Advertisement

Protoplasma

, Volume 256, Issue 2, pp 359–370 | Cite as

Identification of genes revealed differential expression profiles and lignin accumulation during leaf and stem development in tea plant (Camellia sinensis (L.) O. Kuntze)

  • Yong-Xin Wang
  • Rui-Min Teng
  • Wen-Li Wang
  • Ying Wang
  • Wei Shen
  • Jing ZhuangEmail author
Original Article
  • 328 Downloads

Abstract

Lignin is a complex aromatic heteropolymer that plays essential roles in mechanical support, water transport, and response to biotic and abiotic stresses. The tea plant is a leaf-type beverage crop, which serves as a resource for non-alcoholic beverage tea. The content and distribution of lignin in tea plant leaves seriously affect the quality of tea. However, the biosynthetic pathways of lignin remain to be characterized in the tea plant. In the present study, lignin accumulation was investigated in tea plant leaves and stems at three developmental stages. The lignin content continuously increased during leaf and stem development in both tea plant cultivars ‘Fudingdabai’ and ‘Suchazao.’ The lignin distribution and anatomical characteristics of the tea plant leaves coincided with lignin accumulation and showed that lignin is mainly distributed in the epidermis, xylem, and vascular bundle sheath. ‘Suchazao’ exhibits a low lignin content and lacks a vascular bundle sheath. Twelve genes encoding the enzymes involved in the lignin biosynthesis of tea plant were identified and included CsPAL, CsC4H, Cs4CL, CsHCT, CsC3H, CsCCoAOMT, CsCCR, CsCAD, CsF5H, CsCOMT, CsPER, and CsLAC. The expression profiling of lignin biosynthesis-related genes and analysis of lignin accumulation may help elaborate the regulatory mechanisms of lignin biosynthesis in tea plant.

Keywords

Camellia sinensis Lignin Development Gene expression Leaf Stem 

Abbreviations

4CL

4-Coumarate-CoA ligase

C3′H

p-Coumaroyl shikimate/quinate 3′-hydroxylase

C4H

Cinnamate 4-hydroxylase

CAD

Cinnamyl alcohol dehydrogenase

CCoAOMT

Caffeoyl-CoA O-methyltransferase

CCR

Cinnamoyl-CoA reductase

COMT

Caffeic acid O-methyltransferase

F5H

Ferulate 5-hydroxylase

HCT

Hydroxycinnamoyl-CoA shikimate/quinate hydroxycinnamoyl transferase

LAC

Laccase

PAL

Phenylalanine ammonia lyase

PER

Peroxidase

qRT-PCR

Quantitative real-time polymerase chain reaction

Notes

Author contributions

Conceived and designed the experiments: JZ and YXW. Performed the experiments: YXW, RMT, WLW, YW, WS, and JZ. Analyzed the data: YXW. Contributed reagents/materials/analysis tools: JZ. Wrote the paper: YXW. Revised the paper: JZ YXW. All authors read and approved the final manuscript.

Funding

The research was supported by the National Natural Science Foundation of China (31570691).

Compliance with ethical standards

Competing interests

The authors declare that there are no competing interests.

Supplementary material

709_2018_1299_MOESM1_ESM.doc (83 kb)
ESM 1 (DOC 83 kb)

