, Wang W, Kerstetter RA, Schwab W, Korban SS, Davik J, Monfort A, Denoyes-Rothan B, Arus P, Mittler R, Flinn B, Aharoni A, Bennetzen JL, Salzberg SL, Dickerman AW, Velasco R, Borodovsky M, Veilleux RE, Folta KM (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43(2):109–116

    Article  CAS  PubMed  Google Scholar 

  • Stehle F, Brandt W, Stubbs MT, Milkowski C, Strack D (2009) Sinapoyltransferases in the light of molecular evolution. Phytochemistry 70(15–16):1652–1662

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terrier N, Torregrosa L, Ageorges A, Vialet S, Verries C, Cheynier V, Romieu C (2009) Ectopic expression of VvMybPA2 promotes proanthocyanidin biosynthesis in grapevine and suggests additional targets in the pathway. Plant Physiol 149(2):1028–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol (Stuttg) 7(6):581–591

    Article  CAS  Google Scholar 

  • Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao WB, Hao BH, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45(1):59–66

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Mr. Jian-Syun Chen for his generous supply of tea plants. This work was supported by a grant from the National Science Council, Taiwan, R.O.C. (NSC 103-2313-B-005-006).

Author's Contributions

The work presented here was carried out in collaboration between all authors. Dr. Jason T. C. Tzen and Dr. Chin-Ying Yang collaboration defined the research theme, designed experiments and analyzed the data. Dr. Chin-Ying Yang wrote the manuscript. Chih-Hao Chiu carried out the experiments and analyzed the data. Guan-Heng Chen carried out the HPLC analysis.

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Authors and Affiliations

  1. Graduate Institute of Biotechnology, National Chung-Hsing University, Taichung, 40227, Taiwan

    Chih-Hao Chiu, Guan-Heng Chen & Jason T. C. Tzen

  2. Department of Agronomy, National Chung Hsing University, Taichung, 40227, Taiwan

    Chin-Ying Yang

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  1. Chih-Hao Chiu
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  2. Guan-Heng Chen
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  3. Jason T. C. Tzen
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  4. Chin-Ying Yang
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Correspondence to Jason T. C. Tzen or Chin-Ying Yang.

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Chiu, CH., Chen, GH., Tzen, J.T.C. et al. Molecular identification and characterization of a serine carboxypeptidase-like gene associated with abiotic stress in tea plant, Camellia sinensis (L.). Plant Growth Regul 79, 345–353 (2016). https://doi.org/10.1007/s10725-015-0138-7

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  • DOI: https://doi.org/10.1007/s10725-015-0138-7

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