Skip to main content
SpringerLink
Log in

Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Tea plant [Camellia sinensis (L.) O. Kuntze] constitutes one of the most important economic crops in many countries. However, in many areas, tea plants are subjected to high salinity, which severely affects the growth and development of these plants. To understand the potential molecular mechanisms of tea plants in response to salt stress, we used RNA-Seq technology to compare the transcriptomes from tea plants treated with and without NaCl and analyzed the differentially expressed genes (DEGs). In total, 470,738 transcripts and 150,257 unigenes were obtained that had average lengths of 1422.09 and 680.40 nt, respectively, and 28,831 of these sequences were annotated in public databases. In addition, 1769 DEGs were identified, including 947 up-regulated and 822 down-regulated ones. Many of these DEGs were involved in Ca2+ signal transduction, the abscisic acid (ABA) pathway, and mitogen-activated protein kinase (MAPK) cascades. Many DEGs were also transcription factors and key functional proteins involved in salt resistance in tea plants; these genes constitute a regulatory network in response to salt stress. qRT-PCR analyses of nine unigenes were performed to confirm the validity of the data, and the results were highly consistent with the RNA-Seq results. Taken together, these findings reveal the underlying molecular mechanism of tea plants in response to salt stress and could provide many candidate genes for additional studies, especially those involving the genetic engineering and breeding of tea plants that are highly resistant to salt stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apweiler R, Bairoch A, Wu CH et al (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:D115-D119

    Article  PubMed Central  Google Scholar 

  • Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17

    Article  CAS  Google Scholar 

  • Bies-Ethève N, Gaubier-Comella P, Debures A et al (2008) Inventory, evolution and expression profiling diversity of the LEA (late embryogenesis abundant) protein gene family in Arabidopsis thaliana. Plant Mol Biol 67:107–124

    Article  PubMed  Google Scholar 

  • Boudsocq M, Sheen J (2009) Stress signaling II: calcium sensing and signaling. In: Pareek A, Sopory S, Bohnert H (eds) Abiotic stress adaptation in plants. Springer, Dordrecht, pp 75–90

    Chapter  Google Scholar 

  • Cao JM, Jiang M, Li P, Chu ZQ (2016) Genome-wide identification and evolutionary analyses of the PP2C gene family with their expression profiling in response to multiple stresses in Brachypodium distachyon. BMC Genom 17:175

    Article  Google Scholar 

  • Chen L, Zhou ZX, Yang YJ (2007) Genetic improvement and breeding of tea plant (Camellia sinensis) in China: from individual selection to hybridization and molecular breeding. Euphytica 154:239–248

    Article  CAS  Google Scholar 

  • Chen L, Chu C, Lu J, Kong XY, Huang T, Cai YD (2015) Gene ontology and KEGG pathway enrichment analysis of a drug target-based classification system. PLoS ONE 10(5):e0126492

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheong YH, Kim MC (2010) Functions of MAPK cascade pathways in plant defense signaling. Plant Pathol J 26(2):101–109

    Article  CAS  Google Scholar 

  • Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160

    Article  CAS  PubMed  Google Scholar 

  • de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21:677–685

    Article  PubMed  Google Scholar 

  • Deng WW, Wang S, Chen Q, Zhang ZZ, Hu XY (2012) Effect of salt treatment on theanine biosynthesis in Camellia sinensis seedlings. Plant Physiol Biochem 56:35–40

    Article  CAS  PubMed  Google Scholar 

  • Du XL, Wang G, Ji J, Shi LP, Guan CF, Jin C (2017) Comparative transcriptome analysis of transcription factors in different maize varieties under salt stress conditions. Plant Growth Regul 81:183–195

    Article  CAS  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  CAS  PubMed  Google Scholar 

  • Edel KH, Kudla J (2016) Integration of calcium and ABA signaling. Curr Opin Plant Biol 33:83–91

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff NV, Battisti DS, Beachy RN et al (2010) Radically rethinking agriculture for the 21st century. Science 327:833–834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD, Bateman A, Clements J et al (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222-D230