References

  1. Ali MB, Jr MND (2014) Induced transcriptional profiling of phenylpropanoid pathway genes increased flavonoid and lignin content in Arabidopsis leaves in response to microbial products. BMC Plant Biol 14(1):1–14Google Scholar
  2. Armin W, Lloyd D, Hoon K, Lorelle P, Heather F, Diane S, Kirk T, Gerald K, Uwe S, John R (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol 149(1):370–383Google Scholar
  3. Arscott SA, Tanumihardjo SA (2010) Carrots of many colors provide basic nutrition and bioavailable phytochemicals acting as a functional food. Compr Rev Food Sci Food Saf 9(2):223–239.  https://doi.org/10.1111/j.1541-4337.2009.00103.x Google Scholar
  4. Berthet S, Demontcaulet N, Pollet B, Bidzinski P, Cézard L, Bris PL, Borrega N, Hervé J, Blondet E, Balzergue S (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23(3):1124–1137PubMedPubMedCentralGoogle Scholar
  5. Blanchette RA, Biggs AR (1992) Defense mechanisms of woody plants against fungi. SpringerGoogle Scholar
  6. Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54(1):519–546PubMedGoogle Scholar
  7. Bottcher A, Cesarino I, Santos AB, Vicentini R, Mayer JL, Vanholme R, Morreel K, Goeminne G, Moura JC, Nobile PM (2013) Lignification in sugarcane: biochemical characterization, gene discovery, and expression analysis in two genotypes contrasting for lignin content. Plant Physiol 163(4):1539–1557PubMedPubMedCentralGoogle Scholar
  8. Boudet AM, Kajita S, Grima-Pettenati J, Goffner D (2003) Lignins and lignocellulosics: a better control of synthesis for new and improved uses. Trends Plant Sci 8(12):576–581PubMedGoogle Scholar
  9. Bouvier dYM, Bouchabke-Coussa O, Voorend W, Antelme S, Cézard L, Legée F, Lebris P, Legay S, Whitehead C, Mcqueen-Mason SJ (2013) Disrupting the cinnamyl alcohol dehydrogenase 1 gene (BdCAD1) leads to altered lignification and improved saccharification in Brachypodium distachyon. Plant J Cell Mol Biol 73(3):496–508Google Scholar
  10. Cardinal AJ, Lee M, Moore KJ (2003) Genetic mapping and analysis of quantitative trait loci affecting fiber and lignin content in maize. Theor Appl Genet 106(5):866–874PubMedGoogle Scholar
  11. Cheng X, Li M, Li D, Zhang J, Jin Q, Sheng L, Cai Y, Lin Y (2017) Characterization and analysis of CCR and CAD gene families at the whole-genome level for lignin synthesis of stone cells in pear (Pyrus bretschneideri) fruit. Biol Open 6(11):1602–1613PubMedPubMedCentralGoogle Scholar
  12. Chong, Xu CJ, Li X, Ferguson I, Chen (2006) Accumulation of lignin in relation to change in activities of lignification enzymes in loquat fruit flesh after harvest. Postharvest Biol Technol 40(2):163–169Google Scholar
  13. Coates AL, Boyce P, Shaw DG, Godfrey S, Mearns (1999) Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial Kraft pulping. Plant Physiol 119(1):153–164Google Scholar
  14. Coleman HD, Park JY, Nair R, Chapple C, Mansfield SD (2008) RNAi-mediated suppression of p-coumaroyl-CoA 3'-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc Natl Acad Sci U S A 105(11):4501–4506PubMedPubMedCentralGoogle Scholar
  15. Deng WW, Zhang M, Wu JQ, Jiang ZZ, Tang L, Li YY, Wei CL, Jiang CJ, Wan XC (2013) Molecular cloning, functional analysis of three cinnamyl alcohol dehydrogenase (CAD) genes in the leaves of tea plant, Camellia sinensis. J Plant Physiol 170(3):272–282PubMedGoogle Scholar
  16. Donaldson LA, Knox JP (2012) Localization of Cell Wall polysaccharides in normal and compression wood of Radiata pine: relationships with lignification and microfibril orientation. Plant Physiol 158(2):642–653PubMedGoogle Scholar
