Plant Growth Regulation

, Volume 84, Issue 3, pp 481–492 | Cite as

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

  • Siqing Wan
  • Weidong Wang
  • Tianshan Zhou
  • Yongheng Zhang
  • Jiangfei Chen
  • Bin Xiao
  • Yajun Yang
  • Youben Yu
Original paper
First Online:
Received:
Accepted:

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.

Keywords

Camellia sinensis Salt stress DEGs RNA-Seq Molecular mechanism 
This is a preview of subscription content, log in to check access.

Notes

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).

Compliance with ethical standards

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.

Supplementary material

10725_2017_354_MOESM1_ESM.pdf (4 mb)
Supplementary material 1 (PDF 4078 KB)
10725_2017_354_MOESM2_ESM.pdf (3 mb)
Supplementary material 2 (PDF 3081 KB)
10725_2017_354_MOESM3_ESM.pdf (3.9 mb)
Supplementary material 3 (PDF 4009 KB)
10725_2017_354_MOESM4_ESM.pdf (931 kb)
Supplementary material 4 (PDF 930 KB)
10725_2017_354_MOESM5_ESM.pdf (83 kb)
Supplementary material 5 (PDF 83 KB)
10725_2017_354_MOESM6_ESM.docx (44 kb)
Supplementary material 6 (DOCX 43 KB)