    Google Scholar 

  • Haas BJ, Papanicolaou A, Yassour M et al (2013) De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8:1494–1512

    Article  CAS  PubMed  Google Scholar 

  • Hao XY, Horvath DP, Chao WS, Yang YJ, Wang XC, Xiao B (2014) Identification and evaluation of reliable reference genes for quantitative real-time PCR analysis in tea plant (Camellia sinensis (L.) O. Kuntze). Int J Mol Sci 15:22155–22172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  CAS  PubMed  Google Scholar 

  • Ji HT, Pardo JM, Batelli G, Van Oosten MJ, Bressan RA, Li X (2013) The salt overly sensitive (SOS) pathway: established and emerging roles. Mol Plant 6:275–286

    Article  CAS  PubMed  Google Scholar 

  • Jia FJ, Wang CY, Huang JG, Yang GD, Wu CG, Zheng CC (2015) SCF E3 ligase PP2-B11 plays a positive role in response to salt stress in Arabidopsis. J Exp Bot 66:4683–4697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang JJ, Ma SH, Ye NH, Jiang M, Cao JS, Zhang JH (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101

    Article  CAS  PubMed  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594

    Article  CAS  PubMed  Google Scholar 

  • Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277-D280

    Article  PubMed Central  Google Scholar 

  • Koonin EV, Fedorova ND, Jackson JD et al (2004) A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 5:R7

    Article  PubMed  PubMed Central  Google Scholar 

  • Li ZY, Chen SY (2001) Isolation, characterization and chromosomal location of a novel zinc-finger protein gene that is down-regulated by salt stress. Theor Appl Genet 102:363–368

    Article  CAS  Google Scholar 

  • Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323

    Article  CAS  Google Scholar 

  • Li CN, Ng CKY, Fan LM (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91

    Article  CAS  Google Scholar 

  • Li J, Lv XJ, Wang LX, Qiu ZM, Song XM, Lin JK, Chen W (2017) Transcriptome analysis reveals the accumulation mechanism of anthocyanins in ‘Zijuan’ tea (Camellia sinensis var. asssamica (Masters) kitamura) leaves. Plant Growth Regul 81:51–61

    Article  CAS  Google Scholar 

  • Lindemose S, O’Shea C, Jensen MK, Skriver K (2013) Structure, function and networks of transcription factors involved in abiotic stress responses. Int J Mol Sci 14:5842–5878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu CH, Lu RJ, Guo GM et al (2016a) Transcriptome analysis reveals translational regulation in barley microspore-derived embryogenic callus under salt stress. Plant Cell Rep 35:1719–1728

    Article  CAS  PubMed  Google Scholar 

  • Liu JY, Chen NN, Cheng ZM, Xiong JS (2016b) Genome-wide identification, annotation and expression profile analysis of SnRK2 gene family in grapevine. Aust J Grape Wine R 22:478–488

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Marguerat S, Bahler J (2010) RNA-seq: from technology to biology. Cell Mol Life Sci 67:569–579

    Article  CAS  PubMed  Google Scholar 

  • Mehlmer N, Wurzinger B, Stael S et al (2010) The Ca2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis. Plant J 63:484–498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  CAS  PubMed  Google Scholar 

  • Park CY, Lee JH, Yoo JH et al (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Lett 579:1545–1550

    Article  CAS  PubMed  Google Scholar 

  • Postnikova OA, Shao J, Nemchinov LG (2013) Analysis of the alfalfa root transcriptome in response to salinity stress. Plant Cell Physiol 54:1041–1055

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155

    Article  CAS  Google Scholar 

  • Shi HZ, Ishitani M, Kim CS, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song AP, Zhu XR, Chen FD, Gao HS, Jiang JF, Chen SM (2014) A chrysanthemum heat shock protein confers tolerance to abiotic stress. Int J Mol Sci 15:5063–5078

    Article  PubMed  PubMed Central  Google Scholar 

  • Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21

    Article  CAS  PubMed  Google Scholar 

  • Sun JQ, Jiang HL, Xu YX, Li HM, Wu XY, Xie Q, Li CY (2007) The CCCH-type zinc finger proteins AtSZF1 and AtSZF2 regulate salt stress responses in Arabidopsis. Plant Cell Physiol 48:1148–1158