  17. Gedda L (2012) Light-induced expression of genes involved in phenylpropanoid biosynthetic pathways in callus of tea (Camellia sinensis (L.) O. Kuntze). Sci Hortic 133(1):72–83Google Scholar
  18. Giordano A, Liu Z, Panter SN, Dimech AM, Shang Y, Wijesinghe H, Fulgueras K, Ran Y, Mouradov A, Rochfort S (2014) Reduced lignin content and altered lignin composition in the warm season forage grass Paspalum dilatatum by down-regulation of a Cinnamoyl CoA reductase gene. Transgenic Res 23(3):503–517PubMedPubMedCentralGoogle Scholar
  19. Goujon T, Sibout R, Eudes A, MacKay J, Joulanin L (2003) Genes involved in the biosynthesis of lignin precursors in Arabidopsis thaliana. Plant Physiol Biochem 41(8):677–687.  https://doi.org/10.1016/S0981-9428(03)00095-0 Google Scholar
  20. Gui J, Shen J, Li L (2011) Functional characterization of evolutionarily divergent 4-coumarate:coenzyme a ligases in rice. Plant Physiol 157(2):574–586PubMedPubMedCentralGoogle Scholar
  21. Guo DJ, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13(1):73–88.  https://doi.org/10.1105/Tpc.13.1.73 PubMedPubMedCentralGoogle Scholar
  22. Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5(3):224–229.  https://doi.org/10.1016/S1369-5266(02)00257-1 PubMedGoogle Scholar
  23. Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci U S A 96(18):10045–10050PubMedPubMedCentralGoogle Scholar
  24. Jia XL, Wang GL, Xiong F, Yu XR, Xu ZS, Wang F, Xiong AS (2015) De novo assembly, transcriptome characterization, lignin accumulation, and anatomic characteristics: novel insights into lignin biosynthesis during celery leaf development. Sci Rep 5:8259PubMedPubMedCentralGoogle Scholar
  25. Kao YY, Harding SA, Tsai CJ (2002) Differential expression of two distinct phenylalanine ammonia-lyase genes in condensed tannin-accumulating and lignifying cells of quaking aspen. Plant Physiol 130(2):796–807.  https://doi.org/10.1104/pp.006262 PubMedPubMedCentralGoogle Scholar
  26. Li S, Zhou J (2001) Content changes of lignin, cellulose and soluble sugar and their correlations with hollowness during storage in radishes. Journal of Anhui Agricultural UniversityGoogle Scholar
  27. Li CF, Zhu Y, Yu Y, Zhao QY, Wang SJ, Wang XC, Yao MZ, Luo D, Li X, Chen L (2015a) Global transcriptome and gene regulation network for secondary metabolite biosynthesis of tea plant (Camellia sinensis). BMC Genomics,16,1(2015-07-29) 16 (1):560Google Scholar
  28. Li X, Wasila H, Liu L, Yuan T, Gao Z, Zhao B, Ahmad I (2015b) Physicochemical characteristics, polyphenol compositions and antioxidant potential of pomegranate juices from 10 Chinese cultivars and the environmental factors analysis. Food Chem 175:575–584PubMedGoogle Scholar
  29. Liang YR, Liu ZS, Xu YR, Hu YL (2010) A study on chemical composition of two special green teas (Camellia sinensis). J Sci Food Agric 53(4):541–548Google Scholar
  30. Lin JS, Lin CC, Lin HH, Chen YC, Jeng ST (2012) MicroR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytol 196(2):427–440PubMedGoogle Scholar
  31. Liu Q, Luo L, Zheng L (2018) Lignins: biosynthesis and biological functions in plants. Int J Mol Sci 19(2):335PubMedCentralGoogle Scholar
  32. Moura JCMS, Bonine CAV, Viana JDF, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52(4):360–376.  https://doi.org/10.1111/j.1744-7909.2010.00892.x PubMedGoogle Scholar