References

  1. 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 25:3389–3402CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106CrossRefPubMedPubMedCentralGoogle Scholar
  3. Apweiler R, Bairoch A, Wu CH et al (2004) UniProt: the universal protein knowledgebase. Nucleic Acids Res 32:D115-D119CrossRefPubMedCentralGoogle Scholar
  4. Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25(1):25–29CrossRefPubMedPubMedCentralGoogle Scholar
  5. Banerjee A, Roychoudhury A (2016) Group II late embryogenesis abundant (LEA) proteins: structural and functional aspects in plant abiotic stress. Plant Growth Regul 79:1–17CrossRefGoogle Scholar
  6. 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 67:107–124CrossRefPubMedGoogle Scholar
  7. 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 75–90CrossRefGoogle Scholar
  8. 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 17:175CrossRefGoogle Scholar
  9. 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 154:239–248CrossRefGoogle Scholar
  10. 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):e0126492CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cheong YH, Kim MC (2010) Functions of MAPK cascade pathways in plant defense signaling. Plant Pathol J 26(2):101–109CrossRefGoogle Scholar
  12. Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160CrossRefPubMedGoogle Scholar
  13. de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21:677–685CrossRefPubMedGoogle Scholar
  14. 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 56:35–40CrossRefPubMedGoogle Scholar
  15. 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 81:183–195CrossRefGoogle Scholar
  16. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763CrossRefPubMedGoogle Scholar
  17. Edel KH, Kudla J (2016) Integration of calcium and ABA signaling. Curr Opin Plant Biol 33:83–91CrossRefPubMedGoogle Scholar
  18. Fedoroff NV, Battisti DS, Beachy RN et al (2010) Radically rethinking agriculture for the 21st century. Science 327:833–834CrossRefPubMedPubMedCentralGoogle Scholar
  19. Finn RD, Bateman A, Clements J et al (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222-D230Google Scholar
  20. 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 8:1494–1512CrossRefPubMedGoogle Scholar
  21. 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 15:22155–22172CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jakoby M, Weisshaar B, Droge-Laser W et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111CrossRefPubMedGoogle Scholar
  23. 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 6:275–286CrossRefPubMedGoogle Scholar
  24. 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 66:4683–4697CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 59:86–101CrossRefPubMedGoogle Scholar
  26. Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594CrossRefPubMedGoogle Scholar
  27. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277-D280CrossRefPubMedCentralGoogle Scholar
  28. Koonin EV, Fedorova ND, Jackson JD et al (2004) A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes. Genome Biol 5:R7CrossRefPubMedPubMedCentralGoogle Scholar
  29. 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 102:363–368CrossRefGoogle Scholar
  30. Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:323CrossRefGoogle Scholar
  31. Li CN, Ng CKY, Fan LM (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91CrossRefGoogle Scholar
  32. 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 81:51–61CrossRefGoogle Scholar
  33. 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 14:5842–5878CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 35:1719–1728CrossRefPubMedGoogle Scholar
  35. 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 22:478–488CrossRefGoogle Scholar
  36. 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 25:402–408CrossRefPubMedGoogle Scholar
  37. Marguerat S, Bahler J (2010) RNA-seq: from technology to biology. Cell Mol Life Sci 67:569–579CrossRefPubMedGoogle Scholar
  38. 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 63:484–498CrossRefPubMedPubMedCentralGoogle Scholar
  39. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefPubMedGoogle Scholar
  40. Park CY, Lee JH, Yoo JH et al (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Lett 579:1545–1550CrossRefPubMedGoogle Scholar
  41. Postnikova OA, Shao J, Nemchinov LG (2013) Analysis of the alfalfa root transcriptome in response to salinity stress. Plant Cell Physiol 54:1041–1055CrossRefPubMedGoogle Scholar
  42. Ryu H, Cho YG (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155CrossRefGoogle Scholar
  43. 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 97:6896–6901CrossRefPubMedPubMedCentralGoogle Scholar
  44. 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 15:5063–5078CrossRefPubMedPubMedCentralGoogle Scholar
  45. Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21CrossRefPubMedGoogle Scholar
  46. 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 48:1148–1158CrossRefPubMedGoogle Scholar
  47. 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 28:33–36CrossRefPubMedPubMedCentralGoogle Scholar
  48. Upadhyaya H, Panda SK (2013) Abiotic stress responses in tea [Camellia sinensis L (O) Kuntze]: an overview. Rev Agric Sci 1:1–10Google Scholar
  49. 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 58:429–434CrossRefGoogle Scholar
  50. 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 9:244–252CrossRefPubMedGoogle Scholar
  51. 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 7:385PubMedPubMedCentralGoogle Scholar
  52. 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 7:456PubMedPubMedCentralGoogle Scholar
  53. 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:e0166727CrossRefPubMedPubMedCentralGoogle Scholar
  54. Wilkins KA, Matthus E, Swarbreck SM, Davies JM (2016) Calcium-mediated abiotic stress signaling in roots. Front Plant Sci 7:1296CrossRefPubMedPubMedCentralGoogle Scholar
  55. Yamakawa H, Katou S, Seo S, Mitsuhara I, Kamada H, Ohashi Y (2004) Plant MAPK phosphatase interacts with calmodulins. J Biol Chem 279:928–936CrossRefPubMedGoogle Scholar
  56. 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 55:2060–2076CrossRefPubMedGoogle Scholar
  57. 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 21:133–139CrossRefPubMedGoogle Scholar
  58. Yue C, Cao HL, Wang L et al (2014) Molecular cloning and expression analysis of tea plant aquaporin (AQP) gene family. Plant Physiol Biochem 83:65–76CrossRefPubMedGoogle Scholar
  59. Zhang JH, Jia WS, Yang JC, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119CrossRefGoogle Scholar
  60. 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 80:571–585CrossRefPubMedGoogle Scholar
  61. 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 13:78CrossRefGoogle Scholar
  62. 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:e0137447CrossRefPubMedPubMedCentralGoogle Scholar
  63. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefPubMedPubMedCentralGoogle Scholar
  64. Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Siqing Wan
    • 1
  • Weidong Wang
    • 1
  • Tianshan Zhou
    • 1
  • Yongheng Zhang
    • 1
  • Jiangfei Chen
    • 1
  • Bin Xiao
    • 1
  • Yajun Yang
    • 1
    • 2
  • Youben Yu
    • 1
  1. 1.College of HorticultureNorthwest A&F UniversityYanglingChina
  2. 2.Key Laboratory of Tea Biology and Resources Utilization, Ministry of Agriculture, National Center for Tea ImprovementTea Research Institute of the Chinese Academy of Agricultural SciencesHangzhouChina

Personalised recommendations