    Article  CAS  PubMed  Google Scholar 

  • Tatusov RL, Galperin MY, Natale DA, Koonin EV (2000) The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res 28:33–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Upadhyaya H, Panda SK (2013) Abiotic stress responses in tea [Camellia sinensis L (O) Kuntze]: an overview. Rev Agric Sci 1:1–10

    Google Scholar 

  • Wan Q, Xu RK, Li XH (2012) Proton release by tea plant (Camellia sinensis L.) roots as affected by nutrient solution concentration and pH. Plant Soil Environ 58:429–434

    Article  CAS  Google Scholar 

  • Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  CAS  PubMed  Google Scholar 

  • Wang WD, Xin HH, Wang ML et al (2016a) Transcriptomic analysis reveals the molecular mechanisms of drought-stress-induced decreases in Camellia sinensis leaf quality. Front Plant Sci 7:385

    PubMed  PubMed Central  Google Scholar 

  • Wang WD, Sheng XY, Shu ZF et al (2016b) Combined cytological and transcriptomic analysis reveals a nitric oxide signaling pathway involved in cold-inhibited Camellia sinensis pollen tube growth. Front Plant Sci 7:456

    PubMed  PubMed Central  Google Scholar 

  • Wang YX, Liu ZW, Wu ZJ, Li H, Zhuang J (2016c) Transcriptome-wide identification and expression analysis of the NAC gene family in tea plant [Camellia sinensis (L.) O. Kuntze]. PLoS ONE 11:e0166727

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilkins KA, Matthus E, Swarbreck SM, Davies JM (2016) Calcium-mediated abiotic stress signaling in roots. Front Plant Sci 7:1296

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J Biol Chem 279:928–936

    Article  CAS  PubMed  Google Scholar 

  • Yan HR, Jia HH, Chen XB, Hao LL, An HL, Guo XQ (2014) The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol 55:2060–2076

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2014) ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21:133–139

    Article  CAS  PubMed  Google Scholar 

  • Yue C, Cao HL, Wang L et al (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76

    Article  CAS  PubMed  Google Scholar 

  • Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119

    Article  Google Scholar 

  • Zhang SX, Haider I, Kohlen W et al (2012) Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol 80:571–585

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Cai MC, Yu XM, Wang LS, Guo CF, Ming R, Zhang JS (2017) Transcriptome dynamics of Camellia sinensis in response to continuous salinity and drought stress. Tree Genet Genomes 13:78

    Article  Google Scholar 

  • Zhou Y, Yin XC, Duan RJ, Hao GP, Guo JC, Jiang XY (2015) SpAHA1 and SpSOS1 coordinate in transgenic yeast to improve salt tolerance. PLoS ONE 10:e0137447

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the earmarked fund for Modern Agro-industry Technology Research System (CARS-23), the Agricultural Special Fund Project of Shaanxi Province, the China Postdoctoral Science Foundation (Grant No. 2016M602873).

Author information

Author notes

  1. Siqing Wan and Weidong Wang have contributed equally to this work.

Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Siqing Wan, Weidong Wang, Tianshan Zhou, Yongheng Zhang, Jiangfei Chen, Bin Xiao, Yajun Yang & Youben Yu

  2. Key Laboratory of Tea Biology and Resources Utilization, Ministry of Agriculture, National Center for Tea Improvement, Tea Research Institute of the Chinese Academy of Agricultural Sciences, Hangzhou, 310008, China

    Yajun Yang

Authors
  1. Siqing Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weidong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tianshan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jiangfei Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bin Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yajun Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Youben Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yajun Yang or Youben Yu.

Ethics declarations

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wan, S., Wang, W., Zhou, T. et al. Transcriptomic analysis reveals the molecular mechanisms of Camellia sinensis in response to salt stress. Plant Growth Regul 84, 481–492 (2018). https://doi.org/10.1007/s10725-017-0354-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0354-4

Keywords

Search

Navigation