  33. Nurit F, Don LB, Arthur V, Yanir K, Julio S, Evgenia L, Schnitzer PT, Adi DF, Amots H, Leviah A (2013) Transcriptional profiling of sweetpotato (Ipomoea batatas) roots indicates down-regulation of lignin biosynthesis and up-regulation of starch biosynthesis at an early stage of storage root formation. BMC Genomics 14(1):460Google Scholar
  34. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. 29:9Google Scholar
  35. Pradhan MP, Loqué D (2014) Histochemical staining of Arabidopsis thaliana secondary cell wall elements. J Visual Exp Jove 87(87):e51381–e51381Google Scholar
  36. Punyasiri PA, Abeysinghe IS, Kumar V, Treutter D, Duy D, Gosch C, Martens S, Forkmann G, Fischer TC (2004) Flavonoid biosynthesis in the tea plant Camellia sinensis: properties of enzymes of the prominent epicatechin and catechin pathways. Arch Biochem Biophys 431(1):22–30PubMedGoogle Scholar
  37. Riboulet C, Guillaumie S, Méchin V, Bosio M, Pichon M, Goffner D, Lapierre C, Pollet B, Lefevre B, Martinant JP (2009) Kinetics of phenylpropanoid gene expression in maize growing internodes: relationships with cell wall deposition. Crop Sci 49(1):211–223Google Scholar
  38. Robinson AR, Mansfield SD (2009) Rapid analysis of poplar lignin monomer composition by a streamlined thioacidolysis procedure and near-infrared reflectance-based prediction modeling. Plant J 58(4):706–714PubMedGoogle Scholar
  39. Rogers LA, Campbell MM (2004) The genetic control of lignin deposition during plant growth and development. New Phytol 164(1):17–30Google Scholar
  40. Saito K, Fukushima K (2005) Distribution of lignin interunit bonds in the differentiating xylem of compression and normal woods of Pinus thunbergii. J Wood Sci 51(3):246–251Google Scholar
  41. Shen H, Fu C, Xiao X, Ray T, Tang Y, Wang Z, Chen F (2009) Developmental control of lignification in stems of lowland switchgrass variety Alamo and the effects on saccharification efficiency. Bioenergy Res 2(4):233–245Google Scholar
  42. Shen J, Zou Z, Zhang X, Zhou L, Wang Y, Fang W, Zhu X (2018) Metabolic analyses reveal different mechanisms of leaf color change in two purple-leaf tea plant (Camellia sinensis L.) cultivars. Hortic Res 5(1)Google Scholar
  43. Stewart JJ, Akiyama T, Chapple C, Ralph J, Mansfield SD (2009) The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 150(2):621–635PubMedPubMedCentralGoogle Scholar
  44. Thévenin J, Pollet B, Letarnec B, Saulnier L, Gissot L, Maiagrondard A, Lapierre C, Jouanin L (2011) The simultaneous repression of CCR and CAD, two enzymes of the lignin biosynthetic pathway, results in sterility and dwarfism in Arabidopsis thaliana. Mol Plant 04(1):70–82Google Scholar
  45. Tu Y, Rochfort S, Liu Z, Ran Y, Griffith M, Badenhorst P, Louie GV, Bowman ME, Smith KF, Noel JP (2010) Functional analyses of caffeic acid O-methyltransferase and cinnamoyl-CoA-reductase genes from perennial ryegrass (Lolium perenne). Plant Cell 22(10):3357–3373PubMedPubMedCentralGoogle Scholar
  46. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W (2010) Lignin biosynthesis and structure. Plant Physiol 153(3):895–905PubMedPubMedCentralGoogle Scholar
  47. Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, Boerjan W (2012) Metabolic engineering of novel lignin in biomass crops. New Phytol 196(4):978–1000PubMedGoogle Scholar
  48. Wagner A, Tobimatsu Y, Phillips L, Flint H, Geddes B, Lu F, Ralph J (2015) Syringyl lignin production in conifers: proof of concept in a pine tracheary element system. Proc Natl Acad Sci U S A 112(19):6218–6223PubMedPubMedCentralGoogle Scholar
  49. Wang Y, Gao L, Shan Y, Liu Y, Tian Y, Xia T (2012) Influence of shade on flavonoid biosynthesis in tea (Camellia sinensis (L.) O. Kuntze). Sci Hortic 141:7–16.  https://doi.org/10.1016/j.scienta.2012.04.013 Google Scholar
  50. Wang GL, Huang Y, Zhang XY, Xu ZS, Wang F, Xiong AS (2016a) Transcriptome-based identification of genes revealed differential expression profiles and lignin accumulation during root development in cultivated and wild carrots. Plant Cell Rep 35(8):1743–1755PubMedGoogle Scholar
  51. Wang GL, Que F, Xu ZS, Wang F, Xiong AS (2016b) Exogenous gibberellin enhances secondary xylem development and lignification in carrot taproot. Protoplasma 254(2):1–10Google Scholar
  52. Wang J, Ma L, Shen Z, Sun D, Zhong P, Bai Z, Zhang H, Cao Y, Bao Y, Fu C (2017) Lignification of sheepgrass internodes at different developmental stages and associated alteration of cell wall saccharification efficiency. Front Plant Sci 8(e1416)Google Scholar
  53. Weng JK, Mo H, Chapple C (2010) Over-expression of F5H in COMT-deficient Arabidopsis leads to enrichment of an unusual lignin and disruption of pollen wall formation. Plant J 64(6):898–911PubMedGoogle Scholar
  54. Wu ZJ, Li XH, Liu ZW, Xu ZS, Zhuang J (2014) De novo assembly and transcriptome characterization: novel insights into catechins biosynthesis in Camellia sinensis. BMC Plant Biol 14(1):277.  https://doi.org/10.1186/s12870-014-0277-4 PubMedPubMedCentralGoogle Scholar
  55. Wu ZJ, Tian C, Jiang Q, Li XH, Zhuang J (2016) Selection of suitable reference genes for qRT-PCR normalization during leaf development and hormonal stimuli in tea plant (Camellia sinensis). Sci Rep 6(19748):19748PubMedPubMedCentralGoogle Scholar
  56. Xia EH, Zhang HB, Sheng J, Li K, Zhang QJ, Kim C, Zhang Y, Liu Y, Zhu T, Li W, Huang H, Tong Y, Nan H, Shi C, Shi C, Jiang JJ, Mao SY, Jiao JY, Zhang D, Zhao Y, Zhao YJ, Zhang LP, Liu YL, Liu BY, Yu Y, Shao SF, Ni DJ, Eichler EE, Gao LZ (2017) The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Mol Plant 10(6):866–877.  https://doi.org/10.1016/j.molp.2017.04.002 PubMedGoogle Scholar
  57. Xu Z, Zhang D, Hu J, Zhou X, Ye X, Reichel KL, Stewart NR, Syrenne RD, Yang X, Gao P (2009) Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. Bmc Bioinformatics 10(S11):S3PubMedPubMedCentralGoogle Scholar
  58. Xu B, Escamilla-Trevino LL, Sathitsuksanoh N, Shen ZX, Shen H, Zhang YHP, Dixon RA, Zhao BY (2011) Silencing of 4-coumarate:coenzyme A ligase in switchgrass leads to reduced lignin content and improved fermentable sugar yields for biofuel production. New Phytol 192(3):611–625.  https://doi.org/10.1111/j.1469-8137.2011.03830.x PubMedGoogle Scholar
  59. Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16(4):227–233PubMedGoogle Scholar
  60. Zhao H, Lu J, Lu S, Zhou Y, Wei J, Song Y, Wang T (2005) Isolation and functional characterization of a cinnamate 4-hydroxylase promoter from Populus tomentosa. Plant Sci 168(5):1157–1162Google Scholar
  61. Zhao Q, Nakashima J, Chen F, Yin Y, Fu C, Yun J, Shao H, Wang X, Wang ZY, Dixon RA (2013) Laccase is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25(10):3976–3987PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Yong-Xin Wang
    • 1
  • Rui-Min Teng
    • 1
  • Wen-Li Wang
    • 1
  • Ying Wang
    • 1
  • Wei Shen
    • 1
  • Jing Zhuang
    • 1
    Email author
  1. 1.Tea Science Research Institute, College of HorticultureNanjing Agricultural UniversityNanjingChina

Personalised recommendations